Table Of ContentPUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY
CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024
Number3376,26pp.,4figures,2tablesJuly 25,2002
Do Ruffed Lemurs Form a Hybrid Zone?
Distribution and Discovery of Varecia, with
Systematic and Conservation Implications
NATALIE VASEY1 AND IAN TATTERSALL2
ABSTRACT
SincetheirdiscoverybyWesternexplorerstravelingtoMadagascarinthe17thcentury,the
ruffed lemurs have undergone numerous taxonomic revisions. During the 19th and 20th cen-
turies, it was intermittently suggested that black-and-white and red ruffed lemurs hybridizein
nature.Despitethefactthatanaturalhybridzonehasneverbeendocumented,thissuggestion
hasplayedalargeroleindesignatingthetwoformsassubspeciesofthesinglespeciesVarecia
variegata. Through a review and synthesis of historical documents, taxonomic literature,mu-
seum collections, menagerie and zoo records, recent survey work, genetic data, and vocali-
zation data, we examine the evidence for a natural hybrid zone and suggest taxonomic revi-
sions. Our work indicates a more extensive hybrid zone than previously suggested—but one
in which hybridization is the exception ratherthantherule.Furthermore,ourfindingswarrant
upgrading the black-and-white ruffed lemur and the red ruffed lemur from subspecies to full
species, Varecia variegata (Kerr, 1792) and Varecia rubra (E. Geoffroy, 1812). Our results
support the current captive breeding practices of U.S. and European zoos participating in the
ruffed lemur ‘‘Species Survival Plan’’ and the ‘‘European Endangered Species Programme’’.
Lastly, and possibly most importantly, we can now set specific geographic priorities for con-
serving the habitat of these highly endangered lemurs in northern Madagascar.
1Department ofAnatomy,College ofMedicine, HowardUniversity,520WStreetNW,Washington,D.C.20059;
now at Anthropology Department, Portland State University, P.O. Box 751, Portland, Oregon 97207. e-mail:
[email protected].
2Curator,Departmentof Anthropology,AmericanMuseumofNaturalHistory.e-mail:[email protected].
Copyright(cid:113)AmericanMuseumofNaturalHistory2002 ISSN0003-0082
2 AMERICAN MUSEUM NOVITATES NO. 3376
INTRODUCTION tery concerning a natural hybrid zone, and
instead we try to solve this problem here.
The French explorers Franc¸ois Cauche
To assess whether a natural hybrid zone
(1651) and Etienne de Flacourt (1658) pro-
ever existed, we undertook a review and
vided Westerners with the first descriptions
synthesis of historical documents, taxo-
of the Malagasy primate now commonly
nomic literature, museum collections, me-
known as the ‘‘variegated’’ or ‘‘black-and-
nagerie and zoo records, and recent survey
white ruffed’’ lemur. More than a century
work. We also summarize recent genetic
later, these animals were formally named
work on ruffed lemurs and previously pub-
Lemur macaco variegatus by Kerr (1792).
lished work on their vocalizations. These
A related red-and-black form, Lemur ruber,
reviews suggest that hybridization in the
wasnamedshortlyafterwardbyE.Geoffroy
wild probably occurred over a much larger
(1812) and now goes by the common name
area than previously thought, but that it is
of ‘‘red ruffed lemur’’. Tremendous vari-
the exception rather than the rule. Only
ability in coat color and pattern (see fig. 1),
remnants of the hybrid zone habitat as it
the ability of the black-and-white form to
hybridize with the red formin captivity,and existed prior to human interferencemayre-
the relatively recent discovery of the unusu- main, given the subsequent extensive hab-
al life history traits of both ruffed lemurs itat loss north of the Bay of Antongil. Al-
have subsequently spurred repeated taxo- ternatively, it is possible that a poorly doc-
nomic revisions. Currently the two color umented variety or subspecies of ruffed le-
forms are generally classified as subspecies mur has virtually been lost, and that the
of the same species and are united within so-called hybrids are remnants of this pop-
the genus Varecia Gray, 1863 in the strep- ulation; however, there is little substanti-
sirhine primate family Lemuridae. The ating evidence for this. In conservation
black-and-white form is usually known as terms, forest corridors are needed to con-
Varecia variegata variegata and the red nect Varecia populations across the water-
form as Varecia variegata rubra. sheds north of the Bay ofAntongil.Finally,
In his pathbreaking review of lemur sys- the results of our review support upgrading
tematics, Schwarz (1931) alluded to theex- both the black-and-white ruffed lemur and
istence of a natural hybrid zone between thered ruffedlemurtofullspecies,Varecia
the two color forms north of the Bay of variegata (Kerr, 1792) and Varecia rubra
Antongil (northeastern Madagascar; see (E. Geoffroy 1812), as has also been sug-
figs. 2 and 3), but he provided no direct gested by Groves (2001). However, we are
evidence for such a zone. Documentation unable to follow Groves in promoting the
of such a natural hybrid zone would be of pelage variants of the black-and-white spe-
great biological interest in designatinggeo- cies to subspecies status.
graphic priorities for habitat conservation,
for captive management, and forlemursys-
ABBREVIATIONS
tematics generally. However, no recent sur-
veys have located such a zone. The balance AMNH American Museum of Natural History,
of evidence on published record so farrests New York
on the somewhat slim foundation of a sin- BMNH British Museum of Natural History,
gle hybrid specimen housed at the Ameri- London
can Museum of Natural History which was DUPC Duke University Primate Center, Dur-
ham, North Carolina
collected 40 km NW of Maroantsetra by
MCZ Museum of Comparative Zoology,
the Archbold expedition in 1930 (Rand,
Cambridge, Massachusetts
1936; Tattersall, 1982; Buettner-Janusch
MNHN Muse´um National d’Histoire Naturelle,
and Tattersall, 1985), althoughvarioussim-
Paris
ilarly puzzling specimens also exist else-
RMNH Rijksmuseum van Natuurlijke Historie,
where. In writing a review of the natural Leiden
history of Varecia, Vasey (in press) was USNM United States National Museum
disinclined to broach the biological mys- (Smithsonian), Washington, D.C.
2002 VASEY AND TATTERSALL:SYSTEMATICSOF VARECIA 3
NORMATIVE DESCRIPTIONS OF evidence of coat pattern among black-and-
BLACK-AND-WHITE AND RED white ruffed lemurs contradicts the notion of
RUFFED LEMURS a simple north–south cline, although the
modest trend noted by Petter et al. (1977)
Varecia is the largest-bodied genus of the
and Tattersall (1982) toward a reduction in
primate family Lemuridae, possessing an es-
the overall amount of black in the pelage in
pecially long, luxuriant coat relative to other
favor of white toward the south does seem
lemurs. Within this genus the sexes aremore
to hold in a general way. Nonetheless, there
or less identical in body size and pelage col-
is some notable geographic randomizationof
oration. Adult wild Varecia range in body
pelage pattern distribution (see fig. 2 and be-
mass from 2.6 to 4.1 kg (Vasey, in press).
low). Analysis of the matter is complicated
Both black-and-white and red forms possess
by the fact that while ruffed lemur skins are
black fur on the ventrum, tail, inner aspect
quite well represented in museum collec-
of limbs, manus, pes, crown, forehead, and
tions, locality records are not. Moreover, re-
face. Surrounding the face and ears is a ruff
liablefield reportsaresparse.However,there
of long fur: white in black-and-white ruffed
are clearly broad areas within which more
lemurs and red or honey-blond in red ruffed
thanonevariantistobefound(seefig.2and
lemurs. But consistency in coat color and
below). We are thus unable to concur with
pattern ends there, particularly in the black-
Groves (2001) that atleastthreedistinctsub-
and-white variant: Varecia was aptly named
species of Varecia variegata are to be rec-
the ‘‘variegated’’ lemur. In a review pub-
ognized.
lished two decades ago, one of us (Tattersall,
To summarize the data presented in figure
1982) recognized four principal variants 1, in lighter forms (e.g., the variegata vari-
among the black-and-white ruffed lemurs ety), the dorsal fur is white with black re-
(shown in schematic form in fig. 1). Three stricted to the shoulder, the upper arm to the
of these had already been established in the elbow, and front of the thigh (color plate);
mid-nineteenth-century account of I. Geof- whereas in darker forms known from the
froy(1851),whoelaboratedthreevarietiesof north (e.g., the subcincta variety), the dor-
his Lemur varius (‘‘varie´te´s’’ a, b, and c). sum is mainly black with two variably thick
These varieties correspond, respectively, to bands of white fur—one band encircles the
the forms represented by Kerr’s Lemur ma- torso and sometimes extends longitudinally
caco variegatus (Kerr, 1792), Osman Hill’s toward the nape of the neck, and the other
Lemur variegatus editorum (Hill, 1953), and band extends acrossthe rump,downthepos-
Smith’s Prosimia subcincta (Smith, 1833). terior aspect of the thigh, andontothelateral
For other equivalences, see Tattersall(1982), surface of the lower leg. In another variety
who also divided variety b (editorum) into (editorum), the black shoulder patches ex-
two subvariants (b1 and b2). Figure 1 dis- tend posteriorly onto the flanks and meet
plays the basic pelage coloration differences midsagittally, forming a black mantle across
on which the four resulting varieties are the back and shoulders. These various coat
based (see also below). patterns have been illustrated frequently (see
A thorough examination of almost all Historical Documents, Taxonomy, and Illus-
available museum black-and-white speci- trations). Indistinct white rings on the tail,
mens indicates the presence of more pelage- said to resemble those of the ring-tailed le-
color variation than is reflected in these four mur, have also been noted in museum spec-
simple descriptions: an unpublished review imens collected by J.-P. Audebert (Handfest,
by one of us (I.T.) several yearsagorevealed 1968, cited in Ceska et al., 1992) and in liv-
that as many as 10 repeated variants could ing wild animals (Evans et al., 1993–1994).
be recognized in museum collections. How- Dark regions are not always pure black, but
ever, especially in view of the regrettablylit- may grade into silver, light brown, or dark
tle that we know of geographic distributions brown.
(see fig. 2), an infinite multiplication of for- While the variegated coat of the black-
malized variants hardly seems desirable or and-white ruffed lemur has long been
even possible. Examination of the available known, the pied pelage of the red ruffed le-
4 AMERICAN MUSEUM NOVITATES NO. 3376
Fig. 1. Schematic dorsal view of the four pelage variants recognized here among black-and-white
ruffed lemurs. Demarcation between black and white pelage areas is generally but notinvariablysharp;
black noses are usually frosted.
2002 VASEY AND TATTERSALL:SYSTEMATICSOF VARECIA 5
Fig.2. Mapshowingthegeneralareasofdistributionofblack-and-whiteandredruffedlemurs.See
figure 3 for detail of the contact area in the region of Maroantsetra, with field sightings located; refer
to the key at upper left for symbols (filled symbols are museum records, open ones are fieldsightings).
Hatched areas indicate approximate distribution limits and do not imply continuous distribution within
theregionsindicated.Fieldidentificationsindicatedhereintheblack-and-whiteruffedlemurrangesouth
of the Bay of Antongil are by Andrea Katz (Betampona), Elizabeth Balko (Ranomafana/Kianjavato
region), and I.T. (extreme south).
6 AMERICAN MUSEUM NOVITATES NO. 3376
mur has not been fully appreciated (Vasey, tion and accompanying illustration (Buffon,
1997,inpress).Inthisform,dorsalfurvaries 1765: pl. XXVII) represent what is currently
from blood red, to red-orange, to honey- referred to as the variegata variety (see
blond. Bands of white, honey-blond, or light above).Almostthirtyyearslater,Kerr(1792)
red fur may encircle the base of the tail, tar- assigned this form the trinomen Lemur ma-
sus, metatarsus, or digits. White fur may ap- caco variegatus,3 referencing the animal de-
pear on the muzzle and lateral aspect of the scribed by Buffon and providing the vernac-
ankle, extending up to the knee or thigh;and ular English names ‘‘pied vari’’ and ‘‘ruffed
the nape of the neck almost always bears a maucauco’’. Shortly afterward, E. Geoffroy
large patch of white fur (see color plate). A (1796) introduced le ‘‘vari a´ ceinture’’ (the
pale line across the nuchal region, tipped ‘‘vari’’withabelt),currentlyidentifiedasthe
with white laterally, has also been observed. subcincta variety after Smith (1833). Jean
Some of these characteristics were noted by Baptiste Audebert illustrated both of these
E. Geoffroy (1824a), I. Geoffroy (1851), El- black-and-white forms in his monograph,
iot (1913), Hill (1953), Petter et al. (1977), Histoire Naturelle des Singes et Makis (Au-
Tattersall (1982), Hekkala and Rakonton- debert, 1797, pls. V and VI). Buffon, Kerr,
dratsima (1999), and were also illustrated J. B. Audebert, and later E. Geoffroy and
early on (see Historical Documents, Taxon- (1824b) and Pollen (1868) all recounted the
omy, and Illustrations). Tattersall (1982) few details known of these animals in their
found several museum specimens ‘‘much wild state that had been given by Flacourt in
lighter in color than are typical V. v. rubra’’ his Histoire de la grande Isle Madagascar
and likened them to captive-bred hybrids. It (1658: 153):
is now clear, however, that lighter coloration
Ilyadediuersessortesdesinges,ilyenadegrands,
by itself (i.e., honey blond vs. dark red) falls
quisontblancs,&ontdestaˆchesnoiressurlescostez,
well within the normative description, and & sur la teste, ils ont le museau long comme vn re-
deep within the geographic range, of red nard,ilslesnommenta` Manghabeivaricossy4:ceux-
ruffed lemurs: animals from within a single cy sont furieux comme des tigres, ils font tel bruit
dans les bois, que s’il y en a deux, il semble qu’ily
community in the Andranobe Forest, for ex-
en a vn cent. I’en ay eu deux que ie fis porter dans
ample, show all of the variation in coatcolor
nostre barque; mais ils se ietterent dans la mer, ils
and patterning described above, and in par- sont tre`s difficilles a` apprivoiser; si on ne les a de
ticular the honey-blond coloration (color ieunesse.5
plate).
Hybrids and putative hybrids (see color
3Kerr built on a binomen and description published
plate) are black-capped and ventrally black,
earlier by Gmelin—Lemur macaco: corpore nigro and
but vary in the proportions of darker fur on albo mixto (Systema Naturæ, 13th ed.1788). However,
the dorsum. The spectrum generally runs Linnaeus had previously assigned the binomen Lemur
fromapredominantlyrufoushuetoawhitish macaco to the black lemur (Systema Naturæ, 12th ed.
1766). The latter has long been considered a separate
pelage lightly washed with raspberry tones,
species,butinearlydaysitwasconsideredoneandthe
especially near the shoulders and rump. same species as the black-and-white ruffed lemur until
None, however, possesses the precise pat- sufficient numbers of captive animals had passed
terning of coloration typical of either of the through European menageries so that coat colors of
malesandfemalescouldbedistinguishedandhabitsre-
parental populations, although in the occa-
vealed.
sional hybrid the principal effect is of black
4Today the Malagasy vernacular ‘‘varicossy’’
vs. white, with the addition of some reddish ((cid:53)‘‘varikosy’’)referstothewhite-frontedbrownlemur,
fur. Eulemur fulvus albifrons, which is found sympatrically
with the ruffed lemur in the northeast of Madagascar.
The Malagasy vernaculars for black-and-white and red
HISTORICAL DOCUMENTS, ruffedlemursare‘‘varikandana’’(or‘‘varikandra’’)and
TAXONOMY, AND ILLUSTRATIONS ‘‘varinena’’(or‘‘varikamena’’),respectively.
5‘‘There are several kinds of monkey, there are big
Buffon (1765) provided the first scientific ones, which are white, and have black patches on their
ribs,andontheirheads,theyhavealongmuzzlelikea
description of the black-and-white ruffed le-
fox, at Mangabey they call them varicossy: they are as
mur, referring to it simply by the vernacular
fierce as tigers, they make so much noise in the trees,
names ‘‘vari’’ and ‘‘maki-pie’’. His descrip- that if there are two of them it seems that there are a
2002 VASEY AND TATTERSALL:SYSTEMATICSOF VARECIA 7
Earlyinthe19thcentury,theredformwas described as Lemur niger by E. Geoffroy,
named Lemur ruber by E.Geoffroy (1812): 1812) by advancing the species name Lemur
in the vernacular, ‘‘maki rouge’’. A more varius to distinguish it; and he also retained
thorough description of the red form and il- the species Lemur ruber. He further briefly
lustrations of both the red and black-and described varieties a, b, and c of the black-
white forms were later published (E. Geof- and-white form (which, as noted above, cor-
froy 1824a, 1824b, Livraisons XV and respond to the varieties variegata, editorum,
XLIII).AlthoughthebotanistCommersonil- and subcincta, respectively). The English-
lustrated the red form in 1763, his drawings man Gray (1863) introduced the genus Va-
remained unpublished when they were sent recia for the ruffed lemurs, thereby uniting
back to Paris after his death shortly thereaf- the black-and-white form (Varecia varia)
ter. Only after the naturalist Pe´ron returned and the red form (Varecia rubra) at the ge-
to France from Madagascar with skins (ca. neric level using as key characteristics the
1802), and a merchant boat had brought a ruff surroundingtheheadandthetuftedears.
live animal back to FrancefromMadagascar, This generic distinction wasnotimmediately
was Commerson’s drawing of the red form accepted. Gray continued to include the
unearthed from among his papers and a new black lemurs with the ruffed lemurs (Gray
species named (E. Geoffroy, 1824a, 1824b). 1863, 1870, 1871), yet later questioned his
The animal illustrated by Geoffroy and Cu- owntaxonomicrevisions(Gray,1872),based
vier (1824a) depicted the seaborne animal, ontheobservationsofseveralotherscientists
which was then housed at the menagerie in (Bartlett, 1862; Schlegel, 1866; Sclater,
the Jardin des Plantes at the Muse´um 1871). Sclater (1871) correctly observedthat
d’Histoire Naturelle in Paris (now known as among black lemurs the sexes were dichro-
the MNHN). This female possessed a chest- matic, whereas in black-and-white ruffed le-
nut-redcoatdorsally,withwhitebandsoffur murs the sexes had similar coat patterns. It
around each tarsus. Strangely, this animal was also recognized that Lemur varius and
never vocalized. Presumably this is why her Lemur niger differed in their ‘‘voices’’ (vo-
close relationship to the black-and-white calizations; Bartlett, 1862; Sclater, 1871).
form was not yet obvious. Geoffroy and Cu- Despite these caveats, Gray’s examinationof
vier (1824a, 1824b) assumed that, like other specimens in the BMNH, especially those
known lemurs, females and males of the collected by Alfred Crossley in the 1860s,
‘‘maki rouge’’ and the ‘‘maki vari’’ would led him to think that Lemur niger, Lemur
have different coat colors and patterns. varius, and Lemur ruber were ‘‘all one spe-
Not surprisingly in light of ongoing broad cies, extremely variable in colour, some be-
efforts to name and precisely classify the le- ing black, others red, and others white, and
murs during the 19th century, several mile- all the intermediate shades and variations’’
stones in ruffed lemur systematics would be (Gray, 1872). Schlegel, a museum naturalist
passed before 1900. Importantly, however, inLeiden,andPollen,aDutchexplorer,drew
that scientists in different parts of Europe similar conclusions. Noting excessively var-
were sometimes not aware of each other’s iable coloration Schlegel (1866, 1876) con-
work for many years after each had pub- sidered Lemurrubertobenothingmorethan
lished. The French savant I. Geoffroy(1851) a variety of Lemur varius, but was also the
disentangled the ruffed lemur from the black first to remark that Lemur macaco was sex-
lemur (Lemur macaco Linnaeus, 1766, also ually dichromatic, and that compared to Le-
mur varius, it was smaller in size, had a
much weaker voice,and afarlessthick,tuft-
hundred. I had two of them brought on our ship; but
ed, and woolly coat. Having traveled only
they threw themselves in the water, they are very diffi-
culttotameunlessyougetthemwhentheyareyoung’’. through the northwest of Madagascar,Pollen
Note thatin the original French text,the letter‘‘j’’was relied on information provided by natives
printedas‘‘i’’,theletter‘‘v’’as‘‘u’’wheninthemiddle and by other explorers, and on observations
ofaword,andtheletter‘‘u’’as‘‘v’’whenbeginninga
he made on captive ruffed lemurs at theMu-
word. Two editions of Flacourt were consulted for this
se´e de Saint-Denis (Re´union) where he saw
translation (see references), in addition to Tattersall
(1982). a tricolored animal. Without providing any
8 AMERICAN MUSEUM NOVITATES NO. 3376
sources he drew a ratherextremeconclusion, embellished on Schwarz (1931) by stating
lumping all black, white, red, andblack-and- that the red form and variety a (L. v. varie-
white forms into Lemur varius. He claimed, gatus) occur together geographically and in-
moreover, that there were no differences in terbreed in nature. Unfortunately, Hill pro-
color by sex or age, and stated that Lemur vided no documentation for this claim other
ruber had the same habits as the vari, ‘‘with than to cite Schwarz’s observations that hy-
which [presumably in captivity] it lives and brids were produced at the Berlin Zoo, and
mates’’ (Pollen, 1868: 21). So, while some that the hybrids in turn resembled A. Milne-
in this period came to understand that ruffed Edwards and A. Grandidier’s (1890) plates.
lemurs were not sexually dichromatic, were Consequently, the idea (but no documenta-
specifically distinct from black lemurs, and tion)ofanaturalhybridzoneemergedintan-
consisted of two distinct species (e.g., I. dem with a notion (albeit misconstrued) of
Geoffroy, 1851)—and perhaps even of a the geographical distribution of the red and
unique genus (Gray, 1863)—a polar view black-and-white forms.
had also emerged: that animals of all colors Thus, by the mid-20th century, notionsre-
and coat patterns belonged to onesinglespe- ported by Pollen (1868) as unverified claims
cies. had become highly speculative ‘‘facts’’. But
Schwarz (1931) attempted to sort I. Geof- onelastothercluefromthe19thcenturywas
froy’s (1851) three varieties geographically, yet to be seized upon. Schwarz (1931) noted
but acknowledged that many original muse- that ‘‘black-and-white and red specimens
um labels had disappeared and that he had have been collected in the same place by
encountered much difficulty in identifying J.[-P.] Audebert in the coast region north of
geographical names on labels, in literature, the Bay of Antongil’’, citing Jentink of Lei-
and on older maps (Schwarz, 1931: 399– den (Catalogue Syste´matiquedesMammife`r-
400). Schwarz unequivocally stated, howev- es, 1892). Schwarz was alluding to the col-
er, that the red form was a color mutation of lections made by the German-born Josef-Pe-
I.Geoffroy’svarietya,‘‘withwhichitoccurs terAudebert,whoworkedinMadagascarbe-
and interbreeds’’. The only evidence cited in tween 1876 and 1879. His collection was
support of this claim was that crosses born
at the Berlin Zoo resembled some of A. Jentink, using J.-P. Audebert’s collection records, dem-
Milne-Edwards and A. Grandidier’s (1890) onstrated that L. varius occurred north of the Bay of
illustrations (see color plate), which were, Antongil and south as far as Mananare, Vidoutra, and
Mahambo. Elliot indicated that the black-and-white
unfortunately,publishedwithoutdescriptions
formoccursin northeasternMadagacarfromAdenpone
or subspecific designations.
to Cape Masoala at the entrance of Antongil Bay, and
Hill (1953) drew directly upon Schwarz intotheinteriortoBengoa;andthattheredformoccurs
(1931) with regard to taxonomy and distri- in easternMadagascar,fromtheBayofAntongilinthe
bution. He upgraded I. Geoffroy’s varieties north to Masindrano in the south. Many of the place
namescitedbyElliotcannotbelocated(presumablyhe
a, b, and c to the subspecies Lemur varie-
drew these localities from museum labels). His distri-
gatus variegatus (Kerr, 1792), Lemur varie- butionfortheredformmoreaccuratelyreflectsthedis-
gatus editorum Hill, 1953, and Lemur var- tribution for the black-and-white form, assuming Mas-
iegatus subcincta (Smith, 1833), respective- indrano refers to the town bearing this name in south-
eastern Madagascar, not the village bearing this name
ly. He produced a distribution map for the
justsouthofMahalevonaontheBayofAntongil.Kau-
subspecies, taking considerable license in
dern described a subcincta-like animal from one day
building on the information provided by west of Fenerive (‘‘has only a white band around its
Schwarz (1931). This map contains gross er- body’’, Kaudern, 1915, pl. 3, fig. 1), and an editorum-
rors relative to distributional information like animal from south of Tamatave (‘‘almost all white
in the rear’’). Despite the availability of this distribu-
known both at that time and currently (cf.
tionalinformation,Hill(1953:401,Fig.130)illustrated
Pollen, 1868; Jentink, 1892; Elliot, 1913; therangeofL.variegatusasextendingonlyasfarsouth
Kaudern, 19156). Hill (1953: 400) further asTamatave,butwellintothenorthernhighplateauand
all along the northern coastas faras Diego Suarez!He
did not take the recordsfrom southofTamatave,Anta-
6Pollen, collating information from indirect sources,
nanarivo,andpossiblyMasindranointoaccount,where-
stated that Lemur varius (both forms) occurs in the re-
asthedistributionhegaveforruffedlemursinnorthern
gion between Tintingue, Tamatave, and Antananarivo.
Madagascarishugelyexaggerated.
2002 VASEY AND TATTERSALL:SYSTEMATICSOF VARECIA 9
sold to various museums, but most of his c) and indicated that better knowledge of the
ruffed lemurs went to the RMNH in Leiden distribution of thesevarietiesmightultimate-
and were well documented by Jentink ly warrant their recognition as distinct sub-
(1892). It is important to remember that nei- species. Unfortunately, the key for this dis-
ther Schwarz nor Hill had examined theLei- tribution map contained drafting errors; we
den material firsthand, and more will be said reproduce it correctly in the footnotebelow9.
of this in the section below on MuseumCol- Groves (2001) raised the variants of the
lections and Records. black-and-white forms to subspecies of the
Fieldwork and careful study of museum species Varecia variegata.
skins and their provenances by Petter et al. The new distribution data presented by
(1977) and Tattersall (1982) improved our Petter et al. (1977)andTattersall(1982)con-
understanding of the taxonomy and distri- flict in one particularly important way with
butionofruffedlemurs.However,thesestud- those published earlier by Schwarz (1931)
ies by no means resulted in a tidy, discrete and Hill(1953).Thelatterauthorsplacedthe
distribution of the black-and-white forms. lightest form (type a, variegata) farthest
Considering cranial anatomy, social behav- north, interbreeding with the red form north
ior, and the unusual reproductive traits of of the Bay of Antongil, whereas the former
ruffed lemurs, Petter (1962) reintroducedthe determined that it was thedarkestform(type
genus Varecia Gray, 1863 to distinguish c, subcincta) that occurred farthest north,
ruffed lemurs from other members of the largely separated from the red form by the
family Lemuridae. Petter et al. (1977) de- AntainambalanaRiver.Despitethediscovery
scribed and provided locality data, to the ex- of a geographic divide, however, the idea of
tent possible, for seven black-and-white a natural hybrid zone reemerged. Based on
forms. These authors retained the subspecies reports of a rufous brown variant west of the
advanced by Hill in 1953 (V.v. variegata,V. Bay of Antongil, Tattersall (1977) suggested
v. editorum, and V. v. subcincta) and further such animals might be hybrids or a local
described, but did not name, another four. form of V. v. variegata. Later it was noted
The southernmost population then known, that several museum specimens are much
inhabiting the remaining coastal forest south lighter in color than are typical V. v. rubra
of Farafangana, was said to be almostentire- and resemble 50/50 V. v. rubra (cid:51) V. v. var-
ly white dorsally. Like various earlier work- iegata hybrids bred in captivity at theDUPC
ers, Petter et al. (1977) viewed the red form (Tattersall, 1982; Buettner-Janusch and Tat-
as simply another subspecies of ruffed le- tersall, 1985). These authors thought at that
mur—V. variegata rubra. However, unlike time that only one such specimen was both
earlier workers, these authors indicated that wild-caughtanddocumentedtolocality.This
the Antainambalana River (fig. 3) clearly was collected by the Archbold expedition in
separates the red form from the black-and- 1930, 40 km NW of Maroantsetra up the
whiteform,specificallyV.v.subcincta7.This Vohimaro River (Rand, 1936). On this basis,
is the first reference to a geographic divide Tattersall (1982) suggested that V. v. varie-
between the two color forms.8 Tattersall gata and V. v. rubra might be in secondary
(1982) recognized just two subspecies, cor- contact between the confluent Vohimaro and
responding to the red form (V. v. rubra) on Antainambalana Rivers. This suggestion
the one hand, and to all black-and-white prompted several surveys, the findings of
forms combined (V. v. variegata) on theoth- which are reviewed below (see Recent Sur-
er. Building on Geoffroy (1851), he de- veys).
scribedfourblack-and-whitetypes(a,b1,b2, In concluding this section it is appropriate
to summarize the basis upon which a natural
7Black-and-whiteruffedlemurs(subcinctatype)were hybrid zone was proposed. The black-and-
observed at 400 m in the hills to the west of the An-
tainambalanain1969 by Petteret al.(1977:225). 9The correct correspondence between V. variegata
8Hill(1953)producedadistributionmapshowingthis variegatatypesandsymbolsinfigure3.15ofTattersall
divideaswell,butheprovidedneitherprovenancedata (1982: 72) is as follows: type a (variegata) (cid:109); type b1
nor details of the specimens upon which the map was (editorum)(cid:44); type b2 (editorum)(cid:86);typec(subcincta)
based. (cid:77).
10 AMERICAN MUSEUM NOVITATES NO. 3376
Fig.3. MasoalaPeninsulaandregionnorthoftheBayofAntongilanditsmajorwatersheds.Arrows
(fi ) indicate the Vohimaro, Antainambalana, Andranofotsy,andMahalevonarivers.Triangles((cid:109))show
localities where hybrid ruffed lemurs were collected(seetable1).Largedots((cid:118))showlocalitieswhere
more than oneformofruffedlemurwascollectedand/orsighted(seetable2).Stipplingrepresentsarea
of overlap between black-and-white and red ruffed lemurs where hybridization has occasionally oc-
curred. Small dots (●) show other localities mentioned in the text. Andaparaty: black-and-white ruffed
lemurs sighted; Ankorongana: red ruffed lemurs reported to the north (Ambodibilahy Mtn.) and to the
east (Anjanaharibe Mtn.). At nearby Sahantaha village to the south, black-and-white ruffedlemurskept
as pets were apparently captured on the west side of the Antainambalana River. Andranobe Forest: red
ruffed lemurs at this site show all the pelage variations described under the normative description.
Samples used in genetic analyses were collected from this population (Vasey, 1997). Dashed lines
indicate boundaries of the Masoala National Park. Note several narrow corridors bridging forested
blocks.Coordinatesforimportantlocalitiesduringrecentsurveys:Andaparatyvillage15(cid:56)12(cid:57)S,49(cid:56)37(cid:57)E;
