Geographic Variation of Idiurus (Rodentia: Anomaluridae) with Emphasis on Skull Morphometry

2007·1.8 MB·English

by  Anja C. Schunke

PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY
CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024
Number 3548, 22 pp., 12 figures, 12 tables January 15, 2007
Geographic Variation of Idiurus (Rodentia:
Anomaluridae) with Emphasis on Skull Morphometry
ANJA C. SCHUNKE1 AND RAINER HUTTERER2
ABSTRACT
The geographic variation of skull size and shape among populations of flying squirrels of the
genus Idiurus was analyzed with multivariate techniques using up to 57 craniometric characters.
The variability of body size and fur coloration was also studied. The results support the present
division of the genus into two species, Idiurus macrotis and I. zenkeri. Further division, into
subspecies, does not seem to be warranted at present, although distinguishable geographical
populationsexist in West, Central, andEast Africa.
INTRODUCTION Seven species of Anomaluridae are current-
ly recognized (Dieterlen, 1993, 2005) and
Anomaluridae are small to large rodents placed in three or four genera: Anomalurus
restricted to equatorial Africa between lati- (which occasionally contains Anomalurops),
tudes 15uN and 15uS. All except one species, Zenkerella, and Idiurus.
Zenkerellainsignis,areabletoperformgliding Most current authors agree that Idiurus
flight. All anomalurids live in rain forest, consistsoftwospecies,I.macrotisandI.zenkeri
montane forest, or gallery forest. High trees (Misonne, 1971; Rahm, 1988; Nowak, 1991;
provide takeoff and landing sites for glides Dieterlen, 1993, 2005). They are the smallest
and provide hollows for the daytime rest. As members of the family, with head and body
anomalures are nocturnal and seldom main- lengths ranging from about 95 mm in I.
tained in captivity, very little is known about macrotis to about 75 mm in I. zenkeri. These
their biology (Durrell, 1952; Rahm, 1969; animalshaveaglidingmembranesupportedby
Schlitter 1989; Julliot et al., 1998). a cartilaginous rod extending from the elbow
1ZoologischesForschungsmuseumAlexanderKoenig,53113Bonn([email protected]).
2Division of Vertebrate Zoology (Mammalogy), American Museum of Natural History; and Zoologisches
ForschungsmuseumAlexanderKoenig,53113Bonn([email protected]).
CopyrightEAmericanMuseumofNaturalHistory2007 ISSN0003-0082
2 AMERICAN MUSEUMNOVITATES NO. 3548
andalong,sparselyhairedtailthatconsiderably distribution of the data was tested with
exceedstheheadandbodylength. a Kolmogorov-Smirnov test independently
A preliminary analysis of the distributions forbothspecies.Forthistest,specimensfrom
of both species (Schunke and Hutterer, 2000) the northeastern part of the Democratic
revealed that large continuous distributions Republic of Congo were used because the
across the Central African forest belt, as largest numbers of specimens were available
postulated by some authors (e.g. Kingdon, from this area. The same subsets were also
1997), were not supported by specimen-based testedforsexualdimorphismwitht-tests(with
distribution maps, which in contrast suggest the exclusion of specimen of unknown sex).
patchy distributions for both species. For the main analysis, the remaining data
Geographicalisolationmaycausegeneticdrift were submitted to a principal component
andresultinspeciationofpopulationsofthese analysis (PCA). Two PCAs were conducted.
arboreal rodents. To test this hypothesis, we The first was based on the ln-transformed
have analyzed the morphological variation absolute measurements and thus included
among geographical populations of Idiurus variation in size. In the second analysis, linear
species across their entire range from Sierra regression lines of individual ln-transformed
Leone in the west to Tanzania in the east. measurements on ln-transformed palatilar
length (PL, fig. 1) were calculated, and resi-
SPECIMENS AND METHODS duals of the individual measurements on this
line were used instead of original variables
Specimens in 14 museum collections form (Thorpe and Leamy, 1983) to compare only
the basis of our report. In total, we examined shape differences. Palatilar length was chosen
116 Idiurus macrotis and 83 I. zenkeri (appen- asreferencebecauseofitsrelativelyhighvalues
dix 1).Ofthese,craniometricdatatakenfrom (and thus relatively low measuring error) and
63 skulls of I. macrotis and 51 skulls of I. foritsavailabilityfrommostspecimens.
zenkeri were used for the calculations. Only In addition, a PCA was performed for
skulls with all molars completely emerged standard body measurements (collectors’ field
were used in order to exclude juveniles. From data), including total length, tail length, ear
each skull, up to 57 measurements were taken length,andhind-footlength(appendix 2).Total
with an electronic caliper to the nearest length was taken as combined tail length and
0.01 mm (fig. 1, table 1). head and body length, where necessary. Resi-
Variationincolorwasassessedinasampleof dualswerecalculatedforthehind-footlength.
55skinsofI.macrotisand41skinsofI.zenkeri; Aftergroupingthepopulationsaccordingto
colorslidesshowingtheskinsalongwithacolor the results of the PCA (see later), a discrimi-
referencewereusedforcomparison. nant analysis was conducted to specify differ-
The specimens originated from the entire ences between groups.
ranges of the two species (figs. 2–3). We As Idiurus skulls are very fragile, it was
defined six geographical clusters and used rarely possible to take all measurements from
them as operational units: a single skull. Therefore, the PCA was
conducted first with all characters and then
1. WA: West Africa (Sierra Leone, Ivory
repeated after a stepwise exclusion of mea-
Coast, and Ghana; I. macrotis only).
surements that were unavailable for several
2. NWC: Northwestern Cameroon.
specimens. While the number of specimens
3. CEG: Southern Cameroon, Equatorial
increased,thenumberofcharactersdecreased.
Guinea, and Gabon.
By comparing the results, it was possible to
4. CAR: Central African Republic (I.
test their robustness.
zenkeri only).
Examples of typical results with intermedi-
5. DRC: Democratic Republic of Congo.
ate numbers of characters and specimens are
6. TAN: Tanzania (I. macrotis only).
shown in scatter plots for the first and second
The two species were analyzed separately. principal component, or in box plots.
Measurements were converted to logarithms Calculationswereprocessedwiththeprogram
before entering the calculations. The normal SPSS (version 10.0).
2007 SCHUNKE AND HUTTERER: GEOGRAPHIC VARIATION OFIDIURUS 3
Additional statistical details are given in Within I. macrotis, four clusters were formed
appendix 3, tables 8–12. bythefirstandsecondprincipalcomponentfor
logarithmized absolute data (fig. 4, table 8).
INSTITUTIONAL ABBREVIATIONS Thefirstfactorcodesmainlyforsizedifferences.
ThesmallestspecimenscamefromWestAfrica
AMNH American Museum of Natural
andfromnorthwesternCameroon,whilespeci-
History,New York
BMNH British Museum of Natural History, mens from southern Cameroon, Equatorial
London Guinea, and Gabon were considerably larger.
FMNH Field Museum of Natural History, Animals from northeastern Democratic
Chicago Republic of Congo were intermediate in size,
MNHN Muse´umNationald’HistoireNaturelle, withaslightoverlapinoneorbothdirections.A
Paris
singlespecimenfromTanzania(NMW31089)is
MRAC Museum Royal d’Afrique Centrale,
larger than average values of series from
Tervuren
southern Cameroon to Gabon but does not
NHMB Naturhistorisches Museum, Basel
exceedtherangeofvariationinmostcharacters.
NMK NationalMuseumsofKenya,Nairobi
NMNH NationalMuseumofNaturalHistory, Unfortunately, no other skulls from the
Washington,DC Tanzanianpopulationareavailable.
NMW Naturhistorisches Museum, Vienna The second principal component demon-
NRM Naturhistoriska Riksmuseet, Stock- strates differences in shape rather than size. It
holm separates specimens from West Africa and
RMNH Nationaal Natuurhistorisch Museum
northwestern Cameroon, on one hand, and
(Naturalis),Leiden
animals from the Democratic Republic of
SMF ForschungsinsitutSenckenberg,Frank-
Congo andsouthernCameroontoGabon,on
furt
the other.
SMNS StaatlichesMuseumfu¨rNaturkunde,
Stuttgart Calculationsusingtheresidualsforpalatilar
ZMB Museum fu¨rNaturkunde, Berlin length gave basically the same pattern but
were less pronounced than those obtained
RESULTS from logarithmized absolute measurements.
Here the single skull from Tanzania clustered
NORMAL DISTRIBUTION in most plots within specimens from southern
Cameroon to Gabon.
Allmeasurementswerenormallydistributed
Results for I. zenkeri are less pronounced
in both species (p . 0.05).
(fig. 5, table 9). No size differences between
specimens from different localities could be
SEXUAL DIMORPHISM detected with the first principal component.
With the second principal component, a sepa-
The possibility of sexual dimorphism was
checked independently for logarithmized mea- ration (with some overlap) was possible
surementsandforresidualsforpalatilarlength. between individuals from southern Came-
Thirteencharactersdemonstratedsignificant(t- roonandEquatorialGuineaandnortheastern
test,p#0.05)intersexualdifferencesforatleast Democratic RepublicofCongo. Theholotype
one of the species. Although preliminary tests of zenkeri from Cameroon (BMNH 48.885)
withallcharactersyieldedsimilarresults,those has a slightly smaller skull than most other
characters were not used in the final analyses. conspecifics from other localities. Further
Their exclusion made it possible to use all reduction of the number of characters dem-
specimens in a single analysis and to include onstrated that a second specimen (BMNH
skulls of specimens with unknown sex to 48.886)fromCameroonwasevensmaller(not
maximizethesamplesize. shown in fig. 5). From the Central African
Republic only two skulls were available, one
slightly and the other considerably damaged.
PRINCIPAL COMPONENT ANALYSES
Withastronglyreducednumberofcharacters,
After the removal of 13 characters, the they clustered either with the Cameroon and
remaining 44 characters underwent a PCA. Equatorial Guinea population or held an
4 AMERICAN MUSEUMNOVITATES NO. 3548
TABLE1
Cranial andDentalMeasurements Takenfrom SkullsofIdiurus macrotisandI. zenkeri
0: characternotusedin final PCA;1 and2: characterused in analyses;2: characterused in figs. 4to 7.
Abbreviationsas in fig.1.
Code Measurement I.macrotis I.zenkeri Bothspecies
TL Totallength 0 0 0
CIL Condylo-incisivelength 1 1 1
BL Basallength 2 1 1
ZB Zygomaticbreadth 1 1 1
RB Breadthofrostrum 2 1 1
NB Breadthofnasalbones 0 0 0
IOB Interorbitalbreadth 2 2 2
BCB Breadthofbraincase 2 1 1
PL Palatilarlength 2 2 2
PPBL Postpalatinebasallength 1 1 1
DL Lengthofdiastema 0 0 0
FIL Lengthofincisiveforamen 1 2 1
FIB Widthofincisiveforamen 2 2 2
BP4 GumwidthatP4 2 2 2
BM1 GumwidthatM1 2 2 2
BM3 GumwidthatM3 0 0 0
ChB Widthofchoana 2 2 2
BullaL Lengthofbulla 2 2 2
BullaB Widthofbulla 2 2 2
RH Heigthofrostrum 2 2 2
ZH Heightofzygomaticarc 0 0 0
PFZH Heightofprocessusfrontaliszygomatici 0 0 0
SkH Heightofskull 0 0 0
ZP Positionofzygomaticarc 0 0 0
BCH Heightofbraincase 0 0 0
PZB Widthacrossposteriorendsofzygomaticarcs 2 2 2
FIOH Heightofinfraorbitalforamen 2 2 2
FIOB Widthofinfraorbitalforamen 2 2 2
RUL Upperlengthofrostrum 2 2 2
RLL Lowerlengthofrostrum 2 2 2
ML Lengthofmandible 2 2 2
MHA Heightofmandibleatarticularprocess 2 2 2
MHD Heightofmandibleatdiastema 0 0 0
PAA Distancebetweenarticularandangularprocess 2 1 1
PCH Heightofcoronoidprocess 2 2 2
UCL Uppercrownlengthofmolars 1 1 1
UIL Lengthofupperincisor 2 2 2
UIB Widthofupperincisor 2 2 2
UP4L LengthofupperP4 1 1 1
UP4B WidthofupperP4 1 1 1
UM1L LengthofupperM1 0 0 0
UM1B WidthofupperM1 1 1 1
UM2L LengthofupperM2 1 1 1
UM2B WidthofupperM2 1 1 1
UM3L LengthofupperM3 1 1 1
UM3B WidthofupperM3 1 1 1
LCL Lowercrownlengthofmolars 2 1 1
LIL Lengthoflowerincisor 2 2 2
LIB Widthoflowerincisor 2 2 2
LP4L LengthoflowerP4 1 1 1
LP4B WidthoflowerP4 1 1 1
2007 SCHUNKE AND HUTTERER: GEOGRAPHIC VARIATION OFIDIURUS 5
TABLE1
(Continued)
Code Measurement I.macrotis I.zenkeri Bothspecies
LM1L LengthoflowerM1 1 1 1
LM1B WidthoflowerM1 1 1 1
LM2L LengthoflowerM2 0 0 0
LM2B WidthoflowerM2 1 1 1
LM3L LengthoflowerM3 0 0 0
LM3B WidthoflowerM3 1 1 1
intermediate position, depending on the num- length of mandible, and distance between
ber of characters and individuals included in articular and angular process) yielded 94.2%
the respective analyses. correct classifications (tables 2, 11). However,
Calculationswithresidualsgaveremarkably the results for specimens from northwestern
similar results to the ones obtained with Cameroonmustbetakenwithcaution,asonly
logarithmized absolute measurements. five skulls were available from this area.
Size differences between I. macrotis and I. The discriminant analysis gave similar
zenkeri were pronounced, with a considerable results for I. zenkeri populations, with 94.9%
gap in the first principal component (fig. 6, correctly classified individuals (tables 3, 12).
table 10);theywerestronglysupported bythe The characters used were height of rostrum,
majority of characters. width of bulla, and upper and lower rostrum
An interesting result was obtained from length. Unfortunately, only specimens from
a combined analysis for I. macrotis and I. southern Cameroon plus Equatorial Guinea
zenkeri using residuals for palatilar length and the Democratic Republic of Congo
(fig. 7, table 10). While the first principal yielded a sufficient number of measurements
component (not shown) mainly separated I. and could be used in this analysis.
macrotis from northwestern Cameroon and I. macrotis and I. zenkeri may be separated
the southern Cameroon to Gabon region, but from each other by a single character, such as
less clearly animals from West Africa and the height of rostrum, basal length, or palatilar
Democratic Republic of Congo, the analysis length. Each of these characters correctly
yielded no information as to I. zenkeri. classified 100% of the specimens in a discrim-
However, the second principal component inant analysis.
divided the specimens in individuals from Tables 4and5providemeansandrangesof
Democratic Republic of Congo and animals five selected skull measurements of the differ-
from southern Cameroon to Gabon, with ent geographical populations of each species,
a considerable overlap between I. macrotis and figures 8–10 show examples of crania of
and I. zenkeri from the respective areas. The both species. Skulls of all holotype specimens
charactersdemonstratinghighloadingsatthis are figured, with the exception of kivuensis
principal axis were length and width of the Lo¨nnberg, 1917, the skull of which is lost.
bulla, upper length of rostrum, and two
incisor characters.
BODY SIZEAND SKIN CHARACTERS
DISCRIMINANT ANALYSIS A PCA for total length, tail length, ear
length, and hind-foot length (field measure-
Most individuals of the clusters obtained ments) yielded no separation between I.
through the PCA analysis could be identified macrotis and I. zenkeri apart from size
with only few characters. More than 90% of differences (result not shown). The statement
specimenswereclassifiedcorrectly.Inpopula- of Kingdon (1997: 179) that the tail of I.
tions of I. macrotis, a combination of four macrotis ‘‘is proportionately shorter’’ than
characters (height of rostrum, length of bulla, that of I. zenkeri was not supported by the
6 AMERICAN MUSEUMNOVITATES NO. 3548
Fig.1. Definitionoflinearmeasurementstakenfromskulls,asexemplifiedbyaskullofIdiurusmacrotis
(ZMB 22885). Greatest length and width of single teeth (not marked in figure) were also taken. For
abbreviations,seetable 1. Thescale for the dentition represents1 mm andfor the skull, 10mm.
datausedinouranalysis(fig. 11).Thetailsof from all areas strongly overlapped. I. zenkeri
bothspeciesdifferinabsolutelength(tables 6, was not represented by sufficient geographic
7), but the relative length is about the same. samples, so no conclusions were obtained for
Whenlogarithmizedabsolutemeasurements this species.
ofI.macrotisaswellasresidualsforhind-foot Noweightdatawereavailableforanyofthe
lengthwere used forthe PCA, then specimens 80specimens ofI.zenkeri examined. Kingdon
2007 SCHUNKE AND HUTTERER: GEOGRAPHIC VARIATION OFIDIURUS 7
Fig.2. DistributionofI.macrotisbasedonspecimensexaminedandliteraturerecords.Closedsymbols,
specimensexamined;opensymbols,datatakenfromliterature(Sanderson,1940;Kuhn,1965;Rahm,1966;
Adam,et al.1970; Aellen et al.,1970; Julliotet al.,1998). Scalerepresents1,000 km.
Fig.3. DistributionofI.zenkeribasedonspecimensexaminedandliteraturerecords.Closedsymbols,
specimens examined; open symbols, data taken from literature (Rahm, 1966; Jones, 1971; Delany, 1975).
Scalerepresents1,000 km.
8 AMERICAN MUSEUMNOVITATES NO. 3548
Fig. 4. Geographic variation of I. macrotis according to the first and second principal components as
obtainedfromlogarithmizedabsoluteskullmeasurements.Forcharacters,seetable 1.Opensymbols,males;
closedsymbols,females;symbolswithacentraldot,sexunknown;diamonds,WestAfrica;uprighttriangles,
northwesternCameroon;trianglespointingupsidedown,southernCameroontoGabon;circles,Democratic
Republicof Congo;star,Tanzania.
(1997) gives a range of 14–17.5 g for this DISCUSSION
speciesand arangeof 25–35 gforI.macrotis.
Weight data for 14 museum specimens of I. The taxonomic history of the genus Idiurus
macrotis (table 6) range from 23 g to 40 g. is brief. Matschie (1894) described the genus
The coloration of the studied skins ap- and species Idiurus zenkeri based on a single
pearedverysimilarinbothspecies,incontrast specimen from southern Cameroon (fig. 5).
to other anomalurid species (Schunke and Subsequently,Miller(1898)namedI.macrotis
Hutterer,2005).Inbothspecies,thedorsalfur from the same region based on differences in
is grayish brown to dark brown, and the sizeandcoloration(‘‘MuchlargerthanIdiurus
ventral fur is slightly paler. The skin of the zenkeri Matschie; tail and ears relatively
limbs and the tail is lighter colored than the longer; color apparently darker; skull larger;
dorsal fur. I. macrotis specimens from Ghana bony palate narrower; second lower molar
seem to be lighter and more yellowish, but distinctly larger than first’’). Lo¨nnberg (1917)
individuals from Ivory Coast are darker and named Idiurus zenkeri kivuensis from Congo
more brownish, as are most specimens from (‘‘These specimens agree much more in their
Cameroon and the Congo. In I. zenkeri no general characteristics with Idiurus zenkeri
differences could be found between popula- Matschie than with I. macrotis Miller.
tions, except for the holotype of I. zenkeri, Especially the cranial dimensions differ from
which has an entirely blackish skin and dark those of I. macrotis’’). The taxon was sub-
brown fur. sequently given species status by Hayman
2007 SCHUNKE AND HUTTERER: GEOGRAPHIC VARIATION OFIDIURUS 9
Fig.5. VariationofI.zenkeriaccordingtothefirstandsecondprincipalcomponentsasobtainedfrom
the logarithmized absolute skull measurements. For characters, see table 1. Open symbols, males; closed
symbols, females; symbols with a central dot, sex unknown; upright triangles, northwestern Cameroon;
triangles pointing upside down, southern Cameroon and Equatorial Guinea; square, Central African
Republic; circles,Democratic Republicof Congo.
(1946) or considered a synonym of I. zenkeri paler throughout, including the basal fur’’.
(Verheyen,1963),whileDieterlen(1993)listed Hayman (1946), in a review of the genus,
it under I. macrotis, a conclusion that we accepted I. macrotis and I. zenkeri as species,
share. A second, much smaller specimen but also considered I. kivuensis a species (‘‘In
reported by Lo¨nnberg was considered a juve- my view the conclusion must be drawn that
nile but may well be a specimen of I. zenkeri. there are only three species of Idiurus, namely
Unfortunately the skull of the holotype of zenkeri,macrotisandaspeciesintermediatein
kivuensisislost(Verheyen,1963),andtheskull size between these two, for which the name
of the smaller specimen is still inside the skin kivuensis is available’’). He also named a new
and not accessible. However, the general size subspecies I. kivuensis cansdalei (‘‘Differing
of the holotype and the single skull measure- from I. k. kivuensis in the pale general color
ment provided by Lo¨nnberg (1917) led us to above and below, and from I. k. panga in the
the conclusion that kivuensis is rather a syno- general color of the hair tips above being
nym of macrotis than of zenkeri. Allen (1922) between avellaneous and wood brown of
described I. langi and I. panga as new species Ridgway instead of light drab’’). Finally,
fromthenortheasternDemocraticRepublicof Verheyen (1963) named Idiurus zenkeri hay-
Congo.I.langiwasdiagnosedas‘‘[s]izeofand mani from northwestern Cameroon: ‘‘Cette
proportions nearly as in Idiurus macrotis nouvelle sous-espe`ce se distingue de la forme
Miller, but very different in coloration’’, and typique par la longueur totale du corps, la
I. panga as ‘‘[s]imilar to Idiurus macrotis longeur de l’oreille, la plus grande longeur du
Miller, but much smaller and considerably craˆne et par la largeur bizygomatique nette-
10 AMERICAN MUSEUMNOVITATES NO. 3548
Fig.6. SizevariationofI.macrotisandI.zenkerifromthefirstprincipalcomponentasobtainedfrom
logarithmized absolute skull measurements. Forcharacters, seetable 1.
Fig. 7. Shape variation of I. macrotis and I. zenkeri from the second principal component as obtained
from residuals calculatedfor palatilarlength. Forcharacters, seetable 1.