J . Zool., Lond. (1993) 230, 117-134

Systematics and geographic variation of Ethiopian Avvicanthis (Rodentia, Muridae)

AFEWORK BEKELE,

Biology Department, Addis Ababa University, P.O. Box 1176, Addis Ababa, Ethiopia

E. CAPANNA, M . CORTI, Department of Animal and Human Biology, University of Rome ‘La Sapienza’, Via Borelli 50,

Rome 00161, Italy

L. F. MARCUS Queens College of the City University of New York, and American Museum of Natural History,

Central Park West at 79th, New York, N.Y. 10024, USA

AND D. A. SCHLITTER

Carnegie Museum N.H., Museum Annex, 5800 Baum Boulevard, Pittshurgh, PA 15206, USA

(Accepted 30 April 1992)

(With 8 figures in the text)

Arvicanthis, the unstriped grdSS-rdt, is a Widespread genus occurring in many regions of Africa and is a major pest in agricultural farmland. Despite its economic importance for developing countries, the taxonomy of the genus is still in a chaotic state. We used univariate and multivariate morphometrics to investigate two species, A. abyssinicus and A. dembeensis, occurring in Ethiopia. Results show that these taxa are well separated, this contradicting authors who lump all Aruicanfhis as A. niloricus. There is a longitudinal cline in the morphology of A. dembeensis from eastern regions along the Rift Valley. Differences between the species in morphology seem to reflect adaptation to different ecological niches at high (A . ahyssinicus) and low ( A . dembeensis) altitudes.

Contents

Page Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 17 Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 18 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132

Introduction

Arvicanthis is a widespread diurnal and grass-loving African genus (Kingdon, 1974) and is apparently undergoing a process of range expansion. Its reproductive success, especially after the annual dry-season depletion, makes it more successful than other competing rodents and also makes it a major agricultural pest. Many geographic varieties have been described based upon coat colour and size variation. However, the genus deserves further study because of our poor

I I7 0 1993 The Zoological Society of London

118 AFEWORK BEKELE ET A L

understanding of its taxonomy and especially because of its major role in damage to the croplands of Africa.

The taxonomy of the genus is chaotic. Hollister (1919) described 10 forms of Arvicanthis from East Africa. Misonne (1971) and Honaki, Kinman & Koeppl (1982), while acknowledging the great variety of forms, lumped them all under A . niloticus. Delany (1975) recognized two species, A. testicularis and A . niloticus, while Kingdon (1974) accepted A . niloticus and A . lacernatus as distinct. Corbet & Hill (1991) provisionally recognized A . testicularis, A . abyssinicus, A . blicki and A . somalicus.

The genus displays wide karyotypic variability. Studies of A . niloticus from different countries have revealed diploid numbers of 56 (Matthey, 1965), 62 (Viegas-Pequignot et al., 1983) and 46 (Capanna & Civitelli, 1988), whereas A . abyssinicus from an unspecified locality has a 2n=62 (Matthey, 1959). Recently, Volobouev et al. (1 988) described three karyotypic forms of A. niloticus across the sub-Saharan belt differing from each other by chromosomal rearrangements and heterochromatin content.

In Ethiopia, a variety of forms has been described for the genus, depending upon the localities studied. Frick (1914) recognized three forms based upon his collections, including A . hlicki which was recognized as a distinct species by Dorst (1972). Thomas (1906, 1928) and Dollman (191 1) mentioned other forms ofArvicanthis from Ethiopian localities, and Allen (1939) listed at least 1 1 different forms of Arvicanthis. De Winton (1900) recognized the two species A . abyssinicus and A . dembeensis from this region. Ellerman (1 941) mentioned eight forms of Ethiopian Arvicanthis. Dieterlen (1 974) confirmed Pelomys dembeensis as belonging in Arvicanthis. Finally, Yalden, Largen & Kock (1976) recognized the occurrence of four distinct species of Arvicanthis in Ethiopia: abyssinicus, dembeensis, blicki and somalicus.

The occurrence of four Ethiopian species of Arvicanthis has also been supported by Rupp (1980), Demeter (1982, 1983) and Demeter & Topal (1982). Rousseau (1983) confirmed the different species of Ethiopian Arvicanthis, with slight modifications, and showed that the Ethiopian forms are smaller in size than their West African counterparts. Ingersol (1968) suggested a high morphological variability in the Arvicanthis occurring in the eastern part of Ethiopia. Hubert (1976), on the basis of his collection from the Omo Valley in the extreme south- west part of Ethiopia, identified niloticus and somalicus. Wesselman (1984) confirmed that a fossil skull from the Ethiopian Omo Valley resembled A . niloticus.

The present study is an attempt, using morphometric analysis of skull measurements, to determine whether A . abyssinicus and A. dembeensis are really separate species or are only geographic variants. Arvicanthis abyssinicus occurs mainly in the highlands whilst A . dembeensis is considered a relatively ‘lowland’ species (Yalden et al., 1976). At the same time, it has also been reported that populations of these two species occur sympatrically in a few localities (Yalden et al., 1976).

We used univariate and multivariate procedures to investigate population differentiation both within and between these two putative taxa. The analysis also was extended to include samples of A . niloticus and A . testicularis from Egypt and Sudan, respectively, to assess phenetic relationships between these four taxa.

Materials and methods

A total of 407 specimens, 180 of A . abyssinicus and 233 of A . dembeensis, from 16 localities (8 for each species) in Ethiopia were studied (Fig. I , Table I). These were compared with additional specimens of A . testiculuris (n = 24) from Khartoum, Sudan, and of A . niloticus (n = 21) from Tanta, Egypt (Fig. 1).

MULTIVARIATE MORPHOMETRICS IN ETHIOPIAN A R V I C A N T H I S I19

16

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FIG. 1. Map of Ethiopia showing locations ofpopulations of A . dembeensis (A-G, R filled circles) and A . abyssinicus (H- Q, filled triangles) examined. The box inset in the upper right corner is an enlarged map showing Ethiopia (shaded area) and the population ofA. niloticus from Egypt (T, open triangle) and of A . tesiiculuris ( S , open circle) from Sudan. Localities are: A = Lake Tana Area; B = Koka; C =Lake Shala; D= Gardula Area; E = Alemaya; F = Urso River; G = Erer-Gota; H = Simien; I = Dangila; L = Debre Markos; M = Bichana; N = Salale Area; 0 = Muger River; P = Addis A baba; Q = Lemi; R = Awassa Area.

Skull measurements were recorded from specimens preserved at the following museum collections: Zoological Natural History Museum, Addis Ababa; Natural History Museum, London; Carnegie Museum of Natural History, Pittsburgh; National Museum of Natural History, Washington, D.C.; American Museum of Natural History, New York; Museum of Comparative Zoology, Harvard; Field Museum of Natural History, Chicago; and Oklahoma State University Museum, Stilwater.

Specimens were sorted into the ‘species’ A . abyssinicus and A . dembeensis by using the criteria suggested by Yalden et al. (1976): A . abyssinicus has a dark agouti fur on the venter and a mid-dorsal dark stripe, whereas A . dembeensis lacks this stripe and presents a grey to pale agouti ventral fur.

120 AFEWORK BEKELE ET A L .

TABLE I Locality names, symbol of locality. geographic location. altitude in metres and sample size (males and femairs)

of the populations studied of Arvicanthis abySSiItiCuS and of A . dembeensis

Species Locality Symbol

A . demhevnsis Lake T d n d Area Koka Lake Shala Awassa Area Gardula Area Alemaya Urso River Erer-Gota

Dangila Debre Markos Bichana Salale Area Muger River Addis Ababa Lemi

A . abyssinicus Simien

A B C R D E F G

H I L M N 0 P Q

Geographic Altitude co-ordinates (4

12" 0 0 N 37" 2 0 E 1800 08" 24' N 39" 01' E 1650 07" 28' N 38" 30' E 1600 07" 00' N 38" 30' E 1830 05" 38' N 37" 25' E 1300 09" 24' N 42" 01' E 2000 09"41'N 41"38'E 1100 09" 59" 41" 1 9 E 1200

13" 20' N 38" 2 0 E 2900-3700 11" 16" 36"50'E 2100 1 0 21" 37"44'E 2500 10" 27' N 38' 12' E 2700 09" 50' N 38 ' 30' E 2800 09" 31" 38" l5 'E 2400

09" 46' N 38" 53' E 2100 09" 04' N 38' 48' E 2400-2960

Sample size

Males Females

1 1 10 33 38 9 9 7 3 9 12

16 12 16 13 I8 17

I 4 10 8 13 8 12 12 8 8 8 8

37 25 5 7

All specimens examined were assigned to age classes based upon tooth wear and cranial characteristics. A skull is assigned to the young adult or subadult group if the third molar is beginning to wear, the sagittal sutures are nearly fused, and there is slight ridging on the dorsum. A skull with moderate wear of all molars, fused sutures, shiny bullae and presence of ridges is called an adult specimen and a skull with all molars worn forming lakes, the bullae translucent (nearly transparent), and with highly developed ridges is categorized as an old adult.

The 12 linear characters measured on each skull following Rousseau (1983) are: occipito-nasal length (OCN), condylo-incisive length (CTL), zygomatic breadth (ZB), inter-orbital constriction (IOC), breadth of braincase (BBC), length of maxillary toothrow at crown (LMT), width of third molar at crown ( lM3), length of maxillary diastema (LD), length of anterior palatine foramen (LPF), palatal length (PAL), length of tympanic bulla (LTB), and breadth of tympanic bulla (BTB).

Some measurements were not available for every skull in the data set; thus we estimated the missing measurements by use of the procedure AM in thc BMDP computer package (PC version 'May 1984': Dixon, 1983) using the 'METHOD REGR. Six specimens were discarded by the procedure as having too many measurements missing. This left a total of 448 specimens for our analysis. Data were converted into logarithms for all morphometric analyses.

Number Cruncher Statistical System (NCSS version 5.01: Hintze, 1987) was used to make box plots to plot medians and interquartile ranges and to compare univariate patterns of variation The Statistical Analysis System (SAS, PC version 6.04: SAS Institute, 1985) and the Numerical Taxonomic System of Rohlf (1989) (NTSYS-pc, version 1.5) were used for the remaining analyses.

We used a significance level of 0.05. As the data contained 3 age classes for each sex, separate univariate ANOVAs (unbalanced design) were

used to test for differences in age and sex, and an age-by-sex interaction for each character. This was done separately for each species.

As the assessment of between-group variation may be obscured by within-group variation due to individual growth or size differences (Thorpe, 1983), shown to be important in our data (see Results), we

MULTIVARIATE MORPHOMETRICS IN ETHIOPIAN A R V I C A N T H I S 121

investigated for a ‘size/growth’ component to be eventually removed rrom the data by use of multiple group principal component analysis (MGPCA: Thorpe, 1983). This method extracts a ‘size’ vector (thc eigenvector corresponding to the first principal component) from the pooled within-locality covariance matrix. However, a basic assumption for this procedure is that the first principal component within localities has the same orientation: this can be examined by comparing the first eigenvectors corresponding to the first principal component for each locality (Voss, Marcus & Escalante, 1990).

Two versions of this procedure have been written in SAS by use of the procedure IML (matrix language) and are available from the authors (LM or MC). One reproduces Thorpe’s MGPCA (Thorpe, 1983) results and produces new data as principal component scores for further analysis based on the within-principal- component vectors. The other uses the algorithm suggested in Rohlf & Bookstein (1987) based on Burnaby’s procedure (l966), and produces as output scores on the first within-principal component supplemented by the size-adjusted data. The Burnaby-adjusted data or the principal components scores from MGPCA, leaving out thc size vector, will produce the same results in subsequent canonical variate analysis. The principal components of the Burnaby-adjusted data are the same as those for the MGPCA with the size vector removed.

Distinctions between populations and species were assessed by canonical variate analysis (CVA). Canonical variate analysis is a multivariate ordination technique which orders groups along axes of maximum differentiation by maximizing between-group relative to within-group variation. When all of the MGPCA component scores are used as input data for CVA, results are the same as CVA performed on the raw data (Thorpe, Corti & Capanna, 1982; Thorpe, 1983). CVA computed on MGPCA Component scores minus the ‘size’ component produces a ‘size- (growth)-independent’ or ‘size-out’ CVA. The same result, i.e. a ‘size-out’ CVA, is given by a CVA computed on Burnaby-adjusted data. If one is able to show that a significant agc effect is represented in the data among the groups, the MGPCA method will remove these growth effects as well as other within-sample size components of variation.

The difference between the ‘size-in’ and ‘size-out’ analyses can be evaluated by examining the effect of the first principal component of the pooled within-covariance in terms of its contribution to the discrimination among the groups, as a percentage of the sum of the eigenvalucs of B* W-’ where B is the between sums of squares and cross products matrix, and Wis the pooled within-matrix (variant of Campbell, 1980). A routine written in SAS IML performing this analysis is available from one of the authors (LM or MC).

Mahalanobis distances (Dillon & Goldstein, 1984) between group centroids were computed as a part of the canonical variate analysis to assess group affinities. Centroid differences for any 2 localities were tested by use of Hotelling’s T2 test which has Fisher’s F distribution. However, because wc will make all comparisons between localities in a given analysis, the tests are not independent. There are c = k(k - l)/2 comparisons for k localities and we use the Bonferroni (Marcus, 1990; Morrison, 1990) adjustment of dividing the significance level, 0.05 in our case, by c to guarantee our chosen significance level of 0.05.

The Mantel test and associated graphs were used to compare the Mahalanobis distances for the MGPCA ‘size’-adjusted and unadjusted data.

Canonical variate scores were regressed on altitude to test the speculation of Yalden et al. (1976) that the distinction between A . abyssinicus and A . dembeensis might only represent extremes of an altitudinal cline.

Finally, for practical purposes in field work, we used ANOVA to test for differences among species and populations for ratios between inter-orbital constriction and condylo-incisive length, between zygomatic breadth and occipito-nasal length, and between breadth of braincase and occipito-nasal length.

Results

The ANOVAs for age and sex did not show significant sexual dimorphism for specimens of the same age, and therefore no overall sexual dimorphism. There is, however, a clear distinction between age classes f o r all variables. These results are graphically confirmed by notched box plots. In Fig. 2 we show as an example a plot for occipito-nasal length for the largest sample (n = 58) of

122 AFEWORK BEKELE ET A L .

S A 0

FIG. 2. Notched box plot of occipito-nasal length (OCN) for the two sexes (males left, females right) and the three age classes represented in locality Lemi ( A . abyssinicus). S = subadult, A=adult, O=old. Medians are significantly different ( P i 0.05) when the notches of two boxes do not overlap. In this case there is overlap between sexes of the same age class but complete non-overlap between age classes.

A . abyssinicus from Lemi. ‘If the notches of two boxes do not overlap, we may assume that the medians are significantly different’ (Hintze, 1987: Graphics, p. 19). Clearly, the three age classes of subadults, adults and old differ significantly, whereas there is no significant distinction between the sexes of the same age class (Fig. 2). Therefore all further analyses were performed combining males and females.

There are clear differences in size between some species for most variables studied. Typical comparisons are given by box plots for all localities in Fig. 3: results for occipito-nasal length (Fig. 3a) show differences among A . niloticus, the largest, A . abyssinicus, and A . dembeensis, the smallest; whereas for the length of maxillary toothrow at crown (Fig. 3b) there is a clear difference between A . testicularis and the three other species.

Nonetheless, size and shape are essentially multivariate concepts and therefore they are better discussed by the multivariate procedures that we used.

Given that, as we have shown, there is a strong difference among the age classes, we attempted to adjust for age differences and for ‘size’ variation within samples by use of multiple group principal components analysis. The MGPCA coefficients for the first normalized eigenvector are all of the same sign (Table 11), for the pooled within 18 localities’ variance-covariance matrix. The differences of magnitude among coefficients reflect allometric relations that accompany growth: variables with large coefficients show the greatest increase with age, while variables with smaller coefficients are those for breadth of the brain case, tooth measurements, and breadth of the tympanic bulla, which change less over the age classes. This first component was taken to represent general size (including allometry) as the overwhelming effect reflects increased size of the majority of measured variables within samples (Voss et al., 1990). This same analysis has been repeated including the two species A . abyssinicus and A . dembeensis with the 16 localities; the results substantially parallel those including all four species (Table 11). Subsequent analyses that include this first component we call ‘size-in’, and those that exclude this component we call ‘size-

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FIG. 3. Box plots for (a) occipito-nasal length (OCN) and (b) length of maxillary toothrow at crown (LMT) for all localities of the four species: A. dembeensis (A-G, R), A. abyssinicus (H-Q), A. niloticus (T), A . testicularis (S). Localities of A. dembeensis and A. abyssinicus are arranged by decreasing altitude.

124 AFEWORK BEKELE ET A L .

TABLE 11 Character coeficients of the first normalized eigenuectors of the multiple group principal component analysis (pooled within sample covariance matrix) for the 18 localities in the four species (first column); and the 16 localities of the two species

A . abyssinicus and A. dernheensis

Coefficients

Character 18 16

Occipito-nasal length Condylo-incisive length Zygomatic breadth inter-orbital constriction Breadth of braincase Length of maxillary toothrow at crown Width of third molar at crown Length of maxillary diaslema Length of anterior palatine foramen Palatal length Length of tympanic bulbd Breadth of tympanic bulla

0,313 0.337 0,308 0,244 0.124 0,081 0.177 0446 0.429 0.350 0,222 0.159

0.312 0.334 0.312 0.243 0. I26 0.073 0.176 0.447 0.435 0.346 0.224 0.158 -

out’, although we realize that this vector does not summarize all effects of size and we use the terms for convenience.

Figure 4 presents plots of scores for the first three canonical variates. A comparison is made between the size-in and size-out as determined by the MGPCA procedure. The first three canonical variates for size-out explain, respectively, 69.0%, 11.0%0 and 7.4% of variance, and represent 87.45% of the total variation; for the size-in analysis the values are 63.6%, 15.7% and 7.2% for a total of 86.4%. Although the first multiple group principal component-the ‘size vector’- expresses 67.783% of the variance (within group), its contribution to the between-group discrimination is only 5.8% as detected by the method of Campbell (1980).

On the first canonical variate, two different major groupings are clearly identifiable (Fig. 4) for both size-in and size-out. The group with negative scores contains the populations of A . dembeensis, and the positive scores contain the populations of A . abyssinicus, of A . niloticus and o f A . testicularis. Among the positive scores for canonical variate 1, the ordination for the second canonical variate places A . niloticus and A . testicularis at extremes. Note that A . niloticus is separated more from A . dembeensis with size-in while A . testicularis is more separate with size-out. There are small changes in the relative positions of A . dembeensis samples from Gardula (D) and Awassa (R) in the two plots. The localities for A . abyssinicus are more distinct in size-out than in size-in .

The plot of first versus third canonical variates shows additional inter-locality differences for canonical variate 3 (Fig. 4). The Lake Tana (A) and Awassa (R) samples are clearly separated in A . dembeensis, whereas Simien ( H ) and Salale (N) samples are more distinct from the other localities in A . abyssinicus. Some of these differences will be discussed in detail in the context of the effects of altitude and geography.

Populations of the different species are always found to be significantly different. The adjusted Bonferroni significance level is 0-0003 as the 18 localities generate I8* 17/2 = 1 53 comparisons (see

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126 AFEWORK BEKELE ET A L .

Methods for further explanation). Only a few non-significant distances are found in comparisons between localities and these concern populations of the same species (Table 111).

The posterior probability for group classification with size-out shows an average 39.74% of correct classification to locality; this low value depends on the fact that most misclassifications occur between populations of the same species, whereas only 4.5% of specimens are classified as belonging to a different species (Table IV). However, seven of the 21 errors of classification occurred for the Lake Tana A . dembeensis (A), which is a locality very close to A . abyssinicus locality Dangila (I) (see map, Fig. 1) and far from any other locality of A . dembeensis. Two of the seven are assigned to the Dangila locality in this size-out result while the number increases to four in the size-in analysis. The overlap between Lake Tana and Dangila is also indicated by the

TABLE 111 ’Size-in’ (first row) and ‘size-out ’ (second row) Mahalanobis distances between centroids ofthe populations of A. dembeensis (A-G, R ) , A . abyssinicus ( H - Q ) . A . niloticus ( T ) and A . testicularis (S) . Nan-significant distances (according to

Bonferroni’s adjustment, P < 0.003: Marcus, 1990; Morrison, 1990) are in parentheses

B 3.01 3.09

C 2.44 2.48 2.07 2.43

D 3.29 2.79 3.35 3.46 2.59 3.16

E 4.35 2.97 2.63 4.29 4.35 3.14 2.75 4.35

F 3.99 2.08 2.50 3.66 2.48 4.43 2.44 2.97 3.53 2.85

G 3.67 2.09 2.32 3.43 2.13 (1.03) 4.03 2.30 2.72 3.33 2.23 (1‘32)

H 6.58 7.24 7.31 7.03 8.00 9.06 7.58 5.85 2.99 4.91 3.87 4.26 3.27 3.33

I 3.89 6.11 5.08 6.14 6.46 6.67 6.18 4.83 3.38 3.18 2.97 4.27 3.56 3.26 3.32 5.13

L 4.54 6.42 5.48 6.52 6.89 7.11 6.64 3.99 (1.68) 3.81 2.30 2.99 3.86 3.13 2.64 2.79 4.03 (1.89)

M 5.24 6.60 5.87 6.57 7.04 7.09 6.58 3.16 3.03 2.06 4.69 2.22 3.40 3.41 3.01 (1.43) (1.87) 2.90 3.59 2.43

N 4.67 5.43 5.50 5.10 6.24 6.38 5.84 2.33 3.69 3.37 2.89 4.35 (1.95) 3.57 2.57 3.43 3.00 2.74 (1.99) 4.33 3.60 2.82

0 4.55 5.75 5.12 5.50 5.97 6.21 5.64 3.09 2.66 2.63 2.39 (1.89) 3.93 2.29 2.68 2.83 2.29 (1.92) (1-47) 3.02 3.17 2.90 2.47 2.04

P 4.61 6.11 5.33 5.86 6.52 6.65 6.07 3.18 2.49 (1.82) (1.16) 2.49 (1.77) 4.01 (1.74) 2.72 2.75 2.54 (1.35) (1.32) 2.86 3.13 2.20 (1.04) 2.35 (1.68)

Q 4.42 6.00 5.20 5.26 6.51 6.54 6.03 4.20 3.38 3.35 3.49 3.14 2.41 2.70 3.67 3.05 2.57 2.66 3.36 3.18 2.75 4.37 3.95 3.46 3.51 3.38 2.46 2.67

R 3.36 4.73 3.37 5.25 4.47 4.99 4.49 7.73 4.63 5.46 6.24 6.11 5.49 5.51 5.48 3.21 4.81 3.30 5.47 4.53 5.48 4.95 7.08 4.26 4.99 5.82 5.87 4.98 5.11 4.75

S 3.85 3.86 3.64 3.16 4.99 4.07 4.24 8.08 6.24 6.91 7.40 6.34 6.24 6.72 6.31 5.04 3.48 366 3.67 2.76 5.14 4.38 4.42 5.06 3.48 4.07 4.70 3.93 3.55 3.93 3.71 5.00

T 4.90 3.59 4.01 5.25 3.06 3.68 3.14 7.40 6.55 6.75 6.75 5.95 5.93 6.39 6.99 5.27 6.07 4.25 2.58 3.15 4.24 2.03 2.85 2.22 3.42 4.01 3.57 3.06 2.67 2.34 2.67 4.05 4.87 5.11

A B C D E F G H I L M N O P Q R S

MULTIVARIATE MORPHOMETRlCS I N ETHIOPIAN A R V I C A N T H I S 127

TABLE 1V A posteriori classification matrix: number of individuuls classijied in each group, total number of individuals and the estimate of

the classification error. A . dembeensis (A-G, R ) , A . abyssinicus ( H - Q ) . A. niloticus ( T ) , A . testicularis ( S )

Population

Total A B C

A 9 2 3 B 4 4 4 2 c 2 2 1 0 D 1 1 2 E 0 2 2 F O l O ( 3 1 2 3 H O O O 1 0 0 0 L O O 0 M O O 0 N O 0 0 0 0 0 0 P 1 0 0 Q O O O R O O 1 s 0 0 0 T O O 0

D E F G H I L M N O P Q R S T

0 0 0 0 0 2 1 0 0 0 0 1 1 2 0 4 0 8 6 0 0 0 0 0 0 0 0 0 1 2 0 2 1 0 0 0 0 0 0 0 0 0 1 0 0

15 0 1 0 0 0 0 0 0 0 0 0 0 0 0 1 2 0 0 1 0 0 0 0 0 0 0 0 0 0 1 1 0 1 9 7 0 0 0 0 0 0 0 0 0 1 0 2 5 7 1 2 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 1 3 2 1 0 0 1 I 0 0 0 0 0 0 0 1 9 3 5 0 0 1 1 0 0 0 0 0 0 0 2 1 2 1 4 0 0 5 0 0 0 0 0 0 0 0 1 0 0 0 7 2 0 0 0 0 0 0 0 0 0 0 2 0 1 1 9 3 0 0 0 0 0 0 0 0 2 3 5 16 3 5 26 0 1 0 0 0 0 0 0 0 0 0 0 0 3 0 9 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 9 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 2 3 0 0 1 0 2 0 0 0 0 0 0 0 0 0 0 1 8

21 71 18 20 21 29 34 11 18 20 24 10 16 62 12 10 24 21

Error estimate (YO)

57.24 38.03 44.44 25.00 25.93 34.48 64.7 1 9.50

27.78 85.00 41.67 30.00 43.75 58.06 25.00 10.00 4.17

14.29

connection of these two localities in the minimum spanning tree superimposed on the plot of canonical variates 1 and 2 in Fig. 4, even though the distance is great. Three specimens of A . niloticus are assigned to A . dembeensis in this ‘size-out’ analysis, while all are correctly assigned to A . niloticus in the ‘size-in’ results.

A comparison of the ‘size-in’ and ‘size-out’ analyses is summarized by a plot of the Mahalanobis distances (Table 111) for one analysis plotted against those for the other, by use of the matrix comparison procedure in NTSYS-pc (Fig. 5). The A . niloticus distances are all smaller for ‘size- out’, whereas the distances otherwise fall very close to a line through the origin with slope 1 (Fig. 5a). In other words, except for A . niloticus, there is little difference in locality comparisons between the ‘size-in’ and ‘size-out’ analyses (see also Table 111 of Mahalanobis distances). This result is further reinforced by a separate canonical variate analysis of the 16 localities of A . dembeensis and A . abyssinicus. The plot of the Mahalanobis distances for ‘size-in’ and ‘size-out’ shows that they are very similar for these two analyses (Fig. 5b).

An examination of the canonical variate scores for the analysis of these 16 localities produces bivariate plots that give inter-locality comparisons that are somewhat different from those obtained by use of all four species and 18 localities (Fig. 6) . However, we were able to reproduce the pattern of the 16 locality plots by rotating a three-dimensional plot of the first three canonical variates for the 18 localities to a suitable projection (Fig. 6).

When we regressed scores for the first canonical variate (two species, 16 localities analysis) on locality altitude we found a strong effect, with 70.1 % of the variance of the canonical variate 1 scores being explained by this linear relation; the canonical variate 1 scores decrease with increasing altitude. The majority of the effect is due to the difference in means scores between the high-altitude A . abyssinicus whose localities range from 2100 to 3700, and the lower-altitude A . dembeensislocalities which range from 1100 to 2000 m (Table I). However, the altitudinal clines

128 AFEWORK BEKELE ET A L .

(a) 18 Localities

(b) 16 Localities

4 8

Size-out

FIG. 5. Mantel plots of ‘size-in’ (vertical axes) and ‘size-out’ (horizontal axes) Mahalanobis distanccs between group centroids. (a) The plot for the 18 localities included in the four species; filled circles (0) denote distances between A . niloticus sites and all other localities; one distance is not shown as it overlaps with another. (b) The plot of distances for the 16 localities of A . ahyssinicus and A . demheensis.

are significant for each species separately and they are parallel, as the slopes for the two species are not significantly different (Fig. 7). When species means are adjusted for difference in altitude by an analysis of covariance, the species means are still significantly different.

A large difference in the species for the inter-orbital constriction is seen in Fig. 8 for samples at the same altitude, and for this character there is no altitudinal cline. This character and occipito- nasal length show the largest coefficients for canonical variate 1 (Table V). The cline in canonical variate scores represents a subtle shape change in the skulls with altitude in each species.

The ANOVAs computed on the character ratios (IOC/CIL, ZBjOCN, BBC/OCN) showed significant differences (P < 0.001 in the three cases) between the two Ethiopian species. However,

MULTIVARIATE MORPHOMETRICS IN ETHIOPIAN ARVICANTHIS 129

N

$ O - u L A

I A 1

D . B O F

.E G.

R I .

I 1 I

0 CAN 1

-.I IT" 'T

FIG. 6. Plots of canonical variate scores. (a) Plot of the first two canonical variate scores for the 16 localities of A . ubyssinicus (filled triangles, A) and A . dembeensis (filled circles, 0 ) compared with (b) the three-dimensional plot of the first three canonical variate scores for all four species (the vertical axis is the second canonical variate); note the reciprocal congruence in the position of A . ubyssinicus and A . dembeensis centroids.

Fisher's LSD test showed that between-populations comparisons also have significant values when populations of the same species are compared. Therefore the use of these ratios has many caveats.

Discussion

The large distinction between A . delnheensis and A . abyssinicus populations (Figs 2 and 3) is congruent with the evaluation of Yalden et al. (1976) that A . dembeensis and A . abyssinicus occurring in Ethiopia are two separate species. Although we found an altitudinal cline in both species in a canonical variate, the speculation that A . dembeensis might be a lowland form of A . abyssinicus is not corroborated by our data, as clear differences exist for some single characters (Fig. S), and also in the canonical variate adjusted for the altitudinal effect (Fig. 7).

130 AFEWORK BEKELE E T A L .

4 1

-2 -

-4 -, 1000 2000 3000 4600

Altitude (rn)

FIG. 7. Regression of canonical variate 1 against altitude of collection locality: A . abyssinirus, filled triangles (A); A . dembeensis, filled circles (0).

5.5

- E E 0

g 4.0

v

0 rn C (d

i!

5 0, P

rn

-

4.5

11

0 0

0

0

0 $ 0

A A A

A A A A

A ~~

1 2000 3000 40001 Altitude (m)

FIG. 8. Plot of sample means of inter-orbital constriction against altitude for the eight localities each of A . abyssinirus, filled triangles (A), and A . dembeensis, filled circles (0).

MULTIVARIATE MORPHOMETRICS I N ETHIOPIAN A R V I C A N T H I S 131

It is difficult to describe the observed clines in terms of the measured characters, as the first canonical vector represents a complicated combination of individual character effects in either the 'size-in' or 'size-out' analyses (Table V). However, among the characters used, occipito-nasal length and inter-orbital constriction contribute mostly to species and population discrimination relatively to canonical axis one (Table V). There is a general trend which is parallel in A . abyssinicus and A . dembeensis showing that the skull tends, in general, to become thinner with the increase in altitude.

The Lake Tana population (Table I), occurring in the extreme north of the distribution of A . dembeensis (Fig. l), has been described by Rousseau (1983) as the separate species A . lacernatus. Our analysis performed on a larger sample indicates that this population is associated with A . dernbeensis (Fig. 4), and is nearest to the Rift Valley Lake Shala population which is geographically distant (Fig. 1). It is interesting that the minimum spanning tree (Fig. 4) links Lake Tana A . dembeensis and the nearby Dangila A . abyssinicus, though the Mahalanobis distance between these two localities is fairly large (3.9). However, three or four specimens from Lake Tana are assigned to Dangila in the aposreriori assignment of the discriminant analyses (Table IV). At this time it is impossible to say whether the sample may be of mixed origin due to mixed collections or possibly due to hybridization. Additional collection in this potential zone of sympatry is highly desirable. Lake Tana is at a lower altitude and it is hypothesized that genetic exchange may occur between the Lake Tana A . dembeensis and the other populations of that species that we studied only via the lowland Western region; there are intervening mountain blocks between Lake Tana and the remaining localities of A . dembeensis which would prevent direct contact.

The population sampled at Awassa appears to be very similar to the Lake Tana population in the plot of the first two canonical variates; however, it is the most distinctive of the A . dembeensis populations, with the highest positive value in the plot of the third canonical variate (Fig. 4), and must account for a major part of the variance in that canonical variate for that species.

The ordination of the populations of A . dembeensis (Fig. 4), other than Lake Tana and Awassa, is approximately congruent with their geographic location in a rough north-east to south-west

T A B L E v Coeficients o f the,first three canonical variates o f the 'size-in' (columns 1-3) and 'size-out' (columns 4-6) analyses. These coefficienrs are for the logarithms of the 12 original characters (the Size-in'anulysis) and the component scores vf the mulliple

group principal componenzs minus the 'size' component ( X I - X I I , 'size-out ' analysis)

Character

'Size-in' 'Size-out'

CAN1 CAN2 CAN3 PCscores CAN1 CAN2 CAN3

Occipito-nasal length 2.53 -0.49 0.66 XI Condylo-incisive length -0.74 0.62 -0.49 x 2 Zygomatic breadth -0.78 0.60 -0.72 x 3 Inter-orbital constriction 1.39 -0.72 -0.43 x 4 Breadth of braincase 0.15 0.07 0.81 x5 Length of maxillary toothrow at crown -0.44 0.21 0.08 X6 Width of third molar at crown 0.62 0.48 0.40 x 7 Length of maxillary diastema -0.31 -0.19 -0.54 X8 Length of anterior palatine foramen 0.26 0.82 -0.16 x 9 Palatal length -0.72 -0.24 0.89 XI0 Length of tympanic bulla -0.52 0.57 -0.19 x11 Breadth of tympanic bulla -0.28 -0.62 0.95

1.10 0.36 -0.12 0.67 -0.20 0.88

1.57 1.41 0-18 0.35

-0.37 0.43 0.57 0.99 0.12 1.18 0.49 2.15

-0.14 0.40 - 0.27 1.57

-0.03 -0.28 - 0.49 - 1.18

0.65 0.02 0.18

- 1.04 -0.57

0.03 -0.30

I32 AFEWORK BEKELE ET A L .

trend (Fig. 1). The ordering is from Alemaya-Erer-Urso (east of the Rift Valley) to Koka, Shala and Gardula, occurring in the Rift Valley.

The A . abyssinicus sampled are more similar to each other than those of A . dembeensis and we do not discern any clear geographical pattern other than the altitudinal cline discussed above, which is found in both species.

Arvicanthis niloticus and A . testicularis are significantly different from the locality samples for the other two species (Table 111); however, they are more similar to A . dembeensis than to A . abyssinicus (Fig. 4). Their geographical distance from the Ethiopian populations (see Fig. 1) does not allow us to formulate any clear hypothesis of their systematic relationships based upon geography.

One aspect of the size difference between A . niloticus, the largest form in our study (Fig. 3), and the other samples can be explained by a comparison of the ‘size-in’ and ‘size-out’ analyses. An examination of both figures (Figs 4 and 5a) shows that this species is the most sensitive to the difference in the methods of analysis. An explanation for this result is that the size differences for A . niloticus are in the direction of the size differences between individuals within samples (a part of which was age-related). This effect is removed by the ‘size-out’ adjustment and we are suggesting that a major portion of size difference of this species is in the direction of the allometric vector within samples. Figure 5 displays most clearly this effect and shows that the distance between A . niloticus and the other samples were affected the most. Also, the difference in percentages of the amount of variance explained by the within-‘size’ vector (Campbell, 1980) between the analyses including A . niloticus and A . testicularis and excluding them, must be due to this effect in A . niloticus. In all other inter-sample comparisons, the size-out adjustment made little difference in the distances between locality and species centroids (Fig. 5b).

O u r results go against lumping species (Misonne, 1971; Honaki et al., 1982), an attitude which ignores the idea that Arvicanthis is a polytypic genus possibly in the midst of rapid diversification (Capanna & Civitelli, 1988). The growing body of literature showing karyotypic (Capanna & Civitelli, 1988; Volobouev et al., 1988), genetic (Kaminski, Rousseau & Petter, 1984), and morphological (Rousseau, 1983) diversification occurring in the genus also supports the recognition of several species.

Further investigations are needed to refine classification, not only to clarify evolutionary relationships amongst these animals, but to form a firm scientific basis for programmes to control these species that represent one of the major pests in the croplands of Africa, which has an ever- increasing need for maximum potential yield.

We wish to thank the curators and the collection managers of different Natural History museums mentioned in the text for allowing us to examine the specimens. We are grateful to Professor M. V. Civitelli, Dept. of Animal and Human Biology, University of Rome ‘La Sapienza’, for her assistance. This paper is part of the research conducted while the first author was on sabbatical leave from Addis Ababa University and a research visitor at the Department of Animal and Human Biology, University of Rome ‘La Sapienza’, and a Rcsident Museum Specialist in the Mammal Section of the Carnegie Museum of Natural History, supportcd by the Richard King Mellon Foundation. The fourth author appreciates the opportunity to join in this study as a collaborator and appreciates the support of the Department of Animal and Human Biology, University of Rome ‘La Sapienza’, while in Rome.

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