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1.57 (1), 1-64, Februar 1992 ISSN 0044-3468 700 C 21274 F

Z487

ZEITSCHRIFT FÜR
SAUGETIERKUNDE

rgan der Deutschen Gesellschaft für Säugetierkunde

ıustein, Silvia A.; Liascovich, Rosa C.; Apfelbaum, Liliana |.; Daleffe, Lidia; Barquez, R. M.; Reig, ©. A.: Correlates

of systematic differentiation between two closely related allopatric populations ofthe Akodon boliviensis group from

NW Argentina (Rodentia: Cricetidae). — Korrelate von systematischer Differenzierung bei zwei nahe verwandten
allopatrischen Populationen von Akodon aus der Boliviensis-Gruppe des Nordwestens von Argentinien (Rodentia,
Cricetidae) 1
trera, R. A.; Carreno, N. B.; Castro-Vazquez, A.: Correlative genital tract morphology and plasma progesterone

levels during the ovarian cycle in Corn mice (Calomys musculinus). — Beziehungen zwischen Genitaltraktmorpho-

logie und Plasmaprogesteronspiegel während des ovariellen Zyklus von Maismäusen (Calomys musculinus) 14
annoni, Stella M.; Borghi, C. E.; Martinez-Rica, J. P.: New data on the burrowing behaviour of Microtus (Pitymys)
duodecimcostatus. - Neue Angaben über das Verhalten von Microtus (Pitymys) duodecimcostatus beim Graben 23
ye, P.; Hutterer, R.; Löpez-Martinez, N.; Michaux, J.: A reconstruction ofthe Lava mouse (Malpaisomys insularis),

an extinct rodent of the Canary Islands. — Eine Rekonstruktion der Lavamaus (Malpaisomys insularis), einem
ausgestorbenen Nager der Kanarischen Inseln 29
'ssöa, Leila Maria; De Oliveira, J. A.; Dos Reis, S. F.: A new species of Spiny rat genus Proechimys, subgenus
Trinomys (Rodentia: Echimyidae). — Eine neue Art von Stachelratten des Genus Proechimys, Subgenus Trinomys
(Rodentia: Echimyidae) 39
‚mparatore, Viviana M.; Agnusdei, Mönica; Busch, Cristina: Habitat relations in sympatric populations of Ctenomys
australis and Ctenomys talarum (Rodentia, Octodontidae) in a natural grassland. — Habitatbeziehungen bei
sympatrisch lebenden Populationen von Ctenomys australis und Ctenomys talarum (Rodentia, Octodontidae) in
natürlichem Grasland a
issenschaftliche Kurzmitteilungen

sttenheimer, Birgitt; Salamon, M.: Nachweis der Alpenspitzmaus Sorex alpinus (Schinz, 1837) im Naturschutz-
gebiet Seeholz am Ammersee. — Record of Sorex alpinus in the nature reserve Seeholz (Ammersee) in Southern

Bavaria | |
une ardische Inseln).

nzelbach, R.;Boessneck, J. T: Vorkommen der Mönchsrobbe Monac

- A record of the Monk seal Monachus monachus on the Island gf Sal (Cape Verde Islands) 58

»kanntmachung N 1497 =2

ıchbesprechungen 62
LIBRARIES

/erlag Paul Parey Hamburg und Berlin

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Tübingen - W. MAIER, Tübingen - J. NIETHAMMER, Bonn - ©. Anne E. Rasa, Bonn —

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Z. Säugetierkunde 57 (1992) 1-13
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Correlates of systematic differentiation between two closely
related allopatric populations of the Akodon boliviensis group
from NW Argentina (Rodentia: Cricetidae)

By Sırvıa A. BLAusTEIn, Rosa C. LıAscovicH, LILIANA I. APFELBAUM, LIDIA DALEFFE,
R. M. Barauzz and ©. A. Reıc

Grupo de Investigaciön en Biologia Evolutiva, Departamento de Ciencias Biologicas, Universidad de

Buenos Aires, Buenos Aires; Instituto Miguel Lillo, Universidad Nacional de Tucuman, Tucuman,

Argentina; Museum of Vertebrate Zoology, University of California, Berkeley, USA; and Museo
Nacional de Ciencias Naturales, Madrid, Spain

Receipt of Ms. 3. 6. 1991
Acceptance of Ms. 20. 8. 1991

Abstract

Studied external, epigenetic, and continuous morphological characters, karyotypes and allozymic
genetic distances of Akodon alterus und Akodon “tucumanensis”. These forms are closely related
deserving for some authors only subspecies status, but they are restricted to quite different biomes in
the NW of Argentina. Cytogenetic results demonstrated chromosomal identity between them, as
reflected by sharing the same 2n = 40, FN = 40 karyotype with an ıdentical pattern of heterochromatin
and a complete G-band arm-to-arm matching. Allozymic analysıs revealed a low genetic distance
between them, in agreement with previously reported D values for other Akodon species. A. alterus
and A. “tucumanensis” can be differentiated by morphological characters and different habitat
preferences. Previous reports suggested that adaptative divergence played a minor role in the
cladogenesis of Akodon and that the main factor ın its multifarious speciation may have been the
stochastic and sudden fixation of chromosomal mutations eliciting reproductive isolation. A.
“tucumanensis” and A. alterus may be an exception to this rule, or reflect strong habitat differentation
in a single species complex. This example could be analyzed within the framework of a lack of
correlation between organısmic evolution and chromosomal and allozymic evolution.

Introduction

With about 43 living species and a fossil record tracıng their origin back to the Pliocene,
South American mice of the genus Akodon (sensu REıc, 1987, 1989; but see SPOTORNO
1986) äre an interesting case of speedy and bountiful speciation. In view of their
morphological resemblance and the frequency of several species packings in the same
general biotopes, together with the wide range of chromosomal rearrangements and the
high frequency of karyotypic species-specificity, it has been recently suggested that the
main factor in Akodon multifarious speciation may have been the stochastic and sudden
fixation of chromosomal mutations elıciting reproductive isolation. Under this process,
ecological equivalence and morphological resemblance are to be expected, with selection
acting mainly to tune up minor differentiation, but not being the main original agent of
‚species differentiation (REıG 1989). Additionally, the overall speed of the process predicts
small interspecific genetic differentiation, a prediction which has been widely corroborated
(APFELBAUM and Reıc 1989; PATToN et al. 1989).

However, studies aimıng to compare morphological, ecological, chromosomal and
genetic-distances differences between pairs of closely related forms of Akodon supposedly
. involved in recent speciation, are lacking. These studies may be critical to further
understanding the acting forces of speciation in these mice.

We have recently found that the most abundant species of mice in the high alpine steppe

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5701-0001 $ 02.50/0

d Silvia A. Blaustein et al.

(3000 m) of the mountain valleys at “El Infiernillo” in the Aconquija range of Tucumän
Province, was a small pale-coloured akodont, Akodon alterus, which has remained
unnoticed so far at this location. As previously carried out by OLDrIELD THoMAs’
collector EmıLıo Bupın and several other mammalogists, we collected in the subtropical
forest and sugar cane plantations of the lowland environments in Tucumän province
specimens of a small dark species of Akodon currently identified as Akodon boliviensis
tucnmanensis. This species is sympatric and syntopic wıth A. puer (= A. caenosus), A.
simulator, and A. ılluteus, all ot which are clearly separated by their karyotypes, body size,
or other minor morphological differences (BARQUEZ et al. 1980; LıascovicH et al. 1989).
Routine karyotyping demonstrated that the high-grassland pale form is identical in its
chromosomal complement to A. b. tucumanensis, which suggests a close relationship in
spite of their strong ecological differentiation. In contrast with the general model referred
to above, this suggests adaptive geographical speciation. We decided then to further study
the relationships and degree of morphological, allozymic and chromosomal differentiation
among these two forms.

Material and methods

Taxonomy and ecology

Akodon boliviensis, the type species of the genus Akodon, was described by MEYEn (1833) on
specimens from Pichu Pichün, Arequipa Department, Peru. Akodon tucumanensis was described by
ALLEN (1901) on specimens from San Miguel de Tucumän, 450 m, Tucuman Province, Argentina.
CABRERA (1961) considered the Tucumanian form as a subspecies of A. boliviensis proposing the
trinomen A. b. tucumanensis. Another related species, A. spegazzını, was described by THomas (1897)
from lower Rio Cachı, Salta Province, Argentina. Recently, Myers et al. (1990) revised the taxonomy
of several Akodon species from Peru, Bolivia, and the north of Argentina, which they placed together
in a “boliviensis group”, and includes A. boliviensis, A. spegazzini, A. puer, A. subfuscus and A.
juninensis. They suggested that tucumanensis ıs a subspecies of A. spegazzini. We study here
specimens collected near the type locality of A. tucumanensis. As we are not able to decide whether A.
tucumanensis is a subspecies ot A. boliviensis or of A. spegazzini, we will provisionally refer to our
specimens as A. “tucnumanensis”.

Akodon alterus was described by Tuomas (1991a) on specimens from Otro Cerro, at 3000 m, 45
km west of Chumbicha, in La Rioja Province, Argentina. He distinguished them from A. spegazzini
by their drab brown colour instead of the buffy olive of the latter, and “by the absence of the strong
yellowish or buffy suffusion in the fur”. He also referred two specimens as A. alterus from
Chumbicha, at 600 m, Catamarca Province, Argentina, one of which he had previously referred to A.
azarae (THoMmas 1919b). He later (THuomas 1920) described as the same species a series of 8 males and
17 females from La Invernada, at 3800 m and 3 males and 4 females from Potrerillo, at 1500 m, both
localities near “Nevado de Famatina”, in La Rioja Province. CABRERA (1961) considered A. alterus as a
synonym of A. b. tucumanensıs.

We captured 37 specimens (18 males and 19 females) of A. “tucumanensis” in August, 1986 and
June, 1987 in Quebrada de Los Sosa, Tucumän Province, Argentina. Quebrada de Los Sosa is located
approximately 25 km W of the city of San Miguel de Tucumän, on Route 307, at an elevation of
850 m. The area belongs to the Basal Subtropical Forest within the Provincia de Las Yungas (CABRERA
1976). Many epiphytes are present and the forest is largely evergreen. This area is characterized by
Phoebe porphyria (laurel), Cedrela hlloi and Cedrela angustifolia (cedro), Rapanea laetevirens (palo
San Antonio), Tıipuana tipu (tipa), and Tabebuia avellanedae (lapacho) as the most conspicuous trees.
Furthermore, there are shrubs, such as Carıca quercifoha (higuera del monte) and climbing-plants,
Mitostigma latiflorum and Cynanchum trilobulatum (MEYER 1963; CABRERA 1976). Although A.
“tucumanensis” ıs the prevailing species in the trapping site (trapping success for this species was 18 %
in 1986 and 23 % in 1987) we have also captured specimens of A. simulator, A. illuteus, Oligoryzomys
sp., Lutrolina crassicandata and Thylamys sp.

Additionally, at El Infiernillo, 79 km on Route 307, at an elevation of 3000 m, Tucumaän Province,
Argentina, we captured 24 specimens (12 males and 12 females) of a small pale akodont mouse
identified as A. alterus. This locality is separated approximately 220 km from the type localıty of A.
alterus but it belongs to the same biome of high meadow steppe. El Infiernillo belongs to the Provincıia
Prepunena (CABRERA 1976) characterized by the grasses Stipa (probably S. saltensis) and Festuca
(probably F. setifolia), Trichocereus pasacana (cardön) covered by the epiphyte Tillandsia, and plants
of the genus Azorella, Adesmia, and Pycnophyllum. The trapping success was 60 % in 1986 and 85 %
in 1987. A. alterus was documented in a rodent guild in which we collected Oligoryzomys flavescens,

Differentiation in two populations of the Akodon boliviensis group 5)

Phyllotis osilae, Ctenomys tuconax, and Reithrodon aurıtus. In the same locality Darsy (1974)
reported the finding of the latter, together with Andinomys edax and Calomys musculinus. His
reference to A. andınus and Akodon sp. may belong to A. alterus. We had previously collected A.
simulator in the same localıty but in a more rocky habitat (REıG unpubl.). Comparisons with the type
and original specimens of A. alterus in the British Museum of Natural History demonstrated that
specimens from “El Infiernillo” must be ascribed to this species.

In addition to the differences previously described in the flora of El Infiernillo and Quebrada de
Los Sosa, the habitats of both localıities are also remarkably different for most abiotic factors. Total
rainfall measured at Quebrada de Los Sosa and EI Infiernillo are 1432.8 mm/year and 422.8 mm/year,
respectively. The rainfall is seasonally distributed with a peak in summer in both localities. However,
precipitation exceeds 100 mm from November to March ın Quebrada de Los Sosa, while this amount
is achıeved only in January in El Infiernillo. Moreover, there ıs a long dry season in El Infiernillo. The
annual mean temperatures in Quebrada de Los Sosa and EI Infiernillo are 15 °C and 10 °C
respectively.

Morphology

Twenty three specimens of A. alterus and 27 of A. “tucumanensis” were analysed. Skulls were
prepared for examination by the papain technique, modified from Luther (SEARLE 1954) further
stained with alizarın red “S” (NoBAack and NoBack 1944). An analysıs of epigenetic characters was
performed, following GRUNEBERG’s (1952) definition and BERRY’s (1963) and BERRY and SEARLE
(1963) character-state descriptions for Mus musculus, and HEDGESs’ (1969) for Apodemus sylvaticus
and Apodemus flavicollis. We followed Reig’s (1977) nomenclature for enameled molar character-
states. Bilateral traits were studied separately on either side. Some of the skulls were partly damaged
and it was impossible to study all the characters. All determinations were made by the same observer
(SB). We first analysed 45 discontinuous characters, but after preliminary analysis we eliminated some
traits for obvious redundancy, strong correlation, and ambiguous or difficult recognition. Thus, we
studied 35 characters which include the mandibular foramen, frontal wormian, fused frontals,
emplacement of the posterior palatine foramen (right and left) and other 30 characters shown ın
Figures 1, 2 and 3. The MMD statistics modified by S70voLD (1973) was applied. Nine morphomertric
characters were also analysed, as detailed in Figure 1. Discriminant analysıs was performed by means
of STATGRAF statistical package.

Voucher specimens were deposited in the Museo Municipal de Ciencias Naturales “Lorenzo
Scaglia”, Mar del Plata, Argentina (MMP).

Cytogenetics

Twelve specimens of A. alterus and 26 of A. tucumanensis were analysed. Metaphase-chromosome
preparations were obtained from bone marrow of anımals injected with yeast one day before sacrifice,
(LEE and ELDEr 1980). Chromosomal spreads were stained with Giemsa or processed for G- and C-
bands following SEABRIGHT (1971) and BARRoS and PATTon (1985), respectively. Diploid number,
fundamental number (FN), and chromosomal morphology for all specimens were determined.
Fundamental number is the number of autosomal arms. Chromosomes were classified according to
Levan et al. (1964). A modification of Reıc and Kısrısky’s (1969) size proposal as a percentage of the
female haploıd set (FHS) was used classifying “large” those chromosomes > 9% FHS, “medium”
those >5.5% FHS, but < 9%, “small” those > 2% FHS but <5.5% FHS, and “minute” those
<2% FHS.

Allozymic distance

Tissues for. electrophoresis and protein staining from 27 specimens of A. alterus and 31 of A.
“tucnmanensis” were prepared using the techniques employed by ArrELBAUM and Reıc (1989).
Twenty eight presumptive locı were determined: Acid phosphatase (Acph), Aspartate aminotransfer-
ase (Aat-1, Aat-2), Esterase (Es-3, Es-4, Es-5), Fumarase (Fum-1, Fum-2), General Proteins (GP-1,
GP-2), Glucose-6 Phosphate dehydrogenase (G-6pdh), Glycerophosphate dehydrogenase (Gpdh),
Hemoglobine (Hb), Isocitrate dehydrogenase (Idh-1, Idh-2), Lactate dehydrogenase (Ldh-1, Ldh-2),
Leucine amınopeptidase (Lap), Malate dehydrogenase (Mdh-1, Mdh-2), Malic enzyme (Me), Peptid-
ase (Pep-1, Pep-2), Phosphoglucomutase (Pgm-1, Pgm-2, Pgm-3), Superoxide dismutase (Sd), and
Xanthine dehydrogenase (Xdh). All differences in electrophoretic mobility were assumed to be of
genetic origin and inherited in a Mendelian fashion. Alleles are designated alphabetically by their
relative mobility, “a” represents the allele variant that migrates further anodally. Allozymic frequen-
cies for each sample were determined from electrophoretic data and estimated by means of LEVENE’s
(1949) formula for small samples. Estimates of genic heterozygosity were obtained from the
electromorphic genotypes by direct counts and averaged across loci for population estimates of
individual variability (H), proportion of polymorphic locı per population (P), and average number of

4 Silvia A. Blaustein et al.

Fig. 1. Lateral (A), dorsal (B), and ventral views of skull of A. “tucumanensis”: 1-preorbital foramen I,
2-preorbital foramen II, 3-zygomatic plate foramen, 4-frontal foramen, 5-maxillary foramen, 6-
posterior palatine foramen, 7-palatine-alisphenoid suture, 8-foramen sphenoidale medium, 9-ven-
trolateral sphenoidale foramen, 10-foramen hypoglossi, RL-rostrum length, UML-upper molar
length, MB-mastoid breadth, ZB-zygomatic breadth, NL-nasal length, GL-greatest length, RTL-
teeth row length, and IFL-incisive foramen length

alleles per locus (A). Genetic distance was estimated to measure the genetic divergence (NEI 1972)
using the jackknife approach of MuLLER and AyaLA (1982) as implemented in the program of SATTLER
and HırBurn (1985).

Results
Morphology

The percentage occurrence of individual non-metrical characters examined in both samples
are given in Tables 1 and 2. The value of the mean measure of divergence is 4.405276 x 10-2
and its standard deviation 1.055756 x 10-2. The MMD is significant at (approximately) the
0.025 probability level when it is greater than twice its standard deviation (SJ0OvoLD 1973;
NEvEz 1984).

The following characters show strong differences in frequency between the two forms
or are exclusive in one of them (Tables 1, 2), thus affording the main varıables to

Differentiation in two populations of the Akodon boliviensis group 5

Fıg. 2. Detail of the ventro-lateral view of skull of A. “tucumanensis”: 1-orbito-alisphenoid foramen,
2-upper buccino masticatory foramen, 34-buccino masticatory foramen, and 4-alisphenoid strut

Fig. 3. Left upper molar row (A) and left lower molar row (B) of a female of A. alterus from El
Infiernillo, Tucumän Province, Argentina: 1-anteromedian flexus of MI; 2-anteroloph-parastyle of
M1; 3-mesostyle-mesoloph of M1; 4-posteroloph-posterostyle of M1; 5-mesostyle-mesoloph of M2;
6-posteroloph-posterostyle of M2; 7-enterostyle of M2; 8-enterostyle of M1; 9-anteromedian flexid
of mi; 10-mesostylid-mesolophid of mi; 11-posterolophid-posterostylid of mi; 12-mesostylid-
mesolophid of m2; 13-posterolophid-posterostylid of m2; 14-ectostylid of m2; 15-ectostylid of m];
and 16-protostylid of ml

distinguish the two forms: posterior palatine foramen (triple), frontal foramen (absent or
present), foramen sphenoidale medium (absent and double), mandibular foramen (triple),
mesostyle-mesoloph M1 (absent or present), enterostyle M1 (moderate or well-
developed), anteromedian flexid (absent or present), posteroloph-posterostyle Mi (moder-
ate or well-developed), posterolophid-posterostylid of mi (absent and moderatly
developed), posteroloph-posterostyle of M2 (moderate or well-developed).

Sılvia A. Blaustein et al.

Table 1. Percentage occurrence of individual non-metrical skull characters of A. alterus (A.a.) and
A. “tucumanensis” (A.t.)

Character

Zygomatic plate foramen ra
Zygomatic plate foramen rl
Zygomatic plate foramen rm
Zygomatic plate foramen la
Zygomatic plate foramen 11
Zygomatic plate foramen Im
Preorbital foramen I rl

Preorbital foramen I r2

Preorbital foramen I 11

Preorbital foramen I 12

Preorbital foramen II ra
Preorbital ftoramen II rp
Preorbital foramen II la

Preorbital toramen II Ip

Frontal foramen ra

Frontal foramen rl

Frontal foramen r2

Frontal foramen rm

Frontal foramen la

Frontal foramen 11

Frontal foramen 12

Frontal foramen Im

Maxillary foramen ra

Maxillary foramen rl

Maxillary foramen rm

Maxillary foramen la

Maxillary foramen 11

Maxillary foramen Im

Posterior palatine foramen rl (ppf)
Posterior palatine foramen r2 (ppf)
Posterior palatine foramen rm (ppf)
Posterior palatine foramen |1 (pp)
Posterior palatine foramen 12 (ppf)
Palatine-alisphenoid suture rn
Palatine-alisphenoid suture rt
Palatine-alisphenoid suture In
Palatine-alisphenoid suture It
Foramen sphenoidale medium a
Foramen sphenoidale medium 1
Foramen sphenoidale medium 2
For esp. ventrolateral ra

For esp. ventrolateral rp

Character

For esp. ventrolateral Ip
Foramen hypoglossi rl
Foramen hypoglossi r2
Foramen hypoglossi 11
Foramen hypoglossi 12
Alısphenoid canal ra
Alisphenoid canal rp
Alısphenoid canal la
Alisphenoid canal Ip
For. orbito-alisph. x’ ra
For. orbito-alisph. x’ rp
For. orbito-alisph. x’ la
For. orbito-alisph. x’ Ip

For. buccino-mast. sup. ra

For.
For.
For.

buccino-mast. sup. rp
buccino-mast. sup. la
buccino-mast. sup. Ip

For bucc. mast.
For bucc. mast.
For bucc. mast.
For bucc. mast.
For bucc. mast.
For bucc. mast.
Alisphenoid strut ra
Alisphenoid strut rp
Alisphenoid strut la
Alisphenoid strut rp

Frontal wormian a

Frontal wormian p

Fused frontals a

Fused frontals p
Emplacement of the ppf rm
Emplacement of the ppf rs
Emplacement of the ppf rp
Emplacement of the ppf Im
Emplacement of the ppf Is
Emplacement of the ppf Ip

Mandibular foramen ri
Mandibular foramen r2
Mandibular foramen r3
Mandibular foramen Il1
Mandibular foramen 12
Mandibular foramen 13

% A.a. % A.t.

For esp. ventrolateral la

r = right, | = left, a = absent, p = present, 1 = simple, 2 = double, m = multiple, n = anterior,
t = transverse.

Regarding the morphometric analysis, highly significant differences were found
between both groups (DF = 9, X2 = 25.29, at level = 0.003). Analysis of the discriminant
function indicates that the most important variables in the differentiation were in order of
precedence lower molar length (LML), rostrum length (RL), and length of incisive
foramen (IFL) (see Table 3).

Cytogenetics

A. “tucnmanensis” and A. alterus have an identical 2n = 40, FN = 40 karyotype (Fig. 4).
Pairs 1 to 18 are constituted by telocentric chromosomes, while pair 19 is made of

Differentiation in two populations of the Akodon boliviensis group 7

Table 2. Percentage occurrence of individual non-metrical molar characters of A. alterus (A.a.)

Character

Anteromedian flexus MI ra
Anteromedian flexus Mi rm
Anteromedian flexus Mi rd
Anteromedian flexus M1 la
Anteromedian flexus M1 Im
Anteromedian flexus Mi ld
Mesostyle-Mesolph MI ra
Mesostyle-Mesolph MI rm
Mesostyle-Mesolph MI rd
Mesostyle-Mesolph Mi la
Mesostyle-Mesolph MI Im
Mesostyle-Mesolph MI ld
Enterostyle MI ra

Enterostyle Mi rm

Enterostyle Mi rd

Enterostyle Mi la

Enterostyle M1 Im

Enterostyle Mi ld
Anteroloph-Parastyle Mi rm
Anteroloph-Parastyle MI rd
Anteroloph-Parastyle M1 Im
Anteroloph-Parastyle MI id
Posteroloph-Posterostyle MI ra
Posteroloph-Posterostyle MI rm
Posteroloph-Posterostyle MI rd
Posteroloph-Posterostyle MI la
Posteroloph-Posterostyle Mi Im
Mesostyle-Mesoloph M2 ra
Mesostyle-Mesoloph M2 rm
Mesostyle-Mesoloph M2 rd
Mesostyle-Mesoloph M2 la
Mesostyle-Mesoloph M2 Im
Mesostyle-Mesoloph M2 Id
Enterostyle M2 ra

Enterostyle M2 rm

Enterostyle M2 la

Enterostyle M2 Im
Posteroloph-Posterostyle M2 ra
Posteroloph-Posterostyle M2 rm
Posteroloph-Posterostyle M2 rd
Posteroloph-Posterostyle M2 la
Posteroloph-Posterostyle M2 Im
Posteroloph-Posterostyle M2 ld

1230 5%

and A. “tucumanensis” (A.t.)

Character

Antermedian flexid mi rm
Antermedian flexid ml rd
Antermedian flexid mi la
Antermedian flexıid mi Im
Antermedian flexid mi ld
Protostylid ml ra

Protostylid ml rm

Protostylid mi rd

Protostylid mi Im

Protostylid mi ld
Mesostylid-Mesolophid ml ra
Mesostylid-Mesolophid mi rm
Mesostylid-Mesolophid mi rd
Mesostylid-Mesolophid mi la
Mesostylid-Mesolophid m1 Im
Mesostylid-Mesolophid m1 ld
Ectostylyd ml ra

Ectostylyd mi rm

Ectostylyd mi rd

Ectostylyd mi la

Ectostylyd mi Im

Ectostylyd mi ld
Mesostylid-Mesolophid m2 ra
Mesostylid-Mesolophid m2 rm
Mesostylid-Mesolophid m2 la
Mesostylid-Mesolophid m2 Im
Ectostylid m2 ra

Ectostylid m2 rm

Ectostylid m2 la

Ectostylid m2 Im

Ectostylid m2 ld
Posterolophid-Posterostylid mi ra
Posterolophid-Posterostylid mi rm
Posterolophid-Posterostylid mi rd
Posterolophid-Posterostylid mi la
Posterolophid-Posterostylid mi Im
Posterolophid-Posterostylid mi Id
Posterolophid-Posterostylid m2 ra
Posterolophid-Posterostylid m2 rm
Posterolophid-Posterostylid m2 rd
Posterolophid-Posterostylid m2 la
Posterolophid-Posterostylid m2 Im
Posterolophid-Posterostylid m2 ld

e = right, | = left, a= absent, m = moderate, d = development.

metacentric minute chromosomes. Pair 1 ıs large, easy to identify by size from the
remaining autosomal pairs. Pairs 2 to 6 are medium-sized and pairs 7 to 18 are small
autosomes gradually decreasing in size. The X is subtelocentric and the Y is submetacen-
tric, representing 8.40 % and 3.21 % of the complement, respectively. A polymorphism of
the sexual pair has been found in females of both species. Two types of females were
found: females with XX sex chromosomes, and females with XXd sex chromosomes being
the Xd an X-chromosome with a gross deletion in its long arm. In the present report over a
total of 19 A. “tucumanensis” females analyzed, 9 were XX and 10 were XXd and over a
total of 12 A. alterus females, 8 were XX and 4 were XXd. The Xd represents a 3.23 % of

8 Silvia A. Blaustein et al.

Table 3. Measurements (mm) of A. alterus (A.a.) and A. “tucumanensis” (A.t.) holotypes, and
samples of El Infiernillo and Quebrada de Los Sosa

Type
8 BMNH
KO 2TEHA

Greatest length
Rostrum length
Nasal length

Zygomatic breadth
Mastoid breadth

Teeth row length
Incisive foramen length
Upper molar length
Lower molar length

X = mean; SD = standard deviation.

the complement ın A. “tucnmanensis”, and a 3.93 % ın A. alterus. It ıs of interest to notice
that in spite of the X polymorphism the sex ratio was nearly 1:1 in the samples of both
species.

C-bands (Fig. 4) showed that constitutive heterochromatin ıs located in the whole short
arm of the X, the Xd-chromosome and the Y, ın both species. Figure 5 shows a total G-
band correspondence of chromosome arms between A. “tucumanensis” and A. alterus.

A A. "tucumanensis*® A. alterus:

Adna aann an Mnananaan|
nananane en na nnnn na BUT
an an na on n— nn an

an en
16

17

10. u XY x X xXd j

Fig. 4. A. “tucnumanensis” (left) and A. alterus (right) Giemsa-stained karyotypes (A), and C-bands (B)

Differentiation in two populations of the Akodon boliviensis gronp 9

it

6 &

=;

43 13 14 14

Fıg. 5. G-banding pattern comparison between A. “tucumanensis” and A. alterus. Each pair is
composed of one autosome of A. “tucumanensis” (left) and one of A. alterus (right)

Allozymic distance

Of the 28 locı examined electrophoretically, 20 (71.4 %) were monomorphic and fıxed for
the same allele in the two samples. The remaining 8 locı (28.6 %) were polymorphic in one
of the two analysed species. The value of (A) was 1.082 ın A. alterus and 1.111 ın A.
“tucumanensis”, (H) was 7.6 % ın A. alterus and 10% in A. “tucumanensis”, and (P) was
21.42 % in A. alterus and 25% ın A. “tucumanensis”. Estimates of genetic distance (D)
values between the two forms showed an average value of D = 0.0280.

Discussion

There is ample evidence that organismic evolution ıs not always accompanied by
chromosomal and allozymic changes. Against the conclusion of Wırson et al. (1975)
several taxa show high chromosomal differences among synmorphic species, while others
show a high degree of organısmal differentiation within karyotypic invariance (REIG 1984).
In rodents in which chromosomal varıability is the rule, a correlation between the rate of
chromosomal change and speciation rate has been suggested (Wırson et al. 1975; BusH et
al. 1977; AGuıLerA 1980; Imar 1983). Based on the correlation between high species-
diversity and high karyotypic heterogeneity patterns, ReıG (1989) suggested that
chromosomal repatterning could be a prime causative factor of speciogenesis in the
akodontine and in other groups of rodents.

Modern theoretical developments suggest that phenotypic evolution is the result of
changes in developmental programs strongly mediated by the evolution of regulatory genes
with direct influence on epigenesis (ARTHUR 1984). Changes in structural genes, whatever
their adaptative or neutral character, may be inconsequential to evolution. Although

10 Silvia A. Blaustein et al.

chromosomal rearrangements may affect regulatory patterns, some of them may also be
inconsequential to organismal evolution the underlying reorganızation of the DNA may or
may not have phenotypic effects (RosE and DOOLITTLE 1983).

Among Sigmodontinae rodents, Akodon (sensu REıG 1987, 1989) shows a high degree
of chromosomal varıability, their karyotypes ranging from 2n = 14 (in A. “arviculoides”,
YoNnENAGA (1972) to 2n = 52 (in A. longipilis, SPOTORNO and FERNANDEZ 1976). The
exceptions are a few species which share the same 2n = 52 karyotype (GALLARDO 1982;
RODRIGUEZ et al. 1983; LıascovicH et al. 1989). However, these species have been
recently separated as members of the genus Abrothrix (SPOTORNO 1986; BARRANTES et al.
1991), in which case, Akodon is limited to a group of species showing a high degree of
chromosomal heterogeneity. The high level of interspecific chromosomal varıability of
Akodon is not matched by a sharp morphological differentiation. The subtlety of mor-
phological limits among Akodon species is a permanent difficulty to taxonomists and
hampered progress in assessing the status of their species.

The mean genetic dıvergence among Akodon species is very small indeed, and it is only
matched among rodents by a few other exceptional cases. Interspecific genetic distances ın
mammals are regularly greater than D = 0.2 (see APFELBAUM and Reıc 1989). It is
interesting to note that small genetic differentiation is negatively correlated with a high rate
of chromosomal rearrangements in this genus, suggesting that karyotypie repatterning
played a primary role in eliciting species richness, and that genetic differentiation mostly
reflects divergence times. The finding of low levels of genetic distance and of morphologi-
cal similarıty together wıth the relatively eurytopic and generalized habits in Akodon
species allow us to speculate that adaptative divergence played a minor role in its speciose
cladogenesis. Our results of allozymic analysıs revealed a low genetic distance of D = 0.028
between A. “tucnmanensis” and A. alterus. This figure agrees with previously reported
values for other Akodon species. For example, genetic distance between pairwise compari-
son with A. longıpilis/A. xanthorhinus (D = 0.022) A. iniscatus/A. neocenus was D = 0.021
and A. “tucumanensis”/A. molinae was D = 0.030. However, slightly high D values were
found among A. “tucumanensis”/A. puer (D = 0.122), A. “tucumanensis”, A. albiventer/A.
kempi (D = 0.190), and A. azarae/A. cursor (D = 0.154) (APFELBAUM and Reıc 1989; .
PATTon et al. 1989; BARRANTES et al. 1991).

Cytogenetic results have shown chromosomal conservatism between A. “tucumanensis”
and A. alterus as reflected by a complete G-band correspondence. Moreover, both species
share the same chromosomal polymorphism in the X-chromosome. This kind of
chromosomal varıability was also found in other species of the genus which belong to the
group of species of around 40 or more reduced diploid numbers (A. azarae, BIANCHI and
CONTRERAS 1967; LIZARRALDE et al. 1982; A. puer, Kajon et al. 1984; VITULLO et al.
1986; A. neocenus (cited as A. varıns), BIANCHI et al. 1971; A. cursor, YONENAGA-YASSUDA
1979). The meaning of the X polymorphism in Akodon azarae has been discussed by
BıanchHi et al. (1989) and SOLAR et al. (1989).

However, these two forms can be ditterentiated by their external (coloration and body
size), epigenetic, and continuous morphological characters. Additionally, both forms
inhabit quite different ecological habitats in allopatric distribution; A. alterns inhabıts the
high mountain steppes, whereas A. “tucumanensis” ınhabits the humid lower mountain
forests. |

The morphological differentiation between our samples of A. alterus and A.
“tucnmanensis” is indeed comparable to that found in different local populations of small
mammals inhabiting different habiıtats. This would suggest that CABRERA was not wrong in
placing alterns as a junior synonym of boliviensis , or, that both are mere subspecies of the
same species. The small genetic distance, and the lack of chromosomal difference between
the two forms would reinforce this view. However, as there is a strong ecological and a less
marked morphological differentiation between them, and as several Akodon species share

Differentiation in two populations of the Akodon boliviensis group Jul

similar karyotypes and very small allozyme differentiation, we believe that any conclusion
on the taxonomic status of the two forms is untimely. A definite solution must wait further
sampling in intermediate localities and the investigation of ısolation mechanisms.

If the morphologic and ecological differences are enough to consider the two forms as
full species, our results are in agreement with the pattern observed in the 2n = 52 species
now referred to as Abrothrix , which are only distinguished morphologically (see
SPOTORNO 1986; SPOTORNO et al. 1990).

It may be significant that we have failed to obtain laboratory hybrids between A. alterus
and A. “tucumanensis” because the behavior of the couples was strongly aggressive.
Nevertheless, since we also observed a high level of intraspecific aggressiness ın mating
trials of A. “tucumanensis”, this result may not be considered conclusive.

Acknowledgements

We thank G. BARRANTES, M. B. Espınosa, M. ORTELLS, M. PIANTANIDA, C. RODRIGUEZ, C.
QUINTANA, and ©. ScaGLiA for assıstance in field and laboratory work. C. HERKE has the credit of
the drawings of Figures 1 and 2. We thank E. Hasson and M. NAacHman for valuable comments on
the manuscript. This research was supported by Consejo Nacional de Investigaciones Cientificas y
Tecnicas grant PID N° 3085300/85 and by the OEA grant “Biosystematics of Muroid and
Caviomorph Rodents” awarded to ©. A. Reıc.

Zusammenfassung

Korrelate von systematischer Differenzierung bei zwei nahe verwandten allopatrischen Populationen
von Akodon aus der Boliviensis-Gruppe des Nordwestens von Argentinien (Rodentia, Cricetidae)

A. alterus und A. „tncumanensis“ wurden bezüglich ihrer äußerlichen, epigenetischen und kontinu-
ierlichen morphologischen Merkmale, der Karyotypen und der allozymischen, genetischen Abstände
untersucht. Diese beiden Arten scheinen eng miteinander verwandt zu sein, leben aber in zwei
verschiedenen Biotopen im Nordwesten von Argentinien. Die cytogenetischen Ergebnisse zeigen eine
große Übereinstimmung zwischen beiden Arten: eine gleiche diploıde Zahl der Chromosomen (2n =
40), eine gleiche fundamentale Zahl (NF = 40), eine gleiche Heterochromatin-Verteilung und eine
vollständige Homologie der G-Bandenmuster. Die allozymische Analyse ergab ferner eine geringe
genetische Distanz zwischen beiden Arten. Dieses stimmt mit Werten bei Gegenüberstellung von
anderen überein. A. alterus und A. „tucnmanensis“ können aber durch ihre morphologischen
Merkmale und die verschiedenen Habitate voneinander unterschieden werden. Frühere Untersuchun-
gen weisen darauf hin, daß die adaptive Divergenz eine geringe Rolle in der Kladogenese von Akodon
gespielt hat, und daß sich die große artliche Vielfalt auf eine stochastische und schnelle Fixierung von
chromosomischen Mutationen zurückführen läßt, welche zur reproduktiven Isolation geführt haben.
Wir fanden heraus, daß A. „tucumanensis“ und A. alterus eine Ausnahme von dieser Regel darstellen.
Dieses Beispiel kann im Kontext mit der Abwesenheit von Korrelationen zwischen organısmischer
Evolution und chromosomischer, allozymischer Evolution analysiert werden.

References

AGUILERA, M. (1980): Analisis intragenerico de la evoluciön cromosömica en algunos grupos de
mamiferos. In: Ecology and Genetics of Animal Speciation. Ed. by ©. A. Reıc. Univ. Simön
Bolivar Caracas: Equinoccio Edit. Pp. 191-209.

ALLAN, J. A. (1901): New South American Muridae and a new Metachirus. Bull. Am. Museum Nat.
Hist. 14, 405-412.

APFELBAUM, L. 1.; REıc, ©. A. (1989): Allozyme genetic distances and evolutionary relationships in
species of Akodontine rodents (Cricetidae: Sigmodontinae). Biol. J. Linn. Soc. 38, 257-280.

ARTHUR, W. (1984): Mechanısms of morphological evolution. A combined genetic, developmental
and ecological approach. John Wiley and Son. A Wiley - Intersciences Publication.

BARQUEZ, R. M.; Wırrıams, D. F.; Mares, M. A.; GEnoways, H. H. (1980): Karyology and
morphometrics of three species of Akodon (Mammalia: Muridae) from northwestern Argentina.
Ann. Carn. Mus. Nat. Hist. 49, 379-403.

BARRANTES, G. E.; ORTELLS, M. O.; Reıc, ©. A. (1991). New studies on allozyme genetic distance
and varıability in Akodontine rodents (Cricetidae) and their systematic implications. Biol. J. Linn.
Soc. (in press)

12 Silvia A. Blaustein et al.

BARRoSs, M. A.; Parton, J. (1985): Genome evolution in pocket gophers (Genus Thomomys).
Chromosoma 92, 337-343.

BERRY, R. J. (1963): Epigenetic polymorphism in wild populations of Mus musculus. Genetical
Research 4, 193-220.

BERRY, R. J.; SEARLE, A. G. (1963): Epigenetic polymorphism of the rodent skeleton. Proc. Zool. Soc.
London 140, 577-615.

Branchı, N. O.; CHAPELLE, A. DE LA; VIDAL RıoJa, L.; MEranı, M. S. (1989): The sex-determining
zinc finger sequences in XY females of Akodon azarae (Rodentia, Cricetidae). Cytogenet. Cell
Genet. 52, 162-166.

BıancHı, N. O©.; CONTRERAS, J. R. (1967): The chromosomes of the field mouse Akodon azarae
(Rodentia, Cricetidae), with special reference to sex chromosome anomalies. Cytogenetics 6,
306-313.

BıancHı, N. O.; Reıc, ©. A.; Morına, O. J.; DuLout, F. N. (1971): Cytogenetics of the South
American akodont rodents (Cricetidae). I. A. progress report on Argentinian and Venezuelan
forms. Evolution 21, 724-736.

BusH, G. L.; Case, $. M.; Wırson, A. C.; PATTONn, J. L. (1977): Rapid speciation and chromosomal
evolution in mammals. Proc. Nat. Acad. Scı. USA 74, 3942-3946.

CABRERA, A. (1961): Catalogo de los mamiferos de America del Sur. II. Sirenia, Perissodactyla,
Artiodactyla, Lagomorpha, Rodentia. Rev. Mus. Argentino Cienc. Nat. “Bernardino Rivadavia”
(Zool) 4, 309-732.

— (1976): Enciclopedia Argentina de Agricultura y Jardineria. Regiones Fitogeogräficas Argentinas.
Fasciculo I., Editorial ACME.

Day, P. L. (1974): Notes on the distribution of the coney rat, Reithrodon auritus, in Northwestern
Argentina. Am. Midl. Nat. 92, 205-206.

GALLARDO, M. H. (1982): Chromosomal homology in southern Akodon. Experientia 38, 1485-1487.

GRUNEBERG, H. (1952): Genetical studies on the skeleton of the mouse. IV. Quasi-continous
varıatıon. J. Genetics 51, 95-114.

Hepses, $. R. (1969): Epigenetic polymorphism in populations of Apodemus sylvaticus and
Apodemus flavicollis (Rodentia, Muridae). J. Zool. (London) 159, 425-442.

Imaı, H. T. (1983): Quantitative analysıs of karyotype alteration and species differentiation in
mammals. Evolution 37, 1154-1161.

Kajon, A. E.; ScAGLIA, ©. A.; HORGAN, C.; VELAZQUEZ, C.; MERANI, M. $.; REic, ©. A. (1984):
Tres nuevos carıotipos de la trıbu Akodontini (Rodentia, Cricetidae). Rev. Mus. Argentino Cienc.
Nat. “Bernardino Rivadavıa”, XIII, 48, 461-469.

LEE, M. R.; ELDER, F. F. B. (1980): Yeast stimulation of bone marrow mitosis for cytogenetic in
investigations. Cytogenet. Cell. Genet. 26, 3640.

LEvan, A.; FREDGA, K.; SANDBERG, A. (1964): Nomenclature for the centromeric position on
chromosomes. Hereditas 52, 201-220.

LEVENE, H. (1949): On a matching problem arısing in genetics. Annals of Mathematics Statistics 20,
91-94.

LrascovicH, R. C.; BARQUEZ, R. M.; Reıc, ©. A. (1989): A karyological and morphological
reassessment of Akodon (Abrothrix) illuteus Thomas. J. Mammalogy 70, 386-391.

LIZARRALDE, M.; BrancHı, N. O.; MERANI, M. S. (1982): Cytogenetics of South American akodont
rodents (Cricetidae). VII. Origin of sex chromosome polymorphisms in Akodon azarae.
Cytologia 47, 183-193.

MEven, F. J. F. (1833): Beiträge zur Zoologie, gesammelt auf einer Reise um die Erde. Zweite
Abhandlung. Säugethiere. Nova Acta Academy. Cesareae Leop. Carol. Nat. Curiosorum 16,
599-600.

MEYER, T. (1963): Estudios sobre la selva tucumana. La selva de Mirtäceas de “Las Pavas”. Opera
Lilloana X. Universidad Nacional de Tucumän, Instituto Miguel Lillo.

MULLER, L. D.; AyaLa, F. J. (1982): Estimation and interpretation of genetic distance in empirical
studies. Gen. Res. 40, 127-137.

Mvess, P.; PATTon, J. L.; SMITH, M. F. (1990): A review of the boliviensis group of Akodon (Muridae:
Sıgmodontinae), with emphasıs on Perü and Bolivia. Miscell. Publ. Museum of Zoology,
University of Michigan 177, 1-104.

Neı, M. (1972): Genetic distance between populations. Am. Nat. 106, 283-291.

Nevez, W. (1984): Paleogenetica dos grupos pre-historica do litoral sul do Brasil (Parana e Santa
Catarina). Tesıs inedita, Universidad do Sao Paulo.

Noßack, C. R.; NoBack, E. (1944): Demonstrating the osseous skeleton of human embryos and
fetuses. Stain Technology 19, 51-54.

PATTOoNn, J. L.; Myers, P.; SMITH, M. F. (1989): Electromorphic variation in selected South American
akodontine rodents (Muridae: Siıgmodontinae), with comments on systematic implications. Z.
Säugetierkunde 54, 347-359.

Reıc, ©. A. (1977): A proposed unified nomenclature for the enamelled components of the molar
teeth of the Cricetidae (Rodentia). J. Zool. (London) 181, 227-241.

Differentiation in two populations of the Akodon boliviensis group 13

— (1984): Significado de los metodos citogeneticos para la distinciön e interpretaciön de las especies,
con especıal referencia a los mamiferos. Rev. Mus. Argentino Cienc. Nat. “Bernardino Rivadavia”
(Zool) 13, 1944.

— (1989): Karyotypic repatterning as one triggering factor in cases of explosive speciation. In:
Evolutionary Biology of Transient Unstable Populations. Ed. by A. FontpeviLa. Berlin -
Heidelberg: Springer Verlag, pp. 246-289.

Reıc, O. A.; KısLisky, P. (1969): Chromosome multiformity in the Genus Ctenomys (Rodentia,
Octodontidae). Chromosoma 28, 211-244.

RODRIGUEZ, M.; MONTOYA, R.; VENEGAS, W. (1983): Cytogenetic analysis of some Chilean species of
the genus Akodon Meyen (Rodentia, Cricetidae). Caryologia 36, 129-138.

Rose, M. R.; DooL1TTLe, W. F. (1983): Molecular biological mechanisms of speciation. Science 220,
157-161.

SATTLER, P. W.; HıLsurn, L. R. (1985): A program for calculating genetic distance, and its use ın
determining significant differences in genetic similarıty between two groups of populations. ].
Heredity 76, 400.

SEABRIGHT, M. (1971): A rapid banding technique for human chromosomes. Lancet 2, 971-972.

SEARLE, A. G. (1954): Genetical studies on the skeleton of the mouse. IX. Causes of skeletal variation
within pure lines. J. Genetics 52, 68-102.

SjovoLpd, T. (1973): The occurrence of minor non-metrical varıants in the skeleton and their
quantitative treatment for population comparisons. Homo 24, 204-233.

SOLARI, A. J.; Espınosa, M. B.; VıruLLo, A. D.; Meranı, M. S. (1989): Meiotic behavior of
gonosomically variant females of Akodon azarae (Rodentia, Cricetidae). Cytogen. Cell Genet. 52,
57-61.

SPOTORNO, A. ©. (1986): Systematics and evolutionary relationships of Andean Phyllotine and
Akodontine rodents. Thesis, Univ. California, Berkeley.

SPOTORNO, A. O.; FERNANDEZ, R. (1976): Chromosome stability in southern Akodon (Rodentia,
Cricetidae). Mammalıan Chromosome Newsletter 17, 13-14.

SPOTORNO, A. O.; ZULETA, C.; CoRTES, A. (1990): Evolutionary systematics and heterochrony ın
Abrothrix species (Rodentia, Cricetidae). Evoluciön Biolögica 4, 37-62.

THomas, O. (1919a): On some small mammals from Catamarca. Ann. Mag. Nat. Hist. (9) 3,
115-118.

— (1919b): On small mammals from “Otro Cerro”, North-eastern Rioja, collected by Sr. L. Budin.
Ann. Mag. Nat. Hist. (9) 3, 389-400.

— (1920): On small mammals from the Famatina Chain, Northwestern Rioja. Ann. Mag. Nat. Hist.
(9) 6, 417-422.

VITULLO, A. D.; MERANI, M. S.; Reıg, ©. A.; KaJon, A. E.; ScAGLIA, O.; EspINoOsA, M. B.; PEREZ-
ZAPATA, A. (1986): Cytogenetics of South American akodont rodents (Cricetidae): new karyo-
types and chromosomal bandıng patterns of Argentinian and Uruguayan forms. J. Mammalogy
67, 69-80.

Wırson, A. C.; BusH, G. L.; Case, $. M.; Kınc, M. C. (1975): Social structuring of mammalian
populations and rate of chromosomal evolution. Proc. Nat. Acad. Sciences USA 72, 5061-5065.

YOoNENAGA, Y. (1972): Chromosomal polymorphism in the rodent Akodon arviculoides ssp. (2n = 14)
resulting from two pericentric inversions. Cytogenetics 11, 488-499.

YONENAGA-YAssUDA, Y. (1979): New karyotypes and somatic and germ-cell banding in Akodon
arviculoides (Rodentia, Cricetidae). Cytogen. Cell Genet. 23, 241-249.

Authors’ addresses: Sı.vıa A. BLAUSTEIN, Rosa C. LıascovIcH, LiDIA DELAFFE, and ©. A. Reıc
(write for reprints), GIBE, Dpto. de Ciencias Biolögicas, FCEyN, Universidad
de Buenos Aires, Pabellon 2, 4to. pıso, Ciudad Universitaria, Nunez, 1428
Buenos Aires, Argentina; R. M. BARQUEZ, Instituto Miguel Lillo, Universidad
Nacıonal de Tucumän, Miguel Lillo 205, 4000 Tucumän, Argentina; LILIAnA 1.
APFELBAUM, Museum of Vertebrate Zoology, University of California at Ber-
keley, Berkeley, CA. 94720, USA; ©. A. Reıc, also Museo Nacional de Ciencias
Naturales, Jose G. Abascal 2, Madrid, Spain

Z. Säugetierkunde 57 (1992) 14-22
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Correlative genital tract morphology and plasma progesterone
levels during the ovarian cycle in Corn mice
(Calomys musculinus)'

By R. A. CUTRERA, N. B. CARRENO, and A. CASTRO-VAZQUEZ

Laboratorio de Reproduccion y Lactancıa, Centro Regional de Investigaciones Cientificas y
Tecnolögicas Mendoza; and Catedra de Fisiologia Normal, Universidad Nacional de Cuyo,
Mendoza, Argentina

Receipt of Ms. 7. 8. 1991
Acceptance of Ms. 13.9. 1991

Abstract

Described the correlation between genital tract morphology and plasma progesterone in laboratory-
reared corn mice (Calomys musculinus). Morphological traits of the ovary, uterus and vagina were
used to define stages of the estrous cycle and of some anovulatory states. These findings were
correlated with changes in the vaginal smear and in plasma progesterone (as measured by radioim-
munoassay). Estrous cyclicity and ovulation occurred in females caged without males. Plasma
progesterone during the estrous cycle showed both a periovulatory and a postovulatory peak.
Changes in the vagınal smear correlated poorly with ovarıan changes, except the formation of new
corpora lutea, that correlated with a sudden disappearance of cornified cells from the smear. The most
frequent cycle length was 5 days. Finally, two histologically distinct anovulatory conditions were
found associated with basal progesterone levels. The ovarıan cycle of this species is provisionally
classified as type III of Conaway (1971), (spontaneous ovulation, induced luteal phase).

Introduction

Calomys musculinus, the corn mouse, is probably the most widespread species of field
mice in Argentina. It ıs found from near Esquel (43° South latitude) to the tropical
boundaries with Bolıvia and Paraguay, and from the Andes (2230 meters altitude at
Maymarä, the type localıty, province of Jujuy) to sea level in the province of Buenos Aires.
In the humid and temperate Pampa’s grasslands this species acts as reservoir of Junin virus,
the etiologic agent of Argentine hemorrhagic fever (SABATTINI et al. 1977; WEISSENBACHER
and DAMoNTE 1983).

Reproductive mechanisms of the corn mouse may also be interesting in the context of
the evolution of muroid rodents, because South American cricetids are a monophyletic
group (Subfamily Sigmodontinae; Reıg 1980) that probably differentiated from North
American cricetids in the early Miocene (REıG 1982), some 22 million years ago. The
murids (laboratory rats and mice included), whose reproductive biology is, by far, the best
known, only emerged as a distinct group some 15 million years ago (WALKER 1964).

The corn mouse breeds mainly in the spring and summer, but can also reproduce all
year round, particularly when winters are not too severe (Mırıs et al. 1992). In the
laboratory, it has a gestation period of 21 days, a mean litter size of 4.4 to 7.6 young and a
postpartum estrus (DE VILLAFANE 1981; HoDara et al. 1984).

The present paper describe the ovarıan, uterine and vagınal changes occurring during
the estrous cycle of this species, and in two distinct anovulatory conditions that were
found. Also, plasma progesterone levels were measured in both cycling and anovulating
females, and in males.

1 This work ıs dedicated to Professor JoHN W. EvERETT on his 85. birthday.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5701-014 $ 02.50/0

Genital tract morphology and plasma progesterone levels in Corn mice 15

Material and methods

Animals

Colony bred animals were studied after 7-8 weeks of age (fertile copulations can occur as early as the
4th week; DE VILLAFANE 1981). The colony originated in 1983 from wild mice captured in two
localities (La Pega and Nacunän) of the province of Mendoza. Anımals from the two localities have
been bred as separate lines ever since. However, there were no apparent differences between lines, and
all the groups presented here were composed of females from both. The females were kept in groups
of 4-8, in 12 x 20 x 30 cm cages, without males within the cage, under 14 h light/10 h dark, and at
24 °C, and they had free access to a balanced diet and water.

Vaginal smears

Vaginal smears were obtained daily (for periods of 14 to 54 days) in most females, by vaginal lavage
with a small pipette. The smears were dried in an oven, fixed in ethyl ether and absolute ethanol (1:1),
and stained by the method of PapanıcoLAaou (1954), with minor modifications. In some cases, the
material for smearing was not taken, because the vaginal orifice was extremely narrow or closed.

Sacrifices and plasma sampling for progesterone determination

All sacrifices were made in the evening. One hundred and sixty one females were sacrıficed under
ether to establish the correlation between ovarıan histology and the other features of the genital tract.
Vagınal smears were taken from 114 of these females, before sacrificing them at selected stages of the
vagıinal smear. The remaining 47, from which smears were not taken, were sacrificed on random days.
The uterine horns were inspected for the presence of intraluminal fluid, before the genital tract was
removed. The ovarıes and uteri were trimmed of surrounding tissues, and weighed. Ovaries and
vaginas were fixed ın Stieve’s fluid and embedded in paraffın. Tissue sections were stained with
haematoxylin and eosin. The ovaries were sectioned serially.

Additionally, 80 females and 10 males were sacrificed by decapitation and trunk blood was
collected in heparinized tubes for progesterone determinations. Females were sacrificed at selected
stages of the vaginal smear, and were autopsied as described in the above paragraph. Plasma was
separated by centrifugation and kept frozen until the day the radioımmunoassay was performed as
previously described (Bussmann and Deıs 1979; CASTRO-VAZQUEZ and CARRENO 1981).

Ovarian follicles

The largest follicle with no sıgns of atresia, was classıfied as either type 5b, 6, 7 or 8, according to
PEDERSEN and PETERS (1968): 5b-largest preantral follicles; 6-growing follicles with antral lacunae; 7-
growing follicles with a single antral cavity and a well-defined cumulus oophorus; and 8-Graafian
tollicles with a definite cumulus stalk.

Corpora lutea (CL)

They were classıfıed in four classes, that seem to represent the sequence of corpus luteum (CL)
formation and regression, and that were defined as follows: Ia- approximately spherical CLs, with or
without a central cavity (the collapsed ‘channel’ through which the ovum was apparently shed, could
still be recognized in CLs without a cavity); the cavities were sometimes filled with blood cells and/or
fıbroblasts; the luteal cells were large and lightly acidophilic, with clear nuclei and distinct nucleoli;
frequently both hollow and solid CLs were seen in the same animal and, therefore, were considered as
a single class; Ib - spherical CLs with no cavities or ‘channels’, and with luteal cells as in Ia; II- CLs
that were frequently deformed by adjacent structures and showed an increased proportion of
fıbroblasts; most luteal cells were smaller than in Ia or Ib, and their nuclei were usually smaller and/or
darker, and had absent or unconspicuous nucleoli; and III — small and distorted CLs with much
connective tissue surrounding groups of small luteal cells with lightly stained cytoplasm.

Statistics

Multi-group comparisons between means (ovarian and uterine weights) were made by analysis of
variance, using the Tukey test for post-hoc analysis. Multi-group comparisons of the incidence of
vaginal cornification, uterine fluid or old corpora lutea were made with the chi-square test (2-tailed)

16 R. A. Cutrera, N. B. Carreno and A. Castro-Vazquez

for k-samples. Post-hoc analysıs between two groups was made either with the chi-square test or with
the Fisher’s exact probability test, as recommended in SIEGEL (1956). Significance level was fixed at
B2=0.03:

Results
I- Ovarian stages and their associated uterine and vaginal changes

Females that exhibited ovarıan signs of recent or impending ovulation, were classified as
proestrous, estrous, metestrous or diestrous, according to criteria defined below. How-
ever, near 50 % of temales were in one of two anovulatory conditions. The main features of
these ovulatory and anovulatory classes were as follows (see also Tables 1 and 2).

Table 1. Age and body weight, and histological features of the ovary, in female Corn mice in
different ovarian stages

Ovarian stage Number of Age, days Body weight, Type of Type of the
cases (a) g (b) the largest most recent
follicle corpus luteum

Proestrus 63-21 i e 7 none, II or III
Estrus 1302515 a } 8, or recently none, II or III
ruptured ones

Metestrus 163 + 10 18.8 207 Ia
Diestrus 163 +12 19.3 0.8 Ib or II
Atretic cycles 140 #17 16.6 # 0.7 none, II or III
Anestrus 146.5 16.8 # 0.4 none or III

(a) Mean + S.E.M. No significant differences (Tukey test); (b) Mean + S.E.M. “Anestrus’
differed significantly from all groups except “Estrus’ and ‘Atretic cycles’. “Atretic cycles’ differed
significantly from “Proestrus’ and ‘Diestrus’ (p < 0.05; Tukey test).

Table 2. Other ovarian, uterine and vaginal features in female Corn mice in different ovarian
stages (a)

Ovarian stage Ovarian Old corpora Uterine Distended Open Cornified
weight lutea weight uteri vagınas vaginas

(b) mg (c) % (b) mg (d)% (e) % )%

Proestrus 4.9 +04 85.7 60.4+11.3 42.9 58.3 (12)
Estrus 4.3)210:3 85.7 56.5 # 4.6 90.5 { 94.7 (19)
Metestrus 4.4 +0. 65.4 50.052 19:2 i 0 (24)
Diestrus 4.5 30.3 73.9 43.1225 13.0 87. 0
Atretic cycles 3.0 #0.4 69.2 26.9 #4.7 15.4 30.8
Anestrus ZI 10.9 1192.06 0) : 19.3 (57)

(a) Values which are not percentages are expressed as mean + S.E.M. Unless otherwise indicated
in parentheses, the number of cases in each group is the same as ın Table 1; (b) “Anestrus’ and
“Atretic cycles’ differed significantly between them and from all other groups (P < 0.05; Tukey
test); (cl) % of anımals with type II and/or type III corpora lutea. Only “Anestrus’ differed
significantly from all other groups (P < 0.05; Chi-square test); (d) ‘Anestrus’ and “Estrus’ differed
significantly between them and from all other groups (P < 0.05; Chi-square test, followed by Chi-
square or Fisher’s test as “post hoc’ analysis; (e) “Anestrus’ differed significantly from all other
groups. Also, ‘Proestrus’ differed significantly from “Estrus’ and ‘Metestrus’ (P < 0.05; Chi-
square test, followed by Chi-square or Fisher’s test as ‘post hoc’ analysis; (f) “‘Anestrus’ differed
significantly from all groups except “Atretic cycles’. Also, ‘“Atretic cycles’ differed significantly
from ‘Estrus’, ‘Metestrus’ and ‘Diestrus’, and ‘Proestrus’ differed significantly from “Metestrus’
and ‘Diestrus’ (P < 0.05; Chi-square test, followed by Chi-square or Fisher’s test as ‘post hoc’
analysıs).

Genital tract morphology and plasma progesterone levels in Corn mice 17

1 - ‘Proestrus’

Ovaries contained type 7 follicles, but no recent CLs (types la and Ib); type II and/or type
III CLs were present in most cases. The uterus was dilated with fluid, and/or the vagınal
epithelium was cornified, in approximately 50 % of these females; however, the vagina was
closed in 4 out of 14 anımals.

DI st0S3

The ovaries had large Graafıan follicles (type 8) or recently ruptured, unluteinized ones. A
cornified vaginal epithelium, a uterus dilated with fluid, and one or two sets of regressing
CLs (type II and/or III) were found in most cases.

3 - 'Metestrus’

Ovarıes contained newly formed CLs (type la); in 2 cases these contained trapped ova.
Most ovaries also had one or two older generations of CLs (types II and/or III). The
largest growing follicles varıed from stages 5b to 7. The vaginal epithelium had always lost
the cornified layer. The uterus was sometimes dilated with fluid.

4 - "Diestrus’

Ovaries in which the largest follicle was type 5b or 6, and the most recent CLs were either
type Ib (i.e., similar to la, but with no cavities nor ‘channels’) or type II. One or two older
generations of CLs were also common. The vaginal epithelium was never cornıfied and
sometimes was atrophic. The uterus was sometimes dilated with fluid.

5 —- "Anestrus’

The largest follicle was a type 5b (occasıonally, type 6), and follicles in varying degrees of
atresia were typical. The CLs were absent, or old (type III). The uteri were small and
thread-lıke, with no intraluminal fluid. Vagina histology was very varıable: the most
common was a low squamous epithelium, infiltrated with leucocytes. When the vagınal
orifice was closed (62.5 % of cases), the epithelium was atrophic and frequently covered
with a layer of columnar mucous cells. In some cases with open vaginas, however, the
epithelium was cornified. This can be correlated with the occasıonal days of cornification
that interrupt the leucocytic smear pattern of these anımals.

— “Atretie cycles’

The largest growing follicles were type 5b or 6. CLs were absent or regressing (type II or
III). In addition, there was a set of large atretic follicles, that appeared to have interrupted
their growth simultaneously, contrasting with the asynchronous stages of atresia com-
monly found in anestrous ovaries. The incidence of type II and/or type III CLs (indicative
of ovulation in the preceding cycle) did not differ from that in females undergoing
ovulatory cycles, but was significantly higher than in anestrous females. The uteri were
also significantly heavier than those of anestrous females, and were sometimes dilated with
fluid. Vagina histology was as varıable as in anestrus, and cornified epithelia were also
found.

18 R. A. Cutrera, N. B. Carreno and A. Castro-Vazquez

II - Patterns of changes in the vaginal smear

The vaginal smear of females that were not in anestrus at sacrifice (Fig. 1A) was charac-
terized by the cyclic occurrence of waves of nucleated and cornified cells (modal length: 2
days), that were often accompanıed by enlarged and swollen vagınal orifice. The onset of
these epithelial waves was indicated by a decrease in the proportion of leucocytes and the
appearance of cornified cells, sometimes preceded by small, nucleated epithelial cells
(intensely stained with light green). Leucocytes disappeared from the smear only rarely,
although they were definitely reduced in number during the epithelial waves. At the end of
these waves, cornified cells disappeared, and a stage dominated by large, nucleated
epithelial cells, sometimes preceded the ensuing series of predominantly leucocytic smears.
Mucous smears occurred frequently during the leucocytic intervals between epithelial
waves. The vaginal orifice narrowed during these intervals and sometimes closed com-
pletely.

Despite following the vagınal cycle before sacrıficing animals, the vaginal smear
frequently did not correlate closely with the status of the ovary at autopsy. For instance,
proestrous ovaries sometimes coexisted with closed vaginas, or smears that varıed from
fully leucocytie to fully cornified ones, and fully cornified smears, typical of estrus, were

13.3. 154. 7, S ma
DAYS

Fig. 1. Sequence of vaginal cycles in 10 selected cases that were observed during forty days (panel A);
the upper points of each line on panel A indicate the days dominated by epithelial cells (either
nucleated or cornified ones), while the lower points indicate the days of the diestrous intervals. Panel
B shows a histogram of duration of vaginal cycles in 57 females that were not found in anestrus at
sacrifice

sometimes found in anestrous anımals. The disappearance of the cornified layer at
metestrus, however, was clearly and reproducible reflected in the smear and was the only
vagınal event that could be reliably correlated with a change in the ovary.

A histogram of cycle lengths of females that were not ın anestrus at sacrıfice is shown in
Figure 1B. The cycles were considered to begin when cornified cells diısappeared from the
smear, and to continue until the next disappearance of cornified cells: 182 cycles were
recorded, from 57 females. Cycles length was very varıable, wıth a mode of 5 days and a
second frequency peak at 10 days.

On the other hand, females found in anestrus at sacrifice, were characterized by periods

(%) OF CASES

Genital tract morphology and plasma progesterone levels in Corn mice 19

of persistent leucocytic smears and/or closed Table 3. Plasma progesterone concen-
vaginal orifices. In half of these, also, there was tration (nmol/l; mean + S.E.M.) in female
at least one episode of smears dominated by Corn mice in different ovarian stages, and
nucleated and/or cornified cells. However, in males

these periods of epithelial cells were shorter

(modal length: 1 day) than in non-anestrous Rs Br Re
females. terone (a)
III - Incidence of the different phases Den: anne
The frequency of the different ovarıan stages nr, I = 2
was determined ın 47 females that were not Diestrus, type Ib 401+32
smeared, and were sacrificed on random days. Diestrus, type II DR 05227229
Anestrus was frequent (38.3 %), and the “atre- Atretic cycles 12.4 #1.6

Anestrus 16.522313
Males IDEAS]

tic cycle” was infrequent (8.5 %). Proestrus,
estrus and metestrus showed about the same
incidence as the atretic cycle (10.0, 8.5 and (a) Either “Estrus’ or ‘Diestrus, type Ib’
10.6 %, respectively), while diestrus was about diftered en ae n En N a
twice as frequent (23.4 %). Then, if we consid- en re ent

er that cyclic anımals showed a modal cycle

length of 5 days, we can estimate the duration

of proestrus, estrus and metestrus as one day each, and the duration of diestrus as two
days.

IV - Plasma progesterone levels in the different ovarian states and in males

Plasma progesterone differed significantly (P < 0.05; Tukey test) in diestrous females
whether their most recent CLs were type Ib or II. It was higher in mice bearing type Ib
CLs, which were usually found (8 out of 9 cases) on the third day of leucocytic smears,
i.e., approximately on the second day of diestrous (Table 3). Progesterone levels ın type Ib
diestrus were also higher (P < 0.05 or better; Tukey test) than in any other group except
estrus. Conversely, plasma progesterone during estrus was also sıgnificantly higher (P <
0.01; Tukey test) than in any other group except type Ib diestrus. Males, and those females
in anestrus, atretic cycles, proestrus, and metestrus had basal progesterone levels, and did
not differ significantly between them nor with type II diestrus.

Discussion

The vaginal smear pattern of cyclic female corn mice is difficult to interpret if compared
with the common laboratory species, partly because of the lack of a definite indication of
proestrus. Indeed, the corn mouse does not show the surface layer of swollen cells that
occurs at proestrus ın the rat and other mammals (e.g. Long and Evans 1922), and that
brings about the massive shedding of proestrous rounded cells in those species. Another
complicating factor may be the contamination of smears with cells from preceding stages
that may be retained in the double cervicovaginal folds that are typical of the corn mouse
(CASTRO-VAZQUEZ et al. 1987).

It is then important to conclude that nothing can be said about the ovarian status of a
living female, as in field studies, either from the vaginal smear or from the appearance of
the external vagınal orifice on the day of capture. In the laboratory, however, where
vagınal smears can be studied during subsequent days, total cycle length can be estimated
as the distance between two disappearances of cornified cells, since the occurrence of
newly formed CLs (type la) was reliably associated with that vagınal event. Under these

20 R. A. Cutrera, N. B. Carreno and A. Castro-Vazquez

conditions, the length of the cycle most frequently observed was 5 days, although
somewhat longer cycles were also rather frequent, probably indicating the occurrence of
short anestrous periods between the ovulatory cycles.

Short cycles as those described in the corn mouse have not been found outside the
Superfamily Muroidea, but have been also described in many Muridae and Cricetidae,
both from the Old World and from North and South America (AsDELL 1964; JustingEs and
Jounson 1970; Conaway 1954; DEwSBURY et al. 1977), which suggests that this may be an
early acquisition within this Superfamily. This short cycle has been always observed in
association with spontaneous ovulation, and with an induced luteal phase (type III cycle in
the classification of Conaway 1971), and appears typical of short life-span, high reproduc-
tion prey species. It seems that the mechanism of ovulation in the corn mouse is basically
spontaneous, since ovarian evidence of past or impending ovulation was observed in about
60% ot females caged without males. We have not studied, however (and there are no
reports, either) ıf it ıs possible to induce luteal activation by coital or cervicovaginal
stimulation in the corn mouse. Therefore, we can only provisionally classıfy the corn
mouse as bearing a type III cycle. A prolongation of luteal function after genital
stimulation has been reported in some North American cricetids (DEwsBuUrRy and ESTEP
1975; KEnNEY et al. 1977), which are phylogenetically rather close to the South American
ones.

Plasma progesterone in the corn mouse attains maximum levels during estrus and, after
a nadir during metestrus, ıt peaks again in type Ib diestrus. A pattern of progesterone
secretion that includes both a preovulatory (proestrous) and a postovulatory (diestrous)
peak has been reported in many muroid rodents, including the laboratory rat (BUTCHER et
al. 1974; SmitH et al. 1975). It should be noted, however, that what we have designated
here as ‘estrus’ is equivalent to what was called “proestrus’ in those studies. We preferred to
designate this stage as “estrus’ in the corn mouse, since ovulatıon had already occurred in 4
out of 21 “estrous’ anımals that were sacrificed ın the evening, and since ovulation only
occurs about 10 hours later in the rat (EVERETT et al. 1949), ı.e., in the early hours of the
following day. However, both the estrous and the diestrous peaks of progesterone
secretion are remarkably lower in the corn mouse than in the corresponding stages ın the
rat. The low level of circulating progesterone at estrus in the corn mouse may be correlated
with the persistence of uterine fluid during metestrus and diestrus that occurs in some
subjects, since progesterone secretion during the rat proestrus seems responsible for the
rapıd loss of uterine fluid that occurs ın that species (BARNEA et al. 1968). Anovulating
female corn mice, as well as cycling females in stages other than estrus and type Ib diestrus,
had low progesterone levels similar to those found in males. The occurrence of basal
progesterone levels ın late diestrus (type II) indicates that the function of the corpora lutea
formed at ovulatıon is ephemeral, and further suggests that some form of luteal activation
(induced luteal phase) should exist to render implantation possible.

The high incidence of anestrus in laboratory-reared corn mice may be explained, ın
principle, as an effect of (1) some dietary defficiency (for instance, 6-methoxybenzox-
azolinone: BERGER et al. 1981; SANDERS et al. 1981; SCHADLER et al. 1988); (2) grouping
(which may be act either through a pheromonal effect: CHAMPLın 1977; or through
establishing social ranks within the group: BujJaLskA 1973), and (3) prevention of male
exposure (MONTORO et al. 1987). No effort was made here to determining the cause of
anestrus ın our laboratory conditions. It ıs clear, however, that the high incidence of
anestrus is an effect of captivity, since we found (MıLıs et al. 1992) that all feral adult
females are reproductively active when captured during the breeding season.

Genital tract morphology and plasma progesterone levels in Corn mice 2

Acknowledgement

This work was supported by grants from the National Nasen Council of Argentina (CONICET)
and from the University of Cuyo Foundation.

Zusammenfassung

Beziehungen zwischen Genitaltraktmorphologie und Plasmaprogesteronspiegel während des ovariellen
Zyklus von Maismäusen (Calomys musculinus)

Beschrieben wird die Beziehung zwischen der Morphologie des Genitaltrakts und dem Progesteron-
spiegel im Plasma der Maismaus (Calomys musculinus). Morphologische Charakteristika des Ovars,
des Uterus und der Vagina wurden zur Definition der Zyklusphasen und einiger anovulatorischer
Zustände benutzt. Die Befunde wurden mit Veränderungen in Vaginalabstrichen in Beziehung
gebracht sowie mit der Progesteronkonzentration im Plasma (gemessen mit Hilfe eines Radioimmu-
noassay). Bei Weibchen, die ohne Männchen gehalten wurden, traten Ostrus und Ovulation zyklisch
auf. Sowohl während wie auch nach der Ovulation zeigte die Progesteronkonzentration im Plasma
Spitzenwerte. Veränderungen in den Vaginalabstrichen zeigten nur geringe Beziehungen zu Verände-
rungen im Ovar. Die Ausbildung frischer Gelbkörper war allerdings mit dem plötzlichen Verschwin-
den von Zellen des Stratum corneum aus dem Abstrich verbunden. In der Mehrzahl der Fälle betrug
die Länge des Zyklus fünf Tage.

Der Ovarıalzyklus der untersuchten Art wırd in Anlehnung an Conaway (1971) vorläufig dem
Typ III zugeordnet, welcher durch spontanen Eisprung und induzierte Lutealphase charakterisiert ist.

References

ASDELL, $. A. (1964): Patterns of mammalian reproduction. Ithaca: Cornell Univ. Press.

BARNEA, A.; GERSHONOWITZ, T.; SHELESNYAK, M.C. (1968): Assessment of ovarian secretion of
oestrogen during the oestrous cycle by the use of biological criteria. J. Endocr. 41, 281-288.

BERGER, P.]J.; Necus, N.C.; SANDERS, E. H.; GARDNER, P.D. (1981): Chemical triggering of
reproduction in Microtus montanus. Science 214, 69-70.

Bujauska, G. (1973): The role of spacing behaviour among females in the regulation of reproduction
in the bank vole. J. Reprod. Fert., Suppl. 19, 465-474.

Bussmann, L.E.; Deis, R. P. (1979): Studies concerning the hormonal induction of lactogenesis by
prostaglandins F2 alpha in pregnant rats. J. Ster. Biochem. 11, 1485-1489.

BUTCHER, R. L.; CorLins, W. E.; Fuco, N. W. (1974): Plasma concentration of LH, FSH, prolactin,
progesterone and estradiol-17 beta throughout the 4-day estrus cycle of the rat. Endocrinology 94,
1704-1708.

CASTRO-VAZQUEZ, A.; CARRENO, N. B. (1981): A study of the sensory requirements for eliciting the
pseudopregnancy response. Brain Res. 230, 205-220.

CASTRO-VAZQUEZ, A.; CARRENO, N. B.; CUTRERA, R. A.; MARTINEZ, A. R.; Konınckx, A. (1987):
The corn mouse (Calomys musculinus) as an experimental model for reproductive studies. In:
Laboratory Animal Studies in the Quest of Health and Knowledge. Ed. by H. A. ROTHcHILD, A.
ROSENKRANZ and F. A. MouRA DUARTE. Säo Paulo: Sociedade Brasileira de Genetica. Pp.
274-282.

CHAMPLIN, A.K. (1971): Suppression of oestrus in grouped mice: the effects of various densities and
the possible nature of the stimulus. J. Reprod. Fert. 27, 233-241.

Conaway, C.H. (1954): The reproductive cycle of rice rats (Oryzomys palustris) in captivity. ].
Mammalogy 35, 263-266.

Conaway, C.H. (1971): Ecological adaptation and mammalıan reproduction. Biol. Reprod. 4,
239-247.

DE VILLAFANE, G. (1981): Reproducciön y crecimiento de Calomys musculinus murillus (Thomas,
1916). Historia Natural 1, 237-256.

DEwsBURY, D. A.; Ester, D. Q. (1975): Pregnancy in cactus mice: effects of prolonged copulation.
Science 187, 552-553.

DewssBury, D. A.; Ester, D. Q.; LAnIEr, D.L. (1977): Estrous cycles of nine species of muroıd
rodents. J. Mammalogy 58, 89-92.

EVERETT, J. W.; SAWYER, C. H.; MARKEE, ]J. E. (1949): A neurogenic timing factor in control of the
ovulatory discharge of luteinizing hormone in the cyclic rat. Endocrinology 44, 234-250.

FHloDARA, V.L.; Kajon, A. E.; QUINTANS, C. J.; MONTORO, L. $.; MERANI, M. S. (1984): Parämetros
metricos y reproductivos de Calomys musculinus (Thomas, 1913) y Calomys callidus (Thomas,
1916) (Rodentia, Cricetidae). Rev. Mus. Arg. Cienc. Nat. 13, 453-459.

JUSTINES, G.; JoHnson, K. M. (1970): Observations on the laboratory breeding of the cricetine rodent
Calomys callosus. Lab. Anim. Care 20, 57-60.

22 R. A. Cutrera, N. B. Carreno and A. Castro-Vazquez

Kenney, A. M.; LAnIER, D. L.; DEwsBURy, D. A. (1977): Effects of vaginal-cervical stimulation in
seven species of muroid rodents. J. Reprod. Fert. 49, 305-309.

Long, J. A.; Evans, H.M. (1922): The oestrous cycle in the rat and its associated phenomena.
Memor. Univ. Calıf. 6, 1-148.

Mııs, J. N.; ErLıs, B. E.; CHıLos, J. E.; MAIZTEGU1, J. I.; CAstRo-VAZQUEZ, A. (1992): Observa-
tions on reproduction of the corn mouse (Calomys musculinus) on the Argentine pampa. ].
Mammalogy (in press).

MonToRo, L.S.; QUINTANS, C.J.; TANCREDI, A.M.; DonaLpson, M.]J.; HoDara, V. (1987):
Calomys muscnlinus (Rodentia, Cricetidae): its reproduction in captivity. In: Laboratory Animal
Studies in the Quest of Health and Knowledge. Ed. by H. A. ROTHCHILD, A. ROSENKRANZ and
F. A. Moura DUARTE. Säo Paulo: Sociedade Brasileira de Genetica. Pp. 303-308.

PAPANICOLAOU, G.N. (1954): The atlas of exfoliative cytology. Massachussets: Harvard Univ. Press.

PEDERSEn, T.; PETERS, H. (1968): Proposal for a classification of oocytes and follicles in the mouse
ovary. J. Reprod. Fert. 17, 555-557.

Reıc, ©. A. (1980): A new fossil genus of South American cricetid rodents allied to Wiedomys, with
an assessment of the Sigmodontinae. J. Zool. (Lond.) 192, 257-281.

Reıc, O©.A. (1982): Distribuigio geogräfica e histöria evolutiva dos roedores muroideos
sudamericanos (Cricetidae, Sigmodontinae). Rev. Bras. Genet. 2, 333-365.

SABATTINI, M. S.; GONZALEZ DE Rıos, L. E.; Diaz, G.; VEGA, V.R. (1977): Infecciön natural y
experimental de roedores con virus Junin. Medicina (Bs. As.) 37 (Suppl. 3), 149-161.

SANDERS, E. H.; GARDNER, P. D.; BERGER, P. J.; Necus, N. C. (1981): 6-methoxybenzoxazolinone:
a plant derivative that stimulates reproduction in Microtus montanus. Science 214, 67-69.

SCHADLER, M. H.; BUTTERSTEIN, G. M.; FAULKNER, B. J.; Rıce, $. C.; WEISINGER, L. A. (1988): The
plant metabolite, 6-methoxybenzoxazolinone, stimulates an increase in secretion of follicle-
stimulating hormone and sıze of reproductive organs in Microtus pinetorum. Biol. Reprod. 38,
817-820.

SIEGEL, $. (1956): Non-paramerric statistics for the behavioral sciences. New York: McGraw-Hill.

SMITH, M. $.; FREEMAN, M. E.; NEırr, J. D. (1975): The control of progesterone secretion during the
estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels
associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 96, 219-226.

WALKER, E.P. (1964): Mammals of the world. Baltimore: John Hopkins Press.

WEISSENBACHER, M.; DAMONTE, E. B. (1983): Fiebre hemorrägica argentina. Adel. Microbiol. Enf.
Infecc. 2, 119-171.

Authors’ addresses: R. A. CUTRERA, Universit€ Louis Pasteur, Neurobiologie des Fonctions Rhyth-
miques et Saisonnieres, 12 Rue de l’Universite, F-67000 Strasbourg, France;
N.B. CARRENoO and A. Castro-VAZQUEZ, LARLAC-CRICYT, Casilla de
Correo 855, RA-5500 Mendoza, Argentina

- Z. Säugetierkunde 57 (1992) 23-28
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

New data on the burrowing behaviour of Microtus (Pitymys)
duodecimcostatus

By SteLLa M. GIannonT, C. E. BorRGHI and ]. P. MARTINEZ-RıcA

Instituto Pirenaico de Ecologia, CSIC, Jaca, Huesca, Spain

Receipt of Ms. 27. 5. 1991
Acceptance of Ms. 17.9. 1991

Abstract

Described the burrowing behaviour of Pıtymys duodecimcostatus in captivity. The digging patterns
have been found to be different from those reported in earlier papers. Nine different behaviour
patterns were recorded, five of them directly linked to the burrowing activity and the other being
unrelated. The burrowing sequence was studied with respect to the fıve patterns directly related with
the burrowing behaviour. Some differences between males and females were shown in the activities
more or less related to digging. The main conclusion is that Pıtymys duodecimcostatus uses the incisors
as a digging tool ın hard substrata, showing a behaviour similar to that of Arvicola terrestris. This
behaviour seems to depend on the hardness of the excavated soil.

Introduction

Subterranean mammals have been classified by several authors according to the way they
dig into the soil, ı.e., their morphological adaptations and their diıgging behaviour. For
instance, AGRAWAL (1967) distinguishes two kinds of fossorıal rodents according to skull
and forelegs morphological features, while Dusost (1968a, b) distinguishes three kinds of
fossorial mammals: those using only or mainly the forelegs, those using the ıncisors, and
those using teeth and forelegs.

More recently, Gasc et al. (1985) have proposed another classıfıcation which deals not
only with the digging elements, but also with the burrowing modes. They consider two
wide groups according to the parts of the body utilized: those using the forelegs (two sub-
groups, Pıtymys and Eremitalpa) and those using the teeth (also two subgroups, Arvicola
terrestris and Spalax). According to thıs classification, Pitymys duodecimcostatus would
belong to the first group, but there is one difficulty: the Mediterranean vole does not show
any modification of the forelegs for digging. This lack of specialization in the forelegs led
Casınos et al. (1983) to postulate only a behavioural adaptation ın Pıtymys duodecimcos-
tatus, without morphological changes. We have undertaken a study of the digging
behaviour patterns in Pitymys duodecimcostatus, an attempt to add new data to those
supplied by Casınos et al. (1983).

Material and methods

Observations were made on four adult females and three adult males of Pitymys duodecimcostatus
caught in the Aisa valley at an altitude of 1680 m, not far from Jaca, in the Spanish Pyrenees. The
anımals were kept in individual glass boxes. Light followed the normal cycle and temperature was
maintained between 10° and 20 °C. Within the boxes there was enough loose soil to allow digging, and
also fibrous material for nest building. Food in surplus (mainly peanuts and carrots) was supplied.
Sixteen observations were made for each animal except one, a female, for which there were only
thirteen observations possible. Each observation lasted for five minutes, and the different activities
and their durations were noted. The observations were done in an experimental enclosure, a glass-
walled box of 51x 72x4cm containing well-packed moist earth (2.3 kg/cm of compressive

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5701-023 $ 02.50/0

24 Stella M. Giannoni, C. E. Borghi and J. P. Martinez-Rica

strength). The box was joined by a 10cm long pipe to another transparent plastic box of
10x 31 x 16 cm, where the anımal transported the earth away from the former box. Later, observa-
tions were made in soft, unpacked soil (compressive strength 0.35 kg/cm, i.e., about seven times less
than normal soil formerly used) on three adult females and two adult males. The observations were
recorded by hand, vocally and videotape.

Nine different behavioural patterns were recorded, five of them directly linked to the burrowing
activity, the other being unrelated behaviours. The same patterns were found in both sexes. Behaviour
units lasted for different amounts of time, and were recorded as such, not by uniform time units.
Sampling method was, therefore, a sequence record with repetitions excluded and with durations of
each sequence added (SLATER 1978). The behavioural units were the following:

Digging (D): recorded whenever the anımal tore out the earth by means of bites. The incisors
played the main role, and the forelegs were used mainly to push the loose earth below the abdomen.
Both forelegs worked independent by, the body being supported, during the biting phase, by the two
hindlegs and by the non-workingforeleg. From time to time, when the amount of earth below the
body was high, the anımal threw the earth backwards with the hindlegs, in two or three kicks, and
during this phase the body was supported on the forelegs. During the biting act (B) the forelegs were
used for earth accumulatıon (A) and throwing away the earth with the hindlegs (H). Burrowing is,
thus, a composite three-part behaviour.

Turning (T): recorded when the anımal stopped to burrow and turned around by a lateral tumble,
going then to the outside box.

Head pushing (Hp): recorded when the anımal pushed the earth outwards, from the beginning of the
tunnel. The head was used like a bulldozer blade during this activity.

Entrance kicking (Ek): when the anımal was in the small plastic box but near the tunnel
entrance, and kicked away the earth with the hindlegs before entering again into the burrow.

Tunnel kicking (Tk): the animal entered the tunnel, stopped from time to time, accumulated
some earth with his forelegs, and kicked the accumulated earth backwards with the hindlegs. This
movement was quite fast, and happened several times between the entrance and the arrıval at the
digging front.

Grooming (G): this included the common patterns of cleaning the face, the ears and the paws,
followed by a regular washing of the body, which finished with the tail. Often it also included
scratching the sides with a hindleg, which was also cleaned afterwards.
The other behavioural patterns found are: Feeding (F), Resting (R) and Sniffing (S).

Sequence analysis has been carrıed out following a first-order Markov model (FAGENn and YounG
1978). Statistical methods included are the Kolmogorov test for two samples, chi-square test and G
test.

Results
Description of burrowing sequence

Burrowing sequence was studied with the first five types of acts, the other having a very
low frequency. The sequence was independently established for males and for females,
because there were significant differences in the frequency of acts between both sexes on
the Markov model (G test level of significance: p < 0.0001). The analysis was repeated
with only the three burrowing acts (B, A and H) together with the preceding and following
acts, with similar results (G test significance level of sex differences: p < 0.0001).
Sequences were later changed into probabilıties (Fig. 1).

Within the burrowing sequence, biting (B) was followed by accumulation (A) with a
high probability (0.98 for males, 0.93 for females). Accumulation (A) was then followed
by biting (B) more often than by kicking (H) (0.62 for both sexes). After H, the
probability of B was also larger than that of other acts, e.g., going outside the tunnel (IT =
0.74 for males, 0.61 for females). On average, each burrowing sequence was made up of
several repetitions; a low unit was made of three B and two A, while a higher order unit
was made of two low-order units separated by one H. The mean number of repetitions for
each digging act is shown in Figure 2. Also observations were made on the digging activity
of the species in soft, unpacked soil. These show that the animal does not bite (B) at all, but
only accumulates (A) and kicks (H) the earth (Fig. 2). There were significant differences
between the acts in soft and hard soils (G test level of significance: p < 0.0001).

Burrowing behaviour of Microtus duodecimcostatus 25

DIGGING

(M=0.98)
(F=0.90)

(M=0.98)
(F=0.93)

er Forelegs

(F=0.10)

(M=0.62)
(F=0.62)

(M=0.36)
(F=0.36)

Hindlegs
(M=0.26)
(F=0.78)
(M=1.00)
(F=1.00)
TURNING
(M=0.00) (M=0.41)
(F=0.20)
(M=0.17)
(F=0.00)
TINNEIERICKING e—— ————— | „UEISE9.9) _—_ HEAD.PUSHING

(M=0.42)
(F=0.73)

(F=0.50)

ENTRANCE KICKING

Fıg. 1. Burrowing sequence and probabilities of each digging act of Pitymys duodecimcostatus. Within
the box the set of acts is shown specifically belonging to digging activity. (M = males, F = females)

With respect to the more general sequence, with non digging acts included, the
probability of the whole of B being followed by T is 1 in both sexes. T is sometimes
followed by Hp, Ek or Tk. In the males, Ek or Hp have a similar probability, while among
the females Ek has a higher probability of occurrence. Hp can precede Ek or Tk, with a
similar probability in females and a higher probability for the sequence Hp-EK among
males. Tk precedes B with a very high probability in both sexes, and within the burrowing
sequence, the probability of beginning with biting (B) behaviour is very high, 0.98 for
males and 0.90 for females.

26 Stella M. Giannoni, C. E. Borghi and J. P. Martinez-Rica

BE Females (P)

[_] Males (P)

Females and Males (U)

Mean number of repetitions

Bite Forelegs Hindlegs
Acts

Fig. 2. Mean number of repetitions in each digging sequence, of the acts linked to burrowing
behaviour. (P: observation on packed soil; U: observation on unpacked and soft soil)

Duration of sequences

The mean duration of each behaviour in seconds and the corresponding frequence are listed
in the Table for both sexes. Some behaviours, such as feeding (F), last for a considerable
time, but they are not frequent, and hence their total time is low. Other behaviour, such as
digging (D), lasts long and is quite frequent, allowing much time for observation; e.g.,
total observation time of digging was over 70 min for the males and over 2 hours for
females. On the other hand, the shorter behaviour was Ek, with a mean duration of 2.9
seconds in the males and 2.5 seconds in the females. The remaining acts were of
intermediate duration.

There ıs some difference between males and females in the mean duration of each
behaviour. When these differences are significant this is ıindicated ın Table 1. The table also
shows the percentage of time spent by each sex on each type of behaviour. A significant
difference of the total time spent for each behaviour has also been shown (G test level of

Mean duration of each act in seconds for both sexes and percentage of total time spent in each
kind of burrowing behaviour for both sexes

Mean duration Percentage of time
(n) female male female

Digging : (265)
Turning (377)
Head pushing (136)
Ent. kıcking (262)

Tun. kicking ; (394)
Grooming (68)
Feeding (9)
Resting { (54)
Sniffing ß (84)

"p = 0.01, ** p = 0.003 (Kolmogorov-Smirnov test).

Burrowing behaviour of Microtus duodecimcostatus 27

significance: p < 0.001). Both males and females spent the main part of their time with
digging (D = 43 % females and 32.7 % males), followed by the time spent on driving the
earth out of the tunnel (Tk = 26.5 % females and 21.2 % males). The behaviours with the
greatest difference between sexes were resting (R), and turning in the tunnel (T).

Discussion

With reference to the description and Figure 1 (which depicts this sequence) we can see that
Microtus (Pitymys) duodecimcostatus uses mainly the mouth for burrowing, the forelegs to
accumulate soil and the hindlegs to kick the earth away. This agrees with the conclusions of
AGrRAwaAL (1967) tor Pitymys sikimensis, but does not agree with the conclusions of
Casınos et al. (1983). According to these authors, P. duodecimcostatus uses its legs for
burrowing, and Gasc et al. (1985) included this species within the group of hand-diggers,
and even names this group as ‘Pitymys system’.

It ıs possible thus to understand the lack of morphological adaptations for digging at the
forelegs of this vole, because it uses the teeth, not the front feet, as does Pıitymys sikimensıs.
AGRAWAL (1967) stated that the latter species uses its incisors to burrow and that skull and
teeth morphology seem to be highly modified to fossorial activity. Moreover, MATHIAS
(1990) found a strong proodontism both in P. Iusitanicus and ın P. duodecimcostatus, which
is taken to be an adaptation to fossorial life.

Thus, the only remaining problem is the misconception by Casınos et al. (1983) as to
the burrowing method of the Mediterranean vole. The observations made by Casınos et
al. (1983) and by Gasc et al. (1985) appear to be quite reliable. Therefore, the best way of
explaining the discrepancy between their and our results is to suppose ditferences in the
procedures of observation. The most evident of these is the soil supplied to the anımals: the
soil we used was well-packed, moist earth, while that of the tormer authors was loose peat;
due to the need of using a substratum transparent to X rays required for radiocinematogra-
phy. The burrowing behaviour of P. duodecimcostatus changes with the consistency of the
available substratum., Thus, in our observations the normal sequence was: -B-B-B-A-A-
H-B-B-B-A-A-H-B-B-B-, but in different substrata the number of repetitions of each act
and the general pattern could be modified, wıth the number ot bites larger ın hard soıls and
lower or null in soft soils.

The main conclusion is that Pitymys duodecimcostatus uses the incisors as a digging tool
in hard substrates, showing a behaviour similar to that of Arvicola terrestris, according to
the observations of ArroLDı et al. (1976) and LavırLe (1989). In this case the species
should be included in the group called “bite and tear system of Arvicola terrestris” by Gasc
et al. (1985).

Acknowledgements

STELLA M. GIANNONI had a research grant from the Instituto de Estudios Altoaragoneses (Spain);
C.E. BorRGHI had a research grant in the frame of the C.S.1.C.-CONICET agreement between
scientific institutions of Spain and Argentina, and we had the financial support of the project ‘Erosion
in deserted fields’ of the Spanish CICYT. This study will be a portion ot a doctoral thesis of the first
author. We acknowledge and thank the help received from R. SORIGUER, (Estaciön Biolögica de
Donana, Sevilla, R. AnToR, D. GoMEZ, ]J. Isern, Instituto Pirenaico de Ecologia, Jaca and C.
LACADENA. J. GRIESINGER assısted us with the German summary and A. Danson with the English
version.

Zusammenfassung

Neue Angaben über das Verhalten von Microtus (Pitymys) duodecimcostatus beim Graben

Bei ın Gefangenschaft gehaltenen Tieren von Pitymys duodecimcostatus wurde das Verhalten beim
Graben untersucht. Die dabei aufgezeigten Verhaltensmuster unterscheiden sich von denen in früher
veröffentlichten Arbeiten. 9 verschiedene Verhaltensmuster wurden untersucht, von denen 5 mit der

28 Stella M. Giannoni, C. E. Borghi and J. P. Martinez-Rica

Grabaktivität in direktem Zusammenhang stehen. Die übrigen sind unabhängig davon. Die Abfolge
der Grabvorgänge wurde anhand dieser 5 Verhaltensmuster untersucht. Das beim Graben gezeigte
Verhalten zeigte einige Unterschiede zwischen den Geschlechtern auf und scheint von der Festigkeit
der ausgegrabenen Erde abzuhängen. Die Ergebnisse zeigen, daß Pitymys duodecimcostatus bei
hartem Substrat die Schneidezähne benutzt und damit ein ähnliches Verhalten wie Arvicola terrestris
aufweist.

References

AGRAWAL, V.C. (1967): Skull adaptations in fossorıal rodents. Mammalia 21, 300-312.

A1ıroLDI, J. P.; ALTROoccHI, R.; MEyLAn, A. (1976): Le comportement fouisseur du Campagnol
terrestre, Arıvcola terrestris scherman Shaw (Mammalia, Rodentia). Rev. Suisse Zool. 83, 282-286.

Casınos, A.; Gasc, J. P.; REnous, $.; Bou, J. (1983): Les modalites de fouissage de Pıtymys
duodecimcostatus (Mammalia, Arvicolidae). Mammalia 47, 28-36.

Dusost, G.(1968a): Les Mammiferes Souterrains. Rev. Ecol. Biol. Sol. 5, 99-133.

— (1968b): Le Mammifere Souterrain dans son Milieu. Rev. Ecol. Biol. Sol. 5, 136-197.

FAGEN, R. M.; Young, D. Y. (1978): Temporal patterns of behaviors: durations, intervals, latencies,
and sequences. In: Quantitative Ethology. Ed. by P.W. Coıcan. New York: John Wiley and
Sons. pp. 79-114.

Gasc, J. P.; REnous, $.; Casınos, A.; LAVILLE, E.; Bou, ]J. (1985): Comparison of diverse digging
patterns in some small mammals. Fortschritte der Zoologie 30, 35-38.

LAvILLe, E. (1989): Etude Cinematique du Fouissage chez Arvicola terrestris scherman (Rodentia,
Arvicolidae). Mammalıa 53, 177-189.

MarH1as, M. L. (1990): Morphology of the incisors and the burrowing activity of Mediterranean and
Lusitanıan pine voles (Mammalıa, Rodentia). Mammalıa 54, 302-306.

SLATER, P. ]J. B. (1978): Data Collection. In: Quantitative Ethology. Ed. by P.W. Cocan. New
York: John Wiley and Sons. pp. 7-24.

Authors’ addresses: STELLA M. GIANNONI, C.E. BORGHI and J. P. MARTfnEZ-Rıca, Instituto
Pirenaico de Ecologia (CSIC), Apartado 64, E-22700 Jaca, Huesca, Spain

Z. Säugetierkunde 57 (1992) 29-38
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

A reconstruction ofthe Lava mouse (Malpaisomys insularis),
an extinct rodent of the Canary Islands

By P. Boyz, R. HUTTERER, N. LÖPEZ-MARTINEZ and J. MICHAUxX

Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn, Germany; Departamento de
Paleontologia, Facultad de Ciencias Geologicas, Universidad Complutense, Madrid, Spain;
Laboratoire de Paleontologie des Vertebres de !’Ecole Pratique des Hantes Etudes, Montpellier, France

Receipt of Ms. 26. 8. 1991
Acceptance of Ms. 13.9. 1991

Abstract

Described the skeleton and evaluated the form, size and ecological niche of Malpaisomys insularıs, an
extinct rodent of the Canary Islands. The lava mouse was a generalized murid rodent with a head and
body length of about 110 mm and a slightly shorter taıl. Fore and hind limbs exhibit some adaptations
for climbing, a favourable condition in ıts main habıtat, the malpais. There is a notable convergence in
skeletal proportions between the lava mouse, the rock mouse (Apodemus mystacinus), the Galapagos
rice rat (Nesoryzomys narboroughi), and other petricolic rodents which share(d) a similar creviscular
habitat. The reasons for the extinction of Malpaisomys remain obscure. Data from Fuerteventura
show that house mice arrıved shortly before 2000 B. P.; from that time on to present a population
decline of Malpaisomys and a contemporaneous increase of Mus is documented. Possibly the newly
arrıved house mice carried a desease which may have contributed to the extinction of the native
mouse. This is indirectly suggested by a recently described rodent flea, for which the lava mouse may
have been the original host rather than the introduced house mouse.

Introduction

The lava mouse (Malpaisomys insularıs) ıs an endemic Canarıan rodent recently discovered
in subfossil deposits and archaeological sites of Fuerteventura, Lanzarote and Graciosa
(HUTTERER et al. 1988). Together with the shrew Crocıdura canariensis, this rodent
formed the native Holocene terrestrial small mammal fauna of the eastern Canary Islands.
Two thousand years ago Malpaisomys insularıs was extremely common, at least in
Fuerteventura, where innumerable bones were recovered in the Cueva Villaverde (HuT-
TERER et al. 1988). It is not known why such a successful rodent became extinct within a
few centuries, even more because obvious causes such as competition with the black rat do
not hold; our data document the absence of black rats during the extinction process. In
order to understand what happened in the past, we have analysed the isolated bones of
Malpaisomys and, by comparison with a variety of extant rodent species, tried to gain some
. information on its lifestyle from them. The aim of this paper therefore is first to present a
skeletal reconstruction of the lava mouse, secondly to establish its morphological adapta-
tions and to evaluate its ecological niche, and finally to consider the problem of its
extinction.

Material and methods

The main part of the skeletal material of Malpaisomys used during this study was collected in July 1988
by three of us (R.H., N. L.-M., J. M.) during an excavation of the Cueva Villaverde (Fuerteventura),
a project directed by the archaeologists F. HERNANDEZ and M. D. SAncHEZ. We used dry and wet
screening with meshes of three different sizes. In addition we used the material already mentioned in
the description of the genus (HUTTERER et al. 1988). After cleaning and sorting representative samples
of the larger skeletal bones were measured, as shown in Figure 1. Camera lucıda drawings were made
from well preserved bones and used for the reconstruction of the skeleton (Fig. 1). As all our material

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5701-029 $ 02.50/0

30 P. Boye, R. Hutterer, N. Lopez-Martinez and ]J. Michaux

Humerus

Fig. 1. Definitions of the main measurements taken for this study. Drawn after material of Mal-
paisomys insularis from Fuerteventura. (Scale = 10 mm)

consists of isolated bones, the number of vertebrae could not be accurately determined; however,
there is no reason to believe that Malpaisomys deviates from other Murinae which normally have 7
cervical, 13-14 thoracıc, 6-7 lumbar and 2—4 sacral vertebrae (NIETHAMMER and Krarp 1978;
CARLETON and Musser 1984). For the purpose of comparison skeletons of 14 extant rodent species
were prepared and measured (see Table); some data were also taken from RauscH (1976) and from
Boy (1988). Complete skeletons of fossil Muridae are very rare; we studied an almost complete
skeleton of Paraethomys cf. miocaenicus from Upper Miocene diatomites of Hellin, Spain (figured in
Carvo et al. 1978) in the collections of the Department of Palaeontology, University of Madrid, and
we used the information on the Pliocene Apodemus atavus given by RIETSCHEL and STORCH (1974).
For a description and nomenclature of the bones of the postcranial skeleton of a rodent we refer to
ScHIcH (1971).

Results and discussion
Size and form of Malpaisomys

The lava mouse was large, comparable in body size with the rock mouse Apodemus
mystacinus. Our reconstruction of the skeleton (Fig.2) shows an anımal of about 110 mm
head and body length. The vertebral column is little modified and the dorsal and lateral
processes are small. The processus spinosus of the epistropheus is rather small. A
hypertrophied neural spine is not present on the second thoracic vertebra. There are three
sacral vertebrae, the first two of which are usually fused. Their transversal appendices leave
space for two pairs of round foramına sacralıa.

Scapula, humerus, radıus and ulna are similar to any species of Apodemus, except for
their dimensions which will be discussed below. The same applies to the pelvis, femur and
tıbia. The tıbia appears rather long and the crısta tibıalis ıs strongly developed, apparently

A reconstruction of the Lava mouse (Malpaisomys insularis) 31

providing space for a large musculus flexor hallucis and musculus flexor digitorum, both of
which are responsable for the flexibility of the toes. Also the musculus popliteus inserts at
the crista tibialis. This muscle counteracts a rotation in the knee-joint, which is advantage-
ous for a climbing anımal. 54.3 % of the fibula length are not fused with the tibıa.

The hindfoot length ıs difficult to estimate from isolated bones, but judged from the
length of the calcaneus and the metatarsale (Fig. 2), it may have been about 26 mm.

Estimation of the tail length presented a problem. We finally found a simple solution
for this problem, as demonstrated in Figure 3: plotting the known tail length of 14 species
of murıds (see Table) against the width of the second sacral vertebra (where tail-supporting
muscles insert) gives a clear linear relation, which afterwards could be used to estimate the
unknown tail length of Malpaisomys and other extinct rodents. For the lava mouse (mean
width of the second sacral vertebra = 6.1 mm) we estimated a tail length of ca. 105 mm.

The body weight of the lava mouse was about 40 g. This calculation is based on the
relation between head and body length and body weight of 34 species of European rodents
(raw data were taken from NIETHAMMER and Krapp 1978, 1982). The relation ıs highly
significant (r? = 0.95, n = 34); a calculation for a head and body length of 110 mm resulted
in a body weight of 37.9 g, which is very near to the weight of Apodemus mystacinus
(40.9 9).

Biological data

In a previous paper (HUTTERER et al. 1988) we have mentioned that length measurements
of 100 mandibles of lava mice show a bimodal distribution, ıf age classes are treated
separately, which indicates a pronounced sexual dımorphism. There is more evidence for
this assumption in the skeleton: the pelvis shows the same differences in shape (Fig. 4) that
BECKER (1954) described for males and females of 8 European mice and voles. The os pubis
is prolonged in females, while in males it is shorter and the ischium is broader.

Of the mandibles (from a level older than 1730 B.P.) measured, 27.8 % were classıfied
as belonging to age class 1 (juvenile), 55.5 % to age class 2 (subadult to adult) and 16.7 % to
age class 3 (old adult). We found similar values for Mus musculus from recent owl pellets
from Lanzarote: of 100 mandibles 33 % belong to age class 1, 58 % to age class 2 and I %
to age class 3. As the present-day house mice in the Canary Islands live in evidently viable

-s—5e I)
Fig. 2. Skeleton of the lava mouse Malpaisomys insularıs, reconstructed from isolated bones tronı

Cueva Villaverde, Fuerteventura. All elements shown have been found; most of the tail has been
ommitted. (Scale = 10 mm. Drawn by P. Bove)

32 P. Boye, R. Hutterer, N. Löpez-Martinez and J. Michaux

Width of 2nd sacral vertebra
2 |
ie]

\alı
Sl | ) 2 4
or KA

Malpaisomys———

so A0 50 60 70 80 907100 107120 BOTAL ZH Eee
Tail length (mm)

Fıg. 3. The relation between tail length and width of the second sacral vertebra in 14 species of extant
rodents; the width of the second sacral vertebra in Malpaisomys points to a tail length of about
105 mm

populations, we may draw the same conclusion for the ancient population of the lava
mouse. At least we found no evidence for a limited viability, also no teratological bones
and no tooth malformations. However, we have not yet sorted and examined all the
material from all levels of the cave; therefore these comments must be taken as preliminary.

Foraging category and ecological niche

The skeleton of the lava mouse seems to represent a rather general type of murid with no
special adaptations. However, ıf we compare its limb proportions with a set of living
rodents for which the ecology is known, the picture becomes different. Figure 5 shows the
relation between head and body length and the physiological fore limb length (humerus +
radıus) and hind limb length (femur + tibia) for a population of the terrestrial Mus
musculus, and for two species of petricolic rodents, the Spiny mouse Acomys dimidiatus
and the rock mouse Apodemus mystacinus. The dıagram shows that both fore and hind
limbs are relatively longer in the petricolic mice, and longest in the rock mouse, a species
which lives in karstic rock fissures of the Mediterranean and Asıa Minor. The petricolic
snow vole Microtus nivalıs (not shown in figure) also groups nıcely near Acomys and
Apodemus mystacinus; thıs vole is a good climber in rock fissures (BovE 1989).

The mean values for Malpaisomys fall into the range of Apodemus mystacinus. The same
applies to Nesoryzomys narboroughi (not shown in the graph), a lava-dwelling rat endemic
to the Galapagos Islands. We have compared the limb bones of Malpaisomys with those of
Nesoryzomys and Apodemus mystacinus and found them to be very sımilar. The bones of
Nesoryzomys (a member of the Sigmodontinae) are somewhat more heavily built, but those
of A. mystacinus and Malpaisomys are almost indistinguishable.

Subterranean or fossorial rodents (Table; not shown in the graph) group far below the
line for the terrestrial Mus musculns.

Species

Malpaisomys
insularis

Paraethomys
miocaenicus

Micromys
minutus
Grammomys
canıceps

Apodemus
sylvaticus

Apodemus
flavicollis

Apodemus

mystacinus
Acomys

dimidiatus
Microtus

nivalıs

Mus musculus

A reconstruction of the Lava mouse (Malpaisomys insularis) 33

Selected measurements of skeletal elements

Pelvis Femur Tibia

Humerus

Radius

unclassified extinct species

253 16.4

1270
scansorial

8.2

12.4

155
petricolic

16.6

143
It

15.4
terrestrial
10.0

17.

123

Microtus
agrestis
Clethrionomys
glareolus
Apodemus
agrarıus
Arvicanthis
niloticus 2229
fossorial
Spalax
leucodon DM 21162

Arvicola
terrestris i 2 DO 18.8 16.7

2 NIETHAMMER and Krapp (1978). - ° Laboratory strains (Rausch 1976).

The Miocene rodent Paraethomys cf. miocaenicus (Fig.5) goes along with Mus, as does
the Pliocene Apodemus atavus (not shown in figure) for which species we took the
measurements from RIETSCHEL and STORCH (1974). These two extinct species show a
rather unspecialized condition, which we regard as primitive within the Muridae. This
does not necessarıly mean that all fossil rodents were primitive; SCHMIDT-KITTLER and
STORCH (1985) described a skeleton of an Olıgocene ‘sand rat’, Pseudoltinomys (Ther-
domyidae), and KoENIGSwALD et al. (1988) showed that in the Eocene there lived already
highly specialized arboreal rats such as Arluravus (Paramyidae).

The limb proportions of Malpaisomys strongly suggest that the species was a good
climber in rock fissures. This coincides perfectly with the sites where we found fossils of
lava mice in the Canary Islands. Most were in somewhat weathered lava fields of Tertiary
or Quaternary age, for which the Canarıan people use the term “malpais’. Our main
locality, the Cueva Villaverde, is a lava tube in the midst of such an ancient lava field. Only

34 P. Boye, R. Hutterer, N. Löpez-Martinez and ]J. Michaux

Fig. 4. Malpaisomys insularis, sexual dimorphism in the shape of the pelvis. Material from Malpais de
Arena, Fuerteventura. (Scale = 10 mm)

40
Fore limb (Humerus + Radius)

so}

= *
* ©
[m]
20 u Al je
99 Hind Iimb (Femur + Tibia)
5Or
457 x
| N a
40 3
x ®
95 „su B
30 Bo
28
80 90 100 110 120 130 140
Head and body length (mm)
A. mystacinus © Paraethomys *% Malpaisomys
* Acomys DO Mus

Fig. 5. Head and body length plotted against fore and hind limb length for populations of Mus |
musculus, Acomys dimidiatus (data from RauscH 1976) and Apodemus mystacinus (own data); the
values for Malpaisomys insularis and the Miocene Paraethomys cf. miocaenicus are indicated

A reconstruction of the Lava mouse (Malpaisomys insularıs) 93

two localities in the Jandia peninsula (Fuerteventura) are different; there the fossıls were
found below a steep clıff, in the upper parts of which relict plants grow which are
dependent upon high humidity. At the base of this mountain clıff there are large rock
rubble piles which would provide a suitable fissure system for petricolic small mammals.
However, traps set there for small mammals in July 1989 by one of us (R. H.) yielded no
catches at all. In another localıty in the Jandia peninsula we found fossils of lava mice ın
Pleistocene dunes (MıcHAux et al. 1991).

There is no indication that the former habiıtat of Malpaisomys was much different from
the present-day malpais. We therefore hypothesize that the species had its ecological niche
in the malpais zones of Fuerteventura, Lanzarote and adjacent islets, and that its mor-
phological adaptations favoured living and climbing in the creviscular system of the lava
fields. It only had to share this habitat with the endemic shrew Crocidura canariensis
(HUTTERER et al. 1987), at least until the date when the house mouse arrıved.

The extinction of Malpaisomys

From our most ancıent fossil localıties in Fuerteventura and Lanzarote we know that the
native terrestrial small mammals of the eastern Canary Islands were Malpaisomys insularis
and Crocidura canarıensis (HUTTERER et al. 1988; MıcHAux et al. 1991). Our oldest
samples from the Cueva Villaverde comes from a level underlying a horizon dated 1730
B.P. (HERNANDEZ and SANnCHEZ 1986; CARRASCOSA and LÖPEZ-MARTINEZ 1988); in thıs
sample Malpaisomys constitutes 58.9% of the mammals, Crocidura canariensis 38.9 %,
and Mus musculus 2.2 %. In the levels of younger age the proportion of Mus increases
drastically (Carrascosa and LÖPEZ-MARTINEZ 1988), although no quantitative counts of
allmammals are available for the moment. However, the data are sufficient to show that
House mice occurred in Fuerteventura in very low numbers at 1730 B.P., and that they
presumably arrıved in the island a few centuries before, say 2000 B.P.

This was approxımately the time when man arrıved in the Canarıes from neighbouring
Afrıca. OnRUBIA Pıntano (1987) has shown that there are no absolute datations of
archaeological sites ın the Canarıes older than 2490 B.P. (Tenerife: Barranco Hondo) and
1890 B.P. (Gran Canarıa: Los Caserones). A fossil dune deposit wıth remains of endemic
Giant rats, but without archaeologıcal context (erroneously cited as such by ONRUBIA
Pıntapo 1987) at La Aldea, Gran Canaria, was dated as 2080 + 60 B.P. (Cologne
Radiocarbon Laboratory reference number KN-3542; this date was mentioned without
source by LÖPEZ-MARTINEZ and LÖPEZ-JuRADO 1987). This dune deposit also yıelded one
skull and one mandible of Mus musculus, which further supports our assumption of the
arrıval of house mice in the Canary Islands around 2000 B.P. The contemporary arrıval of
man strongly suggests a casual import of mice wıth ships from Africa.

Figure 6 shows that ın a sample from historical times (ca. 800 B.P.; goat and rabbit were
already present) the percentage of Malpaisomys ıs only 10.9% while that of Mus is now
60.7%. In two modern barn owl pellet collections shown in the same figure, the
percentage of Mus ıs 95 and 87.4 %, while Malpaisomys ıs absent.

From our yet limited data we conclude that the populations of the lava mouse declined
since the arrıval of house mice about 2000 years ago, and were progressively replaced by
them. We also show that black or brown rats (Rattus rattus, R. norvegicus) were not
present during the extinction process, and - surprisingly — are even absent in recent owl
pellets from arıd regions of Fuerteventura. Today the black rat exists in Fuerteventura in
cultures and villages, but seems to avoıd the open plain and the lava fields. Apparently ıt
was introduced quite recently.

Our present data suggest that for almost two millennia Malpaisomys and Mus were the
only rodents ın Fuerteventura. It is therefore possible that interactions between these two
species have caused the extinction of the lava mouse. Other factors like climatıc changes or

36 P. Boye, R. Hutterer, N. Lopez-Martinez and J. Michaux

1007|
80 - | |
6073 2

40 7

| —

< 1730 B.P. Historical Recent North Recent South

Ki } Malpaisomys 2 Crocidura U] Mus

Fıg. 6. The percentages of micromammals in fossil and recent barn owl pellets from Fuerteventura.
From left to right: Cueva Villaverde, level older than 1730 B.P. (n = 764); Malpais de Arena,
Historical period, ca. 800 B.P. (n = 183); Villaverde, recent barn owl pellets (n = 240); Barranco de la
Torre, recent barn owl pellets (n = 111)

nn

volcanic activities may have added to this process, but these varıables are unsufficiently
documented. However, CARRASCOSA and LOPEZ-MARTINEZ (1988) have shown that the
house mouse suffered some loss ın size from about 2000 B.P. to present, which indicates
environmental changes. On the other hand the shrew Crocıdura canariensis survived from
the Pleistocene (MıcHaux et al. 1991) into our times and still occurs in high numbers ın the
malpais.

What remains is the fact that the numbers of lava mice declined and those of house mice
increased. Direct competition between the two rodents seems unlikely, as they represent
two distinct sıze classes. We consider the possibility of an indirect impact of house mice on
lava mice, for example through a fatal disease carried by the house mice and consequently
transmitted to the formerly isolated lava mice.

Indirect evidence for a contact between both may be taken from a paper on fleas of
extant Canarıan rodents by BEAUCOURNU et al. (1989). They described a new flea,
Xenopsylla guancha, which they collected from house mice ın Lanzarote; it was not found
in other ıslands of the archıpelago and not previously in the (well-studied) north-western
parts of Africa. According to the authors, the new flea is related to North African species
for which gerbils are the main hosts; therefore they discuss the possible existence of a
vanıshed gerbil in the Canaries.

According to our data house mice arrıved ın the Canary Islands only 2000 years ago.
There is no evidence for gerbils but for Malpaisomys ın Lanzarote and Fuerteventura.
Probably the lava mouse was the original host of the flea Xenopsylla guancha, which later
changed to the house mouse and survived there after its native host had vanished.

Acknowledgements

Our field campain in 1988 was made possible by the invitation of F. HERNANDEZ and M. D. SAnCHEZ
to participate in their archaeological excavation of the Cueva Villaverde. We also thank the Ayun-
TAMIENTO DE LA OLiva for permissions and support. J. FREUNDLICH (C14-Labor, Universität Köln)
kindly provided the radiocarbon datations. We are grateful to J. ADrIan, technical assistent of the
Museum Alexander Koenig, for his careful work of sorting, cleanıng and preparing the fossils and
skeletons, to $. Von GROLL for supplying us with a series of Apodemus mystacinus, and to G. PETERS
for linguistic improvements. This paper was first presented at the 5th Symposium “Fauna and Flora of
the Cap Verde Islands” at Leiden, The Netherlands, October 1989.

A reconstruction of the Lava mouse (Malpaisomys insularis) O7

Zusammenfassung

Eine Rekonstruktion der Lavamaus (Malpaisomys insularıs), einem ausgestorbenen Nager der
Kanarischen Inseln

Anhand von subfossilen Knochenresten wurde das Skelett der Lavamaus Malpaisomys insularis
rekonstruiert und ihr Körperbau, ihre Körpergröße und ökologische Nische abgeschätzt. Die
Lavamaus entsprach einem generalisierten Muriden; die Kopf-Rumpftlänge betrug ca. 110 mm, der
Schwanz war etwas kürzer. Die Vorder- und Hinterextremitäten waren verlängert, eine Anpassung an
die kletternde Lebensweise in den Lavawüsten der Kanarischen Inseln. Die Skelettproportionen sind
bemerkenswert ähnlich denen der Felsenmaus (Apodemus mystacinus), der Galapagosreisratte (Neso-
ryzomys narboroughi) und anderer felsbewohnender Nager, die ebenfalls in dreidimensionalen
Habitaten leben. Die Gründe für das Aussterben der Lavamaus in historischer Zeit sind unklar. Daten
aus Fuerteventura belegen, daß die Hausmaus (Mus musculus) auf dieser Insel um 2000 B.P. eintraf;
von da an läßt sich in subfossilen Eulengewöllen eine Abnahme von Malpaisomys und eine Zunahme
von Mus belegen. Möglicherweise infizierten Hausmäuse die Lavamäuse mit unbekannten Krankhei-
ten; indirekt weist darauf ein nur von Lanzarote bekannter Floh hin, der von Hausmäusen abgesam-
melt wurde. Da Hausmäuse erst in historischer Zeit dort eingewandert sind, kommt als natürlicher
Wirt nur die Lavamaus ın Frage.

References

BEAUCOURNU, J.-C.; ALCOVER, J.-A.; Launay, H. (1989): Les Puces (Siphonaptera) des Iles Canaries.
Description de Xenopsylla guancha n. sp. Vie Milieu 39, 41-48.

BECKER, K. (1954): Geschlechtsunterschiede am Becken von Mäusen (Murinae) und Wühlmäusen
(Microtinae). Zool. Jb. Abt. Syst. 82, 453-562.

BoyE, P. (1988): Vergleichende Untersuchungen zur Anatomie und Biologie der Schneemaus Microtus
nivalıs (Martins, 1842). Diplomarbeit Bonn, 1-200.

— (1989): Zur Kletterfähigkeit der Schneemaus. Deutsche Gesellschaft für Säugetierkunde, Son-
derheft 63. Hauptversammlung, p. 8.

CaALvo, ]J. P.; ELızAGA, E.; LÖPEZ-MARTINEZ, N.; ROBLES, F.; UssEra, J. (1978): El Mioceno superior
continental del Prebetico Externo: Evoluciön del Estrecho Nordbetico. Bol. Geol. Min. 89,
407426.

CARLETON, M.; MusseEr, G.(1984): Muroid rodents. In: Orders and families of recent mammals of the
world. Ed. by S. AnDErson and J. Knox Jones. New York: J. Wiley and Sons. Pp. 289-379.
CARRASCOSA, M. C.; LÖPEZ-MARTINEZ, N. (1988): The House mouse from a prehistoric site ın

Fuerteventura (Canary Islands, Spain). Bonn. zool. Beitr. 39, 237-256.

HERNANDEZ HERNANDEZ, F.; SANCHEZ VELAZQUEZ, M.D. (1986): Fuerteventura: Estado de la
cuestiön con especial referencia a la cueva de Villaverde. Congreso de Cultura de Canarias, Sec.
Argq. Prehistoria, Publ. Gob. Autön. Canarıas.

HUTTERER, R.; LOPEZ-MARTINEZ, N.; MicHavx, J. (1988): A new rodent from Quarternary deposits
of the Canary Islands and its relationships with Neogene and Recent murids of Europe and Africa.
Palaeovertebrata 18, 241-262, 2 pl.

HIUTTERER, R.; LÖPEZ-JURADO, L. F.; VoceL, P. (1987): The shrews of the eastern Canary Islands: a
new species (Mammalıa: Soricidae). J. nat. Hist. 21, 1347-1357.

KOENIGSWALD, W. VON; STORCH, G.; RICHTER, G. (1988): Nagetiere -— am Beginn einer großen
Karriere. In: Messel — Ein Schaufenster in die Geschichte der Erde und des Lebens. Ed. by S.
SCHAAL and W. ZIEGLER. Frankfurt: W. Kramer. Pp. 219-222.

LÖPEZ-MARTINEZ, N.; LÖPEZ-JURADO, L.F. (1987): Un nuevo murido gigante del Cuaternario de
Gran Canaria Canariomys tamaranı nov. sp. (Rodentia Mammalıa). Donana Publ. ocas. 2, 1-60.

MicHAaux, J.; HUTTERER, R.; LöPEZ-MARTiNEZ, N. (1991): New fossil faunas from Fuerteventura,
Canary Islands: Evidence for a Pleistocene age of endemic rodents and shrews. C. R. Acad. Scı.
Parıs, ser. II, 312, 801-806.

NIETHAMMER, ]J.; Krapp, F. (1978): Handbuch der Säugetiere Europas. Bd. 1: Nagetiere I. Wiesba-
den: Akademische Verlagsges.

ONrRUBIA PINTADo, J. (1987): Les cultures prehistoriques des Iles Canaries Etat de la question.
L’Anthropologie, Parıs 91, 653-678.

Rausch, V. (1976): Vergleich von Extremitätenmuskulatur und Extremitätenknochen bei Stachelmaus
(Acomys dimidiatus) und Hausmaus (Mus musculus). Diplomarbeit Bonn, 1-49.

RIETSCHEL, $.; STORCH, G. (1974): Außergewöhnlich erhaltene Waldmäuse (Apodemus atavus Heller,
1936) aus dem Ober-Pliozän von Willershausen am Harz. Senckenbergiana lethaea 54, 491-519.

SCHICH, J. (1971): Funktionelle Deutung anatomischer Baumerkmale am Achsen- und Gliedmaßen-
skelett der Schermaus, Arvicola terrestris scherman (Shaw, 1801). Säugetierk. Mitt. 19, 305-338.

SCHMIDT-KITTLER, N.; STORCH, G. (1985): Ein vollständiges Theridomyiden-Skelett (Mammalıa:
Rodentia) mit Rennmaus-Anpassungen aus dem Oligozän von C£reste, S-Frankreich. Senckenber-
giana lethaea 66, 89-109.

38 P. Boye, R. Hutterer, N. Lopez-Martinez and J. Michaux

Authors’ addresses: R. HUTTERER, P. Boyz, Zoologisches Forschungsinstitut und Museum Alexander
Koenig, Adenauerallee 150-164, W-5300 Bonn 1, Germany; N. L6PEZ-MAR-
TiNEZ, Departamento y UEI Paleontologia, Facultad de C. Geologicas, Univer-
sidad Complutense, E-28040 Madrid, Spain; J. MıcHAux, Laboratoire de Paleon-
tologie des Vertebres de P’E,P. HE ., WS SL, RlacepEBaraıllonsE 34060
Montpellier Cedex, France

Z. Säugetierkunde 57 (1992) 39-46
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

A new species ofSpinyratgenus Proechimys, subgenus Trinomys
(Rodentia: Echimyidae)

By Leıra MarIA PessöA, J. A. DE OLIVEIRA and S. F. Dos Reıs

Departamento de Zoologia, IB, Universidade Federal do Rio de Janeiro, Departamento de Verte-
brados, Museu Nacional and Departamento de Parasitologia, IB, Universidade Estadual de Campinas,
Brazil

Receipt of Ms. 27. 5. 1991
Acceptance of Ms. 16. 9. 1991

Abstract

Described a new species of spiny rat genus Proechimys, subgenus Trinomys based on seven specimens
collected in Conceicäo do Mato Dentro, state of Minas Gerais, southeastern Brazil. The diagnostic
characters of the new species are an elongate and posteriorly wide incisive foramen and a baculum with
weakly developed apical wings. This new species differs from previously described species of the
subgenus by a set of characters including the color of the pelage and skull, teeth, and bacular
morphology.

Introduction

The genus Proechimys comprises the subgenera Proechimys Allen, 1899 and Trinomys
Thomas, 1921 which are distinguished by a series of cranıal, dental, and body traits. In the
subgenus Trinomys the main fold of the molariform teeth extends entirely across the worn
crown and the size of teeth decreases progressively from the premolar to the third molar.
The ridges of the skull are moderately developed, and the infraorbital foramen lacks a
groove for transmission of the nerve (MooJEn 1948). The two subgenera have disjunct
distributions, with the subgenus Proechimys ranging from Nicaragua to northern Para-
guay, whereas the subgenus Trinomys occurs ın the Atlantic forest of eastern Brazil
(dis).

Four species are currently recognized for the subgenus Trinomys, namely Proechimys
dimidiatus (Günther, 1877), Proechimys iheringi Thomas, 1911, Proechimys setosus
(Desmarest, 1817) and Proechimys albispinus (Geoffroy, 1838). A fıfth species, Proechimys
myosurus (Lichtenstein, 1830), was thought by MoojJEn (1948) to be related to P.
albıspinus or even a synonym of this form. The monograph by MoojEn (1948) has
remained a unique source for the study of systematics in the subgenus Trinomys. We have
started a detailed analysis of the varıation and systematics of this subgenus (PEssöA 1989;
PessöA and Reıs 1990; Reıs et al. 1990; PEssöA and Reıs 1991a, b, c, d; Reıs et al. 1991)
and have come upon a species distinguishable from all the forms so far recognized for
Irinomys. In the present study, we describe this new form of Proechimys trom the state of
Minas Gerais, Brazil.

Material and methods

The specimens of Proechimys dimidiatus, P. iheringi, P. setosus, and P. albispinus used for compari-
sons with the new species were identified with the aid of MooJEn’s (1948) diagnoses for cranıal and
pelage characteristics. Hair terminology follows MooJEn (1948) and hair measurements were taken
with an eyepiece micrometer. Capitalized color definitions follow Rıpcway (1912). Cranial measure-
ments defined by MooJeEn (1948) were taken with digital calipers graduated to 0.01 mm, and external
measurements (length of head and body, length of tail, length of hind foot, and length of ear) were

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5701-039 $ 02.50/0

40 Leila Maria Pessöa, J. A. de Oliveira and S. F. dos Reis

obtained from skin tags. Descriptions of bacular morphology were taken from PEssöA and Reıs
(1991d).

Specimens examined are housed in the Museu Nacional (MN), Museu de Histöria Natural da
Universidade Federal de Minas Gerais (MHN), and Museu de Zoologia da Universidade de Säo Paulo
(MZUSP), and are listed as follows: Proechimys dimidiatus (Rio de Janeiro: Tijuca [MN 10344, 10355,
10359, 10362, 10366, 10367, 12814]); Proechimys iheringi iheringi (Säo Paulo: Ilha de Säo Sebastiäo
[MZUSP 218, 221, 222, 2095, 2145, 2146, 2525, 3201, 10072]); Proechimys ıiheringi bonafıdei (Rio de
Janeiro: Teresöpolis [MN 6179, 6181-6183, 6187, 6780, 6782, 6784, 6786, 6787]); Proechimys iheringı
gratiosus (Espirito Santo: Floresta da Caixa Dagua [MN 4018, 5430, 5656, 5674, 5757, 5759, 5767,
5772)); Proechimys iheringi paratus (Espirito Santo: Capela de Säo Braz [MN 4012, 4023, 5455,
5458]); Proechimys iheringi panema (Espiriıto Santo: Campinho [MN 8284-8288]); Proechimys
iheringi denigratus (Bahia: Itabuna [MN 10474, 10476, 10477, 10515, 10517, 10519, 10521,
10523-10525, 10528]); Proechımys albispinus (Bahia: Jequie [MN 13966, 13967, 13969, 14009, 14012,
14013, 14016]); Proechimys setosus (Minas Gerais: Santa Barbara [MHN 131, 149, 870]).

Results
Proechimys moojeni, new species

Holotype: 13380, MN; skull and skin of an adult female specimen; collected by Cory
T. CARVALHO, field number 138, on 25 August 1954.

Type locality: Mata do Dr. DanıEr, Conceicäo do Mato Dentro, Minas Gerais,
Brazıl:.19 70105,43 25V Biss):

Other specimens: Sıx skins and skulls, three from Mata do Dr. Danıer and three
from Boca da Mata in Conceicäo do Mato Dentro.

Distribution: Known only from the type localiıty.

Diagnosis: A Proechimys distinguished from all previously described species of the
subgenus Trinomys by the presence of an elongate and posteriorly wide incisive foramen,
two counterfolds in upper and lower molariform teeth, baculum with weakly developed
apıcal wıngs.
Description

Pelage. — Aristiforms on middorsal region: grayısh basally, gradually blackening
toward tip; total length (mean = 20.35, range = 19.04-21.98); maximum width (mean =
0.63, range = 0.45-0.73). Arıstiforms on outer thighs: Two color types of arıstiforms, both
whitish basally, becoming gray in the median part, one Ochraceous Buff through the tip
and the other gradually blackening toward the tip; total length (mean = 15.85, range =
14.02-18.84); maximum width (mean = 0.46; range = 0.35-0.66). Setiforms on middorsal
region: whitish basally, gradually blackening toward tip but interrupted by an Ochraceous
Orange subapical zone 2.35 to 5.85 long (mean = 3.89); total length (mean = 17.09, range =
15.58-18.78); maximum width (mean = 0.14, range = 0.13-0.15). Setiforms on outer
thighs: Gray basally, gradually blackening toward tip interrupted by an Ochraceous
Orange subapical zone 2.12 to 3.60 long (mean = 2.78); total length (mean = 13.27, range =
11.85-15.27); maximum width (mean = 0.12, range = 0.10-0.15). General color on upper
parts and sides orange brown due to a combination of blackish from the tips of arıstiforms
and Ochraceous Orange ground color from the subapical zone of setiforms. Differentiated
light-colored arıstiforms on outer sides of thighs and rump. Tail bicolored, white below
and brown above in the anterior two-thirds, taıl tip white (Fig. 2). |

Skull. - Elongate and slightly convex; bullae small and smooth; rostrum short but not
stout; transverse ridge of jugal bones not well developed; postorbital process of zygoma
well developed and formed by jugal and squamosal bones; incisive foramen elongate and
posteriorly wide; vomerine sheath incomplete and formed almost exclusively by premaxil-
lae; maxillary part of the vomerine sheath short; posterior palatine foramına at anterior
plane of first molars; mesopterygoid fossa extending forward as far as the anterior plane of
second molars (Fig. 3). Skull and body measurements are given ın Table 1.

A new species of Spiny rat genus Proechimys, subgenus Trinomys 41

MM sspsenus TRINOMYS

200 0 200 600 1000 X
ee — fr

Kilometers \% 2

Fig. 1. Map showing the distribution of the two subgenera of the genus Proechimys (after MOOJEn,
1948). The black star denotes the type locality of the new species of Proechimys

Teeth. - Incisives orthodont, upper and lower molariform teeth with two counterfolds
(Fig. 4).

Baculum. - Elongate and narrow with a straight shaft. Shaft with a slight dorsoventral
curvature and a tappered lateral indentation near mid-shaft. Proximal end straight and
paddle-shaped. The distal end has weakly developed apical wings (Fig. 5).

Comparisons: Proechimys moojeni shares with P. iheringi, P. albispinus, and P.
setosus the aristiform hairs wide and stiff as opposed to P. dimidiatus, whose aristiforms are
narrow and soft. The tail ıs shorter in P. moojeni, P. dimidiatus, and P. albispinus, and
longer in P. iheringi and P. setosus, where it is associated with a penicillated tip. Proechimys
moojeni, P. dimidiatus, and P. iheringi have longer and slightly convex skulls, whereas in ?.
setosus and P. albispinus the skull is shorter and conspicuously convex. The incisive
foramen is posteriorly constricted in P. iheringi, P. setosus, and P. albispinus and widest
posteriorly in P. dimidiatus and P. moojeni (Fig. 6). The latter species differ by the length

42 Leila Maria Pessöa, J. A. de Oliveira and S. F. dos Reis

Fig. 2. Study skin of the holotype of Proechimys moojeni (MN 13380)

Measurements (in mm) of adults of Proechimys moojeni

Specimen numbers 13366 13368 13372 13376 13379 13382
Sex F M M M E M

Length of head and body
Length of tail

Length of hind foot
Length of ear

Greatest length of skull
Condylo-incisive length
Zygomatic breadth
Length of nasals
Interorbital constriction
Palatilar length

Length of upper toothrow
Length of incisive foramen
Width of incisive foramen

of the foramen, which is short in P. dimidiatus and longer in P. moojeni. In Proechimys
dimidiatus the vomerine sheath is complete, whereas it is incomplete in P. moojenı.
Proechimys moojeni always has two countertolds in all molarıform teeth in the specimens
examined, whereas P. albispinus always shows one. The number of molarıform counter-
folds varıes in the remaining species. In P. dimidiatus and P. iheringi this number varies
from two to three, whereas in P. setosus it varıes from one to two. Ihe baculum in ?.
moojeni differs from P. dimidiatus, P. iheringi and P. setosus by the presence of apıcal
wings. From P. albispinus ıt ıs dıstinguished by its smaller size and less developed apical
wings (PEssöA and Reıs 1991d).

Etymology: The name moojeni ıs given to honor Dr. JoAO MoOJEn, whose outstand-
ing and pioneer work laid the foundations for the study of the systematics and evolution of
the genus Proechimys.

A new species of Spiny rat genus Proechimys, subgenus Trinomys 43

Fig. 3. Dorsal, ventral, and lateral views of the skull of the holotype of Proechimys moojeni (MN
13380)

Discussion

In his detailed systematic analysis of the genus Proechimys, MOOJEN (1948) defined the
morphological limits of varıation at the subgeneric, specific, and infraspecific levels.
Moojen (1948) employed the thickness and color of arıstiform hairs, the sıze and shape of
the skull, the shape and structure of the incisive foramen, and the number of molarıform
counterfolds to define the limits of varıation between species in the subgenus Zrinomys.
MoojJEn (1948) combined these traits to characterize the species of Trinomys and appa-
rently no single character could uniquely diagnose the species in the subgenus Trinomys.
Nevertheless, close inspection of the shape and structure of the incisive foramen allows the
unambiguous recognition of each species. The premaxilla and the maxilla form a bridge

44 Leila Maria Pessöa, J. A. de Oliveira and S. F. dos Reis

[ae ir, Sage NE Sea BEE
10mm

Fıg. 5. Ventral (A) and lateral (B) views of the baculum of Proechimys moojeni. The distal part is put to
the top (ventral view) and to the left (lateral view)

that crosses the incisive foramen longitudinally. The premaxillary part ıs always well
developed, whereas the degree of development of the maxillary part shows considerable
variation (MOOJENn 1948). A complete vomerine sheath occurs when the premaxillary and
maxillary parts meet. In P. dimidiatus the vomerine sheath is complete and the maxillary
part is wide and well developed. In P. iheringi the vomerine sheath can be either complete
or incomplete with a short maxillary part. The vomerine sheath is complete in P. setosus
and P. albispinus. The maxillary part ıs short and slender in ?. setosus. The premaxillary
part ot the vomerine sheath in P. albispinus ıs on a level lower than that of the maxillary

A new species of Spiny rat genus Proechimys, subgenus Trinomys 45

Fig. 6. Representative incisive foramına of species of the subgenus Trinomys, genus Proechimys.
A: P. moojeni; B: P. dimidiatus; C: P. iheringi; D: P. setosus; E: P. albispinus

part, which is keeled. In P. moojeni the vomerine sheath is incomplete wıth a short
maxillary part.

Recent studies have shown that bacular morphology can also be used to diagnose
species of the subgenus Trinomys (PessöA and Reıs 1991d). Although several morphologi-
cal characters have been combined to characterize the species of Trinomys, the shape and
structure of the incisive foramen and the sıze and shape of the baculum are good characters
to define species at the morphological level in this subgenus.

Acknowledgements

We thank Dr. U. CaramascaHı, Departamento de Vertebrados, Measen Nacional, Rio de Janeiro, Drs.
P.E. Vanzorını and R.R. SPIEKER, Museu de Zoologia, Universidade de Säo Paulo, SP, and Dr.
G.A.B. pa Fonseca and G. HERRMANN, Departamento de Zoologia da Universidade Federal de

46 Leila Maria Pessöa, J. A. de Oliveira and S. F. dos Reis

Minas Gerais, for allowing access to specimens under their care. We are thankful to Dr. G. SHEPHERD
for revising the English version of the manuscript. We are also indebted to J. R. SOMERA for the
drawings. This research has been supported by grants from Conselho Nacional de Desenvolvimento
Cientifico e Tecnolögico (CNPq), Fundagäo de Amparo ä Pesquisa do Estado do Rio de Janeiro (E-
29/170.339/90), Fundagäo de Amparo a Pesquisa do Estado de Säo Paulo (88/2237-4, 89/0772-1, 89/
3405-0). Work by JAO and SFR was supported by graduate and research fellowships from CNPg,
respectively. LMP is partially supported by a fellowship from Programa de Incentivo A Capacitacäo
Docente (UFR]J).

Zusammenfassung

Eine neue Art von Stachelratten des Genus Proechimys, Subgenus Trinomys (Rodentia: Echimyidae)

Beschrieben wird eine neue Art der Stachelratten, Proechimys (Trinomys) moojeni. Die Typenserie
umfaßt sieben Exemplare von Conceigäo do Mato Dentro aus dem Staat Minas Gerais in Südost-
Brasilien.

Kennzeichnend sind vor allem lange und hinten breite Foramina incisiva sowie ein Baculum mit
schwach entwickelten apikalen Flügeln. Außerdem unterscheidet sich die Art von den anderen, bisher
bekannten Proechimys-Arten ın der Fellfärbung, in der Zahnmorphologie und weiteren Merkmalen
des Schädels und des Baculums.

Literature

MOOJEN, J. (1948): Speciation ın Brazilian spiny rats (Genus Proechimys, Family Echimyidae). Univ.
Kans. Publ., Mus. Nat. Hist. 1, 301-406.

PEssöA, L.M. (1989): Diferenciagäo craniana infraespecifica em Proechimys iheringi Thomas e P.
dimidiatus (Günther). Unpubl. MSc. diss. Univ. Federal Rio de Janeiro.

PEssöA, L. M.; Reıs, $. F. (1990): Geographic varıatıion in Proechimys dimidiatus (Günther). Zool.
Anz. 225, 383-390.

— — (1991a): Cranial infraspecific differentiation in Proechimys iheringi Thomas (Rodentia:
Echimyidae). Z. Säugetierkunde 56, 3440.

— — (1991b): The contribution of cranıal indeterminate growth to nongeographic variation in adult
Proechimys albispinus. Z. Säugetierkunde 56, 219-224.

— — (1991c): Natural selection, morphologic divergence and phenotypic evolution in Proechimys
dimidiatus (Rodentia: Echimyidae). Brazil. J. Genetics 14, 705-711.

— — (1991d): Bacular variation in the subgenus Trinomys, genus Proechimys (Rodentia: Echi-
myıdae). Z. Säugetierkunde 57, (in press).

Reıs, S. F.; PEssöA, L. M.; Borpin, B. (1991): Cranıal phenotypic evolution in Proechimys iheringi
(Rodentia: Echimyidae). Zoologica Scripta (in press).

Reıs, $.F.; PessöA, L. M.; Strauss, R.E. (1990): Application of size-free canonıcal discriminant
analysis to studies of geographic differentiation. Brazil. J. Genetics 13, 509-520.

Rınaway, R. (1912): Color standards and color nomenclature. Washington: Published by the author.

Authors’ addresses: LeıLa Marıa PEssöA, Departamento de Zoologia, IB, Universidade Federal do
Rio de Janeiro, 21941, Rıo de Janeiro, RJ, Brazil; JoAO A. DE OLIVEIRA,
Departamento de Vertebrados, Museu Nacional, 20942, Rio de Janeiro, R],
Brazil; SERGIO F. Dos Reıs, Departamento de Parasitologia, IB, Universidade
Estadual de Campinas, 13081, Campinas, SP, Brazil

Z. Säugetierkunde 57 (1992) 47-55
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Habitat relations in sympatric populations of Ctenomys australis
and Ctenomys talarum (Rodentia, Octodontidae)
in a natural grassland

By Vıvıana M. CoMPARATORE, MONICA AGNUSDEI, and CRISTINA BUscH

Departamento de Biologia, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar
del Plata, Mar del Plata, Argentina

Receipt of Ms. 3. 6. 1991
Acceptance of Ms. 26. 9. 1991

Abstract

Studied the relationship between anımal spatial distribution of two sympatric populations of “tuco-
tucos” (Ctenomys australis and Ctenomys talarum) in Necochea (Buenos Aires Province, Argentina),
and certain environmental varıables. The two species occupy different types of soil and vegetation. C.
australis inhabits areas with sparse vegetation, sandy and deep soils, while C. talarum inhabits areas
with dense vegetation, compact and shallow soils. Seasonally, “tuco-tucos” are also associated with
fine grain variables, as observed in autumn, where the total number of anımals, and the number of C.
australis individuals, were positively correlated with the abundance of grasses, perennials, plants with
reserve organs and creeping habıt plants.

Introduction

Biological factors such as interspecific interactions may play an ımportant role in subterra-
nean rodent distribution. There are very few documented cases of sympatry in subterra-
nean rodents (CONTRERAS and REıG 1965; RusseLL 1968; REICHMAN and BAKER 1972;
WırLLıams and BAKER 1976; MouLTon et al. 1983; PEARsSON 1984). VAUGHAN (1967)
suggested only one subterranean niche exists for herbivorous mammals. Subterranean
mammal distribution, although sometimes parapatric, is seldom sympatric, and since
parapatrıc distribution ıs determined by competition, ıt can be predicted that sympatry
could be transitory (MoULTON et al. 1979).

In the Southern Hemisphere, nearly all Ctenomys species (“tuco-tucos”) present an
allopatrice distribution. In Argentina, only two cases of parapatry have been recorded
(PEARSoN 1984; Reıc et al. 1990); and only one case of sympatry was registered between
Ctenomys australis and Ctenomys talarum ın Buenos Aires Province, from Bahia Blanca to
Monte Hermoso, where these two species occupy different soil and vegetation types
(CONTRERAS and ReıG 1965). We discovered that this distribution extends up to Necochea
and that C. australis does not lıve in allopatry in this area. The fact that this situation has
been maintained over a long period (CoNTRERAS and Reıc 1965), the different corporal
sızes between C. australis and C. talarum, and the manıtest spatial segregation between
both species associated with different soil and vegetation types, all suggest that these
populations coexist in sympatry, with non-overlapping niches. Corporal size differences
between populations have been documented by MarızıA et al. (in press), who determined
that C. australis weighs three times C. talarum.

In the present study, the hypothesis was tested that ©. australis and C. talarum occupy
different habitats in the area of sympatry. In addition, it was determined whether different
anımal categories occupy different habitats according to sex, age and reproductive condi-
tions.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5701-047 $ 02.50/0

48 Viviana M. Comparatore, Monica Agnusdei and Cristina Busch

Material and methods

The present study was conducted in a dune natural grassland (VErRvooRsST 1967; CABRERA and
ZarDını 1978) in Necochea district (Buenos Aires Province, Argentina). The sampling period
extended from November 1987 to September 1988. In each season, an area of approximately 2 ha was
selected inside the overlap zone of both species. In the area studied in spring, distribution areas of C.
australis and C. talarum were clearly delimited. In contrast, in summer, autumn and winter, the
spatial distribution of both species ın the chosen areas was more intermingled, showing greater
heterogeneity than ın spring. Vegetation samples and anımals were taken toward the end of each
season (November-December 1987, February-March, May-June and August-September 1988). In
each area, a 10 by 10 m grid was traced. Vegetation samples were extracted systematically each 10 m.
A soil block of 30 cm diameter and 30 cm depth was collected at each sample site. Then, samples were
separated by hand ın each species aerial and subterranean fractions. The material was dried at 80°C,
and the corresponding dry weights were obtained. A sample by species matrix (aerial plus subterra-
nean biomass/species/sample) was constructed for each season. Twenty-four samples were obtained in
spring, 24 in summer, 31 ın autumn and 48 in winter.

Density and spatial distribution of both populations of “tuco-tucos” were estimated in a

sımultaneous study carried out in the same grids,

Table 1. Seasonal densities (individuals/ha) of by capture and extraction of all the animals pre-

and C Holkrum sent in the studied area (Table 1). Animal species,

localization in the grid, age, sex, weight and

According to Marızıa et al. (in press) reproductive condition were registered (MALrzIa

et al. in press). Once during the duration of the

study, soil hardness and soil depth overlying the

calcareous layer were determined randomly.

Glanstralis 7.4 4,5 4.0 4.6 Twenty five measurements of soil hardness and

Elm Klo 127 Wo depth were obtained with a penetrometer and a
steel bar, respectively, in both species’ zones.

To characterize the vegetation, different
Bono attrıbutes relevant to vegetation spatial heterogeneity and plant-anımal interactions were
assigned to the plant species. The bionomic attributes considered were: perennity, presence of reserve
organs, phenology, pilosity, growth form, presence in modified fields, taxonomic class. Besides
ocular observation, the species descriptions of CABRERA and ZARDINI (1978), and LOMBARDO (1982,
1983, 1984) were consulted. With this information, a species by attrıbutes matrıx (floristic matrix) was
created. This matrix was analysed complementing ordination (Principal Component Analysıs, PCA,
Harris, 1975) and classification (Cluster Analysıs, CA, Orlöcı, 1978) techniques so as to describe
species variation and define species groups. The CA was performed with Nearest Neighbor distance
estimator, simple linkage, and 1-Pearson correlation coefficient for sample distances. Table 2 shows a
list of species present in the area grouped according to the analysis just described.

Each seasonal aerıal plus subterranean biomass/species/sample matrix was multiplied by the
floristic matrix, obtaining an attribute/sample matrix. The four seasonal matrices were appended so as
to obtain an annual matrix of data. The importance of each attribute in the samples was also analysed
complementing PCA and CA so as to describe the principal trends of vegetation heterogeneity.
Sample groups were defined at a level of internal similarity > to 80 %.

To determine which vegetation characteristics were associated with anımal distribution, simple
correlations were established between sample positions along the principal axes of ordination and the
total number of captured anımals, the number of C. australis individuals and the number of C.
talarum individuals, at each sample site. Also, seasonal sample groups of vegetation, at each seasonal
analysis, were related to animal categories which occupied such sites. SYSTAT statistical program was
used to analyse data.

Spring Summer Autumn Winter

Results

Figure 1 corresponds to the annual analysis (samples taken in spring, summer, autumn and
winter) and shows the spatial distribution of samples along the first two axes of the PCA
on the samples/attributes matrix. All the vegetation variables included in the analysis had
positive weights in axis 1, most of them having values over 0.7. Then, axis 1 separates
samples with high from samples with low abundance of the plant attributes evaluated, and
thus is interpreted as an index of vegetation coverage and density. According to this
interpretation, the negative and positive extremes of the axis are denominated “sparse
vegetation” and “dense vegetation”, respectively. Samples with sparse vegetation have

Habitat relations in sympatric populations of Ctenomys 49

Table 2. Vegetation groups, according to ordination and classification techniques, from
a dune natural grassland in Necochea district, Buenos Aires Province, Argentina,
where C. australis and C. talarum show an overlap in their distributions

Group Attributes Species
1 Forbs, Annuals, Geranium dissectum
Cool season species, Lepidium bonariense
Pivotal roots, Gamochaeta spicata
Without reserve organs, Stellaria media
Present in modifield fields Mehlotus indicus
Senecio madagascariensis
Medicago minima
Medicago lupulina
2 Forbs, Perennials, Convolvulus hermanniae
Warm season species, Adesmia incana
Pivotal roots Mesembryanthemum sp.
Oenothera mollisima
Achyrocline satureioides
Margyricarpus pinnatus
Ambrosia tennıfolia
Solidago chilensis
3 Forbs and Grasses, Solanum commersonü
Perennials, Hoydrocotyle bonariensis
With reserve organs, Calystelgıa soldanella
Warm season species, Panicum racemosum
Creeping habit Paspalum vaginatum
4 Grasses, Perennials, Agrostis sp.
Glabrous Poa bonariensis
Sporobolus indicus
5 Grasses, Fibrous roots, Bothriochloa laguroides
Without reserve organs, Stipa neesıana
Erect habıt Stipa trichotoma
Bromus sp.
Lolium multiflorum
Poa annua
Hordeum leporinum
Catapodıum rıgidum
Lophochloa phleoides
6 Annuals, Grasses, Cenchrus pauciflorus

Fibrous roots,
Without reserve organs,

Creeping habit

sandy and deep soils (soil hardness 4.1 + 0.9 kg/cm’, and soil depth 80 # 24 cm), while
those with dense vegetation have compact and shallow soils (soil hardness 29.3 # 8.1 kg/
cm’, and soil depth 57 # 27 cm). Axis 2 opposes samples whose species attributes are
typical of modified fields (annuals, cool season cycle, without reserve organs) to samples
whose species attributes are typical of unmodified fields (perennials, creeping habiıt, with
reserve organs). Three groups of samples were defined by CA: 1. Dense vegetation, with
plant attrıbutes characteristic of unmodified fields. 2. Dense vegetation, wıth plant
attrıbutes characteristic of modified fields. 3. Sparse vegetation, with plant attributes
characteristic of modified and unmodified fields.

Total number of animals, as well as number of individuals of both ©. australis and C.
talarum showed a significant correlation (P < 0.05) with sample position along axis 1 of the
PCA. Total number of anımals and number of C. talarum individuals were positively
correlated with the position of dense vegetation samples, and number of C. australıs

50 Viviana M. Comparatore, Monica Agnusdei and Cristina Busch

Modified field
species

Axis 2 (16%)

Unmodified field
species

Axis 1 (59%)

Sparse vegetation Dense vegetation

m C.austalisO OD C.talarum * Both species

Fig. 1. Ordination of vegetation samples along the first two axes of the PCA of the sample/attributes
matrix: Annual analysıs. Values in brackets show the percentage of the variance explained by each
axis. Symbols indicate presence of C. australis, C. talarum, or both species, respectively. Samples
without anımals were excluded to simplify the diagram. Samples were grouped according to aCA on
the referred matrix

individuals was positively correlated with the position of sparse vegetation samples.
According to these results, two habitats were defined:

a. Typical C. talarum area: dense vegetation, compact and shallow soil;

b. Typıcal C. australis area: sparse vegetation, sandy and deep soil.

C. australis had a body weight three times that of C. talarum (males: 425.3 + 19.8 g vs.
131.6 # 17.2 g, and females: 297.7 + 6.8 g vs. 98.7 + 13.52 g) and a lower population
density (5.15 # 0.76 individuals/ha vs. 11.32 + 2.56 indıviduals/ha), Marızıa et al. (in
press).

In the seasonal analysis, as in the annual one, the principal tendency in data variabilıty
(axis 1, PCA) shows a contrast between sparse and dense vegetation (Figs. 2, 3). Except in
autumn, this contrast explains more than 60 % of the total varıance. This shows that two
environmental subsystems are clearly distinguishable. In autumn (axis 1 explains 47 % of
total varıance) the contrast ıs diluted (Fig. 2). The second tendency in autumn data
variability (axıs 2, PCA), as well as ın the annual analysis, marks a contrast between species
attrıbutes typical of unmodified vs. modified fields: grasses, perennials, presence of reserve
organs, and creeping habıt, vs. forbs, annuals, pivotal roots, respectively. Although less
marked, this second contrast also exists during the remainder of the seasons.

The CA of the autumn data shows four groups of vegetation (Fig. 2.): 1. Dense
vegetation, with plant attrıbutes characteristic of unmodified fields. 2. Dense vegetation,
with plant attrıbutes characteristic of modified fields. 3. Sparse vegetation, with plant
attrıbutes characteristic of modified and unmodified fields. 4. Sparse vegetation, mainly
characteristic of unmodified fields.

The CA of the spring data shows two main sample groups (Fig. 3): 1. Dense vegetation.
2. Sparse vegetation. Both vegetation types have plant attributes characteristic of modified
and unmodified fields. Only four samples are not included in the main groups as a

Habitat relations in sympatric populations of Ctenomys Sul

Unmodified
field species _
C. australis
2 -
C. talarum
oo ®
5 1 Both species
N +
Fort 0 Without animals
N
u
= -1

Modified field -3

species -2 -1 Ö 1 2 g A
Sparse vegetation Axis 1 (47%) Dense vegetation

Fıg. 2. Ordination of vegetation samples along the fırst two axes of the PCA of the sample/attributes
matrıx: Autumn analysıs. Values in brackets show the percentage of the variance explained by each
axis. Symbols indicate presence of C. australis, C. talarum, or both species, respectively. Samples
were grouped according to aCA on the referred matrix

Modified fei® =
species C. australis
OD)
2 C. talarum
© ©
= Both species
Sl A
a Without animals
N
2 0
4
Unmodified
field species 2

-2 -1 6 1 2
Sparse vegetation Axis 1 (60 %) Dense vegetation

Fıg. 3. Ordination of vegetation samples along the first two axes of the PCA of the sample/attributes
matrix: Spring analysis. Values in brackets show the percentage of the varıiance explained by each axis.
Symbols indicate presence of C. australis, C. talarum, or both species, respectively. Samples were
grouped according to aCA on the referred matrix

consequence of some characteristics that are atypical or not relevant in the present context.

In spring, the total number of animals was significantly correlated (P < 0.05) with dense
vegetation samples, and in autumn with samples that had greater abundance of grasses,
perennials, presence of reserve organs and creeping habit. In summer and winter, no
significant correlation was found between the total number of anımals and vegetation
characteristics.

52 Viviana M. Comparatore, Monica Agnusdei and Cristina Busch

In spring and winter, the distribution of C©. talarum is more restricted to dense
vegetation areas (the number of C. talarum individuals showed a significant correlation
with position of samples along axis 1, P < 0.05), while in autumn and summer its
distribution is more dispersed. On the contrary, the distribution of C. australis is more
restrained in autumn (the number of C. australis individuals showed a significant correla-
tion with the position of samples that have greater abundance of grasses, perennials, plants
with reserve organs and creeping habit, P < 0.05) and in summer (significant correlation
with the position of samples that have greater abundance of forbs, glabrous plants, and
plants wıth pıvotal roots, P < 0.05), while in spring and winter its distribution shows a
greater dispersion.

In Figure 4, anımal species and anımal category distribution was superimposed on to
sample distribution along axes 1 and 2 of the PCA on the autumn sample/attribute matrix

6)
en C. talarum 3 -
Unmodified oz | C. australis
field species 3
F fe C. talarum
1:9 WG e m) *
“ EErum Both species
z +
x Without animals
U 0
2
-1.5
Without animals 2
Modified field
species
-3 -1.5 (6) 1-5 3 4.5
Axis 1 (47%)
Sparse vegetation Dense vegetation

Fig. 4. Ordination of vegetation samples along the first two axes of the PCA of the sample/attributes
matrıx: Autumn analysıs and its relation with anımal species and categories. Values in brackets show
the percentage of the varıance explained by each axis. Samples were grouped according to aCA on the
referred matrix. When a vegetation sample group had several anımal categories, subdivisions with
dotted lines were made. C. australis group: 100% adults; 20 % males; Adult mean weight = 337 g +
61; C. talarum 1: 67 % adults (60 % males); 33 % juveniles (100 % females); Adult mean weight = 119
g + 21; C. talarum 2: 67 % adults (100 % males); 33 % juveniles (100 % females); Adult mean weight
=122g + 17; C. talarum 3: 80% adults (100 % males); 20 % juveniles (100 % females); Adult mean
weight = 128 g + 20; C. talarum 4: 83% adults (60 % males); 17 % juveniles (100 % females); Adult
mean body weight = 117g # 26

(Fig. 2). The spatial distribution of the different anımal categories was associated with the
existence of vegetation sample groups. Four sample groups with the presence of C.
talarum, one group with the presence of C. australis, and three groups without animals,
were defined (Fig. 4). A decrease in the percentage of juveniles and an increase in the
percentage of males, was observed through groups 1 to 3 of C. talarum. C. talarum adult
females are only found in groups 1 and 4, whose vegetation presents the greater differences
to those of the C. australis group. Samples with the presence of C. australis and C. talarum
group 3, which is included in the C. australis area, practically do not have annual species,
with pivotal roots, present in modified fields. A vegetation gradient is observed through C.

Habitat relations in sympatric populations of Ctenomys 53

talarum groups 1, 2 and 3, where grasses, perennials, plants with reserve organs and
creeping habit, become increasingly abundant. This association between anımal categories
and vegetation was not observed in the remaining seasons.

Discussion

The principal tendency ın annual and seasonal data varıability shows a contrast between
sparse and dense vegetation, as COMPARATORE et al. (1991) observed in an allopatric
population of C. talarum ın a natural grassland in Mar de Cobo district (Buenos Aires
Province, Argentina). In the annual analysıs, the positive correlation (P < 0.05) between
the total number of anımals and the position of samples along axis 1 (dense vegetation)
could be due to the greater number of C. talarum individuals studied (78 anımals)
compared to C. australıs (38 anımals). This difference ıs related to the greater density of the
C. talarum population in the study site than that of ©. australis, as noted previously. The
results indicate that C. australis generally concentrates in zones with sparse vegetation,
while C. talarum, although present in zones with sparse vegetation, concentrates in those
with dense vegetation (Fig. 1). Sparse vegetation ıs associated with sandy and deep soils,
having low water retention, while dense vegetation is associated with compact and shallow
soils, having higher water retention than the former. These results confirm the hypothesis
that subterranean rodent populations can coexist in sympatry by separating niches. This
confirms CONTRERAS and ReıG’s (1965) observations on the same species.

Moreover, the studied sympatric populations greatly differ in their corporal sizes. C.
talarum adult weight is three times smaller than that of C. australis (Marızıa et al. in press).
Similarly, McNaBg (1966) observed the greater sized species of pocket gopher has narrower
soil tolerances, requiring looser and deeper soils. The smaller species can occupy sandy and
deep soils in areas where the larger species ıs not found, but if the latter one ıs present, the
former would be displaced to marginal and shallower soils. The correlation between the
pocket gopher body size and soil texture may be the consequence of a negative correlation
between body size and burrow temperature, and therefore be related to thermoregulatory
adaptations (McNAB 1966). On the contrary, VLEcK (1979) based this correlation on
energetic adaptatıions. Nevertheless, McNaß’s (1966) and VLEckK’s (1979) explanations are
not mutually exclusive. BEsTt (1973) studied the ecology and distribution of three genera of
pocket gophers and found the largest species presented the most limited distribution and
the broadest range of soil types. The obtained results suggest C. talarum has no environ-
mental limitations to occupy typical areas of C. australis. When the latter ıs absent, the
spatial occupation of C. talarum would be more general. Studying an allopatric population
of C. talarum ın Mar de Cobo district, Buenos Aires Province, Argentina (COMPARATORE
et al. 1991), animals occupied soils with hardness varying from 7 to 52 kg/cm?. On the
contrary, C. australis has physiological constraints (BuscH 1989), due to ıts greater body
sıze, which impede the occupation by this species of the typical C. talarum area.

Vegetation characteristics, where anımal species were studied, vary throughout the
year. Anımal spatial distribution toward the end of spring, is related to the density of
vegetation, and toward the end of autumn to the presence of grasses, perennials, presence
of reserve organs and creeping habit. This suggests that toward the end of autumn, when
vegetation aerıal productivity is low, the animals tend to construct feeding tunnels toward
areas where the mentioned attrıbutes characterize the vegetation. Most of these plants are
green at this time of the year. The results indicate that animals avoıd areas with an
abundance of annuals, plants with pivotal roots, plants present in modified fields and
forbs, which are dry at this time of the year. Conversely, in spring, when vegetation aerial
productivity is high, anımals prefer areas with dense vegetation wıth much green material
available. Furthermore, in autumn and winter, as a consequence of the lower availability of

54 Viviana M. Comparatore, Monica Agnusdei and Cristina Busch

aerial biomass, it would be expected that the percentage of vegetation in the subterranean
fraction of animal dıets would be greater than ın spring and summer. This is in accordance
with our results on diet preferences of these anımals.

In autumn and summer, distribution of C. talarum shows greater dispersion. In
contrast, distribution of C. australis shows a greater dispersion in spring and winter. These
results could be related to the density peaks of each species (Marızıa et al. in press), the
density peak of C. talarum being in May-June (autumn, where its occurrence is less
restricted) and that of C. australis in November-December (spring, also coincident with its
less restricted distribution).

Results of summer anımal capture (Mar1z1a et al. in press) were unexpected as far as the
type of soil was concerned, since only in this season was C. talarum captured in sandy
soils. The scarcity of C. australis in the summer study site could be explained by the
existence of a compact soil barrier that limited its ingress from sandy soil areas where this
species was present in high density. In this condition, C. talarum occupied both its typical
area and that of C. australis. This supports what was stated above that the distribution of
C. talarum ıs not limited by soil hardness in thıs area.

In autumn, it could be observed that anımal category distribution (juveniles, females,
males) varıes concomitantly with the vegetation gradient. No similar relationship was
detected for other seasons, thus suggesting that during certain periods of the year other
factors, such as social behavior or predation, may be stronger determinants of anımal
distribution.

In conclusion, these sympatric species occupy area of differing types of soil and
vegetation. C. australis inhabits areas with sparse vegetation, sandy and deep soils, while
C. talarum inhabits zones with dense vegetation, and compact and shallow soils. Season-
ally, C. australis and C. talarum show a complementation in their spatial distribution. C.
australis has a greater dispersion in spring and winter, and a greater restriction in summer
and autumn. C. talarum has a greater dispersion in summer and autumn, and a greater
restriction in spring and winter. “Tuco-tucos” are also associated with fine grain variables
as observed in autumn, where the total number of anımals, and the number of ©. australıs
individuals, were positively correlated with the samples that had abundance of grasses,
perennials, plants with reserve organs and creeping habıt plants. The data suggest that
other factors, such as social behavior or predation, may play an important role in anımal
spatial distribution.

Acknowledgements

We wish to thank “Grupo Pasturas, Unidad Integrada Facultad de Ciencias Agrarias, Universidad
Nacional de Mar del Plata, y EEA INTA Balcarce” for the use of the computer programs. For many
helpful discussions we thank Dr. Marıa SıLvıa CıD and Dr. Osvarpo Reıc. Financıal assistance was
provided by CONICET, PID No 3-104,000.

Zusammenfassung

Habitatbeziehungen bei sympatrisch lebenden Populationen von Ctenomys australis und Ctenomys
talarum (Rodentia, Octodontidae) in natürlichem Grasland

Untersucht wurde die Raumverteilung zweier sympatrisch lebender Populationen von Tukotukos (C.
australis und C. talarum) in Abhängigkeit von Umgebungsveränderlichen in der Nähe von Necochea
in der Provinz Buenos Aires, Argentinien. Beide Tierarten leben in Gebieten mit verschiedenen
Boden- und Vegetationsarten. C. australis bewohnt Gebiete mit wenig Vegetation und sandigem,
tiefen Boden, während C. talarum Gebiete mit dichter Vegetation und kompaktem, flachgrundigem
Boden bewohnt. Die Tukotuko-Populationen wurden auch in Bezug auf andere Variable untersucht:
Es wurde im Herbst beobachtet, daß die Anzahl von Tukotukos, insbesondere C. australis, positiv
mit folgenden Variablen korreliert war: Häufigkeit von Gräsern, ganzjährigen Pflanzen, Pflanzen mit
Reserveorganen und von am Boden entlangwachsenden Pflanzen.

Habitat relations in sympatric populations of Ctenomys 35)

Literature

Best, T. L. (1973): Ecological separation of three genera of pocket gophers (Geomyidae). Ecology 54,
1311-1319.

BuscH, C. (1989): Metabolic rate and thermoregulation in two species of tuco-tuco, Ctenomys
talarum and Ctenomys australis (Caviomorpha, Octodontidae). Biochem. Physiol. 93, 345-347.

CABRERA, A. L.; ZARDINI, E. M. (1978): Manual de la Flora de los alrededores de Buenos Aires.
Argentina: Acme.

COMPARATORE, V. M.; MaceIrA, N. O.; Busch, C. (1991): Habitat relations in Ctenomys talarum
(Caviomorpha, Octodontidae) in a natural grassland. Z. Säugetierkunde 56, 112-118.

CONTRERASs, J. R.; REIG, ©. A. (1965): Datos sobre la distribuciön del genero Ctenomys (Rodenta:
Octodontidae) en la zona costera de la Provincia de Buenos Aires entre Necochea y Bahia Blanca.
Physis 25, 169-186.

Harrıs, R. H. (1975): A prımer of multivariate statistics. London: Academic Press.

LOMBARDO, A. (1982): Flora Montevidensis. Tomo 1: Uruguay: Intendencia Municipal de Mon-

tevideo.

— (1983). Flora Montevidensis. Tomo 2: Gamopetalas. Uruguay: Intendencia Municipal de Mon-
tevideo.

— (1984): Flora Montevidensis. Tomo 3: Monocotiledöneas. Uruguay: Intendencia Municipal de
Montevideo.

Marızıa, A. 1I.; VassaLLo, A. I.; Busch, C. (1992): Population and habitat characteristics of two
sympatric species of Ctenomys (Rodentia: Octodontidae). Acta Theriol. (in press).

McNAas, B. K. (1966): The metabolism of fossorial rodents: a study of convergence. Ecology 47,
712-733.

MourLTton, M. P.; CHOATE, J. R.; BisseELL, $. J. (1979): Sympatry of pocket gophers on Mesa de Maya,
Colorado. Transactions of the Kansas Academy of Sciences 82, 194-195.

— — — (1983): Biogeographic relationships of pocket gophers in southeastern Colorado. South-
west. Nat. 28, 53-60.

Orröcr, L. (1978): Multivariate analysis in vegetation research. The Hague: Dr. W. Junk Publ.

PEARson, O. P. (1984): Taxonomy and natural history of some fossorial rodents of Patagonia,
southern Argentina. J. Zool., London 202, 225-237.
REICHMANn, O. ]J.; BAKER, R. J. (1982): Distribution and movements of two species of pocket gophers
(Geomyidae) in an area of sympatry in the Davis Mountains, Texas. J. Mammalogy 53, 21-33.
Reıc, ©. A.; Busch, C.; ORTELLS, M. O.; CoNTRERAS, J. R. (1990): An overview of evolution,
systematics, population biology, cytogenetics, molecular biology and speciation in Ctenomys. In:
Evolution of Subterranean mammals at the Organismal and Molecular Levels. Ed. by E. Nevo and
O. A. ReEıs New York: Alan R. Liss. pp. 71-96.

RusseLL, R. J. (1968): Revision of pocket gophers of the genus Pappogeomys. Univ. Kansas Publ.,
Mus. Nat. Hist. 16, 581-776.

VaucHan, T. A. (1967): Two parapatric species of pocket gophers. Evolution 21, 148-158.

VERVOOBRST, F. (1967): Las comunidades vegetales de la Depresiön del Salado. Serie Fitogeogräfica N
7. INTA.

VLEcCK, D. (1979): The energy cost of burrowing by the pocket gopher Thomomys bottae. Physiol.
7700552122255:

WILLIAMS, $. L.; BAKER, R. ]J. (1976): Vagility and local movements of pocket gophers (Geomyidae:
Rodentia). Am. Midl. Nat. 96, 303-316.

Authors’ address: VIVIANA MARTA COMPARATORE, MÖNICA AGNUSDEI and CRISTINA BUSCH, Depar-
tamento de Biologia, Facultad de Ciencias Exactas y Naturales, Universidad
Nacional de Mar del Plata, C.C. 1245, (7600) Mar del Plata, Argentina

Z. Säugetierkunde 57 (1992) 56-57
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

WAISSENSCENEPEITCETESKSEIR ZI TEE DE SEIN GEN

Nachweis der Alpenspitzmaus Sorex alpinus (Schinz, 1837)
im Naturschutzgebiet Seeholz am Ammersee

Von BıRrGITT KLETTENHEIMER und M. SALAMON

Eingang des Ms. 26. 8. 1991
Annahme des Ms. 26. 9. 1991

Die Alpenspitzmaus (Sorex alpınus) gilt als montanes Element und stellt gleichzeitig ein
präglazıales Relikt in europäischen Gebirgen dar. Wie bereits durch einige Funde bestätigt
(KAHMAnn 1952; SPITZENBERGER 1978), kann die Alpenspitzmaus an günstigen klimati-
schen Standorten auch in tieferen Lagen (200-500 m) vorkommen. Diese Populationen
stellen jedoch von den montan-alpinen Vorkommen der Alpen nahezu getrennte Vorkom-
men dar.

Im bayerischen Voralpenland konnte die Alpenspitzmaus bisher nur im Bereich von
Kochel (605 m ü. NN) und von Unterjoch (1013 m u. NN) (KaAHmaAnn 1952) nachgewie-
sen werden. Diese Funde bilden die nördlichen Randpunkte des heutigen Verbreitungs-
kerns.

Nördlich dieses Verbreitungskerns sind vermutlich voneinander isolierte Vorkommen
ım Schwarzwald (LöHRL 1936), ım Harz (SCHULZE 1887; HAENSEL und WALTHER 1969),
in der Schwäbischen Alb (LöHrr 1969), in der Rhön (Pırper 1973; FELTEN 1984), im
Fichtelgebirge (KaHMmAnn 1952) sowie ın der Oberlausitz (AnsoRGE und FRANKE 1981)
bekannt.

Das Naturschutzgebiet Seeholz (553 m ü. NN) umfaßt ein 97 ha großes Gebiet am
Westufer des Ammersees ım Landkreis Landsberg am Lech. Auf den Tonablagerungen des
spätwürmeiszeitlichen Sees ıst ein Eichen-Hainbuchen-Wald vorherrschend, der seewärts
in Weiden-Uferwald übergeht. In Senken und feuchten Dellen finden sich auch krautreiche
Erlen und Erlen-Eschen-Bestände. Zwei streckenweise sehr stark mäandrierende Bäche
mit abgeschnittenen Bachschlingen bilden eine Anzahl von Altarmtümpeln.

In diesem Gebiet wiesen wir ım August 1990 im Rahmen einer Kleinsäugererhebung die
Alpenspitzmaus (Sorex alpınus) nach.

Bei dem gefangenen Individuum handelte es sich um ein adultes Männchen mit einem
Körpergewicht von 6 g. Körpermafse: KR-Länge 75 mm, Schw.-Länge 60 mm, HF-Länge
14,3 mm. Am Schädel und am Unterkiefer wurden folgende Maße abgenommen (Meß-
strecken nach KAHMAnN und VEsMmanIs 1974): Condylobasal-Länge 18,55 mm, Schädel-
kapsel-Breite 9,5 mm, obere Zahnreihen-Länge 9,3 mm, maximale Breite über M? 5,1 mm,
Interorbital-Breite 4,5 mm, Condylar-Länge 9,7 mm, untere Zahnreihen-Länge 5,7 mm,
Coronar-Höhe 4,3 mm, Postcoronar-Höhe 2,4 mm.

Diese Daten entsprechen den von SPITZENBERGER (1990) durchgeführten Messungen
über die Schädelmaße der Populationen der Ostalpen.

Nach SPITZENBERGER (1990) bevorzugt Sorex alpinus zwischen 600 und 1700 m langsam
fließendes oder sickerndes Wasser und ist dort am häufigsten anzutreffen, wo sich am
Bachufer dichte Moospolster bilden. Unter 500 m hingegen ist ihr Vorkommen am ehesten
an tief eingeschnittene, schattigkühle Bachschluchten gebunden.

Der Nachweis der Alpenspitzmaus im Naturschutzgebiet Seeholz am Ammersee (553
ü. NN) ist der bislang nördlichste Fund dieser Spezies im Gebiet des Voralpenlandes.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5701-056 $ 02.50/0

Sorex alpinus im Naturschutzgebiet Seeholz am Ammersee 57

Literatur

ANSORGE, H.; FRANKE, R. (1981): Die Alpenspitzmaus, Sorex alpinus Schinz, 1837, in der Oberlau-
sıtz. Abh. Ber. Naturkundemus. Görlitz 55, 45-48.

BOTSCHAFTER, E. (1957): Die Alpenspitzmaus (Sorex alpinus Schinz, 1837) aus niedriger Höhenlage
im Randgebiet des Bayerischen Waldes. Säugetierkdl. Mitt. 5, 28-30.

FELTEn, H. (1984): Zur Verbreitung der Alpenspitzmaus in deutschen Mittelgebirgen. Natur Museum
114, 50-54.

HaENnSEL, J.; WALTHER, H. (1969): Neues Fundgebiet der Alpenspitzmaus Sorex alpinus hercynicus
(Miller, 1909) ım Harz. Säugetierkdl. Mitt. 17, 119-120.

Kaumann, H. (1952): Beiträge zur Kenntnis der Säugetierfauna ın Bayern. Ber. naturf. Ges.
Augsburg 5, 147-170.

KAHMAnNn, H.; VESMaANISs, I. E. (1974): Morphometrische Untersuchungen an Wimperspitzmäusen
(Crocidura). 1. Gartenspitzmaus Crocidura suaveolens (Pallas, 1811) auf Menorca. Säugetierkdl.
Mitt. 22, 313-324.

LöHrtı, H. (1936): Ein neuer Fundort der Alpenspitzmaus (Sorex alpinus Schinz) und Bemerkungen
über die Systematik der Art. Zool. Anz. 114, 221-223.

— (1969): Die Alpenspitzmaus (Sorex alpinus Schinz) erneut für die Schwäbische Alb nachgewiesen.
Jh. Ver. vaterl. Naturk. Württemberg 124, 280-281.

PıepER, H. (1973): Die Alpenspitzmaus, Sorex alpınus Schinz 1837, ın der Rhön (Mammalıa,
Soricidae). Beitr. Naturk. Osthessen 157-160.

SCHULZE, E. (1887): Sorex alpınus am Brocken. Z. Naturwiss. 60, 187.

SPITZENBERGER, FRIEDERIKE (1978): Die Alpenspitzmaus (Sorex alpınus Schinz). Mammalıa austriaca
1. Mitt. Abt. Zool. Landesmus. Joanneum 7, 145-162.

— (1990): Die Alpenspitzmaus. In: Handbuch der Säugetiere Europas. Band 3: Insektenfresser,
Herrentiere. Hrsg. von J. NIETHAMMER und F. Krapp. Wiesbaden: Aula-Verlag. Pp. 295-312.

Anschrift der Verfasser: Dipl.-Biol. BırcITT KLETTENHEIMER und Dipl.-Biol. MARIO SALAMON,
Oberländerstr. 31, W-8000 München 70, FRG

Z. Säugetierkunde 57 (1992) 58-59
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Vorkommen der Mönchsrobbe Monachus monachus auf Sal
(Kapverdische Inseln)

Von R. KinZELBACH und J. BOESSNECK f

Institut für Zoologie, Technische Universität, Darmstadt

Eingang des Ms. 12. 6. 1991
Annahme des Ms. 26. 9. 1991

Die Mönchsrobbe Monachus monachus (Hermann, 1779) bewohnte ursprünglich weite
Teile des Mittelmeeres und die südlich anschließende atlantische Küste Nordafrikas bis
zum Kap Blanc bzw. bis zum Banc d’Arguin in Mauretanien. Darüber hinaus sind bis in
jüngste Zeit Vorkommen von Madeira und den Kanarischen Inseln bekannt. Die Bestände
sind heute teils erloschen, teils stark ausgedünnt. Der Gesamtbestand soll weniger als 500
Exemplare umfassen (MARCHESssAUX 1990).

Von den Kapverdischen Inseln war die Mönchsrobbe noch nicht bekannt. Daher
erscheint der nachstehende Befund mitteilenswert.

Bei einem Aufenthalt auf der Insel Sal (Repüblica de Cabo Verde) fand der Erstautor am
3.5. 1990 mehrere Skelette von Robben, die vom Zweitautor als der Mönchsrobbe zu-
gehörig determiniert wurden.

Der Fundort liegt im äußersten Südosten von Sal zwischen den Kaps Ponta Jalunca und
Ponta Braco de Sirena (Chiffre KI-AF-1990/07). Um eine kleine Bucht sind abwechselnd
Sandstrand, Blockgründe und kleine Basaltkliffe mit Grotten gelegen. Im oberen Spülsaum
lagen innerhalb einer Küstenstrecke von ca. 500 m mindestens vier verstreute Skelette. Nur
von einem Knochenhaufen wurden stichprobenhaft Knochen mitgenommen, die nachträg-
lich zwei wahrscheinlich zusammengehörigen Individuen zugewiesen werden konnten.

Haut und Weichteile fehlten völlig, ebenso eine sichtbare Verfärbung des umgebenden
Bodens. Der Bleichungs- und Erhaltungszustand ließ ebenso auf längere Exposition
schließen. Wahrscheinlich waren die Tiere im Spätsommer oder Frühherbst 1989 verendet,
vermutlich bald nach der Wurftzeit.

Mit einer nahebei gelegenen Fundstätte fossiler Vögel (BoEssnEcK und KINZELBACH
1992) besteht oftensichtlich kein zeitlicher oder sachlicher Zusammenhang.

Entnommen wurden insgesamt 12-13 Knochenstücke, die mindestens zwei Tieren
zugehören, einem erwachsenen und einem sehr jungen Tier. Adult: 5 Hirnschädelstücke
und 1 Nasenbeinpaar. Infantil: 1 Ulna-Corpus und 1 proximales Radiusende, 2 Rippen
und 1 ventrales Rippenende, 1 Wirbelkörper (dessen Artbestimmung unsicher ist). Eine
Zuordnung zu Sub-Populationen nach van BREE (1978) war noch nicht möglich.

Die Belegstücke befinden sich in der Sammlung des Instituts für Palaeoanatomıe,
Domestikationsforschung und Geschichte der Tiermedizin an der Universität München.

Die Knochen wurden an der Oberfläche im oberen (Winter-)Spülsaum zusammen mit
anderem rezenten Anwurf gefunden. Ihr Erhaltungszustand läßt auf eine Exposition über
ein Winterhalbjahr hinweg schließen. Bei wesentlich höherem Alter wären sie unter der
starken Einwirkung von Sonne, Sandtreiben und Gischt stärker zerfallen und verstreut
gewesen. Dies und die potentielle Zuweisung eng beisammen liegender Knochen zu einem
Mutter- und einem Jungtier weisen darauf hin, daf die Tiere 1989 noch lebten und daß sie
wohl nicht von weither als Kadaver angedriftet sind. Sie lagerten möglicherweise nahe der
Fundstelle und kamen hier oder unweit der Fundstelle im Meer zu Tode.

Für die Existenz von Robben auf Sal in jüngerer Zeit spricht der Umstand, daß ein mit

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5701-058 $ 02.50/0

Vorkommen der Mönchsrobbe Monachus monachus auf Sal 59

Abbildungen nach Tieren befragter einheimischer Fischer Robben kannte; angeblich hatte
er sie jedoch schon lange nicht mehr gesehen. Weiterhin bezieht sich der Name des
benachbarten Kaps „Ponta Braco de Sirena“ („Kap der Sirenengrotte“) vielleicht auf die
Mönchsrobbe, da „sirena“ regional auf Robben angewendet wird. Weiterhin gibt es
folgende Angabe in MATTHEws (1989, S. 253): „Manchmal werden (von Sal) kurze Törns
nach Boa Vista unternommen, bei denen es nicht ungewöhnlich ist, Tümmler, große
Robben und Thunfische zu sehen.“ Leider konnte der Autor noch nicht näher nach seinen
Beobachtungen befragt werden.

Literatur

BoOESSNECK, J.; KINZELBACH, R. (1992): Ein prähistorischer Brutplatz von Seevögeln auf der Insel Sal
(Kapverden). J. Ornithologie (im Druck).

BrEE, P. H. J. van (1978): Notes on differences between monk seals from the Atlantic and the Western
Mediterranean. In: The Mediterranean Monk Seal. Ed. by K. Ronarp and R. Ducuy. UNEP
Technical Series 1, 99. New York: Pergamon Press.

MARCHEssaux, D. (1990): Distribution et statut des populations du phoque moine Monachus
monachus (HERMANN, 1779). Mammalıa 53, 621-642.

MATTHEws, H. (1989): Stromer’s Praktischer Reiseführer. Kapverdische Inseln. Zürich.

Anschrift des Verfassers: Prof. Dr. RAGNAR KINZELBACH, Institut für Zoologie, Technische Universi-
tät Darmstadt, Schnittspahnstr. 3, W-6100 Darmstadt, FRG

BEKANNTMACHUNG

Einladung

Die 66. Hauptversammlung der Deutschen Gesellschaft für Säugetierkunde e.V. findet
vom Sonntag, den 20. September, bis Donnerstag, den 24. September 1992, in Karlsruhe
statt. Gastgeber ist das Staatliche Museum für Naturkunde.

Sonntag, 20. September:

Montag, 21. September:

Dienstag, 22. September:

Mittwoch, 23. September:

Donnerstag, 24. September:

Freitag, 25. September:

Vorläufiges Programm

Anreise

ab 19.00 Uhr:

9.00 Uhr:

9.30 Uhr:

14.00 Uhr:

15.00 Uhr:
17.00 Uhr:
20.00 Uhr:

9.00 Uhr:

14.30 Uhr:
16.30 Uhr:
19.00 Uhr:
20.00 Uhr:

9.00 Uhr:
14.30 Uhr:
15.45 Uhr:

16.30 Uhr:
20.00 Uhr:

Vorstandssitzung

Zwangsloser Begrüßungsabend ım Restaurant
des Schloßhotels, Bahnhofsplatz 2

Hörsaal der Badischen Landesbibliothek,
Erbprinzenstraße 15

Grußworte und Eröffnung der Tagung durch
den 1. Vorsitzenden

Hauptvortrag und Kurzvorträge zum The-
menschwerpunkt „Paläontologie der Säuge-
tieres

Posterdemonstration im Staatlichen Museum
für Naturkunde, Erbprinzenstraße 13
Kurzvorträge ım Hörsaal Landesbibliothek
Mitgliederversammlung

Empfang durch die Stadt Karlsruhe im Rat-
haus, Marktplatz

Hörsaal Landesbibliothek: Hauptvortrag und
Kurzvorträge zum Themenschwerpunkt „So-
zialverhalten der Säugetiere“

Kurzvorträge

Posterdemonstration im Museum

Führung durch das Museum

Filmabend im Museum

Hörsaal Landesbibliothek: Hauptvortrag und
Kurzvorträge zum Themenschwerpunkt
„Chiroptera“

Kurzvorträge

Posterprämierung und Abschluß des wissen-
schaftlichen Programms

Führung durch den Zoo Karlsruhe
Geselliger Abend im Staatlichen Museum für
Naturkunde

Exkursion zu den Mooren an der Hornisgrin-
de im Nord-Schwarzwald

Arbeitstreffen verschiedener Arbeitsgemein-
schaften

Bekanntmachung 61

Alle Interessenten sind zu dieser Tagung herzlich eingeladen. Falls eine persönliche
Einladung gewünscht wird, wenden Sie sich bitte an den 1. Vorsitzenden, Prof. Dr. U.
ScHMIDT, Zoologisches Institut, Poppelsdorfer Schloß, W-5300 Bonn 1 (Tel. 02 28/
73 54 68; Fax-Nr. 02 28/73 54 58).

Das Programm mit der Vortragsfolge wird den Mitgliedern — auf Anforderung auch
Nichtmitgliedern — rechtzeitig vor der Tagung zugesandt. Außer Beiträgen zu den
genannten Themenschwerpunkten werden auch dieses Mal wieder Vorträge und Posterde-
monstrationen zu anderen Fachgebieten der Säugetierkunde berücksichtigt. Bitte melden
Sie Kurzvorträge (15 Min.) und Posterdemonstrationen möglichst frühzeitig, spätestens
jedoch bis zum 30. April (Ausschlußfrist) beim Geschäftsführer unserer Gesellschaft, Prof.
Dr. H. ERKERT, Zoologisches Institut, Auf der Morgenstelle 28, W-7400 Tübingen (Tel.
0 70 71/29 29 58; Fax: 0 70 71/29 46 34) an.

Mit Fragen zum Tagungsort und zur Organisation wenden Sie sich bitte an Herrn Dr.
R. FLösser, Staatliches Museum für Naturkunde Karlsruhe, Postfach 6209, W-7500
Karlsruhesiz(@lel. 0721/17 51 65; Fax: 07 21/17 51 10).

BUGEBESEREEHIUN GEN

McFArLAnD, D.: Biologie des Verhaltens. Evolution, Physiologie, Psychobiologie. Hrsg.
A. STAHNKE und K. VOGLER. Deutsch von W. DREssENn, V. LAskE und B. NIXDoRF.
531 S., 357 Abb., 12 Tab. Weinheim: VCH Verlag 1989. DM 78,-. ISBN 3-527-26479-5

Dieses Buch ist eine überarbeitete und erweiterte Übersetzung der Originalfassung „Animal Beha-
viour“ von 1985. Es soll die Ergebnisse der Verhaltensforschung übersichtlich darlegen und Studenten
der Biologie und auch der Psychologie zur Einführung und als Studienbegleiter dienen. Vorrangiges
Anliegen des Autoren ist dabei, zwischen diesen beiden Wissenschaften eine Brücke zu schlagen und
moderne, in der evolutiven Entfaltung der Arten begründete Denkansätze der vergleichenden
Ethologie darzustellen.

Im Anschluß an eine kurze Einführung in die Verhaltensforschung ist der Stoff in 3 Teile mit
jeweils wiederum 3 zugeordneten Kapiteln in unterschiedlich gewichtete Abschnitte gegliedert. Die
Hauptteile und Kapitel sind wie folgt überschrieben: 1. Evolution des Verhaltens (Genetik und
Verhalten; natürliche Selektion; Evolution und Sozialverhalten), 2. Mechanismen des Verhaltens
(Wahrnehmung bei Tieren; das Tier und seine Umgebung; Lernen), 3. Komplexes Verhalten
(Instinkt; Entscheidungsfindung bei Tieren; die kognitiven Fähigkeiten der Tiere). Den 9 Kapiteln
vorangestellt sind kurze Einleitungen, in denen die Bedeutung folgender Persönlichkeiten für die
entsprechenden Wissenschaftsbereiche geschildert wird: G. MENDEL, CH. Darwın, R. FISHER; J. P.
VON MÜLLER, C. BERNARD, I. PawLow; K. LORENZ und N. TINBERGEN, K. von FRISCH, E. TOLMANn.
Das Buch ist mit vielen Abbildungen illustriert und von ansprechender großformatiger Aufmachung.

Dieses Konzept der Themenzusammenstellung ist neu und abweichend von anderen deutschspra-
chigen Lehrbüchern. Viele Erkenntnisse der allgemeinen und speziellen Zoologie sind integriert und
dienen zur Erklärung vor allem funktioneller Zusammenhänge. Aus der möglicherweise etwas
konservativen Sicht des Rezensenten ergeben sich jedoch erhebliche Zweifel, nicht an der Bedeutung
der Ethologie als eine zoologische Forschungsrichtung, sondern vielmehr an der Art der Darstellung
biologischer Phänomene und der häufig sehr einseitigen, vor allem wenig kritischen und teleologi-
schen Interpretation evolutiver Prozesse. So kann die Aussage im Geleitwort, daß hier die fleißige
Schar der Bearbeiter Hervorragendes geleistet hat und daß mit fachlicher Umsicht ein auch sprachlich
erfreuliches Werk geschaffen wurde, nicht nachvollzogen werden. Das Buch zeigt viele ungeschickte,
über zweifel- bis zu fehlerhaften Formulierungen. In dieser Hinsicht veranlaßt der deutsche Titel
bereits zum Nachdenken, aber es ist auch von „Elternfürsorge“ (gemeint ist parental care), von
„Sinnesökologie“, von „ungünstigen Lebensräumen“ und von „instrumentellem Lernen“ allein in den
Überschriften die Rede. Die sprachlichen Formulierungen sind besonders in jenen Schilderungen
störend, in denen kausale und nach menschlichen Bewertungen anzustrebende, sinnvolle Entwick-
lungszwänge unterstellt werden. Das unglücklicherweise weit verbreitete Wort Strategie gewinnt in
seiner ursprünglichen Bedeutung unterschwellig an Gewicht, obwohl eingangs mehr ım Sinne einer
genetisch bedingten, selektionsabhängigen Adaptation definiert.

Die sachliche Information ist — zumindest ın weiten Teilen des Buches — ebenfalls geeignet,
Verwirrung auszulösen. Sie ist weder konzentriert noch komprimiert, eher ungeordnet, stellenweise
stark simplifiziert und falsch. Viele triviale und banale Aussagen, zahlreiche Widersprüche, Wieder-
holungen, Abweichungen von der Thematik und langatmig geschilderte, einseitig bewertete Parade-
beispiele der Ethologie wechseln einander ab. Viel theoretischer und abstrakter Balast betont die
Bedeutung der Verhaltensforschung. Über taxonomische Regeln wird hinweggesehen, indem häufig
Arten mit "Gattungsnamen ausgewiesen und deutsche Bezeichnungen für Arten entweder ungebräuch-
lich oder falsch sind. Der Leser lernt ferner eine „Aquifinalität“ ne. jedoch nicht den Unterschied
zur Konvergenz; die „natürliche Auslese wirkt auf die physischen Eigenschaften (den Phänotyp) eines
Individuums, zu denen auch sein Verhalten gehört“, (bleibt der Genotyp verschont?); auf $. 28 ist
Lernen vor Schlupf bzw. Geburt nicht möglich, auf $. 30 hingegen doch: „Dreizehenmöwen haben
viele feindvermeidende Anpassungen anderer Möwen verloren“; eine „evolutionäre Strategie“ ist eine

„Verhaltensanweisung, die im Laufe der Evolution entwickelt wurde“; Ähnlichkeiten von Tieren mit
allen von Vegetation oder von anderen Tieren sind eine „Verhaltensweise, mit denen Tiere
versuchen, ihre Feinde abzuwehren“; auf S. 140 ist das menschliche Gehirn „viermal so groß, wıe es
bei Primaten von ähnlicher Statur zu erwarten wäre“, auf $. 168 nur noch dreimal; „Sinnesrezeptoren
sind spezialisierte Nervenzellen“ mit „einem oder mehreren Axonen“; eine Verkürzung des Muskels
ist nur dann möglich, wenn er an beiden Endpunkten nicht fixiert ist; „Protozoen können kein echtes
Nervensystem ausbilden“ (was ist ein unechtes und warum sollten sie?); Plathelminthen haben ein
Strickleiternervensystem; „zum extrapyramidalen System zählen alle nicht-reflexartigen motorischen
Bahnen, die weder im cortico-spinalen noch im pyramidalen System integriert sind“; ın der „Reihen-
folge Fisch, Reptil, Vogel, Säuger“ gibt es „keine fortschreitende Gehirnvergrößerung“, etc. Eine
Konzentration von trivialen und falschen Aussagen wird auf $. 181 erreicht: „Nicht bei allen
Vertebraten sind die Ohren gleich gebaut. So haben etwa Fische und Wale kein äußeres Ohr. Fische
haben auch kein Mittelohr mit Trommelfell und Gehörknöchelchen. Da das Gewebe der Fische eine

Buchbesprechungen 63

ähnliche Dichte wie Wasser hat, können Vibrationen, die am Kopf eintreffen, direkt zum Innenohr
weitergeleitet werden. Einige Fische verfügen allerdings über einen Mechanismus, der ähnliche
Funktionen erfüllt wie die des Innenohrs. Hierbei handelt es sich um die luftgefüllte Schwimmblase,
die durch eine knöcherne Verbindung zum Innenohr das Hörvermögen gewaltig verbessert. Bei
Amphibien und Reptilien bildet das Trommeltell den äußeren Teil des Ohres. Bei Vögeln gibt es einen
Gehörgang (Meatus acusticus), der von der Körperoberfläche zum Trommeltell führt. Eın stäbchen-
ähnlicher Knochen, die Columella, stellt hier eine Verbindung zur Innenoberfläche des Trommelfells
her und tritt mit dem Steigbügel in Kontakt. Bei den Amphibien und Reptilien bilden diese Knochen
Teile des Kiefers, obwohl bei einigen Arten diese Knochen auch Hörfunktionen ausüben.“ Dem
Abschnitt über das Vertebratengehirn und den Beiträgen über Intelligenz und Hirngröße hätte mehr
Sorgfalt nach gründlicherem Literaturstudium gutgetan. Viele Abbildungen sind überflüssig, da sie
nicht zum Verständnis des Textes beitragen. ä

Der Versuch, Erkenntnisse aus Genetik, Anatomie, Physiologie und Okologie unter ethologi-
schen Aspekten zu subsummieren, ist nicht gelungen. Wenn dieses eine Standortbestimmung der
modernen Ethologie sein soll, dann wurde dieser Disziplin ein schlechter Dienst erwiesen, keine gute
PSttatesie, D. Kruska, Kiel

RönHrs, M.; MEYvER, H. (Hrsg.): Studium Generale. Vorträge zum Thema „Mensch und
Tier“. Bd. VII. Hannover: M. u. H. Schaper 1990. 105 S. DM 19.50. ISBN 3-7944-0162-X

Der vorliegende 7. Band der Serie „Mensch und Tier“ enthält die Vorträge zum Studium Generale,
Hannover im WS 88/89. GRUNERT behandelt das Thema „Geburt und Geburtshilfe“ vergleichend
beim Menschen aus historischer und ethnographischer Sicht und beı Säugetieren in ganzer Variations-
breite. Bısping gibt eine Übersicht zum Thema „Seuchen und Geschichte“, vor allem über die großen
Seuchenzüge von Fleckfieber und Pest, und zeigt deren Einflüsse auf Kultur, Lebensweise und
historisches Geschehen auf. Gleichzeitig wird aber auch darauf hingewiesen, daß der Mensch durch
rasche Änderungen der Lebensweise Auftreten und Ablauf der Seuchen beeinflußt hat. H. MEYER
bringt mit seinem Beitrag „10000 Jahre Schwein gehabt“ einen lesenswerten Beitrag zur Kultur-
geschichte des Hausschweins, seine Herkunft und Bedeutung in Mythos, Sage und Religion. FRANKE
berichtet anhand zahlreicher Abbildungen über Tierbilder auf antiken Münzen mit ausführlichem
Kommentar. OHry legt eine umfangreiche, weit ins Detail reichende Abhandlung über WOoLFRAMS
Parsival vor, die eine umfassende Analyse des Pferdebildes im Hochmittelalter bringt und damit
zugleich einen wesentlichen Beitrag zum Menschenbild liefert. Die differenzierte Bewertung des
Pferdes in jener noch autofreien Zeit — auch als Imponierapparat für seinen Besitzer - ist beachtlich.
Die Veröffentlichung wendet sich an einen größeren Interessentenkreis und kann empfohlen werden.
Zahlreiche Abbildungen illustrieren die meisten Beiträge. D. STARcK, Frankfurt/M.

REICHERT, H.: Neurobiologie. Stuttgart, New York: Georg Thieme Verlag 1990. 391 S.
DM 46,-. ISBN 3 13 745301 1

Die Neurobiologie hat sich zu einem eigenständigen Fach entwickelt. In 9 Kapiteln versucht das
Taschenbuch eine kurze Übersicht über Probleme, Methoden und Ergebnisse dieses Forschungs-
zweigs zu geben. Neben einer Darstellung von Struktur, Ontogenese sowie Erhaltung und Reparatur-
vorgängen an Nervensystemen steht die Besprechung der Funktion des Neurons, der Synapse und der
Neuronenverbände mit ihren Teilsystemen (Motorik, Sensorik, Integration) im Mittelpunkt. Das
Abschlußkapitel befaßt sich mit der Frage von Plastizität und Lernvorgängen.

Dem Kapitel zur vergleichenden Morphologie der Nervensysteme (Kapitel 1) würde man mehr
Raum wünschen, damit auch ein Bezug zu aktuellen Forschungsergebnissen möglich ist. Auch die
Auseinandersetzung mit dem Problem „Lernen“ (Kapitel 9) hätte es verdient, stärker vertieft zu
werden, handelt es sich doch hier um ein zentrales Problem der Neurobiologie, an dem intensiv
gearbeitet wird. Diesen kritischen Punkten steht der größere Teil des Buches entgegen, der zunächst
die zelluläre und molekulare Ebene der Neurobiologie aufarbeitet und dabei gleichermaßen Struktur
und Funktion berücksichtigt. Hier wird eine gute Basis geschaffen, auch der aktuellen Forschung zu
folgen. Die breite Darstellung der Leistungen des Nervensystems in systemhaften Zusammenhängen
verbindet dann eine Fülle von Sachinformationen mit der Präsentation einer Forschungsstrategie, die
für die aktuelle Neurobiologie so typisch ist. Eine didaktisch geschickte Darstellung mit klaren und
aussagekräftigen Abbildungen und einem gut strukturierten Text steigert die Attraktivität des
Taschenbuches, dessen hoher Preis den Weg zu der erklärten Zielgruppe (Studierende) allerdings nicht
leichter machen wird. G. REHKÄMPER,Köln

64 Buchbesprechungen

DITTRicH, L.; RIEKE-MÜLLER, A.: Ein Garten für Menschen und Tiere. 125 Jahre Zoo
Hannover. Hannover: Verlagsgesellschaft Grütter 1990. Format 24,5 x 29,5 cm, 228 S.,
über 200 Abb. DM 49,80. ISBN 3-9801063-2-2

Der Band wurde zum 125jährigen Bestehen des Zoologischen Gartens Hannover von seinem
wissenschaftlichen Leiter, L. DITTRICH, und der Historikerin A. RIEKE-MÜLLER gemeinsam verfaßt.
Er schildert das wechselvolle Schicksal dieser Einrichtung, der von ihr verfolgten Ziele und die den
Garten in Anlage und Bauten, Auswahl, Haltung und Präsentation der Tiere prägenden Anschau-
ungen.

1860 geplant, wurde der Zoo von einem Aktionärsverein mit Unterstützung der Stadt Hannover
ins Leben gerufen und 1865 eröffnet. Die wertvollsten Säugetiere der damals enthaltenen etwa 30
Arten waren zweı ım Kölner Zoo geborene Löwen, ein Bison, zwei Axishirsche und zwei Schwarzbä-
ren. Auch weiße Ratten und eine weiße Maus finden sich auf der Liste, was ım Blick auf die
Entstehung von Laborratte und -maus von Interesse sein mag. Die Unterkünfte der Tiere waren mehr
an romantischen Vorstellungen als an dem Wohlbefinden der Insassen orientiert.

Der Kampf um die Finanzierung unter dem Einfluß von Persönlichkeiten, Parteien, Regierungen
und dem Zustand der Wirtschaft steht im Vordergrund. Politische und weltanschauliche Ideen wirken
sich ebenso aus wie der Fortschritt in Tiermedizin und Ethologie sowie die zunehmende Gefährdung
der Tierwelt in der Natur. Verluste durch Seuchen und Gewinn durch Zucht, Tierfangexpeditionen,
Völkerschauen, aber auch die Aussetzung gefährdeter Arten (Arabische Oryx, Mendes-Antilopen)
werden behandelt, das „Hannoversche Modell“ bei der Reduktion von Gehege-Grenzen wie der
Einfluß der Tierhandelsfirma Ruhe. An Beziehungen zu WILHELM BuscH, HERMANN Löns und
RICHARD GERLACH erinnert die Festschrift. Über dıe wichtigsten Persönlichkeiten aus der Gründer-
zeit findet man kurze biographische Abschnitte.

Aus allem ist eine vielseitige, bunt illustrierte Zoogeschichte entstanden, die mit zahlreichen
Literaturhinweisen und Anmerkungen belegt wird. Der Zoologe würde gern noch mehr über das Auf
und Ab ım Tierbestand, über bemerkenswerte Arten, Zuchterfolge oder biologische Arbeiten an den
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ı-Tov, Y.; Makin, D.; Shalmon, B.: The biology of Pipistrellus bodenheimeri (Microchiroptera) inthe Dead Sea area
Israel. — Die Biologie von Pipistrellus bodenheimeri (Microchiroptera) im Gebiet des Toten Meeres in Israel
\<er, C.; Höhmann-Kröger, Hella; Doyle, G. A.: Social relations in groups of Black-capped capuchin monkeys,
Jebus apella) in captivity: mother-juvenile relations from the second to the fifth year of life. - Soziale Beziehungen
ı Gruppen des Gehaubten Kapuzineraffen (Cebus apella) in Gefangenschaft: Beziehungen zwischen Mutter und
Ingtier vom zweiten bis zum fünften Lebensjahr

de Jong, C. G. van: A morphometric analysis of cranial variation in Holarctic weasels (Mustela nivalis). —
‚lorphometrische Analyse der Schädelvariation beim holarktischen Mauswiesel (Mustela nivalis)
ımares, F.; Delibes, M.: Some physical and population characteristics of Egyptian mongooses (Herpestes
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:söa, Leila M.; Dos Reis, S. F.: Bacular variation in the subgenus Trinomys, genus Proechimys (Rodentia:
chimyidae). — Baculumvariation im Subgenus Trinomys, Genus Proechimys (Rodentia: Echimyidae)

ıpster, Edith R.; Perrin, M. R.; Nuttall, R. J.: Postnatal development of three sympatric small mammal species of
»uthern Africa. - Postnatale Entwicklung bei drei sympatrischen Kleinsäugerarten aus Südafrika

senschaftliche Kurzmitteilungen |
tenbach, I. L.; Fenton, M. B.: Bats from Mana Pools National Park in Zimbabwe and the first record of Eptesicus
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‚der, L.; 'T Hart, L.; Bree, P. J. H. van: Further notes on the pupping period in a recently founded colony of Grey
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kov, G.; Danilkin, A.; Hartl, G. B.: Lack of biochemical-genetic variation in native Sika deer (Cervus nippon
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\Ipine ibex (Capra i. ibex). — Ein Vergleich der genetischen Variabilität beim Nubischen (Capra ibex nubiana) u

eim Alpensteinbock (C. i. ibex) MAY i5 19%
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Z. Säugetierkunde 57 (1992) 65-69
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

The biology of Pipistrellus bodenheimeri (Microchiroptera)
in the Dead Sea area of Israel

By Y. Yom-Tov, D. Makın, and B. SHALMON

Department of Zoology, Tel Aviv University, Ramat Aviv, and
Society for Protection of Nature, Elat, Israel

Receipt of Ms. 4.7. 1991
Acceptance of Ms. 31.10. 1991

Abstract

Collecting data on the biology of Pipistrellus bodenheimeri during a survey of the bats of the Dead Sea
area. This species is a year-round resident, hibernating between October and April. Capture rate
during winter was 5% of the summer rate. Lactating females were found between early May and early
September. Females are significantly heavier and larger than males. The bats feed intensively in the
evening and gain about 15 % of body weight within 2 h.

Introduction

Very little work has been carried out on the biology of any bats ın the Near East (ATALLAH
1977-1978; BaTEs and Harrıson 1989; HArrıson 1984; HARRISON and MARIN 1988;
Maxın 1977; MENDELSSOHN and Yom-Iov 1988; QumsıyEH 1965). Pipistrellus
bodenheimeri was described by Harrıson (1960), and it is found from the Dead Sea area
to Aden. It ıs one of the smallest (less than 3 g) and least known species of its genus, and
one of the smallest bats ın the Palearctic region.

The aım of this study is to report data of the biology of P. bodenheimeri which we
gathered during a survey conducted in the insectivorous bats of the Dead Sea area (Yom-
Ioyzerallg9n)).

Material and methods

Study area

The study area is the western and southern coastal plain of the Dead Sea, a long (about 80 km) and
narrow (about 15 km) salt lake which lies 400 m below sea level. It ıs a desert area, wıth mean annual
precipitation of 50 mm which falls only during winter (November-April). Mean daily temperatures of
16-18°C exist in December-February and 32-34 °C during June-August. Mean minimum monthly
temperature is reached in January (11°C) and mean maximal temperature in July (39°C). Mean
monthly relative humidity fluctuates between 35 % (July) and 50% (January) (climatological data
from JAFFE 1988). The coastal plain borders with high cliffs intersected by dry wadı beds. Several small
oases and agricultural settlements exist along the valley, providing drinking water for wildlife. The
vegetation is savannoid desert vegetation, with Acacıa trees near and in the wadı beds and low bushes
of the plain (Danın 1988).

Survey procedure

The study was conducted between April 1988 and January 1990. We made an effort to visit the area
every 3-4 weeks during winter (November-April) and twice monthly during the rest of the year. Most
visits lasted one day, but during the first summer there were several two-day visits. During the first
summer we sampled various localıties along the western shore of the Dead Sea from Aın Fashkha
36°27'E, 31°44'N (Occupied areas) in the north through the oasis of En Gedi 35°26’E, 31°28’N,
and its environs, Nahal Zeelim 35°23’E, 31°21’N, En Bogeq 35°23’E, 31°10’N, Brechot Navit
35°23’E, 31°07’N and south to Neot Hakikar 35°23’ N, 30°55’ N. We caught bats at night using

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5702-065 $ 02.50/0

66 Y. Yom-Tov, D. Makin, and B. Shalmon

monofilament and other mist nets, erected between vegetation and in open areas. We visited several
caves, mostly in En Gedi area, but also near en Bogeq and Mt. Sdom 35°23’ N, 31°05’ N and tried to
identify bats there by direct observation and by sampling the population by mist nets. We also
observed bats near street lights at varıous settlements along the shore. Several bats were caught by
abruptly waving mist nets towards approaching bats near street lights. After the first summer we
concentrated most of our efforts in Neot Hakikar, where we repetitively erected mist nets, about 30 m
long, parallel to the water line of a 40 m diameter irrigation pond. The nets were kept open from about
30 mın before sunset to at least 3 hours after dark (normally 4-6 hours on average each summer night).
Every individual captured was ıdentified to its species and sex, its forearm measured by a digital
caliper to 0.1 mm accuracy and weighted with Pesola spring balances to 0.1 g accuracy. Age was
determined by examining the degree of ossification of the finger joints (Kunz and AntHonY 1982).
Body condition, pregnancy, lactation and testis size were noted in the anımal released on the spot.

Results and discussion

Pipistrellus bodenheimeri was the most commonly found bat in our survey, with a total of
more than 250 individuals netted. It was netted or observed every month of the year, but
mainly between May and September, indicating that ıt is a resident species. The rate of
capture (average number netted ın 30 m net during 3 hrs at the beginning of an evening) in
the summer was 20 times that of
winter (Fig. 1). At least two
possible explanations may ac-
count for this result: 1. The bats
hibernate between October and
Aprıl and arousal rate during
hibernation 217,500, (:20) gor:
2. during winter there are more
water sources available, and the
bats disperse accordingly. We be-
10 lieve that the first explanation is
correct since the number of bats
hunting near street lights ın wın-
ter ıs smaller by an order of mag-
nıtude than that ın the summer.
MONTH P. bodenheimeri was caught
Fig. 1. The average number of Pipistrellus bodenheimerı even at ambient temperatures of
caught during the year in a 30 m long mist net in a 3-hour 11 °C. We did not find a correla-
period at the beginning of an evening in Neot Hakiıkar tion between ambient tempera-
ture at the nıght of netting and
either the number of species or the number of individuals caught. Neither there was a
correlation between the moon phase and the number of bats caught during the summer
(April-October).

Females (n = 143) were significantly (t = 3.3; p < 0.01) heavier than the males (n = 119;
mean body weight 2.9 and 2.5 g, respectively), and had significantly (t=3.1; p <0.001)
greater forearm length (mean 30.1 and 29.2 mm, respectively). Mean body weight (but not
mean forearm length) fluctuated during the year (Fig. 2), reaching a maximum in May and
a minimum in August. The average high body weight in May was probably due to the
improved food conditions in spring and the combined effect of this and pregnancy ın
females. The decline in average body weight towards August was due to the appearance of
young bats, which are easily distinguishable from the adults by having greyer fur,
especially on the abdomen, and incomplete fusion of the epiphysis in the joints of the
fingers. Young bats formed a large proportion (up to 50%) of the netted sample in July
and August. The first young P. bodenheimeri were caught on 14 June 1989. These were

20

Biology of Pipistrellus bodenheimeri 67

Sol o9E16164 47225728: 92

g

4 145.920 6, 2204, 30,8. 2, rd

BODY WEIGHT,

J F M A M J J A S O N D

Fıg. 2. Body weight (a) of male and female Pipistrellus bodenheimeri caught in the Dead Sea area
during the year. Means, SE and ranges. Sample sizes for samples larger than three are given above the
means

2 females weighing 2.9 and 3.0 g, respectively, with forearms measuring 30.3 and 20.9
mm, respectively; and a male, weighing 1.8 g (the lightest P. bodenheimeri ever caught)
with a forearm measuring 27.0 mm. These three specimens composed 12.5 % of the 24
captured during that evening, but the percentage of young bats increased to 45 % and 53 %
of the samples caught in July and August, respectively. The forearms of the young bats
, were not significantly different from those of the adults, but body weight was lighter in
July. In that month adult males were 21 % heavier than the young (t = 5.0, p < 0.001, df =
9), and adult females were 15% heavier (t=3.8, p< 0.01, df=14). In August the
difference decreased and the body weight of young anımals was not significantly different
from that of the adults.

Lactating females were captured from 24 May until 3 July, but evidence of recent
lactation (protruding nipples with no hair 3-5 mm around) was noticed between 2 May
until 7 September. Of the 102 females checked during the summer for sıgns of lactatıion, 90

68 Y. Yom-Tov, D. Makin, and B. Shalmon

30

FOREARM ‚mm.

29 ?

wo
@)

BODY WEIGHT,g.
D
6]]

EEE WESTWErRTER Er

TIME (min)

Fıg. 3. Mean + SE body weight and forearm length of male and female Pipistrellus bodenheimeri
caught in mist nets during the first hours after sunset

had either milk ın their milkglands or protruding nipples. There was no evidence of
synchronized breeding.

Lactating females were observed from early May until early September and this may
indicate that some females give birth twice annually.

Mean body weight fluctuated during the evenings rising from a minımum just after dark
to a maximum about 2 hours later and decreased again (Fig. 3). The difference between
maximum and minimum body weight was significant for females (t = 3.14, p< 0.001), but
not so ın the males (t = 1.82, p= 0.1 > p>0.05). Since mean forearm length was sımilar
during this period, it ıs possible that the increase in body weight was due to intensive
feeding by the bats, which added about 15 % to their weight during the first two hours of
hunting.

Biology of Pipistrellus bodenheimeri 69

Acknowledgements

We are extremely grateful to the rangers of the Nature Reserve Authority (NRA), particularly to Erı
GEFFEN, AVIRAM BARKAI and DavID MENINGER; to the guides of the Society for Protection of Nature
in Israel (SPNI) in En Gedi; YocHaı BAaraK and specially to MORDECHAL Yanıv (Marcello), both of
the Dept. of Zoology, Tel Aviv University, who helped in many ways; Dr. D.L. HArrıson provided
constant advice and encouragement and Dr. N. QumsIvEH made useful comment on an early draft;
Prof. H. MENDELSSOHN translated the German summary; we are very grateful to them all.

This study was partially financed by Keren HaTzvi, SPNI.

Zusammenfassung

Die Biologie von Pıpistrellus bodenheimeri (Microchiroptera) im Gebiet des Toten Meeres in Israel

Daten über die Biologie von Pıpistrellus bodenheimeri wurden während einer Untersuchung über die
Fledermäuse im Gebiet des Toten Meeres gesammelt. Diese Art kommt während des ganzen Jahres
hier vor und überwintert von Oktober bis April. Im Winter wurden nur 5% der Anzahl von
Fledermäusen gefangen, die im Sommer gefangen wurden. Säugende Weibchen wurden von Anfang
Maı bis Anfang September gefunden. Weibchen sind deutlich größer und schwerer als Männchen.
Diese Fledermäuse fressen am meisten mit Beginn der Aktivitätsphase am Abend und nehmen
innerhalb von zwei Stunden 15% an Gewicht zu.

References

ATALLAH, S. I. (1977-1978): The mammals of the eastern Mediterranean region: their ecology,
systematics and zoogeographical relationships. Säugetierkdl. Mitt. 25, 241-320.

Bates, P. J. J.; Harrıson, D. L. (1989): New records of small mammals from Jordan. Bonner Zool.
Beitr. 40, 223-226.

Danın, A. (1988): Flora and vegetation of Israel and adjacent areas. In: The Zoogeography ot Israel.
Ed. by Y. Yom-Tov and E. TCHERnov. Dordrecht: Dr. W. Junk. Pp. 129-157.

HarRrıson, D. L. (1960): A new species of Pipistrelle bat (Chiroptera: Pıpistrellus) from south Israel.
Durban Museum Novitates 5, 261-267.

— (1964): The mammals of Arabia. Vol. 1. Insectivora and Chiroptera. London: E. Benn.

Harrıson, D. L.; Maxın, D. (1988): Significant new records for Vespertilionid bats (Chiroptera:
Vespertilionidae) from Israel. Mammalıa 52, 593-596.

JAFFE, $. (1988): Climate of Israel. In: The Zoogeography of Israel. Ed. by Y. Yom-Iov and E.
TCHERNoOv. Dordrecht: Dr. W. Junk. Pp. 79-94.

Kunz, T. H.; AntHony, E. L. P. (1982): Age estimation and postnatal growth ın the bat Myotis
Incifugus. J. Mammalogy 63, 23-32.

Makın, D. (1977): The biology and distribution of the insectivorous bats of the Land of Israel. M. Sc.
thesis. Zoology Department, Hebrew University, Jerusalem (in Hebrew).

MENDELSSOHN, H.; Yom-Tov, Y. (1988): Mammals. Vol. 7. In: Plants and anımals of the land of
Israel. Ed. by A. Aron. Tel Aviv: Ministry of Defence Publishing House and the Society for the
Protection of Nature in Israel.

QumSIYEH, M. (1985): The Bats of Egypt. Spec. Publ., The Museum, Texas Tech. Univ. No. 23,
102

Yom-Tov, Y.; Makın, D.; SHALMoN, B. (1991): The insectivorous bats (Microchiroptera) of the Dead
Sea area, Israel. Israel J. Zool. (in press).

Authors’ address: Y. Yom-Tov (for correspondence), Department of Zoology, Tel Avıv University,
Ramat Aviv, Israel 69978

Z. Säugetierkunde 57 (1992) 70-76
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Social relations in groups of Black-capped capuchin monkeys,
(Cebus apella) in captivity: mother-juvenile relations from the
second to the fifth year of life

By C. WELKER, HELLA HÖHMANN-KRÖGER, G. A. DoyLe

Zoologie und vergleichende Anatomie - Primatenethologie -, Universität Kassel, FRG

Receipt of Ms. 15. 5. 1991
Acceptance of Ms. 3. 12. 1991

Abstract

For juvenile black-capped capuchin monkeys the mother is the most attractive social partner in the
social group. They approach their mother more frequently than any other group member, prefer to sit
in close bodily contact with her and both groom and are groomed by her more frequently than any
other group member. With respect to grooming-relations sex-differences become apparent with age.
In contrast the mother ıs of no noticeable importance as a partner in social play.

Introduction

Long-term studies on some primate species living in large social groups reveal that the
mother is the most important social partner for her juvenile offspring, continuing even
after they reach adulthood. These results are limited to few species of Old World monkeys
where long-term studies on ındıvıdually known anımals have been conducted - Presbytis,
Macaca, Papio — and where many informations are available on Old World monkeys and
Great Apes regarding maternal-juvenile interactions (for areview WELKER 1985). There are
no comparable studies of New World monkeys. In previous reports, on our long-term
study of the black-capped capuchin, we reported that the mother ıs the most attractive
anımal for the ınfant (WELKER et al. 1987; WELKER et al. 1990). This, of course, is true for
most mammals and, particularly for primates, the close and prolonged mother-infant bond
satisfies both the nutritional and protective needs of a relatively helpless ıinfant. However,
to what extent this bond is maintained, after the ıinfant matures and becomes independent,
is not known.

Breeding success and a high survival rate in the primate station of Kassel University
have yielded quantitative data on mother-juvenile relations ın a large sample of black-
capped capuchin monkeys, Cebus apella, providing us, for the first time, with information
on long-term mother-infant relations in a South American primate species living in large
social groups. Although these results, obtained under artificial laboratory conditions, do
not allow us to extrapolate directly to the wild, we have no reason to believe that the same
individual preferences will not be found under natural conditions.

Materials and methods

All 21 Cebus apella juveniles, which constituted our sample (see Table), were born into a single socıal
group, the Don group, named after the group’s dominant male, at the primate station of Kassel
University. The patterns of social behaviour, which occurred regularly and which were scored by
trained observers in terms of frequency of occurrence, were: active approach (approaching another
individual), passive approach (being approached by another individual), contact sitting, active

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5702-070 $ 02.50/0

Mother-juvenile relations in Cebus apella 71

List of capuchin monkeys the authors report on in this paper, observed by group observations (G)
of focal-animal samplings (F)

The years of life where data were used are marked (X)

Date of Mother Year of life
5% 4.

wı

Pan
Claudia
Daniel
Sarah
Isabelle
Christian
Agnes
Jonaine
Petra
Dennis
Carlos
Lisa!
Justus
Samuel
Cesar
David
Thomas?
Philipp
Jesca
Stephanie
Karın

Sylvia
Erna
Dunka
Sylvia
Teufel
Page
Sanga
Teufel
Sylvia
Dunka
Erna
Sanga
Teufel
Sylvia
Erna
Dunka
Kım
Sylvia
Teufel
Sarah
Kim

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Dos Ss sc SE st Sei seite sel ee eier else ee
<

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x
x
x
x
x
X
x
x
x
x
x
x
x
x

! Lisa died 24. 05. 1984, the data on the third year of life are based on ten months of life, only. -
* Thomas was separated 27. 06. 1985, the data on the second year of life are based on eleven
months of life, only.

grooming, passive grooming, social play. The data were collected by focal-animal observations (F) or
group observations (G). As in a previous paper (WELKER et al. 1987) both data sets were combined
since both methods revealed no differences between the different age/sex groups when frequency
scores were converted to percentages. In the figures the mean of the absolute frequency of the
different behaviour patterns protocolled within one year ıs added (mainly, to give sample sızes for the
data sets).

Three of the capuchin juveniles were observed from year 2 to year 5, i.e., for a total of 4 years. The
others were observed for from one to three years. The total number of juvenile years covered was 53,
36 of which were by the focal-anımal-sampling method and 17 of which were by the group-
observation method.

The focal-anımal sampling method (in sensu ALTMmann 1974) was used on 13 anımals while “all
occurrences of some behaviors” were scored for the remaining 8 anımals. The focal-anımal sampling
method provides a complete record not only of the focal anımal’s actions, but also of behaviours
directed to it by others. Each focal animal was observed daily for 15 minutes each minute being a
separate entity such that ıf one behaviour pattern lasted 10 minutes it was scored 10 times. Group
observations were conducted daily for 60 minutes each two minutes being regarded as a separate unıt
such that if one behaviour pattern lasted for 10 minutes it was scored 5 times. All observation sessions
were conducted randomly during the period from 3.00 p.m. to 7.00 p.m., according to an established
schedule.

The frequency with which juveniles made contact with the mother, in terms of the varıous
categories of behaviour scored, converted to a percentage, was compared statistically wıth an expected
percentage based on the assumption that all members of the group are equally attractive as social
partners. Subject to minor fluctuations in group size, over the period of time during which this
research was conducted, this value would be about the same for all mother-juvenile dyads observed.

All statistical tests were performed using the Mann-Whitney test with the level of statistical
significance set at p < 0.05. The data of one individual collected over one year was taken as one
independent sample for statistical purposes.

72 C. Welker, Hella Höhmann-Kröger, G. A. Doyle
Results

Figure 1 indicates that both male juveniles (Year 2, p < 0.001; Year 3, p < 0.001; Year 4, p
< 0.005; Year 5, p < 0.05) and female juveniles (Year 2, p < 0.005; Year 3, p < 0.025; Year
4, p < 0.001; Year 5, p < 0.005) approach their mothers sıgnificantly more often than
expected, females sıignificantly more often than males of the same age (Year 3, p < 0.025
and Year 4, < 0.005 respectively). Even at five years the same trend is still apparent (p <
0.1). These differences hold whether we compare absolute or percentage frequencies from
the third year of life on. The higher percentage frequency of approaches to the mother by
juvenile daughters ın the second year of life is due to the fact that they approach group
members less frequently than do males.

Figure 2 reveals that sons and daughters were approached by their mothers significantly
more often than expected (sons - Year 2, p < 0.001; Year 3, p < 0.001; Year 4, p < 0.005;
Year 5, p < 0.05:/daughters - Year2, p <= 0.005; Year 3, < 0.025; Year 4, PL 30.0020:
5, p < 0.005). From four years daughters were approached by their mothers significantly
more frequently than were sons (p < 0.05). This difference between the sexes is not upheld
statistically, however, ıf absolute frequencies are compared instead of percentage frequen-
cıes. With the exception of the fıfth year of life, when males were approached less often
than were females by their mothers, there was no difference between the sexes in this
regard.

The behaviour pattern most frequently observed among mothers and juvenile offspring
is contact sitting. Figure 3 shows that, for all four age categories under consideration,
mothers sıt in close contact wıth both sons and daughters significantly more frequently
than with other group members (sons — Year 2, p < 0.001; Year 3, p < 0.001; Year 4,
p < 0.005; Year 5, p < 0.025: daughters — Year 2, p < 0.001; Year 3, p < 0.005; Year 4,
P=0.00, Mear Ip 005).

Grooming is a particularly important social behaviour and figure 4 reveals that both
daughters and sons, irrespective of age, groom their mothers significantly more frequently
than they groom other group members (sons — Year 2, p < 0.025; Year 3, p < 0.05; Year 4,
p < 0.005; Year 5, p < 0.05: daushters - Year 2, p <'0.0015 Year 3, pr 0.00 wre
p < 0.001; Year 5, p < 0.005). At each age level, and ın terms of both absolute frequency
and percentage frequency, daughters groom their mothers more frequently than do sons
these differences being significant from year 3 (Year 3, p < 0.025; Year 4, p < 0.005; Year
5, p < 0.05). The tendency to groom the mother increases with age.

Figure 5 shows that mothers groom both their male and female juvenile offspring
sıgnificantly more frequently then they groom other members ot the social group (sons —
Year 2, p < 0.001; Year 3, p < 0.001; Year 4, p < 0.005; Year 5, p = 0/05-@dawshresse
Year 2,p < 0.001; Year 3, p < 0.005; Year 4, p < 0.001; Year 5, p < 0.005). Male juveniles
are relatively more attractive to their mothers than are female juvenile offspring. Interest
on the part of the mother in grooming her infants of either sex declines wıth age.

When one considers both active and passive grooming together (Figs. 4 and 5, absolute
frequencies) ıt ıs clear that, as they become older, daughters become the more active
partners in the mother-ınfant dyad.

In contrast to the affıliatıve behaviour patterns mentioned thus far, figure 6 reveals that
the mother is of no more importance as a partner in social play to her juvenile offspring of
either sex than are other group members and, in fact, is of significantly less importance as a
partner in social place to her juvenile sons than are other members ot the socıal group (Year
2,p. 0.0012 Years, pr=9:00L:97ear4,,pr 0.005, Mean 5, pP 35}

73

Mother-juvenile relations in Cebus apella

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C. Welker, Hella Höhmann-Kröger, G. A. Doyle

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Fig. 5. Passive grooming. (As for figure 1)

75

76 C. Welker, Hella Höhmann-Kröger, G. A. Doyle
Discussion

In juvenile black-capped capuchins the mother remains the most important individual in
the social group irrespective of the age of the juvenile. Contact established in the first year
of life of the infant (WELKER et al. 1987, 1990) is important for the juvenile growing up
within the social group, irrespective of the presence of younger sıblings. With regard to the
behaviour patterns contact sitting, approach and grooming, relations between mothers and
juvenile offspring are especially close. These data may be compared with those from other
primate species. The results suggest that in South American primates generally, and
certainly in the black-capped capuchin, kin-relations are important for the development of
the individual living in a social group. The data in respect of contact sitting suggest a
particularly close relationship between mothers and daughters. While the reciprocal
grooming relationship between mothers and offspring remains close throughout the
juvenile period it ıs with respect of this category of social behaviour that differences
between sons and daughters begin to emerge. In the mother-son dyad the mother remains
the more active partner while, in the mother-daughter dyad, the daughter becomes the
more active partner approaching her mother more frequently and grooming her more
frequently than the mother approaches and grooms her daughter. In this way daughters
appear both to establish and maintain close relations with their mothers thereby forming
matrı-clans and kin-based subgroups within the social group. Contact between mothers
and sons, on the other hand, declines wıth age. This gradual weakening of kin relationships
suggests a paving of the way, under natural conditions, for the male eventually to leave the
social group into which he was born.

Acknowledgements

The authors wısh to thank K. BourcGeo1ıs, B. HoLLsTEIN, H. ROLAND, S. SCHULZ, G. WERNER for
participating in data collection. The study was supported by grants of the German Research
Foundation (DFG).

Zusammenfassung

Soziale Beziehungen in Gruppen des Gehaubten Kapuzineraffen (Cebus apella) in Gefangenschaft:
Beziehungen zwischen Mutter und Jungtier vom zweiten bis zum fünften Lebensjahr

Für Jungtiere des Gehaubten Kapuzineraffen ist die Mutter der wichtigste Sozialpartner der Gruppe.
Sie suchen ihre Mutter häufiger auf als irgendein anderes Gruppenmitglied, sitzen mit ihr in engem
Körperkontakt, putzen sie häufiger als andere Kapuzineraffen und werden von ihr gleichfalls auffällig
häufig geputzt. Als Spielpartner ist die Mutter jedoch für ihre heranwachsenden Kinder durchgängig
unattraktiv. Geschlechtstypische Unterschiede im Verhalten sind vor allem bei der gegenseitigen
sozialen Körperpflege aufzeigbar. Mit zunehmendem Alter werden hier Töchter die aktiveren Partner
in der Mutter-Kind-Dyade, Söhne dagegen bleiben die passiveren.

References

ALTMANN, ]. (1974): Observational study of behavior: sampling methods. Behaviour 49, 227-267.

WELKER, C. (1985): Zur Sozialstruktur der Primates. Anthrop. Anz. 43, 97-164.

WELKER, C.; BECKER, P.; HÖHMANN, H.; SCHÄFER-WITT, C. (1987): So relations in groups of the
black-capped capuchin Cebus apella in captivity. Interactions of group-born infants during their
first 6 months of life. Folia primatol. 49, 33-47.

— — — — (1990): Social relations in groups of the black-capped capuchin (Cebus apella) ın
captivity. Interactions of group-born infants during their second half-year of life. Folia primatol.
54, 16-33.

Authors’ addresses: Prof. Dr. CHRISTIAN WELKER and Dr. HELLA HÖHMANN-KRÖGER, Zoologie
und vergleichende Anatomie — Primatenethologie —, Universität Kassel, Hein-
rıch-Plett-Str. 40, D-3500 Kassel, FRG; Prof. Dr. GERALD A. DoyLe, Primate
Behaviour Research Group, University of the Witwatersrand, 1 Jan Smuts
Avenue, Johannesburg, South Africa

Z. Säugetierkunde 57 (1992) 77-93
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

A morphometric analysis of cranial variation in Holarctic
weasels (Mustela nivalis)

By C. G. van ZYLL DE JONG

Canadıan Museum of Nature, Ottawa, Canada

Receipt of Ms. 9. 9. 1991
Acceptance of Ms. 2. 12. 1991

Abstract

Morphomerric relationships of Holarctic weasels (Mustela nivalıs), based on cranıal varıables, were
analyzed by multiple discriminant function analysis. The results show that all geographic populations
of this weasel, except the Egyptian weasel (subpalmata), form part of a morphological continuum,
thus supporting the contention that they represent one species. The greatest amount of variation is
found in the western Palearctic, which suggests that the species has a long history in that part of the
world and probably evolved there. The morphometric groupings do not correspond to current
infraspecifie classification in detail. A division of M. nivalıs into three subspecific groups is supported
by the data. These are: 1. nıvalis, comprising all small forms of the boreal zones of the Holarctic
Region; 2. vulgarıs, the intermediate to large forms inhabiting the temperate and mediterranean areas
of the western Palearctic and 3. pallıda, a central Asıan form. The evidence suggests that the Egyptian
weasel is a separate species, M. subpalmata.

Introduction

The least weasel (Mustela nivalıs) has an extensive Holarctic distribution stretching from
North Africa and Europe across Asıa into North America. Over this vast area thıs mustelid
displays such an unparalleled degree of varıation, particularly ın size, that the systematic
relationships among different geographic populations have long been uncertain.

More than fıve decades ago, G. M. Arten (1933) combined the small forms from North
America and northern Asıa into one species. In this regard he followed Kuropa (1921),
who had previously described a new Japanese form as a subspecies of the North American
least weasel (M. rıxosa). Shortly after, OGnev (1935) recognized a single species of small
weasel, M. nıvalıs, ın the Palearctic Region, a view shared by ELLERMAN and MORRISON-
ScoTT (1951). The latter authors stated that the same species perhaps also occurred ın
North America. On that continent most mammalogists, following Harr (1951) and Harı
and Keıson (1959), continued to regard the North American least weasel as a distinct
species, M. rıxosa. Later, Harı (1981) changed his opinion and included the American
form in M. nivalıs, cıting REICHSTEIN (1957) for the change. However, REICHSTEIN’s study
focused on geographic varıation and sexual dimorphism in Europe. The analysıs of hıs data
led him to the conclusion that the small morph (“Zwergwiesel”, M. minuta Pomel) is not
specifically distinct from the larger morph (“Mauswiesel”, M. nivalıs L.). However, the
conclusion that North American and Eurasian small morph weasels are conspecific was not
based on his own analysis, but REICHSTEIN (1957) attrıbutes it to a personal communica-
tion from ZIMMERMANN. Subsequent studies on large numbers of skins and skulls from
Europe (Mazakr 1970), on chromosomes (MANDAHL and FREDGA 1980) and experimental
cross-breeding (FRANK 1985) all support the earlier conclusion that there ıs only one
species M. nivalıs in Eurasia and that the small form is only subspecifically distinct.
Cytogenetic comparisons of Eurasian and North American weasels (JARRELL 1983) extend
this support to the inclusion of the Nearctic least weasel, M. rixosa, in M. nivalıs. Despite

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5702-077 $ 02.50/0

78 C. G. van Zyll de Jong

the evidence in support ot a single species, the belief that two species coexist in some areas
continued to persist and some authors (KuURTEN and AnDERSON 1980; CoRBET 1987)
maintained that the taxonomic uncertainty had not been adequately resolved. The lack of
direct morphometric comparisons among populations from the entire distributional range
has, undoubtedly, contributed to the persistence of this uncertainty. The present study
aims at filling this lacuna, by taking a global view of the morphomerric interrelationships
among populations across the entire Holarctic range.

The objectives of the present study are to: 1. analyze and describe cranial variability in
M. nivalıs across ıts entire distributional range, using a multivariate approach; and 2.
reevaluate the taxonomic status and evolutionary relationships of small and large morphs.

Materials and methods

The total sample on which this study is based, comprised 542 adult skulls, including 263 skulls
examined and measured by me, supplemented by data on 279 skulls published by REICHSTEIN (1957).
The breakdown by subspecies, sex, localıty and collection of the specimens examined, arranged by
nominal subspecies and geographic subsamples, ıs as follows: BM = British Museum of Natural
History; USNM = U. S. National Museum of Natural History; NMC = Canadian Museum of
Nature; APM = Alberta Provincial Museum.

M. n. nivalıs: 12 males, 2 females, 3 undetermined. Northern Europe: males, Norway 1 (BM);
Sweden 1 (USNM); females, Russia 1 (BM); Western Sıberia: males, 10 (NMC); females 1 (BM);
undetermined 3 (BM).

M. n. vulgaris: 47 males, 15 females, 3 undetermined. Western Europe: British Isles, males 9 (BM), 5
(USNM), females 5 (USNM), undetermined 2 (USNM); France, males 6 (BM), 4 (USNM), females 1
(BM), undetermined 1 (BM), Netherlands, males 12 (BM), females 2 (BM), 1 (USNM); Central
Europe: Czechoslovakia, males 1 (USNM), females 1 (BM), Hungary, males 1 (BM), Germany, males
3 (BM), females 1 (USNM), Roumanıa, males 1 (USNM), Switzerland, males 5 (USNM), females 4
(USNM).

M. n. boccamela: 30 males, 10 females, 3 undetermined. Italy and Mediterranean France: France,
males 1 (BM); Italy, males 3 (BM), 4 (USNM), females 1 (BM), undetermined 1 (BM), Sardinia, males
2 (BM), Sıcıly, males 2 (BM), Balkan Peninsula: Greece, males 1 (BM), Crete, males 1 (BM),
Yugoslavia, males 3 (BM), females 1 (BM), Iberian Peninsula: Spain, males 5 (BM), 1 (USNM),
females 2 (BM), 2 USNM), undetermined 1 (BM), Azores, undetermined 1 (BM), Balearıc Islands,
males 1 (BM), females 1 (BM); Southwestern Asıa: Afghanistan, males 1 (BM), Turkey, males 4 (BM),
1 (USNM), females 1 (BM), 1 (USNM), Iran, males 1 (BM), females 1 (BM).

M. n. numidica: 3 males, 1 undetermined. Northwest Africa: Algerıa, males 2 (BM), Morocco, males
1 (USNM), Tunis, undetermined 1 (BM).

M. n. subpalmata: 8 males, 9 females, 2 undetermined. Egypt: males 3 (BM), 5 (USNM), females 3
(BM), 6 (USNM), undetermined 2 (USNM).

M. n. pallida: 6 males, 1 undetermined. Central Asıa: Djarkent (= Panfılov), males 6 (BM),
undetermined 1 (BM).

M. n. pygmeae: 24 males, 5 females, 1 undetermined. Eastern Siberia: males 21 (USNM), females 4
(USNM), Eastern Asıa: Korea, males 1 (USNM), females 1 (USNM), Manchuria, males 2 (USNM),
undetermined 1 (USNM).

M. n. russelliana: Szechwan, females 1 (BM).

M. n. rıxosa: 26 males, 15 females, 2 undetermined. Canada: Alberta, males 2 (NMC), 6 (APM),
females, 2 (NMC), 5 (APM), undetermined 1 (APM), British Columbia, males 5 (NMC), Manitoba,
males 1 (NMC), Northwest Territories, males 3 (USNM), 4 (NMC), females 2 (NMC), undeter-
mined 1 (NMC), Quebec, males 1 (NMC), Saskatchewan, males 4 (NMC), females 6 (NMC).

M. n. allegheniensis: 11 males, 4 females. Eastern United States: Indiana, males 5 (USNM), females 1
(USNM), Maryland, females 1 (USNM), North Carolina, males 1 (USNM), Pennsylvanıa, males 1
(USNM), females 1 (USNM), Tennessee, males 1 (USNM), Virginia, males 1 (USNM), West
Virginia, males 2 (USNM), females 1 (USNM).

M. n. campestris: 7 males, 3 females; Central Great Plains: Missouri, males 2 (USNM), females 2
(USNM), North Dakota, males 3 (USNM), South Dakota, males 2 (USNM), females 1 (USNM).

A morphometric analysis of cranial varıation in Holarctic weasels 79

M. n. eskimo: 4 males, 4 females, undetermined 2; Alaska-Yukon: Alaska, males 1 (USNM), 1
(NMC), females 3 (USNM), undetermined 1 (NMC), Yukon, males 2 (NMC), females 1 (NMC),
undetermined 1 (NMC.).

There is no generally accepted subspecific classification of M. nivalis. In the main, I have followed
ELLERMAN and MORRISON-SCOTT (1951) in the application of subspecific names to Palearctic
populations, with some modifications based on HEPTNER et al. (1974). For North American forms I
have followed Haır (1981). Specimens of undetermined sex were diagnosed by discriminant function
analysıs and included ın the appropriate sample.

Thirteen measurements were made on each skull, using a digital caliper capable of measuring to
0.01 mm. The cranıal measurements taken (as defined by van ZyLL DE Jong 1972, except for #1), are:
1, condylobasal length (CBL); 2, interorbital width (IOW); 3, width between postorbital processes
(WPOP); 4, orbitonasal length (ONL); 5, width of the postorbital constriction (WPOC); 6, basal
skull width (BSW); 7, mastoıd width (MW); 8, zygomatic width (ZW); 9, buccal length of P4 (LP4);
10, greatest width of P4 (GWP4); 11, lingual length of M1 (LM1); 12, greatest diameter of MI
(GDMI); 13, length of the mandibular premolar-molar series (Lpm). Measurements 1, 2, 7 and 8 were
supplemented with data from REIcHSsTEINn (1957).

Multigroup discriminant function analysıs (BIOSTAT II MDA, PımENTEL and SMITH (1986) was
used to discriminate among geographic samples of weasels using 12 varıables. This analysıs was done
to assess the global variation ın size and shape of the skull. The geographic areas and nominal
subspecies represented in the analysıs comprised the following: 1. Canada (rıxosa); 2. eastern United
States (allegheniensis); 3. central Great Plains (U. S.) (campestris); 4. Alaska-Yukon (eskimo); 5.
eastern Sıberia (pygmaea); 6. eastern Asıa (pygmaea); 7. central Asıa (pallida); 8. western Siberia
(nivalis); 9. northern Europe (nivalis); 10. central Europe (vulgaris); 11. western Europe (vulgaris);
12. southwestern Asıa (boccamela); 13. Balkan Peninsula (boccamela); 14. Italy and adjacent
mediterranean France (boccamela); 15. Iberian Peninsula (zberica); 16. northwest Africa (numidica);
17. Egypt (subpalmata).

A smaller number of varıables, but a larger number of geographic samples (including REICHSTEIN’s
data) were used to increase resolution in the area of greatest geographic variation. The geographic
areas represented in this analysıs were as above, but central Europe is represented by separate samples
for: 1. northern Germany; 2. central and western Germany; 3. southern Germany; 4. Silesia; 5.
Poland; 6. Switzerland; and 7. Sardınia ıs separated from Italy.

Both sets of samples were also subjected to distance analysıs, using the generalized distance (D), to
study the morphometric relationships among geographic poulations. To this end, the matrix of
generalized distances among geographic forms was analyzed by cluster analysıs (UPGMA, SNEATH
and SokAaL 1973). Males and females were analyzed separately.

Results
Cranial variation in males

The results of the multiple discriminant function analysis of the subsamples of males are
presented in table 1 and figure 1. The graph (Fig. 1) shows the centroid of each group and
the dispersion of individuals around them (polygons) plotted onto the first two canonical
varıates. The relative importance of the different varıates in the discrimination of samples is
listed in table 1 and shown by the character vector diagram in figure 1. A little over 70
percent of the cranıal varıation is explained by the first canonical axis, 16.29 percent by the
second and 4.11 by the third axis (Table 1). All varıates, except ONL contribute to a
considerable extent to discrimination on the fırst axıs. This axis discriminates among sıze
classes, from small on the left to large on the right. On the second axis, BSW and GWP4
contribute to discrimination to an important degree (Table 1).

The bivariate plot of the centroids and their respective polygons clearly shows an
ordination into two separate nonoverlapping groups, with M. n. subpalmata on the one
hand and all the other geographic samples on the other. A closer examination reveals that
the latter group is composed of two, or three, subsidiary groupings. On the left of the
graph we see the largely overlapping polygons representing the small North American,
Siberian, eastern Asian and northern European forms and on the right a sımilar overlap-
ping cluster of the larger forms from temperate Europe, the Mediterranean area and
southwestern Asia. These two clusters are linked by the sample from central Europe. A

C. G. van Zyll de Jong

80

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A morphometric analysıs of cramıal varıatıon in Holarctic weasels 81

Table 1. First three standardized canonical vectors from the discriminant function analysis of 12
cranial variables from Mustela nivalis

The number in parentheses is the percentage of the varıance of each varıable contributed to the

Variable

eBE
IOW
WPOP
ONL
WPC
BSW
MW
LP4

canonical axis

Standardized canonical vectors

1

0.451 (92.53)
0.203 (69.73)
-0.232 (50.16)
-0.014 (1.22)
0.267 (64.66)
0.026 (0.20)
0.119 (41.55)
-0.171 (81.84)

2

-0.070 (0.13)

0.388 (15.35)
-0.881 (43.40)
-0.048 (0.90)
-0.635 (22.13)

2.331 (95.28)
-0.395 (27.50)
-0.088 (1.30)

3

-0.024 (0.00)
0.602 (2.09)
0.250 (0.20)
-0.810 (14.27)
0.027 (0.00)
-0.748 (0.55)

(9.84)

(4.48)

Cumulative
percent

No
2.
Ds
4.
Is
6.
7:
8.
9

. GWP4 0.071 (40.69) 0.304 (45.10 \ (0.00)
. LM1 0.263 (96.16) —9,1 29° (Uli ; (0.34)
. GDMI 0.310 (69.10) —0.605 (15.83
. Lpm 0,254: (71785) —0.458 (14.04

Percent

trace 70.70 16.29 4.11

Cumulative

percent 70.70 86.99 91.09

Test of equality of group centroids: F = 7.35 with 96 and 1081 degrees of freedom. P<0.001.

Table 2. First two standardized canonical vectors from the discriminant function analysis of four
cranial variables from Mustela nivalis males

Numbers in parentheses represent the percentage of the varıance of each variable contributed to the
canonical vector

Variable

Standardized canonical vectors Cumulative
1 p) percent

1. CBL -0.698 (98.13) 1258 99.32
2. IOW 0.122 (72.86) -0.484 (4.3 N,
3. MW -0.399 (86.62) 2.544 (13.2 99.89

4. ZW -0.036 (11.04) -0.919 (26.85 37.89

Percent trace 87.78 6.95
Cumulative percent 87.78 94.73

Test of equality of group centroids: F = 11.46 with 88 and 1905 degrees of freedom. P<0.0001.

third subsidiary group is represented by the small sample from Central Asıa situated
below, and marginally overlapping the two previous groups. The character vectors (Fig. 1
and Table 1) indicate that the boreal and temperate weasels differ from one another
principally in size, lying along a common size axis, which slopes gently from left to right.
The sample from central Asia is somewhat intermediate in size relative to the last to
groups, but differs from them to some extent in the shape of the skull (relatively greater
WPOP, WPC and Lpm). The Egyptian weasel (subpalmata), on the other hand, differs
from all the others in size, as well as ın shape (relatively broader BSW, GWP4 and IOW).

The results of a UPGMA cluster analysis of the matrix of Generalized Distances among
‘the geographic populations are shown in the form of a phenogram (Fig. 2). All small
northern forms make up one cluster, which is joined by the central Asıan form at a lower

82 C. G. van Zyll de Jong

8=-

Fig. 2. Distance phenogram summarizing the morphometric relationships among 17 geographic
samples of male Mustela nivalıs. A: Canada (rixosa); B: Alaska-Yukon (eskımo); C: Western Siberia
(nivalis); D: Eastern Sıberia (pygmaea); E: Eastern Asıa (pygmaea); F: Northern Europe (nıvalıs); G:
Eastern U.S. (allegheniensis); H: Central Great Plains, U.S. (campestris); I: Central Asıa (pallida); ]:
Balkan Peninsula (boccamela); K: Italy (boccamela); L: Southwestern Asıa (boccamela); M: Central
Europa (vulgaris); N: Iberian Peninsula (zberica); ©: Western Europe (vulgarıs); P: Northwestern
Afrıca (numidica); Q: Egypt (subpalmata)

level (4.47), and all large temperate and southern forms constitute a sımilarly structured
cluster. The Egyptian weasel is most remote and joins the others at D = 7.91.

It ıs clear from examining the above results, that the greatest cranıal varıation is found ın
the western Palearctic. Results of the discriminant function analysis of a larger number of
geographic samples, but a smaller number of varıates (CBL, IOW, MW, and ZW,
including REıcHsTEIn’s [1957] data) provided increased resolution of the general pattern of
variation ın this area. The broad pattern of geographic varıation that emerged from the
analysıs ıs depicted in two ways. Firstly, the results are shown as a graph of the centroids
and their 95% confidence circles on the first two canonıcal axes (Fig. 3). Secondly, to
place the varıation in a geographical context, the results are projected on a map of the
distributional range as graphic indices of each population’s morphometric state and as
generalized distances between neighboring populations (Fig. 4).

The plot of the centroids shows the weasel populations arranged from small, on the

83

A morphometric analysis of cranial variation in Holarctic weasels

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84 C. G. van Zyll de Jong

Fig. 4. Geographic variation in the skulls of male Mustela nivalıs. The squares indicate the mor-
phometrie position of the regional forms on the first canonıcal axis from smallest (no black) to largest
(all black). The numbers and lines joining the squares give the generalized distance (D) and a
comparative measure of the spatial separation of neighboring populations represented by the samples.
In North America and Asıa from east to west: Eastern U.S. (allegheniensis); Central Great Plains,
U.S. (campestris); Canada (rixosa); Alaska-Yukon (eskımo); Eastern Sıberia (pygmaea); Eastern Asıa
(pygmaea); Central Asıa (pallida); West Siberia (nıvalis) (north); Southwestern Asia (boccamela)
(south). In Europe and North Africa from north to south and east to west: Northern Europa (nivalıs);
Poland (nivalis); Northern Germany (nivalis); Central and Western Germany (vulgarıs); Sılesia
(vulgaris); Southern Germany (vulgaris); Western Europe (vulgaris); Switzerland (vulgarıs); Balkan
Peninsula (boccamela); Italy (boccamela); Sardınıa (boccamela); Iberian Peninsula (zberica); Azores;
Egypt (subpalmata); Northwest Africa (numidica)

right, to large forms on the left (see table 2 for standardized canonical vectors). The
centroids with their largely overlapping confidence regions form a graded series from small
boreal forms to intermediate temperate forms, to large mediterranean forms, whereas the
Egyptian weasel is separated from all the others by a distinct gap.

The distribution of morphological forms and D values separating neighbours show
clearly that the samples from boreal areas across North America and Eurasia, although
separated by large distances in space, differ from each other relatively little morphomerri-
cally (Fig. 4). In the western Palaearctic, on the other hand, there is considerable

A morphometric analysis of cranial varıation in Holarctic weasels 85

Table 3. Results of univarıiate Newmann-Student-Keuls test on four varıables of male weasels

Sample designations as in Fig. 3

CBL | IOW
Subspecies Subset Sample Subspecies Mean Subset

rıxosa 6.34
eskimo 6.61
allegh 6.78
campes 6.79
pygmae 6.98
pygmae 7.01
nivalı

nıvali

vulgar

vulgar

pallıd

vulgar

vulgar

vulgar

vulgar

vulgar

ıberic

boccam

boccam

numidi

boccam

boccam

subpal

rıxosa
allegh

eskimo

pygmae

pygmae
nivalı

nivali
campes
vulgar
vulgar
pallıd
vulgar
vulgar
vulgar
vulgar
iberic
vulgar
boccam
boccam
boccam
boccam
numidi

subpal
MW ZW

rIxosa eskimo
eskimo rixosa
allegh allegh
pygmae nıvalı
nivalı pygmae
campes campes
pygmae nivalı
pallid pygmae
nivalı pallıd
vulgar vulgar
vulgar vulgar
Be Den
vulgar vulgar
vulgar vulgar
vulgar vulgar
iberic iberic
vulgar vulgar
boccam boccam
numidi numidi
boccam boccam
boccam boccam
boccam boccam

subpal subpal

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morphometric change over relatively small distances, generally taking the form of a north-
south cline of increasing size. The smallest morphs occur in northern Europe and the
largest in the Mediterranean area. The existence of this size cline was demonstrated
previously by REıcHstein (1957). Exceptions to this general north-south trend are the
populations from higher altitudes in Southern Germany and Switzerland. These are
markedly smaller, approaching the boreal forms in size.

86 C. G. van Zyll de Jong

ao a uu oo m - x The results of the a post-
eriori Student-Newmann-

Keuls multiple range test

confirm the generally north-

1 south gradual size varıation
in geographic samples and

the gap between subpalmata

and all the others (Table 3).

2. The only gap, in the largely
overlapping nonsignificant

subsets, is that between the

a smaller central European
forms (I-L) and the western
European-Iberian subset
(OS).

No

Cranial variatıon
in females

The results of the analyses
of female skulls were sımilar
to those obtained for the
6 - males. Females were rep-
resented in lower numbers
in collections and were lack-
ing entirely for some of the
geographic subsamples. Be-
cause of the reduced geo-
graphic representation of fe-
8 - males and the sımilarıty of

the results for both sexes, it

suffices to lıst the standar-

dızed canonical vectors
= (Table 4) and to show the

we results of the cluster analysıs
Fıg. 5. Distance phenogram summarizing the morphometric rela-
of the distances among

tionships of 11 geographic samples of female Mustela nivalıs. A:
Canada (rıxosa); B: Eastern U.S. (allegheniensis); C: Alaska- samples of temales {rom
Yukon (eskimo); D: Eastern Siberia (pygmaea); E: Central Great different geographic areas
Plains, U.S.: (campestris); F: Italy (boccamela); G: Iberian Penin- (Fig.5). Ihe clustering of
sula (zberica); H: Southwestern Asia (boccamela); I: Central female weasels in three main
Europe (vulgaris); J: Western Europe (vulgaris); K: Egypt (sub- clusters representing boreal
palmata) small sized, temperate to
mediterranean intermediate-
to-large sıze and Egyptian weasels parallels that of the males closely. The maın difference
between male and female samples is the generally smaller distance (D) between the female
centroids and the larger distance separating the Egyptian females from all the rest.

The results of the analysıs of geographic varıatıion based on four characters (Figs 6 and
7), likewise, resemble those of the males closely, with little varıation in the north from
North America to northern Europe and relatively precipitous size change from north to
south ın Europe. The smaller intercentroid distances among female samples, compared to
those among male samples, are again noticeable, as well as the much greater distance of the
subpalmata centroid from all others. The results of the Student-Newmann-Keuls test of

A morphometric analysıs of cranial varıation in Holarctic weasels 87

Table 4. First three standardized canonical vectors from a discriminant function analysis of 12
cranial variables from Mustela nivalis females
Numbers in parentheses represent the percentage of the variance of each variable contributed to the
canonical vector

Variable Canonical vectors Cumulative
1 2 3 percent

@BE
IOW
WPOP
ONL
WPC
BSW
MW
LP4

. GWP4
10. LMI1
11. GDM1
12. Lpm

ll.
2,
S
4.
5:
6.
7.
8.
9

0.864 (99.99)
0.514 (82.35)
0.149 (89.11)
0.386 (91.98)

-0.548 (97.44)

-0.410 (62.85)

-0.201 (93.10)

-0.143 (88.79)

-0.076 (38.01)
0.344 (98.43)

0.558 (96.39)
0.723 (97.76)

-0.010 (0.00)
1.398 (16.44)
0.019 (0.03)
-0.634 (6.70)
0.499 (2.17)
-1.883 (35.75)
0.331 (6.84)
0.310 (11.20)
0.491 (43.30)
-0.264 (1.56)
0.657 (3.60)
-0.592 (1.76)

-0.026 (0.00)
1.020 (1.19)
-0.854 (10.85)
-0.757 (1.30)
-0.567 (0.38)
1.006 (1.39)
-0.084 (0.06)
0.000 (0.00)
0.872 (18.68)
-0.022 (0.00)
0.023 (0.00)
-0.824 (0.46)

100

Percent

trace 92.28 6.41 1.30
Cumulative

percent 92.28 98.70 100

Test of equality of group centroids: F = 7.76 with 36 and 133 degrees of freedom. P<0.001.

the four varıables (Table 5) confiırms the continuous nature of the size varıation and the
smaller differences among female samples, with the obvious exception of the sample of
subpalmata. The greater difference between subpalmata females and females of all the
others forms, compared to that in the males, points to the existence of a male-female size
relationship in Egyptian weasels that differs from that in the other taxa. This brings us to a
consideration of sexual dimorphism of size.

Variation in sexual dimorphism of size

REICHSTEIN (1957) pointed out that the difference in size between the sexes in M. nivalıs
increases with overall size. In the present samples, for instance, the difference in mean
condylobasal length of males and females of the small boreal forms ıs relatively slight, wıth
the length of the female skull averaging 93 % of that of the male skull (range 90-97 %). In
the large mediterranean morphs, on the other hand, the difference is much greater. The
female skull length in these forms averages only 85% of the male skull length (range
83-88 %). An apparent exception is the Egyptian weasel. The mean condylobasal length of
the female Egyptian weasel sample constituted about 90 % of the mean of the same length
in males.

To investigate the relationship of sıze in females and males further, the logarıthm of the
mean condylobasal length of females was plotted against that of males of the same
geographic population. Inspection of the resulting pattern suggests a linear relationship of
size between the sexes in geographic populations of M. nivalıs, with the exception of the
Egyptian sample, which clearly deviates from the common trend (Fig. 8). The equation
describing the relationship (Model II regression, SOKAL and ROHLF 1981) shows that size
in females increases at a lower rate than that in males, ı.e. the relation is allometric. The
goodness of fit index (r? = .86) indicates that the regression describes the relationship
effectively. The mean size of the female Egyptian weasel predicted by the regression
(38.0 mm) is less than the actually observed value (43.5 mm). Thus the growth rate in
females approaches that of the males more closely in this taxon.

88 C. G. van Zyll de Jong

Table 5. Results of univarıate Student-Newmann-Keuls test on four variables in female weasels

Sample designations as in Fig. 6

GBE IOW
Subspecies Subset Sample Subspecies Subset

zZ

rıxosa

allghe

pygmae

rixosa |
|
|
eskimo |
|
|

eskımo
Pygmae
allegh
vulgar
campes
vulgar
vulgar
vulgar
nivalı
boccam
boccam
vulgar
vulgar
boccam
iberic
subpal
MW ZW

eskimo eskimo
rıxosa pygmae
pygmae rıxosa
vulgar vulgar
allegh allegh
nivalı vulgar
vulgar campes
campes vulgar
vulgar nivalı
vulgar boccam
boccam vulgar
vulgar boccam
Da
occam vulgar
boccam boccam
iberic iberic

subpal subpal

I»

N

campes
vulgar
vulgar

|

|

|

|

|

|
vulgar |
|

|

|

|

|

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vulgar
nivali
boccam
vulgar
vulgar
boccam
boccam
iberic

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—

N

OS <ez zz ng oe Tag

Seen ee ae ee

Table 6. First two standardized canonical vectors from the discriminant function analysis of four
cranial variables from Mustela nivalis females

Numbers in parentheses represent the percentage of the variance of each variable contributed to the
canonical vector

Variable Standardized canonical vectors Cumulative
1 2 percent

PE@BI° 0.411 (88.38) 1.092 (9.34)
2. IOW -0.445 (93.61) 0.898 (5.72)
3. MW 0.441 (87.24) 1175, 097)
4. ZW 0.559 (93.52) -0.486 (1.06)

Percent trace 9227, 5.47.
Cumulative percent 97.74

Test of equality of group centroids: F = 6.190 with 64 and 452 degrees of freedom. P<0.0001.

89

A morphometric analysıs of cranial variation in Holarctic weasels

m

LOLIOISOd e P9109S UEMUY99ZS WOAF vurıJossnı "u "y jo usunads af3uıs e sauasaadaı ysuase ay] "(vrrugpdgns) 1dA37 :© :(rauagı)
epnsuruog UENIOg] :q !(PJowv290g) Ajeıy :O :(srdjna) eisaps :N *(P]2W02909) eısy unmısomynog :W ‘(sıurdjna) edong usa: “(szurdjna)
Aueunad) Usa, pur JenUs) :y] :(savdjna) Aueunsd umynoN :f :(vJ9wv590g) epnsurusg uesjegg :] (szirdjna) puepozumg : :(sıurdgna)
AueUL9H UIDYINOS :9) !(sıyparu) odoang ursy11on :7 :(vorıudkd) ELIOAIS UAOISE/T 27 :(82450duuv2) "Sy ‘surefq 28919 fenus) :q !(sısunuagsarp)
Sn woiseH :D (0150) uOyNnA-eyseIy :q :(psoxzı) epeuey :y "parepnapes 919m suswmads xıs ueyn ssof 70 sapdures 107 SOpPAII 99U9PIJUO9
ON 'sıjparu vjossn >fewoay Jo sapdures Jıydeı3093 /] Fo soppa19 Huap1Juo9 %, 6 HANaadsaı pur spronuss ayı 3urmoys ydeı3 jesıuouey '9 ‘327

90 C. G. van Zyli de Jong

Fig. 7. Geographic varıation in the skulls of female Mustela nivalıs. In North America and Asıa from
east to west: Eastern U.S. (allegheniensis); Central great plains (campestris); Canada (rixosa); Alaska-
Yukon (eskimo); Eastern Sıberia (pygmaea); Southwestern Asıa (boccamela). In Europe and North
Africa, from north to south and east to west: Northern Europe (nivalis); Northern Germany
(vulgaris); Central and Western Germany (vulgaris); Sılesia (unlgarıs); Southern Germany (vulgaris);
Western Europe (vulgarıs); Switzerland (vulgaris); Balkan Peninsula (boccamela); Italy (boccamela);
Iberian Peninsula (zberica); Egypt (subpalmata). Further details as in Fig. 4

Discussion

The results of the craniometric analyses presented above support the view that all Holarctic
weasels of the taxa included in this study are members of one varıable species, with the
notable exception of subpalmata. The latter taxon differs both morphometrically and with
respect to sexual dimorphism of size from all the other taxa. These differences suggest the
possible existence of underlying genetic and/or epigenetic mechanisms in subpalmata that
differ from those in the other taxa. There is thus sufficient evidence to suspect that
subpalmata may have evolved independently for a consıderable period of time and may be
specifically distinct from M. nivalıs. This requires confirmation from the study of other
character sets, including molecular data.

A morphometric analysis of cranial varıation in Holarctic weasels 91

Mean d‘ Condylobasal Length (mm)
30 35 40 45

1.65

z
o Y= 0.5683 + 0.6004X €
S r2= 0.86 E
— ‘Ss
5 o
(y) e
Bo} ®
2 Br
31.55 —
[< 77)
° 3
° [eo]
° 5
[o) ke)
—/ e
[o)
= ©
o©+
e
y)
®
s

1.45
1.45 1.55 1.65

al Log Condylobasal Length

Fıg. 8. Sexual dimorphism of size in Mustela nivalıs. The equation describes the linear relationship
between sıze of males and of females in populations of M. nivalis (without subpalmata) varying in size
from small to large; r” is a measure of goodness of fit. A: Canada (rixosa); B: Alaska-Yukon (eskimo);
C: Eastern U.S. (allegheniensis); D: Central Great Plains, U.S. (campestris); E: Eastern Siberia
(pygmaea); F: Northern Europe (nivalis); G: Switzerland (vulgaris); H: Central and Western
Germany (vulgaris); I: Southern Germany (vulgaris); J: Northern Germany (vulgaris); K: Western
Europa (vulgaris); L: Silesia (vulgaris); M: Southwestern Asia (boccamela); N: Italy (boccamela); O:
Iberian Peninsula (zberica); P: Egypt (subpalmata)

All other taxa in this study represent overlapping gradations ın morphology and share a
common sexual size dimorphism. Both, morphology of the skull and the difference in size
between the sexes, are predominantly effectuated by overall size. The conclusion is that
these taxa constitute one species, M.nivalıs. The results of the morphomertric analysıs do not
agree with the great number of subspecies recognized ın the literature and suggest that a
reduced number would be more realistic. A complete taxonomic revision, using all available
characters and maximum geographic representation, is indicated. Such a revision clearly lies
outside the scope of the present study. However, the results of this analysıs support a
breakdown of the populations studied into three subspecific groups: 1. The nıvalıs group. A
group of small weasels, characterized by white winter pelage and distributed throughout the
northern coniferous biome of Eurasia and North America. 2. The vulgaris group (including
boccamela and numidica). A group of intermediate to large sized weasels, characterized by
brown winter pelage and distributed ın the temperate deciduous biome and Mediterranean
region of the western Palearctic region. 3. A Central Asıan group of intermediate sızed
weasels (pallida), with white winter pelage (HEPTNER et al. 1974).

92 C. G. van Zyll de Jong

This represents a reduction in the number of taxa distinguished by Frank (1985) in the
western Palearctic. As FRANK (1985) pointed out, and the results of this study confirm,
vulgaris and boccamela are difficult to delineate. Populations designated to these sub-
species form a gradual north-south clıne, lacking the marked morphological discontinuity
that characterizes the transıtion between nivalıs and vulgaris. They are, therefore, best
combined into one taxonomıc category. The existence of a numidica group, postulated by
FRANK (1985) as being an independent species (type locality: Tangiers, Morocco) most
closely resembling the ancestor of least weasels, is not supported by the morphometric
evidence. The northwest African sample is morphometrically not distinct from other
Mediterranean weasels (it is closest to samples from the Balkan [D = 0.92] and Italy [D =
1.81]). It seems, therefore, likely that M. nivalis invaded North Africa via Spain during the
late Pleistocene, like other Palearctic elements. The weasel from Crete (galianthas), one of
the insular forms included in the presumed ancestral numidica group by FRANK (1985), is
represented by one specimen. It was scored and plotted a posteriori (Fig. 3) to gain some
idea about its possible affınities. Its position indicates that ıt ıs similar to other forms from
the Mediterranean area and closest to the topotypic sample of boccamela from Sardınia.
The time of ısolation of the northwest Afrıcan and island populations in the Mediterranean
from those on the European mainland may be comparable to that of the eastern Siberian
and North American populations. The respective morphometric differences are approxi-
mately of the same magnitude, a consideration that lends some support to this assumption.

The small Central Asıan sample ıs from one localıty (Dzharkent = Panfilov) in east
Kazahkstan. More samples from central Asıa will have to be studied before a clear picture
of geographic varıatıon in the area can emerge. A single specimen from Szechwan ıs similar
to the boreal Asıan and North American forms (Fig. 6), which suggests that the species
entered China from the north.

The great varıation of the species in the western Palearctic and the fossil record
(KurTEn 1968) suggest that M. nivalıs evolved here. It appears highly likely that the small
northern forms (nivalis) evolved most recently, under the prevailing boreal conditions of
the Pleistocene glaciations. Their adaptations to boreal conditions having been perfected,
they subsequently spread east throughout northern Asıa, invadıng North America only
during the late Pleistocene.

Acknowledgements

I am grateful to the persons in charge of the collections at the British Museum (Natural History) and
the U.S. National Museum of Natural History for allowing me to examine specimens in their care.
Donna NAUGHTON prepared the final illustrations.

Zusammenfassung

Morphometrische Analyse der Schädelvariation beim holarktischen Mauswiesel (Mustela nivalıs)

Die Schädelvarıabilität der Mauswiesel (Mustela nivalis) aus verschiedenen Teilgebieten des holarkti-
schen Artareals wurde morphometrisch untersucht. Schädelmafe erwachsener Tiere wurden multi-
variaten Diskriminanzanalysen unterzogen, um eine Klärung in der Systematik der Mauswiesel
herbeizuführen. Die Ergebnisse dieser Analysen zeigen, daß die Populationen verschiedener Teil-
gebiete, außer die ägyptische (subpalmata), einem morphologischen Kontinuum angehören und
hauptsächlich in der Größe variieren. Diese Beobachtung stützt die Behauptung, dafs diese Populatio-
nen einer Art zuzuordnen sind. Die morphometrischen Daten ermöglichen eine Teilung in drei
phänotypisch ähnliche subspezifische Gruppen: die nivalis-Gruppe, kleine Wiesel der borealen
Gebiete der Holarktis; die vulgarıs-Gruppe, mittel- bis großwüchsige Wiesel, welche die gemäßigten
und mediterranen Gebiete der westlichen Palaearktis bewohnen, und eine zentralasiatische Gruppe
(pallida). Das ägyptische Wiesel ist wahrscheinlich eine selbständige Art.

A morphometric analysis of cranial varıation in Holarctic weasels 93

References

ALLEn, G. M. (1933): The Least Weasel a circumboreal species. J. Mammalogy 14, 316-319.

CoRBET, G. B. (1978): The mammals of the Palaearctic Region: a taxonomıic review. London, Ithaca:
Cornell Univ. Press.

ELLERMAn, J. R.; MORRISON-SCOTT, T. C. S. (1951): Checklist of Palaearctic Mammals. London:
Brit. Mus. (Nat. Hist.).

FRANK, F. (1985): Zur Evolution und Systematik der kleinen Wiesel (Mustela nıvalis Linnaeus, 1766).
Z. Säugetierkunde 50, 208-225.

Haut, E. R. (1951): American Weasels. Univ. Kansas Publ. Mus. Nat. Hist. 4, 1-466.

— (1981): The mammals of North America. 2. ed. New York: John Wiley and Sons.

Haus, E. R.; Kerson, K.R. (1959): The mammals of North America. New York: Ronald Press.

HEPTNER, V. G.; Naumov, N. P.; JÜRGENSoN, P. B.; SLuDsKI, A. A.; CIRKOVA, A. F.; BANNIKOV,
A. G. (1974): Die Säugetiere der Sowjetunion. Bd II: Seekühe und Raubtiere. Jena: VEB Gustav
Fischer.

JARREL, G. H. (1983): Holarctic similarıty of chromosomes in the weasel, Mustela nivalıs: G- und C-
banding in an Alaskan specimen. Mammalian Chromosomes Newsletter 24, 207-212.

Kuropa, N. (1921): On three new mammals from Japan. J. Mammalogy 2, 208-211.

Kurrt£n, B. (1968): Pleistocene Mammals of Europe. London: Weidenfeld and Nicolson.

KurTEn, B.; AnDERsoNn, E. (1980): Pleistocene Mammals of North America. New York: Col. Univ.
Press.

MANDAHL, N.; FREDGA, K. (1980): A comparative chromosome study by means of G-, C-, and
NOR-bandings of the weasel, the pygmy weasel and the stoat (Mustela, Carnıvyora, Mammalıa).
Hereditas 93, 75-83.

Mazax, V. (1970): Comments on the problem of Mustela minuta. Lynx 11, 40-44. (Czech. with
English summary.)

Ocnev, S. I. (1935): Mammals of the USSR and adjacent countries. Vol. 3: Carnıvora. Moscow.
English Translation: Jerusalem, 1962.

PiMENTEL, R. A.; SMITH, ]J. D. (1986): BIOSTAT II: A multivariate statistical toolbox. Sigma Soft,
Placentia, California.

REICHSTEIN, H. (1957): Schädelvariabilität europäischer Mauswiesel (Mustela nivalıs L.) und Her-
meline (Mustela erminea) ın Beziehung zu Verbreitung und Geschlecht. Z. Säugetierkunde 22,
151-182.

SNEATH, P. H. A.; SokaL, R. R. (1973): Numerical Taxonomy. San Francisco: W. H. Freeman and
Co.

SOoKAL, R. R.; RoHLF, F. J. (1981): Biometry. New York: W. H. Freeman and Co.

ZYLL DE Jong, C. G. van (1972): A systematic review of the Nearctic and Neotropical river otters
(Genus Zutra, Mustelidae, Carnivora). Life Sciences Contribution 80, Royal Ontario Museum.

Author’saddress: Dr. C. G. van ZYLL DE Jong, Canadian Museum of Nature, P.O. Box 3443,
Station “D”, Ottawa, Ontario, Canada, K1P 6P4

Z. Säugetierkunde 57 (1992) 94-99
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Some physical and population characteristics of Egyptian
mongooses (Herpestes ichneumon L., 1758) in southwestern
Spain

By F. Paromares and M. DELIBES

Estacion Biolögica de Donana, Sevilla, Spain

Receipt of Ms. 26.7. 1991
Acceptance of Ms. 9.10. 1991

Abstract

Studied physical and population characteristics of Egyptian mongooses, Herpestes ichneumon, in
southwestern Spain using trapping and radio-tracking. Males and females differed (p = 0.04) ın body
mass (3142 and 2823 g, respectively). Females were more often trapped than males (1.8F:1M), and
adult than young (1.8A:1Y). Copulations occurred mainly (63.6%) ın March and April, and births
(77.8%) ın May, June and July. The mean number of cubs per litter was 2.7 # 0.8 (N = 7). Density
for adult individuals was estimated as 1.2 ind./km?. Annual survival rates were very low, oscillating
between 0.13 in 1988/89 for adults and the same figure ın 1987/88 for young, and 0.6 in 1987/88 for
adults. After two years, life expectancy did not exceed 3%. Of 16 dead mongooses, only 6.3 % were
due to natural causes (predation), 25% unknown, and the remainder from human activities, both
direct (illegal hunting) and indirect (road kills).

Introduction

Egyptian or large grey mongoose, Herpestes ichnenmon, ıs the only herpestid (WOzENn-
CRAFT 1989) with free-ranging populations ın Europe (CORBET 1984; CARPANETO 1990),
where its distribution is limited to the southwestern quadrant of the Iberian Peninsula. At
the end of the last century ıt occurred in northwestern regions of Spain as well (DELIBES
1982). The species ıs included in the Spanish Vertebrate Red Data Book, where its status is
considered “unknown” (Icona 1986).

Except for some general data (VALVERDE 1960, 1967), and studies on its diet (DELIBES et
al. 1984; PALOMARES and DELIBEs 1991a, 1991b) and distribution (DELIBES 1982), the
biology and ecology of the Egyptian mongoose in Europe remain unknown. Recently,
radio-tracking studies on time budget and spacing have been carried out ın Donana
Natıonal Park (BELTRAN et al. 1985; DELIıBESs and BELTRANn 1985; PALOMARES 1990;
PALOMARES and DeLises 1991c). Here we describe some aspects of the physical and
population characteristics of Egyptian mongooses in Donana, including body mass,
external measurements, sex and age proportions, reproduction, density, survival rates, and
causes of mortality.

Material and methods

Trappıng of mongooses and marking with radıo-collars were carried out from September 1987 to
September 1989 at Coto del Rey (Northern Donana National Park, SW Spain, approx. 37°9’N
6° 26’ W) (PaLomares 1990). Coto del Rey ıs almost completely reforested by pines, Pinus pinea, and
eucalyptus, Eucalyptus sp., with undergrowth mainly of Halimium halimıfolium. Small natural
streams, where Fraxinus sp., Populus alba, Pistacia lentıscus and Rubus sp. grow, also occur. Patchily
distributed over the area, assocıations of Lentiscus are found at sites with a higher water table. The
climate is subhumid Mediterranean, characterized by dry, hot summers and wet, mild winters. The

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5702-094 $ 02.50/0

Some physical and population characteristics of Egyptian mongooses 95

terrain is flat and the soil ıs sandy. For more information about the study area, see VALVERDE (1958)
and Rıvas-MARTINEZ et al. (1980).

Captured anımals were sexed, weighed, and aged according to tooth wear (adults, with definitive
and completely developed teeth; immatures, with definitive teeth, but with some teeth still growing;
and young, with one milk tooth or more). The following body measurements were taken for every
animal: head-body length, tail (terminal hairs not included) length, hilt height, hind-foot length and
ear length.

Birth dates were obtained by estimating the age of the young individuals from body mass, head-
body length and tail length when trapped, following BEn-Yaacov and Yom-Tov (1983). Courtship
and copulation dates were estimated by direct observations from radio-collared individuals, and from
data ot birth dates, assuming a gestation period of 60-70 days (Kınacpon 1977; BEN-YAAcCoV and
Yom-Tov 1983). The number of cubs per birth was obtained from observation of famıly groups with
at least one radio-collared individual, and by examining two pregnant females. Additionally,
information on copulations, births, and litter size obtained in other sites in southern Spain and from
captive individuals between 1973 and 1977 is also included.

Density was estimated from radio-tracking data of adult individuals. It was based on home range
size and the percentage of overlap of the minimum area (minimum convex polygon method) where the
trapping was undertaken (or trapping area; see McLErLan 1989, for a description of method). Since
most mongooses were caught and tracked in 1988-89, we use the data from thıs period, although they
are completed with those of the previous year (since home ranges seemed very stable although its
dwellers changed; PALOMARES 1990). The home range of each individual was estimated by use of the
minimum convex polygon method (MACDONALD et al. 1980), using only animals localized for 20 or
more isolated times (time between locations was at least 4 hours; SwIHART and SLADE 1985; REYNOLDS
and LAUNDRE 1990).

Rates of survival (annual and total for the two study years, for both adult and young, immatures
included) were estimated from daily survival for the tracking period using MICROMOR program
(Heısey and FurLer 1985). Radio-collared mongooses and untagged anımals frequently sighted
together, were included in the analysıs. Causes of death were determined from autopsy. The annual
period to estimate survival rates of the young (see HEısey and FuULLErR 1985) was early July to early
February, the only period in which they were sighted and trapped in the study area (PALOMARES
1990).

Results
Physical characteristics

Only body mass was significantly different between males and females (means of 3142 g
and 2823 g, respectively; p = 0,04, “t” test; Tab. 1). No other difference was significant
(p > 0.05), although males appeared to be larger (Tab. 1).

Sex and age rates

Of 25 captured mongooses 9 were males and 16 females (1M:1.8F); the ratio dıd not differ
significantly from equality (x? = 1.960, p = 0.162; Exact Test of WELLs and KınG 1980). A

Table 1. Mean and standard deviation (SD) of body mass (g) and external measurements (mm) of
adult male and female Egyptian mongooses caught from September 1987 to September 1989 in
Donana National Park

The “t” test and probability (p) values for comparisons of traits between sexes are given

Mass’ Head-body* Tail-base* Hilt® Back foot* Ear®
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD

Males BD 20577612052.6.72.. 25100 HA4926 024,3 212.97 28.3 7186.99 15.
Een2les9,823, 3 1777.4, 1529:7. 19.843353 723.7,,0210.8%17.2, 90.6072.

a
ar

ec SD 0.297 1.530 0.193 0.716 0.409
p 0.040 0.771 0.144 0.851 0.495 0.689

“N = 9 and 12 for males and females, respectively. — BN = 8 and 11 for males and females,
respectively.

96 F. Palomares and M. Delibes

higher proportion of females was found in both young-immature (3M:6F) and adult
(6M:10F) individuals. None of these proportions differed significantly from the expected
1:1 ratio (X’ = 0.78 and 0.51, p= 0.622 and 0.722, respectively), possibly due to small
sampling sıze.

Young were trapped less often than adults (7 young, 2 immature and 16 adults; 1:1.8
between non-adults and adults). This proportion most likely changes throughout the year,
since, as suggested by trapping data, the young grow quickly and can hardly be differenti-
ated from adults at 9-12 months of age (PALOMARES 1990).

Reproduction

Courtship and copulation took place from early February to early June, with the peak
frequency (63.6 %) ın March and April, and births from mid April to mid August, with the
peak frequency (77.8%) from May to July (Figure). VALVERDE (1967) observed two births
in July and August. In captivity copulation was observed in January, March, April, May,
June and October (Figure).

6) ee e00 ewoee «eo e«o COPULATION °

BIRTH ® ......a."..."6e0exr

ee Tea en ra una Togre Tees rn TEEeetete sen pe nem; Soc seems Vogue Erese Zmeeee)
JAN FEB MAR APR MAY JUN JUL AUG SER OCT NOV

MONTH

Copulation and birth dates of Egyptian mongooses in Spain. Black circles = data obtained during
field work of this study; open circles = observations obtained in captivity; asterisks = data from
VALVERDE (1967)

The numbers of cubs observed ın four family groups were 2, 3, 3, and 2. In two
pregnant females 3 and 4 foetuses could be detected. On the other hand, a captive female
gave birth to 2 cubs, and another had 3 foetuses. In total, the mean number of cubs per
birth was 2.7 + 0.8.

Density

Nine adult mongooses inhabited their entire or partial home range in the trapping area
between January and August of 1989. However, the number of locations for a male was
insufficient for estimating home range size, and this information was replaced by the data
of another adult male, which occupied the same space one year previously. The total
number of localızations for 3 males and 6 females was 807 (mean = 89.7, SD = 80.0, range
= 20-259). Mean individual percentage of home range overlapping with the trappıng area
was 34.4 % (SD = 16.6, range = 4.0-61.4). Estimated density of adult mongooses was 1.2
ind./km?. If we consider the above-estimated proportions of young and immature indi-
viduals in the population, the total density would be near 2 ind./km?.

Some physical and population characteristics of Egyptian mongooses N

Causes of mortality and survival rates

Twenty-four of 25 trapped mongooses were equipped with radıo-collars. Of these, one
adult female was shot, one young female was killed by a dog, Canıs lupus f. fam., or lynx,
Felis pardina, and one adult male was caught ın a poacher’s foot-trap. The radıo-collars of 3
other adult females, stopped sending, probably due to death of the anımal. At least once,
local people said that they had been killed

by poachers. Of 5 mongooses not equipped Table 2. Numbers of individuals controlled
with radio-collars but used to stay with a (NC), deaths (ND) and survival rates of adult
radio-collared animal, 4 might have died: and young Egyptian mongooses in Coto del
two cubs of the shot female, and the other Rey during each study year

two which were no longer observed after a 9% % confidence limits are shown in parentheses.
poacher had set foot-traps in their core Number of days/mongoose for each period and
ee age class was 592 and 707 in adults, and 209 and

NEST EBErEmose cases confidence in 426 in the young, for 1987/88 and 1988/89,
respectively

tervals are wide, annual survival rates were

very low, oscillating between 0.13 ın 1988/
89 for adults and the same figure in 1987/88
for young, and 0.6 in 1987/88 for adults Aehlke

Survival

(Tab. 2). For adults, differences between 1987/88 0.60 (0.22-1.0)

years were significant (Z= 2.03, p= 1988/89 0.13 (0.02-0.95)

0.0212). After two years, life expectancy Total 0.08 (0.01-0.73)

did not exceed 8% for both the adults and Young

young (Tab. 2). 1987/88 0.13 (0.01-1.0)
1988/89 0.22 (0.04-1.0)

We have additional data since December
1985 on mortality of sıx mongooses from
other locations in Donana National Park.
From 16 dead mongooses, 2 died ın foot-traps, 2 others in road kills, 1 was captured ın a
snare, 1 was shot and 10 died from unknown causes. The last category includes 2 shot
female cubs, and 2 young and one adult female most likely trapped by poachers. Accepting
the evidence as valid, at least 56.3 % of these deaths were caused by illegal hunting, 12.5 %
by indirect human actıon (road kills), 25 % by unknown causes, and only 6.3 % by natural
causes (predation).

Total 0.03 (0.0 -0.78)

Discussion

Mongooses of Donana have greater body mass than individuals trapped throughout
southern Spain and Israel, and ın both places body mass was significantly different for each
sex (BEN-Yaacov and Yom-Tov 1983; DELIBES et al. 1984). In Israel (the only country
with data), head-body length was also sıgnificantly different between males and females.

Females were more often trapped than males; however, this situation is rare ın
carnıvores (e.g., GORMAN 1979; BusKIRK and LINDSTEDT 1989, for a review in mustelids;
FULLER 1989; HELLGREN and VAUGHAN 1989). This result is usually attributed to the
greater movements and larger home ranges of males, which are thus more inclıned to enter
traps (see BuskırKk and LinnpsTept 1989). Male mongooses had, as a rule, larger home
ranges than females, and a higher number of core areas (PALOMARES 1990). This should
have produced a higher probability of capture which, however, was not found. Since more
young females than males (both roaming in family group; PALOMAREs 1990) were also
trapped, perhaps an unequal sex ratio could be the cause. Nevertheless, the spacing system
of mongooses (with several females inside the territory of an adult male; PALOMAREs 1990)
could produce a reversed proportion is less favourable areas, where the males searching for
an unoccupied territory would superabound. In captures in Cädız country (southern

98 F. Palomares and M. Delibes

Spain) more males than temales (30M:11F) occurred (DELIBEs, unpubl.). Adding the data
of Donana to the last mentioned site, the sex ratio is IM:1F (N = 66).

Copulation and birth dates, and oftspring sıze obtained in this study, are similar to data
presented by DÜcker (1965) for captive individuals. Nevertheless, with our method to
calculate offspring sıze there ıs no guarantee for a lose of cubs, prior to observation dates.
In fact, during the tracking period, a young was killed by a dog or lynx, and 2 others were
lost under unusual circumstances (most likely killed by poachers), while still accompanied
by their mothers. Birth dates overlap with yearly peaks of rabbit (Oryctolagus cuniculus)
density (BELTRAn 1991). Rabbits are the main prey of mongooses ın this area (PALOMARES
and DELIBEsS 1991b).

Mongoose density outside the trappıng area ıs lower than inside, since we studied the
more favourable habiıtats and sıtes. On the other hand, a weak point of our method lies in
the territoriality of the studied species and in the setting-up of the study-area boundaries.
Both problems were solved by the home range exclusivity of mongooses in Dofiana,
especially males (PALOMAREs 1990), and the determination of a “trapping area” according
to McLELLAN (1989).

The lower survival rates and higher mortality due to human actions prove again that a
National Park status ıs not sufficient guarantee of species conservation (DAsMAnn 1983),
especially in the case of carnıvores which need large home ranges and usually inhabit edges
of protected areas (FERRERAS et al. 1991). Only a high birth rate and immigration from
other areas with lower mortality can explain the survival and the high relative density of the
species in the study area.

Acknowledgements

The research was supported by DGICYT (project PB87-0405). One of the authors (FP) received a
postdoctoral grant from Consejo Superior de Investigaciones Cientificas. N. BUSTAMANTE and R.
FraGAa reviewed the English version and C. KELLER translated the German summary.

Zusammenfassung

Einige Daten zur Populationsbiologie des Ichneumons (Herpestes ichneumon L., 1758)
in Südwest-Spanıen

Eine Population des Ichneumons (Herpestes ichneumon) wurde über einen Zeitraum von zwei Jahren
in Südwestspanien (Nationalpark Donana) mit Hilfe von Fallenfängen und Radiomarkierung unter-
sucht. Daten zu Körpergewicht und Größe, Geschlechtsproportionen, Altersstruktur, Fortpflan-
zung, Populationsdichte, Überlebensrate und Sterblichkeitsursachen werden mitgeteilt. Die
Geschlechter unterscheiden sich nur im mittleren Gewicht (3142 g bei Männchen und 2823 g beı
Weibchen). Weibchen fingen sich öfter in Fallen als Männchen, unabhängig vom Alter (1,8W:1M).
Paarungen wurden hauptsächlich im März und April (63,6%), Geburten im Mai, Juni und Juli
(77,8%) registriert. Die Wurfgröße betrug 2,7 # 0,8 (N = 7). Die Populationsdichte für adulte
Ichneumons wird auf 1,2 Ind. /km? geschätzt. Die “ährliche Überlebensrate war trotz breiter Konfi-
denzintervalle sehr niedrig; 0,6 (1987/88) und (0, 13 (1988/89) für Adulte, und 0,13 (1987/88 für
Jungtiere. Wenn beide Jahre miteinbezogen rrandlen. dann überschreiter die Über er %,
sowohl bei Adulten wie bei Jungtieren. Die Mortalität von 16 aufgefundenen Tieren war in 6,3 % der
Fälle auf natürliche Ursachen (Prädatoren) zurückzuführen; 25 % der Fälle bleiben ungeklärt, und in
den übrigen Fällen waren entweder illegale Jagd oder der Straßenverkehr verantwortlich.

References

BELTRAn, J. F. (1991): Temporal abundance pattern of the wild rabbit in Donana, SW Spain.
Mammalıa (in press).

BELTRAN, ]J. F.; Derısges, M.; IBÄNez, D. (1985): Immobilization and marking of the Egyptian
mongoose, Herpestes ichneumon (L.), in Spain. Z. Säugetierkunde 50, 243-244.

BEn-Yaacov, R.; Yom-Iov, Y. (1983): On the biology of the Egyptian Mongoose, Flerpestes
ichneumon, in Israel. Z. Säugetierkunde 48, 34-45.

Buskirk, $. W.; LINDSTEDT, $. L. (1989): Sex biases in trapped samples of mustelidae. J. Mammalogy
70, 88-97.

Some physical and population characteristics of Egyptian mongooses 99

CARPANETO, G. M. (1990): The Indian grey mongoose (Herpestes edwardsi) ın the Circeo National
Park: a case of incidental introduction. Mustelid and Viverrid Conserv. 2, 10.

CoRBET, G. B. (1984): The mammals of the Palearctic Region: a taxonomic review (Supplement).
London: British Museum (Natural History).

Dasmann, R. F. (1983): The relationship between protected areas and indigenous peoples. In:
Proceeding of the World Congress on National Parks. Ed. by J. D. McNezry and K.R. MILLER.
Switzerland: IUCN. Gland.

Deriıses, M. (1982): Notas sobre la distribuciön pasada y actual del meloncillo Herpestes ichneumon
(L.) en la Peninsula Iberica. Donana Acta Vert. 9, 341-352.

DELIBES, M.; AYyMERICH, M.; CuzsTa, L. (1984): Feeding habits of Egyptian mongoose or Ichneumon
in Spain. Acta Theriol. 29, 205-218.

DeLises, M.; BELTRANn, J. F. (1985): Activity, daily movements and home range of an ichneumon or
Egyptian mongoose (Herpestes ichneumon) ın Southern Spain. J. Zool. (Lond.) 207, 610-613.
Dücker, G. (1965): Das Verhalten der Schleichkatzen (Viverridae). Handbuch der Zoologie Berl. 8,

148.

FERRERAS, P., ALDAMA, ]. J.; BELTRANn, J. F.; DELıBEs, M. (1992): Rates and causes of mortality in a
fragmented population of Iberian Iynx, Felis pardina (Temmick). Biol. Conserv. (in press).

FULLER, T. K. (1989): Population dynamics of wolves in North-Central Minnesota. Wildl. Monog.
105, 141.

GoRrman, M.L. (1979): Dispersion and foraging of small Indian mongooses, Herpestes auropunctatus
(Carnıvora: Viverridae) relative to the evolution of socıal viverrids. J. Zool., Lond. 187, 65-73.

Heısey, D. M.; FuLLer, T. K. (1985): Evaluation of survival and cause-specific mortality rates using
telemetry data. J. Wildl. Manage. 49, 668-674.

HELLGREN, E. C.; VAUGHAN, R. (1989): Demographic analysıs of a black bear population ın the Great
Dismal Swamp. J. Wildl. Manage. 53, 969-977.

Kıncpon, J. (1977): East afrıca mammals. An atlas of evolution in Africa. Vol. IIla. London:
Academic Press.

MacponaLD, D. W.; Bauı, F. G.; HoucH, N. G. (1980): The evaluation of home range sıze and
configuration using radıo tracking data. In: A Handbook on Biotelemetry and Radio Tracking.
Ed. by C.J. Amzaner and D.W. Macponaın. Oxford: Pergamon Press, Pp. 405-424.

I Torslän, B. N. (1989): Dynamics of a grizzly bear population during a period of industrial
resource extraction. I. Density and age-sex composition. Can. J. Zool. 67, 1856-1860.

PALOMARESs, F. (1990): Ecologia y organizacıön socıal del meloncillo, Herpestes ichneumon, L., en el
Parque Nacional de Donana. Ph. D. Thesis, Univ. Granada, Spain.

PALOMARES, F.; DELIBES, M. (1991a): Alimentaciön del meloncillo Herpestes ichneumon y de la gineta
Genetta genetta en la Reserva Biolögica de Donana, S.O. de la Peninsula Iberica. Donana Acta
Vert. 18, 5-20.

— — (1991b): Dieta del meloncillo, Herpestes ichneumon, en el Coto del Rey (Norte del Parque
Nacional de Donana, S.O. de Espana). Donana Acta Vert. 18, (in press).

— — (1991c): Ecologia comparada de la gineta Genetta genetta (L.) y el meloncillo Herpestes
ıchneumon (L.) (Mammalia; Viverridae) en Donana (SO de la Peninsula Iberica). Bol. R. Soc. Esp.
Hist. Nat. (Sec. Biol.) 87, 269-278.

REynoLDs, T. D.; LAUNDRE, ]. W. (1990): Time intervals for estimating proghorn and coyote home
ranges and daily movements. J. Wildl. Manage. 54, 316-322.

Rıvas-MARTINEZ, S.; CosTA, M.; CASTROVIEJO, $.; VALDES, E. (1980): Vegetacion de Donana
(Huelva, Espana). Lazaroa 2, 1-189.

SWIHART, R. K.; SLADE, N. A. (1985): Influence of sampling interval on estimates of home-range size.
J. Wildl. Manage. 49, 1019-1025.

VALVERDE, J. A. (1958): An ecological sketck of the Coto Donana. British Birds 51, 1-23.

— (1960): Vertebrados de las Marismas del Guadalquivir. Arch. Inst. Aclim. Almeria 9, 1-168.

— (1967): Estructura de una comunidad de vertebrados terrestres. Mon. Est. Biol. Donana 1, 1-218.

Weııs, H.; Kınc, ]J. L. (1980): A general “Exact test” for NxM contingency tables. Bull. Southern
California Acad. 79, 65-77.

WOZENCRAFT, W. C. (1989): The phylogeny of the recent Carnıvora. In: Carnıvore Behavior,
Ecology, and Evolution. Ed. by J.L. GrrtLeman. London: Chapman and Hall. Pp. 495-535.

Authors’ address: FRANcISCO PALOMARES and MıGuUEL DELIBEsS, Estaciön Biolögica de Donana,
CSIC, Apdo. 1056, E-41080 Sevilla, Spain

Z. Säugetierkunde 57 (1992) 100-102
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Bacular variation in the subgenus Trinomys, genus Proechimys
(Rodentia: Echimyidae)

By Leıra M. PessöA and $. F. Dos Reıs

Departamento de Zoologia, IB, Universidade Federal do Rio de Janeiro and Departamento de
Parasitologia, IB, Universidade Estadnal de Campinas, Brazil

Receipt of Ms. 15. 5. 1991
Acceptance of Ms. 16.9. 1991

Abstract

Bacular morphology and variation in the four species of spiny rats of the subgenus Trinomys, genus
Proechimys ıs described. Each species can be uniquely diagnosed on the basis of bacular morphology
alone. Proechimys dimidiatus and P. iheringi have similar overall bacular morphology, although they
differ noticeably from P. setosus and P. albispinus. The latter two species differ markedly in the
morphology of the baculum.

Introduction

The spiny rats included ın the subgenus Trinomys Thomas, genus Proechimys Allen, occur
in eastern Brazil from the state of Bahıa to the state of Säo Paulo. According to MOOJEN
(1948) four species are recognized in the subgenus Trinomys: P. dimidiatus (Günther), P.
iheringi Thomas, P. setosus (Desmarest), and P. albispinus (Geoftroy). These species can be
diagnosed on the basıs of a combination of traits that include the size, shape, and color of
arıstiform hairs, morphology of the skull, and pattern of cheekteeth counterfolds (MOOJEN
1948), although substantial overlap in the distribution of character states among the species
makes ıdentification a rather difficult task. To date there have been no studies of bacular
morphology in the subgenus Trinomys. In thıs note we describe bacular morphology and
varlatıon in the four species of the subgenus Trinomys.

Material and methods

The specimens employed in this study were ıidentified using a combination of pelage and skull traits
described by Moojen (1948). Phallı were removed from skins of preserved specimens deposited ın the
mammal collection of the Museu Nacional (UFR]J) and immersed in water for 24 hours. Bacula were
dissected from surrounding tissues under the binocular microscope. Only adult specimens, age classes
8-10 of Patron and RoGers (1983), were used in this study. The following samples were examined:
P. dimidiatus (state of Rio de Janeiro: Tijuca [n = 5]); P. iheringt (state of Espirito Santo: Santa Teresa
[n = 5]); P. setosus (state of Minas Gerais: Juiz de Fora [n = 2]), Peti [n = 1], Lagoa Santa [n = 1]);
P. albispinus (state of Bahia: Jaguaquara [n = 1], Jequie [n = 4)).

Results and discussion

The baculum in the subgenus Trinomys ıs an elongate and narrow structure with a straight
shaft (see Figure and Table). This structure varies, however, in the shape of the proximal
and distal ends and in the development of the dorsoventral curvature. In P. dimidiatus the
shaft does not show any development of a dorsoventral curvature but it has a lateral
indentation near mid-shaft. The proximal and distal ends are evenly round, and the latter

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5702-100 $ 02.50/0

Bacular variation in the subgenus Trinomys, genus Proechimys 101

shows no development of apical wings or median depression. In P. iheringi the shaft has a
slight dorsoventral curvature in the proximal third, and shows an indentation near the
distal end. The distal end is slightly concave and has no apıcal wings or median depression.
The shaft broadens near the proximal end and is tapered in the tip. The baculum in
P. setosus does not show a dorsoventral curvature and has a lateral indentation near the
posterior tip. The proximal and distal ends are nearly square. The proximal end is slightly
paddle-shaped and the distal end has no apical wings or median depression. In P. albispinus
the baculum has a dorsoventral curvature and slightly tapered lateral indentations near
mid-shaft. The proximal end ıs paddle-shaped and pointed. The distal end has well
developed apical wings with a pronounced median depression (Figure).

10 mm
Ventral (A) and lateral (B) views of bacula of species of the subgenus Trinomys, genus Proechimys.
The distal part is put to the top (ventral view) and left (lateral view). 1: P. dimidiatus, 2: P. iheringi,
3: P. setosus, 4: P. albispinus

Four measurements were taken from bacula of the four species and are shown in Table
1. Proechimys dimidiatus, P. iheringı, and P. setosus bacula are similar in greatest length of
shaft (Table). These species are also sımilar in body size (MooJEn 1948). On the other
hand, P. albispinus has the smallest body size among the species of Trinomys (MOOJEN
1948) but it has the largest baculum.

Overall bacular morphology ıs sımilar ın both P. dimidiatus and P. iheringi although
their bacula differ noticeably from those of P. setosus and P. albispinus. The latter two
species also ditfer markedly ın bacular morphology. MoojJEn’s (1948) assessment of
specific variation in the subgenus Trinomys revealed several cranıal characters shared by P.
dimidiatus and P. iheringi and by P. setosus and P. albispinus. He actually ımplied a close
morphological relationship between P. dimidiatus and P. iheringi. The morphological

Means and (standard deviations) for measurements taken from bacula of the four species of
Proechimys of the subgenus Trinomys

Characters Taxon
P. dimidiatus P. iheringi P. setosus P. albıspinus

Greatest length of shaft
Maximum width of proximal end
Maxımum width of distal end
Least width of shaft

102 Leila M. Pessöa and S. F. dos Reis

similarity found by MoojJEn (1948) for the latter species is indeed corroborated by bacular
morphology. On the other hand, the similarıty between P. setosus and P. albispinus
established on the basıs of cranıal morphology (MooJEn 1948) is not supported by bacular
morphology.

Parron (1987) recently reviewed morphological varıation and systematics in the
subgenus Proechimys and showed that the baculum can be either long and narrow or
massıvely long and broad. Parron (1987) also showed that bacular morphology in
addition to skull morphology allowed the definition of nıne groups of species in the
subgenus Proechimys. We showed here that each species ın the subgenus Trinomys can be
uniquely diagnosed by the morphology of the baculum. We believe this is an important
result because the degree of distinctiveness ın bacular morphology among species of
Trinomys ıs not matched by the amount of varıation known to exist in the skull and pelage.
The skull and pelage have tradıtionally been employed in the taxonomy of the subgenus
Trinomys, but have not always allowed correct ıdentification of taxa. It should also be
pointed out that, whereas ın the subgenus Proechimys the baculum can be useful to define
groups of species (PATTon 1987), ın the subgenus Trinomys this structure is diagnostic at
the species level.

Acknowledgments

We are indebted to Prof. ]J. F. Da Cruz and Dr. ULisses CARAMASCHI, Museu Nacional, UFR]J, for
allowing us to examine specimens under their care. We are also indebted to Dr. G. FonsEca and G.
HERMANN, Universidade Federal de Minas Gerais, for the donation of one specimen used in this
study. J. R. SOMERA made the drawings of the bacula. Research supported by funds from Conselho
Nacıonal de Desenvolvimento Cientifico e Tecnolögico (CNPq), Fundagäo de Amparo & Pesquisa do
Estado do Rio de Janeiro (E-29/170.339/90), Fundacäo de Amparo & Pesquisa do Estado de Säo Paulo
(88/2237-4, 89/0772-1, 89/3405-0). Work by SFR ıs partially supported by a research fellowship from
(CNPq). LMP is partially supported by fellowship from Programa de Incentivo a Capacitacäo
Docente (UFR]).

Zusammenfassung

Baculumvariation im Subgenus Trinomys, Genus Proechimys (Rodentia: Echimyıdae)

Morphologie und Variation von Bacula werden für 4 Arten von Stachelratten des Subgenus Trınomys,
Genus Proechimys beschrieben. Danach kann jede Art eindeutig diagnostiziert werden. Dennoch sind
die Bacula von Proechimys dimidiatus und P. iheringi einander in Form und Ausmaßen ähnlicher,
gegenüber denen von P. setosus und P. albispinus jedoch deutlich verschieden.

Literature

MOOoJEN, J. (1948): Speciation ın the Brazilian spiny rats (Genus Proechimys, Family Echimyidae).
University of Kansas Publications, Museum of Natural History 1, 301-406.

Parron, J. L. (1987): Species groups of spiny rats genus Proechimys (Rodentia, Echimyidae).
Fieldiana: Zoology, n.s. 39, 305-345.

Patron, J. L.; ROGERs, M. A. (1983): Systematic implications of non-geographic variation in the
spiny rat genus Proechimys (Echimyidae). Z. Säugetierkunde 48, 363-370.

Authors’ addresses: LeıLa M. Pessöa, Departamento de Zoologia, IB, Universidade Federal do Rio
de Janeiro, IlIha do Fundäo, 21941, Rıo de Janeiro, RJ, Brazil; SERGIO F. Dos
Reıs, Departamento de Parasıtologia, IB, Universidade Estadual de Campinas,
13081, Campinas, SP, Brazil

|
Z. Säugetierkunde 57 (1992) 103-111
© 1992 Verlag Paul Parey, Hamburg und Berlin

ISSN 0044-3468

Postnatal development of three sympatric small mammal species
of southern Africa

By EDITH R. DEMPSTER, M.R. PErRIn, and R. J. NuTTaLı

Department of Zoology and Entomology, University of Natal, Pietermaritzburg, South Africa

Receipt of Ms. 16.5. 1991
Acceptance of Ms. 30.10. 1991

Abstract

Four species of small mammals occur sympatrically in an arıd area of the southwestern Cape Province.
Females of all four species produced young after capture during a field excursion in September 1990.
Postnatal development of three species, namely Tatera afra, Acomys subspinosus and Elephantulus
edwardii, is reported for the first time, and compared with recorded data for the fourth species,
Aethomys namaquensıis.

T. afra produced altricıal, nıpple-clinging young, while young of E. edwardii were precocıal and
did not nipple-cling. A. subspinosus produced semi-precocial young which grew rapidly. Young of A.
namaquensis are reported to be altrıcial, but the level of development at birth is more advanced than
that of T. afra.

Differences in habitat and body size cannot account for the different life-history styles of these
four species. Congenerics of each species included in this study exhibit similar life-history styles, with
the exception of Acomys species, and it is suggested that altriciality/precociality is a phylogenetically
conservative character in small mammals.

Introduction

Many theories have attempted to explain differences ın life history styles of mammals
(PERRIN 1989). Adult body size, environment and phylogeny are just three of the factors
which have been implicated in the selection of particular life history styles in anımals.
WESTERN (1979) found that gestation time, growth rates, age at first reproduction,
lifespan, birth mass and litter mass are all allometrically scaled to adult mass in mammals.
NEAL (1990) reviewed pre- and postnatal growth and development of 29 genera of African
muroid rodents. He found that adult body mass had a strong influence on birth mass,
gestation time, foetal growth rate, postnatal growth rate and litter growth rate. There was
little evidence for phylogenetic effects on developmental parameters.

STEARNS (1983) and CREIGHTON and STRAUSss (1986) agree that most parameters of
postnatal development of mammals scale to adult body size, but there appear to be
phylogenetic constraints on the evolution of lıfe-histories, and these differ from lineage to
lineage.

The role of environment ın selection of life history styles has been reviewed by SıBLy
and Carow (1985). Environmental conditions may determine the growth rates of oftspring
and age-specific survivorship, but internal constraints and trade-ofts also influence life
history strategies (SıgLy and CaLow 1985). BurpA (1989) found no correlation between
length of postnatal development and habitat, diet, social structure, climate, or ability/
inability to vary metabolic rate in several rodent taxa.

The present study arose as a result of a field excursion to the Niewoudtville district of
the Cape province. This area falls within the Western Mountain Karoo vegetation type
(Acocks 1988). Very little soil covers the stony ground, which consists of shale, fine-
grained sandstone and granıte. Mean annual rainfall is less than 150 mm, most of which

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5702-103 $ 02.50/0

104 Edith R. Dempster, M. R. Perrin, and R. J. Nuttall

falls in winter. Vegetation consists of little grass and small, widely-scattered bushes
(Acocks 1988).

Three rodent species of the subfamilies Gerbillinae (Tatera afra) and Murinae (Acomys
subspinosus, Aethomys namaquensis) and one macroscelid species, Elephantulus edwardi,
were trapped on the farm Sewefontein, and females of all species produced young after
capture. Postnatal development of three species, 7. afra, A. subspinosus and E. edwardii
has not been recorded previously. Thus an opportunity was provided for recording the
postnatal development of these species, and for comparing the development of four
sympatric species of different genera and different body size.

Materials and methods

Five female Elephantulus edwardi; 4 temale Tatera afra;, 3 female Acomys subspinosus; and 4 female
Aethomys namaquensis were live-trapped between 13. and 15. September 1990.

Individuals were caged singly after capture and returned to the animal house at the University of
Natal, Pietermaritzburg. E. edwardii were housed in 60 x 30 x 30 cm glass terrain; all other species
were kept in laboratory rodent cages. Rodent species were fed a mixture of seeds and rat cubes,
supplemented with carrots, greens and insects. E. edwardii were fed “Pronutro”, insects and
sunflower seeds.

Young were weighed on a Sartorıus U6300 balance, correct to 0.1 g, and hindfoot measurement
was taken correct to 0.1 mm as an index of physical growth. Measurements commenced at birth-1 day
old, and were taken at intervals of 1-3 days until young were 40-50 days old.

Postnatal growth rates were calculated for the relatively linear phase of increase in mass and

E-mB
hindfoot length (Case 1978). Growth rate was calculated as _— where mE = measurement at

end of growth phase; mB = measurement at bırth; t = time in days from birth to end of linear growth
phase. Average growth curves were constructed by calculating mean mass and hindfoot length of all
young in each 2-day age class.

Physical development was assessed on the days of weighing. Developmenal criteria used in
assessing the level of physical development were as follows: ear pinnae folded down and attached to
the head or folded back and free of attachment, lower or upper incisors erupted, eyes open or closed,
degree of hair proliferation (a dark pigmentation of the skin was taken to represent the beginning of
haır proliferation), toes fused or separate. The ages at which young were first attached to and
spontaneously detached from the nipples were recorded, if nıpple-clinging occurred. Weaning was
judged to have begun when young were first seen eating solid food, and was complete when young
were no longer suckled.

Results

The number ot litters for each species, litter sızes, and longest interval between capture and
birth of young are shown in Table 1. All females of the species 7. afra, A. subspinosus and
E. edwardii were pregnant when captured. In addition, three out of four Aethomys
namaquensis gave bırth to 3, 4 and 4 young within 2 weeks of capture.

Growth curves for mass and hindfoot length of T. afra, E. edwardii and A. subspinosus
are shown in Figs. 1 and 2. The postnatal development of Aethomys namaquensis has been
described previously (NEAL 1990), and is not included ın the present study.

Table 1. Numbers of litters, litter sizes, and longest interval from capture to birth of young
of T. afra, A. subspinosus and E. edwardii

T. afra A. subspinosus E. edwardıi

Number of litters 4 3
Litter sızes 3,4,4,5 ER)
Longest capture-Birth interval 18 days 27 days

Postnatal development of three sympatric small mammal species 105

A

508
48
38
28

19

Mass (g)

8 18 28 38 408
Age (days)

Fıg. 1. Mean mass (+ s.e.) of A: Tatera afra, B: Acomys subspinosus, C: Elephantulus edwardii

Body dimensions, growth rates, and timing of physical developmental parameters are
shown in Table 2. Results show a clear difference ın level of development at birth among
the neonates of the three species. 7. afra neonates were small relative to adult mass, A.
subspinosus neonates were larger relative to adult mass than T. afra, and E. edwardıi
neonates were the largest relative to adult mass. When mean litter mass relative to adult
mass was considered, 7. afra still had the smallest litter mass (17.3 % of adult mass), while
A. subspinosus and E. edwardii had litter masses of 46.5% and 42.5% of adult mass,
respectively.

Growth rates in mass and hindfoot length were most rapıd for 7. afra, although at 30
days of age, young of this species had achieved only 30 % of adult mass and 78 % of adult
hindfoot length. A. subspinosus had reached 87 % of adult mass at 30 days old,and 94 % of

106 Edith R. Dempster, M. R. Perrin, and R. J. Nuttall

Hindfoot length (mm)

8 18 28 38 408
Age (days)

Fig. 2. Mean hindfoot length (# s.e.) of A: Tatera afra, B: Acomys
subspinosus, C: Elephantulus edwardıı

adult hindfoot length after
only 16 days. E. edwardıı
had reached 65 % of adult
mass and 95% of adult
hindfoot length by 30 days
of age.

Physical development
proceeded at different
rates ın the three species.
T. afra neonates were hair-
less, unable to crawl effec-
tıvely, blind, and had toes
fused and ear pinnae fused
to the head. Hair began to
emerge from approximate-
ly 7 days of age, at which
time the ear pinnae became
detached from the skin of
the head. Young were
firmly attached to the
nıpples and were dragged
with the mother when she
moved. Incisors emerged
at about 1O days and a
groove was noticed be-
tween the two lower in-
cısors. Eye-opening was
recorded at 18-21 days,
and shortly after this,
young were seen detached
from the nipples, eating
solid food, and moving
freely away from the nest.

A. subspinosus neonates
were also naked and blind
at birth, but haır was viısı-
ble 1-2 days after bırth,
ear pinnae were free, and
toes were separated within
2 days of birth. Nipple-
clinging was not observed
in A. subspinosus. Incisors

erupted at approximately 7 days, and eyes opened at 9-10 days, at which time young were

able to walk efficiently.

E. edwardii neonates were fully furred at birth, with eyes open, incisors erupted, ear
pinnae free and toes separated. They were first observed eating solid food at 12-16 days.
Nipple-clinging did not occur in this species, and neonates were fully mobile from bırth.

Postnatal development of three sympatric small mammal species 107

Table 2. Summary of body dimensions, litter, size, growth rates, and timing of certain
developmental features in T. afra, A. subspinosus and E. edwardii

Characteristic T. afra A: subspinosus E. edwardii
Adult body mass? (g) x 95.0 (n = 15) 21.3 (n = 26) 50.4 (n = 16)
Range 781413 17-25 36-65

Birth mass # s.e. ee ee) IE NS)

Birth mass % adult mass 4.3 % 15.5 % 23.6 %

Litter sıze 4.0 (n=4) 3.0 (n=3) 1.8 (n=5)

Litter mass % adult mass 173% 46.5 % 42.5 %

Growth rate (g/day) 0.82 0.55 0.59

Linear growth phase 0-43 days 0-28 days 0-38 days

Adult hindfoot (mm) x 37.7 (n = 15) 17.0 (n = 26) 34.6 (n = 16)
Range 28-40 13-19 33-36

Birth hindfoot # s.e. ZI ORT 9742 0,2 DS /u = 02

Birth % adult hindfoot 21.0 % 57.0 % 74.3 %

Growth rate (mm/day) 0.64 0.55 0.30

Linear growth phase 0-39 days 2-13 days 1-25 days

Age (days) at development

Ear pinnae free 6-7 0-1 0
Dorsal hair 6-8 1 0
Ventral hair 12 1 0
Toes separated 10-16 0 0
Incisors erupt 10 7. )
Eyes open 20 9-10 0
Attached to nipples 1-3 - -
First unattached 22-24 - -
Efficient walking 24 9-10 0
Eat solid food 22-23 ? 12-16

* Data from SKINNER and SMITHERS (1990).

Discussion

The distinetion between altrıcıal and precocıal young has been applied to many bird and
mammal species. Precocial mammals are fully furred, have their eyes open, and are fully
mobile shortly after birth. By contrast, altrıcıal young are naked, blind, helpless, and
unable to maintain their body temperature. Of the species included in the present study, EZ.
edwardi ıs clearly precocıal, while 7. afra bears altrıcıal young. A. subspinosus neonates
fall between the two extremes, and are classıfied here as semi-precocial.

Differences ın the mass of individual neonates at birth are related to the length of the
gestation period ın precocıal and altrıcial species (NEAL 1990). The gestation period for the
species reported here ıs not precisely known; however, all pregnant 7. afra gave birth
within 18 days of capture, while A. subspinosus and E. edwardi produced young at
intervals up to 30 days from capture. This corresponds with observations of a short
gestation period for 7. brantsu (22 days) and 7. leucogaster (28 days) (ScoTT 1979), longer
gestation period (45 days) in A. dimidiatus (Ar-KHauıLı and DeranyY 1986), and a
gestation period longer than 50 days in E. rufescens (NEAL 1982; RATHBUN et al. 1981), E.
intufi (TRrıpp 1972) and Macroscelides proboscideus (RATHBUN 1979). Litter sızes were
smaller for the semi-precocial A. subspinosus and precocial E. edwardii than for the altrıcıal
T. afra, and individual mass and litter mass relative to adult mass were more than two times
greater in the semi-precocial and precocıal species than in 7. afra. These results agree wıth
the general trends for precocial and altrıcial species of African rodents (NEAL 1990).

108 Edith R. Dempster, M. R. Perrin, and R. J. Nuttall

Near (1990) reported that postnatal growth rates of altrıcial and precocial rodent
species were positively correlated with birth mass, ı.e. larger neonates grew faster than
smaller neonates. This was the case in the present study, in which young of the larger
rodent neonate, 7. afra, grew at a faster rate than the smaller rodent neonate, A.
subspinosus. E. edwardii young had a faster growth rate in mass than A. subspinosus, but
the hindfeet of E. edwardiı grew more slowly than either of the rodent species.

The present study describes postnatal development in three small mammal species
which inhabit the same macro-environment, but employ different reproductive strategies.
A fourth species, Aethomys namaquensis, occurs ın the same habitat, and bears small
altrıcıal young which nipple-cling for the first 2-3 weeks of life (Near 1990). The
synchrony of reproduction in the four species trapped in the area was remarkable; 15 of the
16 temales trapped were pregnant. Environmental differences and differences in body mass
cannot explain the range of reproductive strategies exhibited by these species.

Reference to postnatal development of other Tatera species, Acomys species, Elephan-
tulus species, and Aethomys species reveals that many of the patterns observed in this study
are shared by other species of each genus. Reproductive parameters are summarized in
Table 3. Three southern African Tatera species, T. afra, T. brantsii and T. lencogaster have
a short gestation period, altrıcıal young, low birth mass relative to adult mass, litter mass
approximately 17% of adult mass, and hindfoot length 21-25 % of adult size (SCOTT
1979). T. brantsır ıs a partial nıpple- -clinger, while 7. lencogaster does not nipple- cling
(ScoTT 1979; NEAL 1990). Age at eye-opening is approximately 20 days in all three species.
Mean litter sıze ıs 2.95 for T. brantsu, 3.22 for T. lencogaster (ScoTT 1979) and 4.0 for
T. afra. Postnatal growth rate in mass ıs 1 g/day for T. lencogaster and T. brantsı.

Three Acomys species are non-nipple-clingers, wıth gestation periods longer than 4
weeks (NEAL 1983; AL-KHaLıLı and DELAnY 1986). Individual neonates weigh 13-18 % of
adult mass, and lıtter mass is 31-47 % of adult mass. A. dimidiatus (AL-KHauıLı and
DeELany 1986) and A. wılsoni (HUBBARD 1972) neonates are fully furred and have their eyes
open at birth, while A. subspinosus and A. hystrella (HuBBAarp 1972) develop these
characters a few days after bırth. Litter size of 1-3 neonates is characteristic of four Acomys
species for which information ıs available (Near 1990), and postnatal growth rates ın two
species are lower than growth rates of Tatera species (AL-KHaLıLı and DELAnNY 1986).

Three Aethomys species are nıpple-clingers, bearing small altrıcıal young ın litters of
3-4 young. Birth mass ıs 3-6 % of adult mass in all 3 species, and litter mass 13-25 % of
adult mass. Eyes open at 8-14 days of age, and incisors are present at bırth ın all three
species. Growth rates vary from 0.45 g/day for A. namaquensis (NEAL 1990) to 1.6 g/day
for A. kaiseri (CHEESEMAN 1981).

E. edwardıi, E. rufescens (NEAL 1982; RATHBuN et al. 1981) and E. intufi (Trıp 1972)
bear litters of 1-2 precocıal neonates which do not nipple-cling. Litters of 1-4 young, wıth
a mean litter size of 2.2, have been recorded for E. rozetı (SEGUIGNES 1989). Litter mass
varıes from 28% of adult mass in E. rufescens (NEAL 1982) to 42.5 % of adult mass ın E.
edwardii. Gestation periods of 51 days for E. intuft, 57 days for E. rufescens and at least 75
days for E. rozeti have been recorded (Trıpp 1972; RATHBUN etal. 1981; SEGUIGNES 1989).
Growth rate in mass varied from 0.59 g/day for E. edwardiü to 1.0 g/day in E. intufi
(Trıpp 1972).

Figure 3 presents the results of weighted pair-group cluster analysis of 11 species, based
on eight developmental characters. Characters were selected on the basis ot avaılability of
information in the literature and included litter sıze, litter mass relative to adult mass,
gestation period, age at eye opening, age at incisor emergence, age at appearance ot fur,
nipple- clinging, growth rate ın mass. The resulting dendrogram clearly demonstrates the
grouping of congenerics in clusters, wıth the exception a one species of Acomys. The
differences among species, while not clearly related to habitat or body mass, clearly
represent the distinction between altricıial, semi-precocıial and precocıal species.

109

Postnatal development of three sympatric small mammal species

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110 Edith R. Dempster, M. R. Perrin, and R. J. Nuttall

Tatera afra

Tatera brantsii

Tatera leucogaster
Acthomys chrysophilus
Aethomys kaiseri
Aethomys namaquensis
Acomys subspinosus
Acomys dimidiatus
Elephantulus edwardii
Elephantulus rufescens

Elephantulus intufi

Ip 5
0.81 0.84 0.87 0.91 0.94 0.97 1.00

Fig. 3. Dendrogram derived from weighted-pair group cluster analysis based on a correlation matrix of
eight developmental characters (listed in text). Values along x-axis are similarities

With the accumulatıon of information on neonatal development of several species
belonging to the same genus, it is apparent that the level of development of young at birth
is fixed with a genus. Thus three Tatera species, four Gerbillurus species (DEMPSTER and
PERRIN 1989; DEMPSTER and PERRIN 1991), three Mus species (NEAL 1990) all have altrıcıal
young. Three Otomys species and three Acomys species have precocıal young (NEAL 1990),
with A. subspinosus and A. hystrella (HuBBAarD 1972) bearing semi-precocial young. All
elephant-shrew species are reported to bear precocial young (RATHBUN 1979). The
designation of “semi-precociality” ıs unclear: Near (1990) classifies Aethomys species as
here despite the fact that all developmental events such as eye opening, incisor eruption,
and hair growth occur earlıer than ın Tatera species. Clearly the altricial-precocıal
distinction represents a continuum, with species exhibiting different levels of altrıcıal or
precocial development.

This study has clearly shown that the most important factor influencing the develop-
mental strategies of the species included here ıs altricial/precocial development, which is a
phylogenetically conservative character ın small mammals.

Zusammenfassung

Postnatale Entwicklung bei drei sympatrischen Kleinsäugerarten aus Südafrika

Vier Arten kleiner Säuger kommen gemeinsam in einer trockenen Region der südwestlichen Kappro-
vinz vor. Mehrere Weibchen aller dieser Arten warfen Junge, nachdem sie während einer Feldexkur-
sion im September 1990 gefangen worden waren. Erstmalig wird hier über die Frühentwicklung der
drei Arten, Tatera afra, Acomys subspinosus und Elephantulus edwardii berichtet. Die erhobenen
Daten werden ferner mit entsprechenden Ergebnissen der vierten Art, Aethomys namaquensıis,
verglichen.

Postnatal development of three sympatric small mammal species 111

T. afra brachte pflegebedürftige, an der Brustwarze haftende Junge zur Welt, während die Jungen
von E. edwardii frühreıf waren und nicht an der Brustwarze hafteten. A. subspinosus brachte Junge in
einem Zwischenstadium hervor, die aber sehr schnell wuchsen. Die Jungtiere von A. namaquensis
gelten zwar als pflegebedürftig, aber ihr Entwicklungsstadium bei der Geburt ist weiter fortgeschrit-
ten als bei 7. afra.

Verschiedene Habitate und Körpergrößen können diese Unterschiede nicht erklären. Andere
Arten der untersuchten Gattungen zeigen ähnliche Entwicklungsabläufe, mit Ausnahme der Acomys-
Arten. Nesthocker- und Nestflüchter-Ontogenesen werden daher als phylogenetisch konservative
Merkmale bei diesen Kleinsäugern bewertet.

References

Acocks, J. P. H. (1988): Veld types of South Africa. 3rd. Ed. Memoirs of Botanical Survey of South
Africa 57. Botanical Research Institute, South Africa.

Aı-KnHarıı, A. D.; Derany, M. J. (1986): The post-embryonic development and reproductive
strategies of two species of rodents in south-west Saudi-Arabia. Cimbebasıa (A) 8, 175-195.
Burpa, H. (1989): Relationships among rodent taxa as indicated by reproductive biology. Z. zool.

Syst. Evolut.-forsch. 27, 49-57.

Case, T. J. (1978): On the evolution and adaptive significance of postnatal growth rates in the
terrestrial vertebrates. Q. Rev. Biol. 53, 243-282.

CHEESEMAN, C. L. (1981): Observations on the reproductive biology and early post-natal develop-
ment of two species of African rodents. Mammalıa 45, 483-492.

CREIGHTON, G. K.; STRAuss, R. E. (1986): Comparative patterns of growth and development in
cricetine rodents and the evolution of ontogeny. Evolution 40, 94-106.

DE GRAAFF, G. (1981): The Rodents of Southern Africa. Durban: Butterworths.

DEMPSTER, E. R.; PERRIN, M.R. (1989): Maternal behavior and neonatal development in three species
of Namib Desert rodents. J. Zool., Lond., 218, 407-419.

— — (1991): Neonatal development of Gerbillurus vallınus and G. setzeri. Madoqua (in press).

HUBBARD, C. A. (1972): Observations on the life histories and behaviour of some small rodents from
Tanzanıa. Zool Afric. 7, 419-449.

NEAL, B. R. (1982): Reproductive biology of the rufous elephant shrew, Elephantulus rufescens
(Macroscelididae) in Kenya. Z. Säugetierkunde 47, 65-71.

— (1983): The breeding pattern of two species of spiny mice, Acomys percivali and A. wilsoni
(Muridae: Rodentia) ın central Kenya. Mammalıa 47, 311-321.

— (1990): Observations on the early post-natal growth and development of Tatera leucogaster,
Aethomys chrysophilus and A. namaquensis from Zimbabwe, with a review of the pre- and post-
natal growth and development of African muroid rodents. Mammalıa 54, 245-270.

PERRIN, M.R. (1989): Alternative life-history styles of small mammals. In: Alternative Life History
Styles of Anımals. Ed. by M.N. Brurton. Dordrecht: Kluwer Academic Publ. Pp. 209-242.
RATHBUN, G. B. (1979): The socıal structure and ecology of elephant-shrews. Z. Tierpsychol. Suppl.

20, 1-76.

RATHBUN, G. B.; BEAMANn, P.; MALINIAR, E. (1981): Capture, husbandry, and breeding of rufous
elephant-shrews, Elephantulus rufescens. Internat. Zoo Yearb. 21, 176-184.

ScoTT, E. (1979): A comparison of postnatal development ın south African myomorph rodents.
Unpubl. M. Sc. thesis, Univ. Natal, Pietermaritzburg.

SEGUIGNES, M. (1989): Contribution & l’etude de la reproduction d’Elephantulus rozetı (Insectivora,
Macroscelididae). Mammalıa 53, 377-386.

SıgLy, R. M.; Carow, P. (1985): Classification of habıtats by selection pressures: a synthesis of life-
cycle and r/K theory. In: Behavioural Ecology: the Ecological Consequences of Adaptive
Behaviour. Ed. by R.M. Sısry and R.H. SmitH. Oxford: Blackwell Scientific. Pp. 75-90.

SKINNER, J. D.; SMITHERS, R. H. N. (1990): The mammals of the Southern African Subregion.
Pretoria: University of Pretoria.

STEARNS, $. C. (1983): The influence of size and phylogeny on patterns of covarıation among lıfe-
history traits in the mammals. Oikos 41, 173-187.

Trıpp, H.R.H. (1972): Capture, laboratory care and breeding of elephant shrews (Macroscelididae).
Lab. Anım. 6, 213-224.

WESTERN, D. (1979): Size, life history and ecology in mammals. J. Ecol. 17, 185-204.

Authors’ addresses: EpıTH R. DEMPSTER and M.R. PERRIN, Department of Zoology and Entomol-
ogy, University of Natal, P.O. Box 375, Pietermaritzburg 3200, RSA, and R.].
NUTTALL, Department of Ornithology, National Museum, P.O. Box 266,
Bloemfontein 9300, RSA

Z. Säugetierkunde 57 (1992) 112-115
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

WISSENSCHZIETFICHETZRURZMITEETEIIINIGEIN

Bats from Mana Pools National Park in Zimbabwe and the first
record of Eptesicus rendalli from the country

By I. L. RAUTENBACH and M. B. FENTON

Transvaal Museum, Pretoria, South Africa and Department of Biology, York University, North York,
Ontario, Canada

Receipt of Ms. 28. 10. 1991
Acceptance of Ms. 3. 12. 1991

The bat fauna of Africa ıs not well documented compared to other African mammals. For
example, while the bats of Zimbabwe have received some attention (FENTON 1975;
SMITHERS and Wırson 1979; HuTTon 1986), at most locations there has been no specific
survey of bats. Even at Mana Pools National Park on the Zambezi River (15°44’S;
29°21’E), the site of some bat research (e.g. ALDRIDGE.et al. 1990; FENTON et al. 1990;
OBRrıst et al. 1989), there ıs virtually no information about the bat fauna.

Between 18:00 and 21:00 we used 12 m mist nets (126 net hours in November 1987) and
two macro-mist nets (36 net hours in June 1990; RAUTENBACH 1985) to sample bats at sites
within 10 km of the headquarters of Mana Pools National Park. We sampled sites in the
dry woodland some distance away from the river, and on the flood plaın of the Zambezi
River ın the predominately Acacıa albida woodland along the Zambezi River, a park-like
habıtat wıth dispersed tall canopy trees and little understory (DunHAM 1989). Here we
record the first record of Eptesicus rendallii from Zimbabwe and the occurrence of 20
species of bats in Mana Pools National Park (Table 1), 15 of which are recorded for the fırst
time.

The bats recorded for Mana Pools National Park are compared with the species
compositions of two other sites in southern Africa (Table 1). These bat faunas are typical of
open woodland in southern Africa. Nycticeins schlieffenii and Scotophilus borbonicus
together accounted for 80 % of the 136 bats netted at Mana Pools National Park between
18:00 and 21:00 over 12 nıghts ın June 1990. In comparing the faunas (see Table), ıt ıs clear
that a number of species are rarely encountered, while others are taken only in the
immediate vicinity of their roosts. The larger species richness recorded for Pafuri, may be
ascribed to greater ecological complexity and more intensive surveying.

Eptesicus rendallii ıs widespread in open woodland savannahs of subsaharan Africa
(SMITHERS 1983) and ranges southwards into northern Botswana (SMITHERS 1971), central
Zambia (Anserı 1978), southern Malawi (AnseLL and DowsETT 1988), and the Tete and
Mocambique distriets of Mocambique (SMITHERS and LoBAo TELLO 1976). Our specimens
are the first from Zimbabwe and they have been prepared as standard skin and skull
vouchers and deposited ın the national mammal collection of the Transvaal Museum. In
wing characteristics (aspect ratio 6.71 male, 6.18 female; wingloading 7.81 N m”? and
6.93 N m?) and size (6.0 and 6.5 g) these bats would be included in the Group 1 of
ALDRIDGE and RAUTENBACH (1987), species with high flight manoeuvrebility that should
forage in relatively cluttered situations.

We prepared standard bone marrow karyotypes from the two E. rendalli using the ın
vivo technique of Roggıns and Baker (1978) as modified by BAkER et al. (1982). At least

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5702-112 $ 02.50/0

113

Bats from Mana Pools National Park in Zimbabwe

Ad, = = snarsnA Sn1J941Ssıdıd]

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wundvg> vpııopv] % % — NGISIMJI STOoLW
2 ppıuvpv] x 2% I ns1oq194g9S en
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1uassuonarıun sSJOWOIO x — =: ıKuums sngdojougy
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st (310779 Surpdures opgesedu1os 107) a„9uepunge JAnepL saıIs OM1 I9yIO JyI 10F uMoys Jıe yıeg Jeuonen] s[oog euey woAy sıeq Fo sıaqwunu jenase aya afıyyy\

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114 I. L. Rautenbach and M. B. Fenton

five representative chromosome spreads were examined from each bat to determine diploid
(2n) and fundamental numbers (FN). Photomicrographic enlargements of suitable spreads
were used in the final analyses and to prepare a karyogram.

Our data show that the standard karyotype of E. rendallii is 2n = 38, FN = 50, and the
autosomal complement ı is seven pairs of bi-armed chromosomes, and a size-graded series
of 11 acrocentric pairs. A prominent secondary constriction Is apparent near the centro-
mere of one of the larger pairs of acrocentric chromosomes. The X chromosome is a large,
submetacentric, and the Y a small submetacentric. Our findings agree with the earlier
description of the karyotype of E. rendalliı (McBee et al. 1987), with the exception of the
Y chromosome, which is described for the first time.

Some workers (e.g. HELLER and VOLLETH 1984) would group E. rendallii together with
other karyotypically varıable Eptesicus-like African bats, as Pipistrellus since they deviate
from what is considered to be the typically conservative karyotype of ‘true’ Eptesicus
(2n =50). Based on bacular morphology others (e.g., Hrn and Harrıson 1987) also
consider E. rendallıı as a Pipistrellus. However, the complexity of the problem makes it
prudent to report our record as Eptesicus rendallii, pending the results of more in-depth
systematic studies.

Acknowledgements

We thank the Director of the National Parks and Wildlife Management Department for permission,
and Warden F. BuvEyE and C. JaKkoPOo for advice and assistance in the field. R. B. MARTIN, Assistant
Director (Research) provided logistical help, while M. B. Cumming, M. K. MUSGRAGCE, J. $. TAyLoR
and T. VoLpers helped in the field. This study was supported by grants from the Natural Sciences and
Engineering Research Council of Canada to MBF and the South Afrıcan Foundation for Research
Development to ILR.

References

ALDRIDGE, H. D. J. N.; OBrısT, M.; MERRIAM, H. G.; FEnTon, M. B. (1990): Roosting, vocalizations
and foraging by the African bat, Nycteris thebaica. J. Mammalogy 71, 242-246.

ALDRIDGE, H. D. J. N.; RAUTENBACH, I. L. (1987): Morphology, echolocation and resource
partitioning in insectivorous bats. J. Anımal Ecology 56, 763-778.

AnseLı, W. F. H. (1978): The mammals of Zambia. Chilanga: The National Parks and Wildlife
Service.

AnseıL, W. F. H.; DowseEtT, R. J. (1988): Mammals of Malawi: an annotated check lıst and atlas.
Zennor: The Trendrine Press.

BAKER, R. J.; Haıpuk, M. W.; RossBıns, L. W.; CADEnA, A.; Koor, B. F. (1982): Chromosomal
studies of South American bats and their systematic implications. Special publ. Museum Texas
Tech. Univ. 6, 303-327.

DunHam, K. M. (1989): Long-term changes in Zambezi riparıan woodlands, as revealed by photo-
panoramas. African J. Ecology 27, 263-275.

FENnToN, M. B. (1975): Observations on the biology of some Rhodesian bats, including a key to the
Chiroptera of Rhodesia. Life Sciences Contributions, Royal Ontario Museum 104, 1-27.

FENTON, M. B.; SwANEPOEL, C. M.; BRIGHAM, R. M.; Hıck£Ey, M. B. C. (1990): Foraging behaviour
and prey selection by large slit-faced bats (Nycteris grandis; Chiroptera: Nycteridae). Biotropica
22, 2-8.

HELLER, K.-G.; VOLLETH, M. (1984): Taxonomic position of “Pipistrellus societatis” Hill, 1972 and
the karyological characteristics of the genus Eptesicus (Chiroptera: Vespertilionidae). 77001:
Syst. Evolut.-forsch. 22, 65-77.

Hırr, J. E.; Harrıson, D. L. (1987): The baculum ın the Vespertilioninae (Chiroptera: Vesper-
tilionidae) with a systematic review, a synopsis of Pipistrellus and Eptesicus and the descriptions of
anew genus and subgenus. Bull. British Museum (Natural History), Zoology Series 52, 225-305.

Hurron, J. M. (1986): The status and distribution of bats ın Zimbabwe. Cimbebasıa (A) 8, 219-236.

McBex, K.; SCHLITTER, D. A.; Roggins, R. L. (1987): Systematics of African bats of the genus
Eptesicus (Mammalia: Vespertilionidae). 2. Karyotypes of African species and their generic
relationships. Annals Carnegie Museum 56, 213-222.

OBRrısT, M.; ALDRIDGE, H. D. J. N.; FEnton, M. B. (1989): Roosting and echolocation behavior of
the Afrıcan bat, Chalinolobus variegatus. J. Mammalogy 70, 828-833.

RAUTENBACH, I. L. (1985): A new technique for the efficient use of macro-mistnets. Koedoe 28,
81-86.

Bats from Mana Pools National Park in Zimbabwe 115

Rosgıns, L. W.; BAKER, R. ]J. (1978): Karyotvpic data for Afrıcan mammals, with a description of an
in vivo bone marrow technique. Bull. Carncyie Museum of Natural History 6, 188-210.

SMITHERS, R. H.N. (1971): The mammals ot Botswana. Museum Memoir No 4. Salisbury: Trustees
of the National Museums of Rhodesia.

— (1983): The mammals of the Southern African Subregion. Pretoria: University of Pretoria.

SMITHERS, R. H. N.; Losao Terro, J. L. P. (1976): Check lıst and atlas of the mammals of
Mocambique. Museum Memoir No 8. Salisbury: Trustees of the National Museums and Monu-
ments of Rhodesıa.

SMITHERS, R. H. N.; Wırson, V. J. (1979): Check list and atlas of the mammals of Zimbabwe
Rhodesia. Museum Memoıir No 9. Salısbury: Trustees of the National Museums and Monuments.

Authors’ addresses: I. L. RAUTENBACH, Iransvaal Museum, P.O. Box 413, Pretoria, 0001 South
Africa, and M. B. FENToNn, Department of Biology, York University, North
York, Ontario, Canada, M3J 1P3

Z. Säugetierkunde 57 (1992) 116-117
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Further notes on the pupping period in a recently founded
colony of Grey Seals (Halichoerus grypus) in the Netherlands

By L. VEDDER, L. ’T HART, and P. J. H. van BrREE

Harbour Seals Rehabilitation and Research Centre, Pieterburen, The Netherlands

Receipt of Ms. 19.8. 1991
Acceptance of Ms. 1.11. 1991

In a short paper published previously (’T HarT et al. 1988), we reported on the birth of
Grey Seals, Halichoerus grypus (Fabricius, 1791), living on and near a high lyıng shoal off
the Frisian Island of Terschelling, the Netherlands. In that recently founded colony,
consisting of only young anımals, in the second week of January 1985, the fırst two just-
born Grey Seals were observed. The next two years, two very young specimens were seen
during the last week of January, three newly born Grey Seals during the first week of
February and 10 days later again two just-born pups were observed. Then we drew
attention to the fact that the founders of the colony in the Netherlands almost certainly
came from the Farne Islands, where the pupping period is from mid October till mıd
December with a peak around November 7 th.

We believed it interesting to tollow the development of the Dutch colony of Grey Seals,
in particular the changes ın the reproduction period. Thanks to the observations of the
pilots of the Aır Force base at Leeuwarden, and the staff of the lighthouse “De Brandaris”
on the island, we could gather a number of data, supplemented by data on very young
animals found beached after heavy storms on nearby Iyıng ıslands and on the coast of the
continent (Table).

Births of Grey Seals in the Netherlands per decade, season 1987/88 to 1990/91

To these births must be added a newly-born male found late October/early November 1990

at

1987/1988

1988/1989

1989/1990

1990/1991

The data compiled in the table show clearly a shift of the pupping period to an earlıer
date in the season. This shift confirms the observations by BACKHOUsE and HEWER (1957)
that primiparous Grey Seals give bırth later in the season than females which had already
one or more pups. We wonder whether the trend to reproduce at an earlıer date will
continue till there will be a similar period of pupping in the Netherlands as ın the Farne
Islands colony, or than the more southern situated colony in the Netherlands will have its
own reproduction period.

We like to thank sincerely all the persons who helped us in obtaining the data, in particular messrs.
HEssEL WIEGMAN, OTTO ÖVERDIIJK and the staff of the lighthouse “De Brandaris“.

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Pupping period of Halichoerus grypus in the Netherlands 117

References

BACKHOUSE, K. M.; HEwER, H.R. (1957): A note on spring pupping in the Grey Seal. Proc. zool.
Soc. London 128, 593-596.
HART, L. T’; MOESKER, A.; VEDDER, L.; BREE, P. J. H. van (1988): On the pupping period of Grey

Seals, Halichoerus grypus (Fabricius, 1791), reproducing on a shoal near the Island of Terschelling,
the Netherlands, Z. Säugetierkunde 53, 59-60.

Authors’ addresses: Drs L. VEDDER and L. Tr’ HART, Zeehondencreche, Hoofdstraat 94a, NL-9968
AG Pieterburen; Dr. P. J. H. van BrEE, Dept. Mammals, Instituut voor

Taxonomische Zoölogie, Mauritskade 61, NL-1092 AD Amsterdam, The
Netherlands

Z. Säugetierkunde 57 (1992) 118-119
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Lack of biochemical-genetic variation in native Sika deer
(Cervus nippon hortulorum) from the far east
of the Asian continent

By G. Markov, A. Danııkın and G. B. HArTL

Institute of Zoology, Bulgarian Academy of Science, Sofia, Bulgaria, Institute of Evolutionary
Morphology and Ecology of Animals, Academy of Sciences of the USSR, Moscow, USSR and
Forschungsinstitut für Wildtierkunde der Veterinäarmedizinischen Universität Wien, Vienna, Austria

Receipt of Ms. 11. 7. 1991
Acceptance of Ms. 26. 8. 1991

In contrast to varıous other deer species (see HARrTL et al. 1990, for review), Sıka deer
(Cervus nippon) has only poorly been investigated for biochemical-genetic variation.
Population genetic data are available only from representatives of the Japanese subspecies
Cervus nippon nıppon, introduced into Great Britain and Ireland, and from hybrids of this
subspecies with the Red deer (Cervus elaphus scoticus; see HARRINGTON 1973). A
multilocus investigation including 11 RBC/plasma enzyme systems was performed by
HERZOG (1988) without detecting polymorphism or differences from the Red deer except
for 6-phosphogluconate dehydrogenase, where the occurrence of genetic polymorphism ıs
indicative for hybrid populations of Red and Sika deer.

In order to examine genetic varıatıon in native Sıka deer from the easternmost point of
Asıa, possıbly belonging to the subspecies C. n. hortulorum (RATCLIFFE 1987), whole
blood samples of 43 individuals from a population in Primor’e (USSR) were collected
during the hunting season of 1989/1990. The blood was fractioned ınto plasma and
erythrocytes and stored frozen at -20°C. Horizontal starch gel and agarose gel elec-
trophoresis, blood protein and enzyme staining as well as the interpretation of band-
patterns were done as summarızed by HAarTL and HÖGer (1986), HARTL et al. (1986) and
HARTL and FERRAND (1991). The following blood proteins and enzymes were screened
(abbreviation, E.C. number and gene locı scored are given ın parentheses): hemoglobin
(Hb, alpha and beta chain, Ab-a, Hb-Pß), transferrin (Tf, 7f), lactate dehydrogenase
(LDH, E.C. 1.1.1.27, Zdh-2), NADH-diaphorase (DIA, E.C. 162 DEI A waunlase
(CAT, E.C. 1.11.1.6, Cat), aminoacylase-1 (ACY-1, E.C. 3.5.1.14, Acy-1), and glucose
phosphate isomerase (GPI, E.C. 5.3.1.9, Gpi-1).

None of the gene locı investigated was polymorphic in the Sıka deer. When compared
to band-patterns in the Red deer (C. e. hippelaphus), allelic differences were observed at the
Hb-ß and the Cat locus. Whereas the lack of genetic varıation in introduced Sika deer (C.
n. nippon; HERZOG 1988) can be explained by genetic drift and inbreeding, which are
frequently associated with the artificial foundation of populations (comp. HARTL et al.
1986; HAarTL 1989), this result was not to be expected in our native Sıka deer population.
As far as the evolutionary rate of proteins is concerned, some of the blood proteins and
enzymes investigated showed considerable genetic varıation ın other deer species (see
HarTL et al. 1990, and references therein). Further studies are required to elucidate the
population history and distribution of Sıka deer in our study area as well as ıts genetic
structure to detect a possible threatening by genetic pauperization. Concerning the genetic
differences from the Red deer, the fiıxation of alternative alleles at two out of eight locı ıs ın
accordance with allozyme differentiation at the species level.

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Lack of biochemical-genetic varıation in native Sika deer lo)

Acknowledgement

The authors are grateful to AnıTa HAIDEN for excellent technical assistance.

Literature

HARRINGTonN, R. (1973): Hybridisation among deer and its ımplications for conservation. Irish
Forestry J. 30, 64-78.

HAaRTL, G. B. (1989): Die genetische Variabilität von Wildsäugern und die Folgen der Isolation. In:
Die Illusion der Arche Noah - Gefahren für die Arterhaltung durch Gefangenschaftszucht. Ed. by
E. SCHNEIDER, H. OELKE, H. Gross. Göttingen: Echo-Verlag. pp. 127-138.

HARTL, G. B.; FERRAND, N. (1991): Genetic polymorphism of transferrin (7f) and the hemoglobin
alpha chain (Hb-a) in the brown hare (Lepus europaeus). Anim. Genet. (submitted).

HarTL, G. B.; Höcer, H. (1986): Biochemical varıation in purebred and crossbred strains of
domestic rabbits (Oryctolagus cuniculus L.). Genet. Res., Cambridge 48, 27-34.

HARTL, G. B.; SCHLEGER, A.; SLOWAK, M. (1986): Genetic varıability ın fallow deer, Dama dama L.
Anım. Genet. 17, 335-341.

HARTL., G. B.; WırLıng, R.; Lang, G.; Kreın, F.; KÖLLer, J. (1990): Genetic varıability and
differentiation in red deer (Cervus elaphus L.) ot Central Europe. Genet., Select., Evol. 22,
289-306.

HERZOG, $. (1988): Polymorphism and genetic control of erythrocyte 6-phosphogluconate dehy-
drogenase in the genus Cervus. Anım. Genet. 19, 291-294.

RATCLIFEE, P. R. (1987): Distribution and current status of sıka deer, Cervus nıppon, ın Great Britain.
Mammal Rev. 17, 39-58.

Authors’ addresses: Dr. G. Markov, Bulgarian Academy of Science, Institute of Zoology, 1, Ruski
bul., BG-1000 Sofia, Bulgaria; Dr. A. Danııkın, Academy of Sciences of the
USSR, Institute of Evolutionary Morphology and Ecology of Animals, Moscow,
USSR; Dr. G. B. HarTL, Forschungsinstitut für Wildtierkunde und Ökologie,
Veterinärmedizinische Universität Wien, Savoyenstraßfe 1, A-1160 Vienna,
Austria

Z. Säugetierkunde 57 (1992) 120-123
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

A comparison of genetic diversity in Nubian ibex (Capra ibex
nubiana) and Alpine ibex (Capra i. ibex)

By M. Stüwe, K. T. ScRIBNER and P. U. ALKkoN

Conservation and Research Center, National Zoological Park, Smithsonian Institution, Front Royal,
USA; Department of Zoology, University of Georgia, Athens, USA; Jacob Blaustein Institute of Desert
Research, Ben Gurion Univerity, Sede Boger, Israel

Receipt of Ms. 28. 5. 1991
Acceptance of Ms. 2. 8. 1991

Alpine ibex (Capra ı. ibex) have shown a remarkable recovery in recent decades after
almost becoming extinct in the last century (GRoDINSKY and STÜwE 1987). The recovery
was the result of an alpine-wide, though largely uncoordinated conservation effort,
re-establishing ibex populations through reintroductions and translocations (STÜWE and
NIEVERGELT 1991). Despite the dramatic increase in ibex population numbers and often
strong population growth, little attention has been given to the relationships of reintroduc-
tion methodology (i.e. number of founders, sex ratio, and number of releases) and
population genetic characteristics.

Maintenance of heterozygosity levels or minimization of loss of genetic varıability has
become a primary goal in the population management of vulnerable species (LANDE and
BARROWCLOUGH 1987). Recent population surveys have shown that genetic varıabilıty in
alpine ibex was low when compared to that in natural populations of other ungulate species
(STÜWE and SCRIBNER 1989; RanDi et al. 1991). Genetic similarity among ibex populations
was related to stocking history, probably as a result of genetic drift occurring during
reestablishment of the populations (StÜüwe et al. 1991). A detailed analysis of the effects of
such management actions on the genetic diversity of the newly founded populations may
aid the development of strategies for future reintroductions of locally extinct populations
of ıbex and other species. To determine whether low alpine ıbex genetic diversity was a
result of management actions or was a phenomenon reflecting species-wide evolutionary
history, we compared alpıne ıbex wıth Nubian ibex (Capra ibex nubiana), using the same
genetic methodology. The latter were chosen as a control because no unmanaged alpine
ibex populations exist, and the Nubian ibex appears to be the taxa geographically and
systematically closest related to alpıne ibex. We chose a population in the Negev desert
currently numbering about 400 individuals (ALkon and Man 1988). Several Nubian ibex
populations have suffered severe population reductions in the past (BAHARAV and
MEIBOOoM 1981; KrAUSMAN and SHaw 1986; HaBıBı and GRAINGER 1990). However,
there is no evidence that the Negev population has undergone the repetitive reductions ın
population size, and the intensive management actions alpine ıbex experienced ın recent
times.

Blood was analyzed from 149 alpine ibex captured 1988 through 1990 ın the four
French populations Bargy (n = 22), Champagny (n = 10), Encombre (n = 14), and
Maurienne (n = 37), the three Swiss populations Saastal (n = 29), Jollital (n = 5), and Mont
Pleureur (n = 11), and the Italian population Gran Paradiso (n = 21). An additional 39
blood samples were obtained from Nubian ibex, caught in 1988 ın Avdat Canyon National
Park and Zin Nature Reserve, near Sede Boger, Israel. Blood samples were obtained from
live anımals immobilized with Xylazine-based tranquilizing drugs (STÜwE and SCRIBNER
1989).

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Comparison of genetic diversity in Nubian ibex and Alpine ibex 121

Fourteen enzymes encoded at 15 locı were examined for polymorphisms using horizon-
tal starch-gel electrophoresis (MANLOVE et al. 1976): albumin (ALB), phosphoglucomut-
ase-3 (PGM-3; EC 2.7.5.1), hemoglobin (HB), glucose phosphate isomerase-1 (GPI-1;
EC 5.3.1.9), creatine kinase-2 (CK-2; EC 2.7.3.3), glucose-6-phosphate (G-6-P; EC
1.1.1.49), malate dehydrogenase-1 (MDH-1; EC 1.1.1.37), 6-phosphogluconate dehy-
drogenase (PGD; EC 1.1.1.44), malic enzyme-1 (MOD-1; EC 1.1.1.40), purine nuc-
leoside phosphorylase (NP; EC 1.6.2.2), lactate dehydrogenase-1 (LDH-1; EC 1.1.1.2),
eurythacytic acıd phosphatase (EAP), peptidase-B (PEP-B; leucyl glycyl glycine as
substrate; EC 3.4.11) and indophenol oxidase-1,2 (IPO-1,2; EC 1.15.1.1). Inıtial sample
treatment and analysis followed STÜwE and SCRIBNER (1989).

Differences in levels of multi-locus heterozygosity were tested using contingency chi-
square analysıs (SOKAL and RoHLF 1981).

The percentage of polymorphic locı (13.3% and 20.0 %), mean number of alleles per
locus (1.2 and 1.5), and average direct-count heterozygosity (0.048 and 0.087) were all
lower ın alpıne than in Nubian ibex, respectively (Table). Differences in multi-locus
heterozygosity were significant (x? = 24.64, P < 0.001, df = 3).

Direct-count estimates of average heterozygosity, mean number of alleles per locus, percent of
polymorphic loci, and allele frequencies at seven variable loci in alpine and Nubian ibex

Alpine Nubian Locus Alpıne Nubian Locus Alpıne Nubian
ibex ibex ibex ibex ibex ibex

NP 118 0.000 0.026 MDH-2 70 0.000 0.013 PGD 90 0.003
NP 100 1200072299497 2 MDETE25109251700075,0:987 7BGD 100 0.997

Dz Dres 0510, 1.000, Samplesize 149
MOD-1 100 1.000 0.231 LDH-1100 0.490 0.000 Avg. H 0.048
MOD-1 111 0.000 0.769 PEP-B 100 0.678 0.000 # of alleles 2

EAP 86 oa olo2e DEP BH ON 0322 00.7600, Srelymlouiı 133
EAP100 1.000 0.974 PEP-B136 0.000 0.231

Locus designations are provided in the text.

Average RoGERSs (1972) genetic distance between Nubian and alpıne ıbex was 0.106, far
exceeding the genetic distance among alpıne populations (mean: 0.021, range:
0.002-0.058). However, this relationship ıs based on few locı, and ıs primarıly due to the
presence of unique alleles and frequency differences. Allelic variation among the 149 alpine
ibex was detected at three locı out of 15 locı analyzed; PGD, LDH-1 and PEB-B. Among
39 Nubian ibex, sıx locı were varıable: NP, MOD-1, EAP, MDH-2, PEB-B, and PGD.
Of the seven locı variable among both taxa, only one locus (LDH-1) was fixed in Nubian
ibex as compared to four locı (NP, MOD-1, EAP, and MDH-2) fixed in alpine ıbex (Table
1). In addition, the PGD 90 allele was present in only one individual in alpine ibex
(frequency: 0.003) but was found at a much higher frequency in Nubian ibex (0.205),
indicating progressing fixatıion among alpine ibex. The PEB-B 112 allele was found in both
taxa, while the PEB-B 100 allele was found in alpine ibex and the PEB-B 136 allele was
found in Nubian ıbex only (Table).

Alpine and Nubian ıibex are not sympatric and there are no fossil indications they ever
were since the radiation of Capra ın the third faunal zone of the Pleistocene. Their
taxonomic status is controversial. Both are considered subspecies by many authors (see
SCHALLER 1977 for review), although HEPTNER (1966), and HaArTL et al. (1990) separate
them as species. HArTL et al. (1990) calculated the genetic distance by biochemical
comparison of one individual each of alpine ibex, Nubian ibex, markhor (Capra falconer:),
and Bezoar goat. Of these four taxa only alpine and Nubian ıbex had previously been

122 M. Stüwe, K. T. Scribner and P. U. Alkon

considered subspecies (SCHALLER 1977). However, HaRrTL et al. (1990) found the greatest
genetic distance between just those two, and suggested that these taxa also be considered
separate species.

Since the separation of alpıne and Nubian ibex from their common ancestor, allelic
varıiation could either have been lost (through drift or selection), or added (through
mutation). This could have occurred either as a natural consequence of intrinsic population
processes, or as a result of manıpulative processes in either of the taxa. We believe genetic
divergence between alpıne and Nubian ıbex should not be based solely on time since
common ancestry as used ın genetic distance calculations. Such calculations assume on
homogeneity of evolutionary rates within independent lineages. However, the severe
population manipulations experienced by alpıne ıbex since the 16th century (STÜwE and
NIEVERGELT 1991) very likely contributed to the shifts ın allele frequencies, the loss of
alleles, and the significantly lower level of heterozygosity observed today. The low genetic
diversity discussed for Alpıne ıbex populations (HARTL 1986; STÜwE and SCRIBNER 1989;
Ranoı et al. 1991) as well as the observed genetic distance between alpine and Nubian ibex
may thus be due in part to stochastic effects associated wıth human intervention rather than
deterministic processes alone.

It ıs difficult to assess the significance of the degree of genetic dıvergence between
Nubian and Alpine ıbex ın the absence ot molecular markers which exhibit alternative
fiıxatıion, and in light of the strong influence of human manipulations. Without further
genetic comparisons within the genus Capra our results do not warrant a classıfıcation of
alpıne ibex and Nubian ibex as separate species, and we therefore accept the systematic
evaluation by SCHALLER (1977).

Acknowledgements

We thank H. ANTHAMATTEN, B. Bassano, H.-]. BLANKENHORN, P. DOLLINGER, D. FELLAY, D.
GAUTHIER, C. GRODINSKY, J. E. Gross, $. G. KOHLMANN, J.-P. MARTINOT, B. NIEVERGELT, V.
PERACINO, W. SCHEFFRAHN, C. STAUFFER, and H. ZEHNDER for their great contribution to various
aspects of this study. The study was supported by World Wildlife Fund - Switzerland; Schweizer
Bund für Naturschutz, Basel; and the Goethe Foundation for the Arts and Sciences, Zürich.
Additional support was provided by the Blaustein International Center for Desert Studies and the
Mitrani Center for Desert Ecology, and through contract DE-AC09-76SR00-819 between the U.S.
Department of Energy and the University of Georgia’s Institute of Ecology. Electrophoretic analyses
were conducted at the Savannah River Ecology Laboratory.

References

Aıxkon, P. U.; Man, $. (1988): Nubian ibex Capra ıbex nubiana. Caprinae Report, JUCN Species
Survival Commission.

BaHARAv, D.; MEIBOOM, U. (1981): The status of the Nubian ibex Capra ıbex nubiana in the Sinai
desert. Biol. Conserv. 20, 91-97.

GRODINSKY, C.; Stüwe, M. (1987): With lots of help alpine ıbex return to their mountains.
Smithsonian 18, 68-77.

HaBıgı, K.; GRAINGER, J. (1990): Distribution and status of Nubian ıbex ın Saudi Arabia. Oryx 24,
138-142.

HARTL, G. B. (1986): Steinbock und Gemse im Alpenraum - genetische Variabilität und biochemische
Differenzierung zwischen den Arten. Z. zool. Syst. Evolut.-forsch. 24, 315-320.

HAaRTL, G.; BURGER, H.; WırLıng, R.; SUCHENTRUNK, F. (1990): On the biochemical systematics of
the Capriniı and Rupicaprını. Biochem. Syst. Ecol. 18, 175-182.

HEPTNER, N. G.; NasIMoOVIscHa, A. A.; BannIKov, A. G. (1966): Die Säugetiere der Sowjetunion.
Band 1: Paarhufer und Unpaarhufer. Jena: Gustav Fischer Verlag.

Krausman, P. R.; SHaw, W. W. (1986): Nubian ibex in the Eastern desert, Egypt. Oryx 20, 176-177.

LAnDE R.; BARROWCLOUGH, G. F. (1987): Effective population size, genetic varlatıon, and their use ın
population management. In: Viable populations for conservation. Ed. by M. E. SouLE. Cam-
bridge: Cambridge University Press. 87-123.

MANLOVvE, M. N.; SMITH, M. H.; HiLLesTan, H. O.; FULLER, $. E.; Jonns, P. E.; STRANEY, D. ©.
(1976): Genetic subdivision in a herd of white-tailed deer as demonstrated by spatial shifts in gene
frequencies. Proc. Ann. Conf. Southeastern Assoc. Game and Fish Comm. 30, 487492.

Comparison of genetic diversity in Nubian ibex and Alpine ibex 123

Ranpı, E.; Tosı, G.; Toso, $.; LORENZINI, R.; Fusco, G. (1991): Genetic varıability and conserva-
tion problems in Alpine ıbex, domestic and feral goat populations (genus Capra). Z. Säugetier-
kunde 55, 413-420.

Rogers, J. $S. (1972): Measures of genetic similarity and genetic distance. Studies in Genetics, VII.
Univ. Texas Publ. 7213, 145-153.

SCHALLER, G. B. (1977): Mountain Monarchs. Chicago, London: The University of Chicago Press.

SoKAL, R. R.; RoHLF, F. J. (1981): Biometry. 2nd Ed. San Francisco: W. F. Freeman.

STÜwE, M.; NIEVERGELT, B. (1991): Recovery of Alpine ibex from near extinction: the result of
effective protection, captive breeding, and reintroductions. Appl. Anim. Behav. Sci. 29, 379-387.

STÜWE, M.; SCRIBNER, K. T. (1989): Low genetic varıability in reintroduced Alpine ibex populations.
J- Mammalogy 70, 370-373.

STÜWE, M.; SCRIBNER, K. T.; GAUTHIER, D. (1991): A genetic comparison of French alpıne ibex
populations (Capra 1. ıbex) and implications for their management. Travaux Scientifiques du Parc
National de la Vanoise 8, (in press).

Authors’ addresses: MICHAEL STÜWE, Conservation Center, Front Royal, VA 22630, USA; Kım
SCRIBNER, Department of Zoology, University of Georgia, Athens, GA 30602,
USA; PHıL Aıkon, Jacob Blaustein Institute of Desert Research, Ben Gurion
University, Sede Boger, Israel 84990

BUCTHBESERECHUNGEN

WEHNER, R.; GEHRING, W.: Zoologie. 22., völlig neu bearbeitete Auflage. Stuttgart, New
York: Georg Thieme 1990. 816 S., 406 Abb., 30 Tab. DM 48,-. ISBN 3-13-367422-6

Dies ist eine Neuauflage des 1922-1969 in 17 Auflagen erschienenen „Grundriß der allgemeinen
Zoologie“ von ALFRED Künn, der in 18.-21. Auflage unter dem Titel „Allgemeine Zoologie“ von E.
HaADoRrN und R. WEHNER fortgesetzt wurde. Die letzte gründlich umgearbeitete Fassung aus dem Jahr
1974 ist inzwischen veraltet. Das nun vorliegende Buch wurde zwar ın der Grobgliederung mäßig, in
Stoff und Abbildungen aber stark verändert. Unter den Abbildungen sind viele zweifarbig, außerdem
gibt es als Neuheit eine Reihe von Licht-, TEM- und REM-Fotos. Der Umfang ist gegenüber der
letzten Auflage erheblich erweitert. Die Kapitel über Zytologie, Vererbung und Entwicklung stam-
men von W. GEHRING, die übrigen von R. WEHNER. Die beiden Autoren hatten also die schwierige
Aufgabe, große Bereiche der Zoologie überblicken und kompetent darstellen zu müssen. Der Vorteil
ist eine einheitliche und geschlossene Behandlung des Stoffes mit kensequent befolgten Definitionen
und Begriffen und zahlreichen Querverweisen. Auch die Versuchung, Teilgebiete zu bevorzugen und
andere zu vernachlässigen, ist dadurch eingeschränkt. Erfreulich ıst das Bemühen, die experimentellen
Belege und die Geschichte grundlegender Anschauungen wie in der Zytologie und Vererbung zu
skizzieren, damit das Verständnis zu erleichtern und den Text aufzulockern. Ob die moderne Genetik
so ausführlich noch ın eine „Zoologie“ hineingehört, wäre zu überlegen, ungeachtet der Tatsache, daß
sich die vorliegende Darstellung wirklich spannend liest. Die Autoren werden allerdings auch den
Intentionen des Begründers ALFRED Kühn insofern gerecht, als dieser stark genetisch orientiert war.

Bei der Beurteilung eines solchen Buches fragt man: Wurde die Zoologie vollständig und
ausgewogen abgehandelt? Ist alles Wichtige enthalten, wurde nichts vergessen? Sınd die mitgeteilten
Fakten notwendig und ausreichend? Was wurde aufgegeben, was neu aufgenommen? Ist das Aufgege-
bene tatsächlich überflüssig, das neu Aufgenommene hinreichend gesichert? Bildet das Buch heute
noch eine gute Wissensgrundlage und einen Überblick über das Fach?

In der Einleitung weisen die Autoren darauf hin, daß in der Molekular- und Zellbiologie wie auch
in Ethologie, Okologie und Evolutionsbiologie besonders große Fortschritte zu verzeichnen seien.
Diese Kapitel sind in der Tat am stärksten verändert. Proteinsynthese, Zellkontakte, Immunologie,
hüpfende Gene, Rotroviren, der Zellstammbaum des Nematoden Caenorhabditis, homoetische
Mutationen bei Drosophila, molekulare Mechanismen der Hormonwirkung, die Zugorientierung der
Vögel, die Soziobiologie und der Kladismus sind nur einige Stichworte. Neue Erkenntnisse klären
ehemals offene Fragen, korrigieren falsche Vorstellungen und ermöglichen es bisweilen, bekannte
Tatsachen unter übergeordneten Gesichtspunkten zusammenzufassen. Insofern müssen sie nicht
unbedingt zu einer Stoffvermehrung führen. In anderen Fällen allerdings verleiten sie dazu, wichtige,
jedoch schon länger unumstrittene Grundlagen zurückzustellen zugunsten erst später geklärter
Folgefragen. Für den Anfänger ergeben sich daraus Lücken, die er auf andere Weise schließen muß,
die ıhm aber das Verständnis erschweren. So erscheinen aus heutiger Sicht Abschnitte aus der 19.
Auflage wie „die Zelle im Gewebeverband“ oder das dihybride Kreuzungsschema für Rinder, die
Genwirkkette des Phenylalanıns bei Drosophila oder auch das Schema für das Zustandekommen des
Kniesehnenreflexes vielleicht antiquiert. Ihr Fortfall macht die Zoologie aber wieder ein Stück
abstrakter. Ein Teil der alten Abbildungen wurde in verkleinerter Form wiedergegeben wie der
Gewebeschnitt eines Schwammkörpers, in dem nun noch weniger von den Choanozyten zu erkennen
ist als früher. Ausgeglichen wird dieser Nachteil durch meist prägnantere Zeichnungen. Diese sind fast
stets gründlich beschriftet und erklärt und sind auch meist notwendig. Aber auch alte, scheinbar
unproblematische Darstellungen sollten gründlicher überdacht werden. So werden in Abb. 12.92
Selachier- und Teleosteer-Herz verglichen. Der wohl auffallendste Unterschied — reduzierter Bulbus
cordis, dafür Bulbus arteriosus bei Teleosteern, kommt nicht zum Ausdruck. Dafür fehlen die bei den
Selachiern nicht eingezeichneten Sinu-Atrialklappen dort in Wahrheit nicht, und was im Knochen-
fisch-Schema als „Perikard“ bezeichnet wird, kommt dort in Wahrheit nicht vor.

Der Schultergürtel eines Vogels (Abb. 12.86) ist in folgenden Punkten weniger richtig als in der
älteren Auflage: Humerus gelenkt nicht allein am Coracoid, sondern auch an der Scapula: Furcula-
Spitze ist mit Sternum-Spitze meist sehnig verbunden, liegt jedenfalls nicht darüber; Coracoid setzt
seitlich am Sternum und nicht ventral an. Beim Säugerhaar sitzt der Musculus arrector pili auf der
falschen Seite. Der Schnitt durch die Amphibienhaut gibt die Umrisse der Drüsenepithelzellen ın
Schleim- und Körnerdrüse falsch wieder. Bei Pferd und Mammut zeigen Pfeile zu den Kauflächen der
Molaren nicht auf Zement-, sondern Dentinflächen.

Wie bei den Abbildungen, so auch beim Inhalt: Unter einer Vielzahl folgerichtiger, genauer, gut
verständlicher und einprägsamer, richtiger Darstellungen stößt man gelegentlich auf Fehler. Die
Sehnervenfasern werden auch bei den Säugern im Zwischenhirn verschaltet (s. 371), der Frosch hat
keinen Neocortex ($. 372), Amygdala ist keine Rindenstruktur ($. 373). Bildweite ist nicht gleich
Brennweite (Abb. 7.14 C), auch die Neunaugen haben in Ruhe nahakkomodierte Augen ($. 413).
Talpa und Scalopus dürften entgegen $.516 auf einen gemeinsamen, bereits grabenden Vorfahr

Buchbesprechungen 125

zurückgehen. Das Fehlen eines Brustbeins bei Archaeopteryx kann man nicht gut als Reptilienmerk-
mal ansehen, wenn fast alle Reptilien ein Sternum besitzen ($. 553). Auf den Galapagos-Inseln gab es
vor Ankunft des Menschen nicht bloß zwei, sondern etwa 9 terrestrische Säugerarten (s. $. 562). Beim
biologischen Artbegriff ($. 576/577) spielt immer noch eine „Morphospezies-Definition“ eine verwir-
rende Rolle. Es kann nicht für ein einheitliches Phänomen zwei nicht deckungsgleiche Definitionen
geben. Die Morphologie liefert Kriterien, mit deren Hilfe man die Grenzen von Biospezies oft ohne
allzu großen Aufwand erkennen kann, aber sie definiert keine Biospezies. Die Amphibien besitzen
durchaus einen Sinus venosus (s. 735), bei den Säugetieren sitzt das Foramen ovale nicht im Ventrikel,
sondern im Interatrialseptum des Herzens. Der Metatarsus 1 der Vögel ist frei und entgegen S. 763
nicht in den Tarsometatarsus einbezogen, dieser enthält dafür auch ein Metatarsale 4. Hylobittacus ist
keine Skorpionsfliege (S. 482, 483), sondern eine Mückenhaft.

Diese und weitere kleine Fehler verlieren sich glücklicherweise in dem reichhaltigen Inhalt. Die
klare Gliederung mit farblich hervorgehobenen „Boxen“ und Tabellen wie auch neue Ideen, z.B. die
Aufteilung des Verhaltens-Kapiıtels oder die Einbeziehung der Bioluminiszenz ın das Bewegungs-
Kapitel sorgen für Abwechslung und zusätzliche Spannung bei der Lektüre des weithin sehr fesselnd
dargebotenen Inhalts. Der Verweis auf speziellere Literatur und Übersichtsreferate in den „Verhand-
lungen der Deutschen zoologischen Gesellschaft“ der letzten 15 Jahre regen zu vielseitiger Vertiefung
an. Insgesamt eine erstaunliche Arbeitsleistung. Der Inhalt geht sicherlich weit über das hinaus, was
ein Student im Grundunterricht noch bewältigen kann. Das Buch ist eigentlich jedem Zoologen zu
empfehlen, der in der Explosion des Wissens einen handlichen Überblick sucht.

J. NIETHAMMER, Bonn

WALSER, K.; BosTEDT, H. (Hrsg.): Neugeborenen- und Säuglingskunde der Tiere.
Stuttgart: Ferdinand Enke Verlag 1990. 576 pp., 251 Abb., davon 84 farbig auf 32
Farbtaf., 120 Tab. DM 198,-. ISBN 3-432-38381-6

15 Autoren aus Deutschland und je-einer aus der Schweiz und den USA haben ein klar gegliedertes
und praxisorientiertes Buch verfaßt, welches vom Verlag mit technischer Sorgfalt und optisch sehr
ansprechend herausgegeben wurde.

In den einleitenden drei der insgesamt zwölf Kapitel werden folgenden Probleme behandelt:
1. Anatomische und physiologische Grundlagen des Neugeborenen; 2. Das Verhalten der Neugebo-
renen und Säuglinge; 3. Grundlage der Ernährung von Neugeborenen. Es schließen dann drei Kapitel
an, welche für dıe Aufzucht und Pflege neugeborener Säuger von besonderer Bedeutung sind:
4. Fütterungspraxis; 5. Die Haltungsbedingungen für Jungtiere von der Geburt bis zur Entwöhnung;
6. Pränatale Entwicklungsstörungen.

Die folgenden sechs Kapitel des Buches dürften besonders für den tierärztlichen Praktiker hilfreich
sein. Es werden die Krankheiten von Fohlen, Kälbern, Schaf- und Ziegenlämmern, Ferkeln, Hunde-
und Katzenwelpen sowie von Neugeborenen und Säuglingen verschiedener Zoo- und Wildsäugetier-
arten behandelt. Bei den Krankheiten werden Vorkommen und Bedeutung, klinisches Bild, patholo-
gischer Befund, Diagnose und vor allem die Therapie nebst möglichen Komplikationen geschildert.

Vornehmlich zu den praxisorientierten Kapiteln finden sıch auf 32 Farbtafeln Darstellungen zu
Krankheitsbildern. Dabei ist jede der Farbtafelseiten mit einem kräftigen Farbbalken gekennzeichnet,
so daß das Auffinden de Illustrationen erleichtert wird. Ein mehr als zehnseitiges Register erschließt
den Inhalt des Bandes.

Ein bedeutender Vorzug des Buches besteht darin, daß viele Einzelabschnitte der Kapitel jeweils
durch eine eigene weiterführende Literaturliste abgeschlossen werden. Den Herausgebern und
Autoren ist auch dafür Anerkennung zu zollen, daß sie die Herkunftspublikationen der Daten in den
sehr reichlich im Text verteilten Tabellen klar nennen. Viele - auch moderne — Lehrbücher erfüllen
diese eigentlich selbstverständliche Bedingung leider nicht!

Die Schilderung der normalen und pathologischen Verhältnisse bei Haustieren macht einen großen
Anteil des Buches aus. Es wird sicherlich auch von Säugetierkundlern und von Personen, die mit der
Pflege von Neugeborenen und Jungtieren befaßt sind, mit Nutzen zu Rate gezogen werden. In diesem
Zusammenhange sind die Ratschläge und praktischen Hinweise für die mutterlose Aufzucht von
jungen Säugetieren besonders hervorzuheben. P. LANGER, Gießen

WÜNNENBERG, W.: Physiologie des Winterschlafes. Mammalia depicta, Heft 14, Beiheft
zur Zeitschrift für Säugetierkunde. Hamburg und Berlin: Paul Parey 1990. 98 S., 34 Abb.,
16 Tab. DM 58,-. ISBN 3-490-12118-X

Mit dem Wunsch nach einer Verlängerung des menschlichen Lebens taucht auch heute immer wieder
die Frage auf, ob sich das irdische Dasein nicht durch einen „künstlichen“ Winterschlaf unterbrechen
ließe, um es später wieder „in alter Frische“ weiterzuführen. Ganze Forschergenerationen haben
versucht, das Geheimnis des „Winterschlafes“ zu lüften. Die Zahl der Untersuchungen geht in die

126 Buchbesprechungen

Tausende. Es gibt viele aufregende Entdeckungen; von der Lösung des Rätsels sind wir aber noch weit
entfernt. Was ist Winterschlaf? Sicher ist es keine „Pause“ vom Leben. Die vorliegende Publikation
gibt eine Reihe grundsätzlicher Antworten. Es war dabei notwendig, die Begriffe „Homoiothermie“
und „Poikilothermie“ neu zu definieren und sie mit der Problematik zu Überwinterung zu versehen.
Die wichtigsten Merkmale des natürlichen Winterschlafes (Inaktivität, Stoffwechselreduktion, ernied-
rıgte Körpertemperatur und Erregbarkeit) erlauben heute eine Zuordnung zu dem Phänomen des
Torpors. Der Hauptabschnitt beginnt mit den Steuerungsmechanismen (exogene und endogene
Faktoren). Sıe veranlassen die Vorbereitungen auf den Winterschlaf (Vorratsspeicherung, Anlage von
Fettdepots, Aufsuchen oder Herstellen geeigneter Winterquartiere). Nur nach Abschluß dieser
Maßnahmen kann ein Winterschlaf auch zum Erfolg führen. Erst jetzt ändert sich die Temperaturkon-
trolle mit einem kennzeichnenden Wechsel zwischen Torpor- und Euthermiephasen, wobei sich in
der Wintermitte nıcht nur die tiefsten Körpertemperaturen, sondern auch die längsten Schlafperioden
einstellen. Zur Deutung dieser Zyklen werden „Sollwertverstellungen“ bei der Regelung der Körper-
temperatur herangezogen. In enger Verbindung damit kommt es zu Minimaleinstellungen in allen
wichtigen Organsystemen (Herz, Kreislauf, Atmung, Stoffwechsel, Elektrolyt- und Wasserhaushalt,
Nervensystem, endokrines System). In zahlreichen Fällen lassen sich bereits ursächliche Zusammen-
hänge darstellen, insbesondere die entscheidenden energetisch-ökonomischen Prozesse. Trotz der
Fülle an Informationen bleiben die eigentlichen „Auslöser“ des Winterschlafes bis heute im Dunkeln.
Auch die Untersuchungen über mögliche „Triggersubstanzen“ haben hier noch keinen Durchbruch
erzielt.

Das Beiheft ist in erster Linie für die Studierenden der Biologie und Medizin gedacht. Es ist in
deutscher Sprache abgefaßßt. Aus der kaum noch überschaubaren Literatur wurden über 350 Zitate
ausgewählt, die teilweise noch weitere Übersichten enthalten. In allen Abschnitten bietet das Heft
Anregungen in dieses faszinierende Gebiet „einzusteigen“. E. KULZER, Tübingen

HaräAsz, N.: The vertebrate olfactory system. Chemical neuroanatomy, function and
development. Budapest: Akademiaı Kiadö 1990. 281 S. DM 60,-. ISBN 963-05-5634-0

In diesem Buch werden morphologische und neurochemische Befunde sowie die zentralnervösen
Anteile des Geruchssystems dargestellt. In einem sehr ausführlichen und mehr als 40seitigen Litera-
turverzeichnis werden die Quellen, auf denen der Autor seine Darstellung gründet, zusammengestellt.

Nach einer kurzen Einleitung werden die verschiedenen Ebenen des Geruchssystems besprochen.
Dabei wird jeweils über die licht- und elektronenmikroskopisch untersuchbare Struktur, über
biochemisch-molekulare Prozesse und gegebenenfalls auch über phylogenetische Differenzierungen
berichtet. Nach Schilderung der Rezeptoren der Geruchswahrnehmung (31 S.) und der Fila olfactorıa
(hier „Nervus opticus“ genannt) (9 S.) folgt dann als Hauptteil des Buches auf 145 S. die Besprechung
des Bulbus olfactorius. Die Zytoarchitektonik, die synaptische Organisation, die Glia-Anteile, die
chemischen Differenzierungen, wie auch funktionelle und ontogenetische Aspekte werden für den
Bulbus olfactorius ausführlich geschildert, und auch die Plastizität dieser Struktur wird besprochen.

Der Tractus olfactorius, übergeordnete olfaktorische Zentren und akzessorische Systeme, wie
beispielsweise das Vomeronasal- oder Jacobson’sche Organ werden in kurzen Abschnitten vorgestellt.
Wenn auch in diesem Buch strukturelle und neurochemische Gesichtspunkte den Schwerpunkt der
Betrachtungen bilden, so wird doch kurz auf sechs Seiten die verhaltensbiologische Bedeutung des
Geruchssystems bei Vertebraten dargestellt, wobei besonders die Entdeckung und Unterscheidung
von Geruchsstoffen sowie das Erlernen und Erinnern von Geruchsqualitäten und deren Bedeutung für
Ernährung und Fortpflanzung berücksichtigt werden. Ein achtseitiges Kapitel, welches sich mit der
Bedeutung des Geruchssystems für den Menschen beschäftigt, schließt den Text ab.

Die Fülle der Daten wird durch einen etwa zehnseitigen Index erschlossen, und das Buch kann mit
seiner Hilfe als Nachschlagewerk genutzt werden. P. LANGER, Gießen

PıecHock1, R.: Die Wildkatze. Neue Brehm-Bücherei 189. Wittenberg Lutherstadt: A.
Zıemsen 1990. 232 S., 98 Abb., 26 Tab. DM 30,50. ISBN 3-7403-0226-7

RupoLr PIECHocKI, der Autor dieser Neuerscheinung aus der Neuen Brehm-Bücherei, hegt seit
seiner Jugend ein leidenschaftliches Interesse für die Waldwildkatze, Felis sılvestris sılvestris. Dement-
sprechend konnte er während seiner langjährigen Tätigkeit am Zoologischen Institut in Halle viele
Daten und Materialien über diese versteckt lebende Säugerart zusammentragen und bearbeiten. In
dieser Artmonographie faßt er alte, überlieferte Angaben mit neueren aus dem gesamten Verbrei-
tungsgebiet und eigenen Untersuchungsergebnissen an regionalen Vorkommen (über 100 Individuen)
zusammen. Das Büchlein ist inhaltlich gegliedert in die Abschnitte: Einleitung, Benennung, fossil
belegtes Vorkommen, Systematik, Verbreitung in Europa, Morphologie und Anatomie, Biologie und
Okologie, Schutz und Hege, Literatur, Register.

Sehr ausführlich wird auf 62 Seiten die heutige vermutete und auch nachgewiesene Verbreitung ın
den verschiedenen europäischen Ländern dokumentiert, besonders genau für die alten Bundesländer

Buchbesprechungen 127

und das Gebiet der damaligen DDR. Nachweise in Form von Direktbeobachtungen, Spuren,
Totfunden, Fängen etc. werden häufig mit Orts- und Zeitangaben belegt. Morphologische und
anatomische Besonderheiten werden dann auf 48 Seiten beschrieben und in Maßen und Gewichten mit
statistischen Sicherungen mitgeteilt. Hier wird auch auf Unterscheidungsmerkmale zwischen Wild-
und Hauskatze und das Erkennen von Blendlingen näher eingegangen.

Das Kapitel über Biologie und Ökologie (68 S.) ist ebenfalls sehr informativ, obwohl gerade hier
viele Fragen unsicher oder gar nicht beantwortet werden können. Die Darstellungen vieler Einzelbe-
obachtungen enthalten zum Teil recht abweichende Angaben über Habitatsansprüche, Reviergrößen
und Dichten. Über das Verhalten im Territorium ist kaum etwas bekannt, und auch ein Aktivitäts-
rhythmus ist nur unter Bedingungen von Gefangenschaftshaltung erstellt, aus der freien Natur jedoch
nur ungenau bekannt. Telemetrische Untersuchungen an mehreren Individuen wurden bislang nur in
Ansätzen in Schottland und Lothringen durchgeführt. Die Angaben zur Fortpflanzungsbiologie
entstammen ebenfalls fast ausschließlich Beobachtungen aus zoologischen Gärten. Geschlechtsreife
vor Erreichen des 1. Lebensjahres, Ranz im Februar-März und mittlere Tragzeit von 68 Tagen (63-70)
scheinen arttypisch. Für Schottland, Mitteleuropa und den Kaukasus wird eine zweite Brunft im
Hochsommer angeführt, in Ausnahmen sogar eine dritte.

Insgesamt liegt eine umfassende Dokumentation vor mit vielen anekdotenhaften Schilderungen
und Einzelbeobachtungen belebt, allerdings nicht frei von mehreren Wiederholungen. Die Tatsache,
daß bei Wild- und Haustiertorm der Katze mehrfach von zwei Arten gesprochen wird, ist allerdings
aus zoologischer Sicht störend. D. Kruska, Kiel

VANDER WALL, S. B.: Food hoarding in animals. Chicago and London: The University of
Chicago Press 1990. 445 S., Abb., Tab. Kart. $ 34.50. ISBN 0-226-84735-7

Futterspeichern kommt bei Säugetieren (vor allem Insektenfressern, Raub- und Nagetieren), Vögeln
(besonders Greifvögeln, Eulen, Kleibern, Meisen und Corviden) und Arthropoden (Spinnen, Käfern,
Hautflüglern) vor, wobei Sammlen jeglicher Nahrung, die zu künftigem Gebrauch gehandhabt wird,
unter diesen Begriff fällt. Der Autor, der sich vor allem mit dem Anlegen von Vorräten bei Corviden,
in erster Linie amerikanischen Tannenhähern, befafst hat, behandelt die Art, Verteilung und Liege-
dauer von Vorräten, wie sie vor Entdeckung durch Konkurrenten geschützt und vom Besitzer
wiedergefunden werden, welche Vor- und Nachteile mit ihrer Anlage verbunden sind und unter
welchen Umständen Futterspeichern in der Evolution entstanden sein könnte. Reizvoll ist hier
besonders die Koevolution zwischen Futterspendern (Pinus-Arten) und ihren Nutznießern (Tannen-
hähern) und die Rolle von Samen versteckenden Tieren für die Verbreitung bestimmter Pflanzenarten.
Beispiele für die innerartliche geographische Variabilität der Sammeltätigkeit, für Unterschiede ım
Jahreslauf oder zwischen den Geschlechtern und Futterarten werden behandelt. Die Sammelbereit-
schaft ist bei Weidenmeisen wie Waldmäusen im Kurztag groß, ım Langtag gering und wird
offensichtlich über den Einfluß der Fotoperiode auf die Sexualhormon-Produktion gesteuert. Bei
Laborratten wurden Abnahme der Eintragebereitschaft mit zunehmender Temperatur und wachsen-
dem Körpergewicht registriert. Spezielle Kapitel besprechen die futterspeichernden Arten in systema-
tischer Folge. Obwohl im Schriften-Verzeichnis etwa 1500 verwertete Zitate aufgeführt werden, sind
noch viele Fragen offen. Das hängt sicherlich mit der großen Variabilität von Speicherverhalten und
der Schwierigkeit zusammen, Vorräte in der Natur aufzufinden, bestimmten Individuen zuzuordnen
und die Nutzungsrate zu ermitteln, um nur einige vordergründig zu erfassende Daten zu nennen.
Zudem ist es oft schwer zu entscheiden und eine Frage der Interpretation, ob nicht sofort verzehrtes
Futter, als Vorrat gewertet wird, wie Tab. 9.4 über die Eulen zeigt. Danach hätte Bubo virginianus
Nager und Hasen, Bubo bubo und Athene nociua nonpasserine Vögel „gespeichert“. Dies deutet auf
einmalige, nicht generalisierbare Feststellungen.

Schlecht ausgewertet ist die europäische und vor allem deutschsprachige Literatur. Der Feldham-
ster (Cricetus cricetus), Inbegriff des Vorratsspeicherers unter den Nagetieren, wird nur einmal auf
S. 263 unter Hinweis auf Nowak und ParaDıso (1983), eine Sekundärquelle, kurz erwähnt. Auf der
gleichen Seite wird behauptet, der deutsche Name „Hamster“ sei vom Verb „hamstern“ abzuleiten. Es
dürfte wohl umgekehrt sein. Ahnlich dürftig sind die Bemerkungen etwa über Gliriden. Arvicola
kommt namentlich überhaupt nicht vor. Diese Mängel ungeachtet, lohnt sich die Anschaffung des
Buches, das insgesamt vielseitig, anregend, gut verständlich, wohl geordnet und ansprechend bebil-
dert ist. J. NIETHAMMER, Bonn

PETERS, G.; HUTTERER, R. (eds.): Vertebrates in the Tropics. Bonn: Zoologisches
Forschungsinstitut und Museum Alexander Koenig 1990. 424 pp., soft-bound, numerous
illustrations and tables. DM 85,- (including postage). ISBN 3-925382-32-1

This book publishes the “Proceedings of the International Symposium on Vertebrate Biogeography
and Systematics in the Tropics” held in Bonn, June 5-8, 1989. It contains 33 chapters, of which 12
refer exclusively to mammals. Some of the other articles present reviews that deal with vertebrates ın

128 Buchbesprechungen

general and to a minor extent also refer to mammals. Each paper starts with an abstract and gives a list
of relevant literature. Thus, efficient overviews and introductions are presented.

After short introductory remarks of the editors, four chapters deal with the paleontology and

paleobiogeography in the tropics. In one of the chapters STORCH discusses the paleogeographical
jigsaw puzzle of the Eocene mammalian fauna from Messel near Darmstadt. HAFFER presents aspects
of allopatric speciation and also considers mammalıan taxa.
The following part of the book, consisting of six chapters, presents “New Data and Discoveries”.
In one of the chapters HUTTERER and YALDEN introduce two new shrew species from Ethiopian relic
forests and two other papers deal with rodents: VAN DER STRAETEN and Dupu comment on Praomys
from Zaire and ALBERICO on geomyids from South America.

The most extensive section of the book, consisting of 21 chapters, deals with “Patterns, Analyses
and Models”. There are generalizing articles that cover mammals from Angola (FEILER), the
Philippines (HEAnEY and RıckArr) and Peru (PATTon et al.). CLAEssen and DE VREE deal with the
chiropteran genus Epomophorus that has a wide distribution in tropical Africa. Results of electropho-
retic studies on Crocidura are presented by MADDALENA, and HUTTERER and TRANIER discuss the
immigration of Suncus murinus into Africa and Madagascar. DIETERLEN deals with rodents of the
Afrıcan rain forest and in a very informatively illustrated contribution GRUBB gives an excellent
introduction into “Primate geography in the Afrotropical forest biome”.

A final chapter by Sayver et al. deals with the necessity of conservation of vertebrate diversity in
tropical forests through appropriate management.

The well-produced book includes many informative illustrations and a wealth of data that - in
some cases - are presented ın extensive tables as appendices to their articles. This publication is a useful
source of information for those zoologists that are interested in tropical vertebrates.

P. LANGER, Gießen

Kıncoon, J. Island Africa. The Evolution of Africa’s Rare Anımals and Plants. London:
Collins 1990. 287 pp., num. fıgs. £ 25.00. ISBN 00-219-443-0.

Amongst mammalogists, JONATHAN KINGDon needs no introduction since his monumental seven
volume work on East Afrıcan mammals has become an invaluable source of reference. Several
exhibitions of his anımal drawings and paintings in London and Oxford (in Germany at Gießen and
later in the Senckenberg Museum of Frankfurt) have aroused both academic and public interest.

His new book provides a platform for the Tanganyıka-born artıst and biologist from which he
makes his plea for unique, rare or endangered anımal and plant species. He offers his synoptic view of
Afrıca’s flora and fauna which he follows through a series of ecological “islands”. With the artıst’s eye,
supported by admirable knowledge of taxonomic and functional relationships, he uncovers evolution-
ary processes and dependencies, which the expanding species Homo sapiens threatens to disrupt
forever. Kınapon’s concentrated expeditions through unique African ecosystems are aesthetic and
scientific eye-openers demanding our active participation ın realistic conservation concepts.

The generously illustrated book follows an endemism concept which the author displays ın 13
chapters, each consisting of a biogeographic example which he treats like treasures (e.g., Horn of
Afrıca, Zaire basin — “an evolutionary whirlpool” etc.). He proposes new strategies, lists endemic
species, reserves and parks in appendices — whoever is engaged ın scientific work ın Africa should
study Kınspon’s “Islands”. R. R. Hormann, Gießen

OoRscHOT, D. E.; Jones, D. G.: Axonal Regeneration in the Mammalian Central
Nervous System. A Critique of Hypotheses. Advances in Anatomy, Embryology and
Cell Biology. Vol. 119. Berlin, Heidelberg, New York, London, Paris, Tokyo and Hong
Kong: Springer Verlag 1990. 121 pp., 38 fıgs, 17 tabs. DM 89,-. ISBN 0-387-51757-X

In contrast to other tissues, the central nervous system (CNS) has very limited possibilities to
regenerate after injury. Axonal regeneration is such a possibility and thus its explanation ıs a problem
of scientific and practical relevance and a large amount of papers is dealing with this phenomenon. In
four chapters the authors present 1. a survey on hypotheses, 2. in vivo experiments and 3. in vitro
experiments to explain regeneration in the CNS before they come to 4. conclusions. It is pointed out
that many hypotheses which try to explain the failure of the CNS to regenerate as other tissue does,
lack sufficient experimental verification. Thus, in vitro experimental approaches are discussed as a
possibility to help solving this problem. Finally five hypotheses are presented “as the most worthy of
consideration in enhancing the CNS regenerative response. These are the proliferation of non-
neuronal cells, incompatibility between neuronal and non- -neuronal cells, vascular permeability, the
absence of specific growth factors and the somal response”. None of these hypotheses is said to
explain alone the regenerative response, but taking together parts of these hypotheses would help to
gain further insights.

The review of OoRSCHOT and JONES is a very useful survey not only for those, who are engaged
scientifically into this problem, but also for neurobiologists in general. G. REHKÄMPER, Köln

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ZEITSCHRIFT FÜR
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SÄUGE

rgan der Deutschen Gesellschaft für Säugetierkunde

kOliveira, J. A.; Lorini, Maria Lucia; Persson, Vanessa G.: Pelage variation in Marmosa incana (Didelphidae,
arsupialia) with notes on taxonomy. — Variation des Haarkleides von Marmosa incana (Didelphidae, Marsupia-
a) mit Anmerkungen zur Taxonomie 129

a, J.-S.; Weber, J.-M.: Characteristics and distribution of breeding dens of the Red fox (Vulpes vulpes) in a
ountainous habitat. - Kennzeichen und Verteilung von Aufzuchtbauen beim Rotfuchs (Vulpes vulpes) in einem
‚ebirgigen Habitat 7
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‚nalbeuteldrüsen der Hauskatze, Felis silvestris f. catus. — The cytology of a highly specialized sebocyte, as
‚emonstrated in the holocrine glands of anal sacs in the domestic cat, Felis silvestris f. catus 144

ıbelli, A.; Dyzenchauz, F.; Ramos, A.; De Rosa, N.; Wainberg, R.; Reig, O. A.: Cytogenetics and karyosystem-
-tics of phyllotine rodents (Cricetidae, Sigmodontinae). Part Ill. - Zytogenetik und Karyosystematik von phyllotinen

‚odentia (Cricetidae, Sigmodontinae). Teil Ill 155
auchi, ©. D.; Busch, Christina: Burrow structure in the subterranean rodent Ctenomys talarum. — Die Struktur
ar Baue von Ctenomys talarum, einer unterirdisch lebenden Nagerart 163

(ano, Eulalia; Barbosa, A.: Distribution patterns of small mammal fauna along gradients of latitude and altitude in
orthern Spain. — Verteilung der Kleinsäugerfauna entlang von Breiten- und Höhen-Gradienten in Nordspanien 169
Isenschaftliche Kurzmitteilungen

t, C. R.: The use of fur colour characters to distinguish the sibling species Sorex araneus und Sorex coronatus
nsectivora, Soricidae): a field test in a zone of parapatric contact. — Die Benutzung von Fellfärbungsbesonder-

siten zur Unterscheidung der Schwesterarten Sorex araneus und Sorex coronatus (Insectivora, Soricidae): Ein
reilandtest in einer Zone mit parapatrischem Kontakt 176
Bree, P. J. H.; Mohd Khan bin Momin Khan: On a Fishing cat, Felis (Prionailurus) viverrina Bennett, 1833, from
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Z. Säugetierkunde 57 (1992) 129-136
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Pelage variation in Marmosa incana (Didelphidae, Marsupialia)
with notes on taxonomy

By J. A. DE OLIvEIRA, MarIA LucıaA LoRrINI, and VAnESssA G. PERSSON

Museu Nacional, Universidade Federal do Rio de Janeiro, and Musen de Historia Natural “Capao da
Imbnia”, Curitiba, Parana, Brazil

Receipt of Ms. 28. 10. 1991
Acceptance of Ms. 6. 12. 1991

Abstract

Described and analysed pelage patterns of Marmosa incana, on the basis of museum specimens over
the whole geographic range of the species. Three pelage types were identified by the length and texture
of the dorsal hairs. Consistent occurrence of these pelage types in different age and sex classes along
the year refute previous hypotheses of geographic varıation and pelage seasonality and point to an
intrinsic determination of the pelage types. The taxonomic status of the forms formerly included in
Tare’s (1933) incana section ıs discussed and possible causes of sexual dımorphism ın pelage are
surveyed.

Introduction

With forty-seven recognized species (HonAackt et al. 1982), the genus Marmosa is the most
diverse taxon of Neotropical marsupials. In Tarte’s (1933) classıcal revision the genus
Marmosa was defined comprising five major species groups, each one subdivided in
sections. Although recent authors (e.g. Pine 1972; KırscH 1977) have suggested that
Marmosa could be split into different genera, this taxon has remained undivided, as
formerly claimed by TATE, except by the brief proposition of GARDNER and CREIGHTON
(1989), in which Marmosa (s. 1.) was divided in five genera coincident to a great extent with
the five species groups of TATE (1933). At the specific and subspecific levels the study of
TATE (1933) remains the only detailed description of the varıation in Marmosa, especially
in what concerns the forms analysed in the present study. For this reason, TATe’s (1933)
assignment of species and species groups will be followed hereafter.

The incana section of TATE’s (1933) noctivaga group comprises two species that occur
in eastern Brazil: Marmosa incana (Lund, 1841), which is the genotype of the genus
Marmosops according to GARDNER and CREIGHTON (1989), and M. scapulata (Burmeister,
1856). These two forms are mainly distinguished by the presence of conspicuous stiffened
hairs in the scapular regions of the latter species. In addition to the modified pelage of M.
scapnlata, TaTE (1933) also ıdentified sexually dimorphice long and short pelages to
characterize subspecies of Marmosa incana. In a recent interpretation of the same pelage
varıation, EMMons (1990) ıdentified the long and short furs of Marmosops incanus as
seasonal coats, and ascribed a third pattern showing a “collar” ot new hair to a molt stage.

The first intend of this study is to bring a more comprehensive description of pelage
patterns in the incana section. In order to understand the determinants of the pelage
varıation we also analyse the occurrence of the pelage patterns in relation to age, sexual and
seasonal variation.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5703-129 $ 02.50/0

130 J. A. de Oliveira, Maria Lucıa Lorini, and Vanessa G. Persson

Material and methods

A total of 311 museum specimens was analysed in this study. Localities, sample sizes, and museum
acronyms are as follows: MN = Museu Nacional, Rio de Janeiro; UFMG = Departamento de
Zoologia, Universidade Federal de Minas Gerais; MBML = Museu de Biologia Mello-Leitäo;
MHNCI = Museu de Histöria Natural “Capao da Imbuia”.

Bahia: Feira de Santana (1, MN); Ilheus (83, MN); Jaguaquara (2, MN); Jequie (3, MN); Serrinha (6,
MN). — Minas Gerais: Alem Paraiba (64, MN); Almenara (1, UFMG); Caratinga (1, UFMG);
Conceigäo do Mato Dentro (9, MN); Gräo Mogol (5, MN); Juiz de Fora (6, MN); Lagoa Santa (15,
MN); Parque do Ibitipoca, Lima Duarte (1, UFMG); Mocambinho, Manga (8, MN); Parque Florestal
do Rio Doce, Marlıeria (4, UFMG); Ponte Nova (2, MN); Caraga, Santa Bärbara (21, UFMG); Rio
Casca (1, UFMG); Sete Lagoas (3, UFMG); Värzea da Palma, Serra (2, UFMG); Parque Nacional da
Serra da Canastra (1, UFMG); Turmalına (1, MN) Vargem da Lapa (2, UFMG); Volta Grande (6,
MN). -— Espirito Santo: Campinho (1, MN); Cariacica (6, MBML); Castelo (3, MBML); Nova
Lombardia (1, MN); Santa Tereza (13, MBML). - Rio de Janeiro: Ilha Grande, Angra dos Reis (4,
MN); Pogo das Antas, Sılva Jardım (2, MN); Säo Joao Marcos (1, MN); Teresöpolis (10, MN);
Tijuca, Rio de Janeiro (5, MN); Tingua, Nova Iguassu (1, MN). - Parana: Pıraquara (2, MHNCI). —
No locality: (14, MN).

Date of collecting and sex were obtained from original tags. In order to determine the age of specimens
we used a modification of the system proposed by TRıBE (1990) which is based on the sequence of
eruption of molarıform teeth (classes 1 to 6) and wearing of M4 (classes 6 and 7). We noted that the
angle of placement of M4 ıs individually variable, sometimes resulting in abnormal wearing of thıs
tooth. Consequently, we analysed additional wearing of M1-M3. Beginning of class 6 ıs readıly
identifiable by incompletely erupted PM3; to classıfy individuals with fully erupted PM3, scores were
attrıbuted to three consecutive stages of M1-M4 wearing, the first being posteriorly allocated to age
classe 6 and the last two stages to age class 7 (7! and 7").

Types of pelage were identified on the basis of length and texture of dorsal fur. Medium pelage

a9)

Wur®

we 2

| |
| >

Fig. 1. Dorsal view of individuals of each pelage pattern described. a: type A; b: type B; c: type C

Pelage varıation in Marmosa incana 131

length was measured with a millimetric ruler at the mid-dorsum of each specimen. The texture was
estimated by touch and classified in soft, coarse and stiffened categories. Hairs from the back, scapular
and throat region of representative individuals of each sex and pelage pattern were observed under a
binocular microscope with a drawing tube to assess gross morphologic differences and to draw the

distinct hair types.

Samples from states of Bahia, Minas Gerais and from combined localities from the states of Rio de

Janeiro, Espirito Santo and Parana, con-
gruent with geographical distances and
ranges of the subspecies of M. incana
proposed by TATE (1933), were examined
separately. Distributions of pelage pat-
terns by age, sex and month were found
to be sımilar in the three samples, but the
respective sample sizes became much re-
duced when analysed monthly. There-
fore, we tabulated the frequencıies at each
pelage pattern by age, sex and by month
for all specimens. Animals that had been
kept in captivity were excluded from the
analyses.

The occurrence of an orange to rust
brown staıin around the mammary area is
an indication of pregnancy and nursing
(BARNES 1977), and was used to deter-
mine reproductive status in females. Re-
productive condition in males ıs more
difficult to determine from external
markings, and was assessed by histologi-
cal examination of testes for sper-
matogenic activity in two available males
(MN 29 006 and MN 29 007).

Results

The following three patterns were
identified in the analysıs of the haırs
of the back. Type A (Fig. la) shows
a uniform dorsal fur, shiny, brown-
ish gray, with soft and long haırs,
length 8-12 mm (Fig. 2a). In type B
(Fig. 1b) the dorsal pelage ıs also
uniform and brownish gray, but
coarse, dull and short, haırs length
5-8 mm (Fig. 2b). The most conspic-
uous pattern, type C (Fig. Ic), ex-
hibits an heterogeneous dorsal coat:
the scapular region shows modified
broadened and stiffened yellowish
hairs, length 5 mm (Fig. 2c), extend-
ing backwards, reaching the mid-
dorsal region in some specimens. In
the interscapular area the fur is shor-
ter (4 to 9mm long) and dull
grayısh, with some modified hairs
mixed to the normal ones; the re-
mainder dorsal pelage is similar to
type A, with hairs 10 to 12 mm long.

Fıg. 2. Hair types associated with each pelage pattern.
a: dorsal hair of pelage types A and C; b: dorsal hair of
pelage type B; c: scapular hair of pelage type C

132 J. A. de Oliveira, Maria Lucia Lorini, and Vanessa G. Persson

Pelage type A comprises individuals ranging from age classes 3 (the younger individuals
of our sample) to 6 in both sexes, as well as 61 % of the males of age class 7! (Fig. 3). Only
females showed pelage type B, which occurred in 13 % of the individuals of age class 6, and
in the entire age class 7 (7! and 7!'). Pelage type C was found only among males, in 6% of
age class 6, 39 % of age class 7! and 100% of age class 7.

25 27 50 47 1 17 32 19 n

SS
—

100%

N

75%

IRQ
SINHHIHNNEN
RER

S
\
S
d

50%

25%

LILIIIS

3-4-5 6 TE 7 age

0%

BE TYPE A TYPE B TYPEC

Fig. 3. Frequency (percent) of pelage patterns by age classes

The ventral pelage is ivory white ın the three patterns described, with soft and long haırs
in type A and C, whereas short and coarse in type B. In the throat region all males of
pelage type C show modified hairs similar to that of the scapular region. In pelage type A,
although occupying a much smaller area, the modified throat haırs are also present in 12 %
(n = 6) of the individuals of age class 6 and in 40% (n = 4) of age class 7.

In four males (MN 8296, 11 147, 13 367 and 24 684) of pelage type A and age classes 6
and 7', we observed a very small area of modified stiffened hairs on both sides of the neck,
near the scapular region. One class 7! female (MN 17 158) showed an atypical condition of
pelage with venter and anterior half of dorsum with pelage type B and posterior half with
pelage type A. This pattern was also found ın another female specimen (MN 11 157, skin
only).

Tabulation of the occurrence of pelage patterns by month (Fig. 4) reveals that type A
occurs throughout the year, more often from January to August and decreases toward the
end oftthe year. Pelage type B shows low frequencies between January and July, and shows
higher frequencies from September to November. Type C is seldom present from
February to May and its frequency increases from July on.

Discussion
Pelage patterns

The patterns of pelage identified here have already been partially described in the literature.
Type A is the most often mentioned, possibly because it ıs the most common in nature,
occurring in both sexes from age class 3 (at least) to age class 6. This is the basıc pelage
pattern of Marmosa incana according to TATE (1933), reported for both sexes of M. ıncana
paulensis and for males of M. incana bahiensis and M. incana incana. This pelage type was
referred to by Emmons (1990) as the winter coat, occurring from May to August.

Pelage varıation ın Marmosa incana 133

\
N
N
N
\

SS

ZI

JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEZ
BEE TYPE a ZA TvPE B NS TYpec
Fig. 4. Frequency of pelage patterns by month

TATE (1933) was the first to ıdentify pelage type B, and related it to females of M. incana
incana and M. incana bahıensis. Emmons (1990) described thıs short fur as a summer coat,
oceurring between January and April.

Pelage type C was first reported in the description of Grymaeomys scapulatus Burmei-
ster, 1856, which is Marmosa scapulata for TATE (1933). EmMmons (1990) suggested that
this pattern represents a moult stage between the summer and winter coats in Marmosops
incanus, restricted from September to December, and pointed out that it was once
described as a different species.

Our results do not indicate that pelage types A and B are alternate seasonal coats.
Although pelage type A exhibited higher frequencies between January and August and
type B was more common between September and December, we find types A and B
concomitantly distributed along all the year. Moreover, absence of pelage type A among
individuals exhibiting accentuated molar wearing (age class 7!') and absence of pelage types
B and C among individuals of age classes 3, 4, and 5 throughout the year are evidence that
the change from long (type A) to short (type B) fur is a single and definitive event.

We have evidence, nevertheless, for a transition from pelage type A to B and from A to
C. The sıx specimens stressed above, four males with incipient stiffened scapular pelage
and the two females with short/long dorsal pelage, are thought to represent intermediate
conditions between pelage types A und C and types A and B, respectively. These
specimens were collected between August and September (males) and between September
and October (females), periods in which we notice an ınversion in the ratıos between
frequencies of pelage types A/C and A/B in the year (Fig. 4).

In contrast, ordinary moulting is represented in our sample in seven individuals of
pelage type A, which show an incipient layer of new soft hairs under the long dorsal haırs.
Close inspection of the associated hairs did not reveal the stiffened characteristic hair of
type C, nor the individuals in moult were restricted to a determined part of the year.

In regard to the relation between sex and pelage, our results also do not corroborate the
assertion by TATE (1933) that the long (type A) and short (type B) pelages are sexually
dimorphic furs. In fact, type A represents the monomorphic pelage for both sexes,
occurring from age 3 to 6. On the other hand, the available data demonstrate that pelage
types B and C are related to secondary sexual dımorphism in the incana section. There ıs

134 J. A. de Oliveira, Maria Lucia Lorini, and Vanessa G. Persson

also an apparent association between these pelage patterns and sexual maturity. Only
pelage type B females showed the stained mammary region, which is an indication of
reproductive activity. As for the males, it is interesting to note that the individuals of
pelage type A examined, although as old as age class 7, did not show any spermatogenic
activity. It seems, therefore, that pelage type C is achieved in concern with the sexual
maturity.

These results indicate that the pelage patterns described represent distinct age and sex
related stages in all studied populations of the incana section. Whereas only the age
component is responsable for the distinct pelages of youngs and sub-adults, the age, sex
and sexual maturity determine the dimorphic adult pelages B (females) and C (males). The
“seasonal” component is but a function of different age fluctuations along the year, and
cannot account for the determination of pelage variation in the incana section.

Taxonomic remarks

Some taxonomic implications result from the conclusion above. The modified scapular
pelage, diagnostic of Marmosa scapulata, ıs in fact the adult (maturated) male pelage
observed in all populations of the incana section. Therefore, Grymaeomys scapulatus
Burmeister, 1856, ıs a subjective junior synonym of Marmosa incana (Lund, 1841). The
fact that adult males of M. incana match the M. scapulata pelage pattern was already noted
by TRıBE (1987), who pointed out a possible conspecifity of these two forms.

Examining the holotype of M. scapnlata (Berlin Museum 2330) TATE (1933) verified
that the skin was faded to light brownish. In BuURMEISTER’s (1856) original description,
hairs were “at base slate gray, then pale yellow-red, and last cinnamon”. This bandıng
pattern agrees very closely to that we found in specimens of M. incana, and results ın a
grayısh dorsal colour, brownish washed above.

TATE (1933) was the first to recognize the close relationship between M. scapulata and
M. incana, and notwithstanding cranıal and distributional similarities between these taxa,
the pelage differences convinced him of the distinctiveness of M. scapulata. Apparently, no
male skins of age class 7!" (where all males show pelage type C) were available to TATE
(1933). Noteworthly, the only male specimen ot Marmosa incana reterred by TATE (1933)
to be very old (Copenhagen 132) had no skin. This insufficient sample probably contri-
buted to the recognition of M. scapulata as a full species.

In his review, TATE (1933) recognized three subspecies of Marmosa incana, based
mainly on pelage traits. Marmosa incana incana and M. incana baihensis, characterized by
sexual dimorphism in pelage length (short in females and long ın males) differed by the
presence of gular stiffened hairs in males of the former subspecies. These forms were
distinguished from M. 1. paulensis ın which both sexes showed long fur (type A). In our
study, which covers the total geographic range of M. incana, and includes topotypic series
of M. incana incana and M. incana paulensis, the pelage type B (short fur) and the gular
stiffened hairs in males are present in all subsamples in some individuals of classes 6 and 7'
and in all representatives of age class 7. Consequently, as far as pelage is concerned, the
subspecific structure of M. incana proposed by TATE (1933) is inconsistent and should be
reconsidered, because it is based on age rather than on geographical differences. Appar-
ently, the pelage diagnoses proposed by TATE (1933) for the subspecies of Marmosa incana
result from young-biased samples of the populations described as M. 1. bahiensis and M. ı.
paulensis ın relation to the nominal subspecıes.

Sexual dimorphism

A further implication of our study relates to sexual dimorphism in pelage in M. ıncana.
Pelage of adult males (type C) differs strikingly from that of adult females (type B), juveniles,

Pelage varıation in Marmosa incana 135

and subadults (type A). A less conspicuous difference ıs found between adult females and
younger individuals of both sexes. As far as we know this ıs the first marsupial to show
sexual dimorphism in pelage structure.

According to Raus (1977), sexual selection is the most important mechanism affecting
male’s colour and structures used ın displays. Although territorial and reproductive
behavior in M. incana ıs unknown, the modified scapular pelage in males with upstanding,
self-coloured and frontally positioned hairs (Fig. 5) may perform a role in socıal interac-
tions among adult individuals, and could be related to sexual selection.

Fıg. 5. Live adult male of Marmosa incana showing pelage type C. Note darker line formed by the
gray bases of longer hairs adjacent to the modified scapular pelage

Apparently, the occurrence of differentiated adult pelage has not been referred to ın
female mammals. This may be due to either extreme rarıty of this phenomenon in the wild,
or to overshadowing by relatıvely greater distinctiveness of males. In the case of M. incana,
the differentiated pelage type B could be a consequence of epigenetic interactions hindering
the full manifestation on females of a fixed male trait. An alternative hypothesis would deal
with selection upon pelage in females, the short fur possibly representing an advantage
either in the heat improvement to the young in the teat attachment phase, or in the
recognition of the female reproductive status. At any rate, the actual causes of the
differentiated female pelage remain to be demonstrated.

136 J. A. de Oliveira, Maria Lucia Lorini, and Vanessa G. Persson

Acknowledgements

We are greateful to the curators of the institutions who kindly allowed access to the mammal
collections. We express our gratitute to C. DOS SANTOS for the histological preparations and to M.
PEssoA for the drawings. Drs A. LANGGUTH and S$. F. Dos Reıs read a first version of the manuscript
and provided valuable comments. Dr H. R. PEArson kindly revised the English version. Work by the
authors was partially supported by graduate fellowships from Conselho Nacional de Desenvol-
vimento Cientifico e Tecnolögico - CNPa.

Zusammenfassung

Variation des Haarkleides von Marmosa incana (Didelphidae, Marsupiaha) mit Anmerkungen zur
Taxonomie

Die Haarkleider der südamerikanischen Beutelratte Marmosa incana werden beschrieben; nach der
Länge und der Struktur der Rückenhaare können drei verschiedene Haarkleider (A, B, C) unterschie-
den werden. Alle drei Kleider treten zu fast jeder Jahreszeit auf; dies widerspricht früheren Theorien,
die von geographischer Variation oder einem saisonalen Haarkleidwechsel ausgingen. Statt dessen
besteht offenbar eine Relation zwischen dem Auftreten von Haarkleid B und der sexuellen Aktivität
der Weibchen und dem von Haarkleid C und der sexuellen Aktivität der Männchen. Auf der
Grundlage der neuen Befunde wird die Taxonomie verschiedener Formen der incana-Gruppe von
Tate (1933) diskutiert, und die möglichen Ursachen eines Sexualdimorphismus ım Haarkleid von
Säugetieren werden besprochen.

Literature

BARnES, R. D. (1977): The special anatomy of Marmosa robinsoni. In: The biology of marsupials. Ed.
by Don Hunsaker ll. New York, London: Academic Press. Pp. 387412.

Emmons, L. (1990): Neotropical rainforest mammals. A field guide. Chicago, London: University of
Chicago Press.

GARDNER, A. L.; CREIGHTON, G.K. (1989): A new generic name for TaTE£’s (1933) microtarsus group
of south american mouse opossums (Marsupialia: Didelphidae). Proc. Biol. Soc. Wash. 102, 3-7.

Honackı, J. H.; Kınman, K. E.; Koeppr, J. W. (1982): Mammal species of the world; a taxonomic
and geographic reference. Lawrence, Kansas: Allen Press.

KırschH, J. A. W. (1977): The classification of marsupials. In: The biology of marsupials. Ed. by Don
HunsakEr II. New York, London: Academic Press. Pp. 1-48.

Raııs, K. (1977): Sexual dimorphism in mammals: avian models and unanswered questions. Amer.
Natur. 11, 917-938.

TATE, G. H. H. (1933): A systematic revision of the marsupial genus Marmosa. Bull. Amer. Mus.
Nat. Hist. 66, 1-250.

TRIBE, C. J. (1987): A mastofauna do Estado do Rio de Janeiro, com especial referencia & ordem
Polyprotodontia (Marsupiais). Unpubl. MSc Thesis, Museu Nacional, Rio de Janeiro.

TRIBE, C. J. (1990): Dental age classes in Marmosa incana and other didelphoids. J. Mammalogy 71,
566-569.

Authors’ address: JoAO A. DE OLIVEIRA, MARIA Lucia LorınI and VANESSA G. PERSSON, Secäo de
Mastozoologia, Museu Nacional (UFRJ), Quinta da Boa Vista, s/n°, CEP 20 942
Rio de Janeiro, RJ, Brazil

Z. Säugetierkunde 57 (1992) 137-143
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Characteristics and distribution of breeding dens of the Red fox
(Vulpes vulpes) in a mountainous habitat

By J.-S. MEıaA and J.-M. WEBER

Institut de Zoologie, Universite de Neuchatel, Switzerland

Receipt of Ms. 28. 10. 1991
Acceptance of Ms. 27. 1. 1992

Abstract

Described the red fox breeding dens of a 30 km? area and compared them to the non- breeding dens.
Dens were searched and controlled since 1986. In 1990 every den was characterized to examine their
distribution and characteristics. The total number of dens was 62 (0.33/km?). 19.4% of them were
used for cubbing (1.88/km?). No significant difference in the characteristics of breeding and non-
breeding dens was found except for the number of entrances, which was higher in the breeding dens.
Man-made structures could be used as breeding dens as well as dens dug by badgers. The breeding
dens were not further distant from roads and houses than the other dens. The breeding dens were not
evenly spaced in the area and the same ones were generally used over several years. Results showed
that the use and distribution of breeding dens was limited by the number of suitable sites. The number
of breeding dens could be used to estimate the number of foxes in an area but this requires information
on the social organization of the special fox population.

Introduction

Dens are used by the red fox Vulpes vulpes for two different activities: 1. as resting sites
during the non-active period (non-breeding dens), 2. as sıtes for birth and rearıng of cubs
(breeding dens). Some dens are used for both activities. Several papers have described the
characteristics of fox dens in different habıtats (e.g. Fuchs 1973; EIBERLE 1975; WEBER
1983; Roman 1984; IOKEM 1985; PaAQuoT and Lıso1s 1986), but there are only few data on
breeding dens (HEwson 1986; NAKAZoNo and Ono 1987; BROCHIER 1989). The question
ot breeding dens is important because it could provide useful information about a fox
population, i.e., number of foxes, recruitment, and level of urbanızation. In this paper we
compare some characteristics of the breeding dens with the non-breeding dens, and show
their distribution and use, using data obtained in a mountainous area ın Switzerland.

Material and methods

Since 1989 and after a preliminary study of three years (PARATTE 1989) we monitored the fox
population of a 30 km? area in the Swiss Jura Mountains. The study area is described in WEBER et al.
(1991). The relief is karstic and the soils are shallow and unsuitable for burrowing, except in some
small areas with peat. Roads and farms are numerous and evenly spaced.

Dens were found by walking systematically throughout the study area, using fox tracks in the
snow during winter. Starting in March, every den was controlled every week in order to assess the
presence of cubs. The occupation of a den by a fox family was confirmed by direct observation. In
summer 1990, we checked every known den or den site in order to study their distribution and their
characteristics. Fach one was characterized using:

1. The type of habitat. Four categories were distinguished:
forest (20.1% of the study area), wooded pasture (25.2 %), pasture (31.9%), and fertilized
meadow (22.8 %). For “forest” two subcategories were made: “forest” and “forest’s edge”.

2. The type of substratum. The different possibilities were:
a) den dug in the earth among spruce root system (“spruce root system”) by foxes or badgers;

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5703-137 $ 02.50/0

138 J--S. Meıa and ]J.-M. Weber

b) den dug in bare earth (“earth”); c) den situated ın rocks (“rocks”); d) den situated in dumping-
grounds, man-made accumulations of stones, wood, fire proof garbadges, ... (“dumping-
ground’ ”); e) combinations between these four categories: 1.e., den with some entrances in the earth
among spruce root system and some in bare earth (“spruce root system/earth”).

The number of entrances: N.

The distance to the nearest road (main roads only) Dr.

The distance to the nearest house: Dy.

The distance to the nearest breeding den (for breeding dens only).

1% test the distribution of the breeding dens, we compared the observed nearest distances between
breeding dens with the nearest distances obtained by a simulation programme which set 12 points
randomly (with the same probability for each surface unit) on the surface corresponding to the study
area. Simulation was repeated 1500 times.

on 1 E07)

Results
Number and density

In spring 1990, the total number of dens regularly used by foxes in the study area was 62.
Twelve of them (19.4 %) were used by 11 fox families as breeding dens: one family having
moved, one week after the first emergence of cubs, to another den. Counting only one den
for this family, the density of dens was therefore 1.88/km? and for breeding dens 0.33/km?

(Fig. 1).

: secondary road;
AAA: limits of the study area; *: breeding dens; @: non-breeding dens; spotted: wooded areas

: major road;

Fig. 1. Location of the dens in the study area in 1990.

Characteristics and distribution of breeding dens of the Red fox 139

Characteristics

Six of the 12 breeding dens were situated in forests, all within 10 to 80 m of the edge,
3 immediately on the edge of forest, and 3 in wooded pastures. This situation did not differ
from the location of the non-breeding dens (Fisher exact probability test, p > 0.05),
(Table 1). Comparison of observed number of dens and expected number of dens in the
different habitats showed a clear preference for covered areas: forests and wooded pastures

(able).

Table 1. Comparison of the location of breeding and non-breeding dens

Breeding dens Fisher test

(N = 12)

Non-breeding dens
(N = 50)

Forest
Wooded pastures

(50 %) 17 (34%)
25 (50%)

(6%)

(10%)

Pastures 3
Forest edge 5

Habitat and proportion Breeding dens (N = 12) Non-breeding dens (N = 50)

(%) of study area

Binomial test Binomial test

Forests
(20.1 %)

Wooded pastures
(25.2 %)

Pastures
(31.9 %)

Fertilized Meadows
(22.8 %)

p<0.05 p<0.05
p<0.05
p<0.05

p<0.05

obs. = observed; exp. = expected.

Most of the breeding dens (57.1%) were situated in “spruce root system/earth“
substratum; the proportion of the non-breeding dens ın this category was lower (Fisher
test, p < 0.05). Other substrata were “rocks/earth”, “dumping-ground”, or “spruce root
system” (Table 3). Two breeding dens were a complex of two dens situated at a distance of
30 m and 80 m, respectively, and used simultaneously by the famıly (this explains the N =
14 ın Table 3).

Table 3. Comparison of the substratum of breeding and non-breeding dens

Breeding dens Fisher test

(N = 14)

Non-breeding dens

(N = 50)

“Spruce roots system”
“Rocks”

“Spruce root system/earth’”
“Rocks/earth”

(7.1%)
(7.1%)
(57.2 %)
N)

(38 %) p <0.05
(32 %) n.Ss.
(18 %) P2=0:05
(4 %) n.s.

“Dumping-ground”

“Rocks/dumping-ground”

“Spruce root system/rocks”

(21.5 %)
(0%)
(0%)

(4%)
(2%)
(2%)

n.S.
n.Ss.
n.S.

140 J.-S. Meia and ]J.-M. Weber

All breeding dens had 4 or more entrances (4 < N < 48), whereas 72 % of non-breeding
dens had less than 4 entrances. The number of entrances was significantly greater than in
non-breeding dens (Mann-Whitney U Test, p < 0.05). The number of entrances was
related to the type of substratum: more entrances were found when digging is possible - in
“spruce root system/earth”, “rocks/earth” — while dens in “spruce root system” and in

“rocks” had less entrances (Kruskal-Wallis One-Way ANOVA, p < 0.05).

Distribution

As already illustrated in Figure 1, the breeding dens in our area were not evenly but rather
randomly spaced. No significant difference was found by comparing the observed and the
sımulated distributions (Mann-Whitney U Test, p > 0.05).

The breeding dens were sometimes very close to houses (125 m < Dy = 900 m) or roads
(50 m < Dr <= 750 m). No significant differences were observed between the breeding dens
and the non-breeding dens (Mann-Whitney U Test, p > 0.05).

Use of breeding dens

The first sıgns of occupation of a breeding den were found on April 17th. Removal of 8 fox
families by their parents was observed between May 16 and July 12, the disturbance
sources being cattle and man. Only one family moved to an already known den (situated at
a distance of 1000 m), others were seen in the breeding den area but their new den sites
were not found.

Nine of the 12 breeding dens which were occupied in 1990, were also used in 1986, ’87,
’88, ’89, or ’91. Two dens were used for cubbing 5 times during the sıx year period. Five
dens were used 3 times, and the other two twice. The number of breeding dens over the sıx
year observation period varıed from 3 (1988) to 12 (1990) (Table 4).

Table 4. Use of breeding dens
Data from 1986-1988 according to PARATTE (1989)

1989 1990
N=11 N=12

“Combes” +++ +++
“ Assesseur” +++ +++
“Biche” +++
“Tuilerie” +++ +++
“Brandt Nord” +++
“Brandt Sud” +++
“Puce” +++
“Robert” +++
“Bousset” +++

N = total number of fox breeding dens, +++ = den used.

Discussion

Except for the number of entrances, there was no significant difference ın the characteris-
tics of breeding and non-breeding dens. The preference for covered areas was already
noticed by WEBER (1983), PAQuor and Lıso1s (1986) and IOKEMm (1985). Only NAKAZONO
and Ono (1987) observed that foxes used dens in open land rather than in densely
vegetated areas. However, there is no contradiction between these two results which

Characteristics and distribution of breeding dens of the Red fox 141

correspond to two different strategies of the fox to assure the security of the den by using
either a discrete site or a site with far visibility (Arrtoıs 1989). In fact, foxes are
opportunists concerning their dens. They do not dig their own dens when other pos-
sibilities are available (WEBER 1983). Thus, in our area, most of the dens that had been dug
were made by badgers Meles meles and we observed either an alternate use by foxes and
badgers or, in large dens, the possibility of cohabitation. The use of man-made structures
(i.e. dumping-grounds) has been reported by WEBER (1983), PAQuoT and Lisors (1986)
and BROCHIER (1989). However, a mınımum distance to human habitations (50 m)
occurred in our area; no vixen chose a site for her cubs directly close to or ın a house, as
urban foxes have been observed to practise (HAarrıs 1977). We noticed that, when a
breeding den was close to sources of human disturbance, the site was very densely covered
and the cubs emerged only at night. The high number of entrances of breeding dens seems
to be a constant characteristic (WEBER 1983; NAKAZoNO and Ono 1987) and probably
corresponds to the need for the cubs to escape quickly into shelter.

The difference between breeding dens and non-breeding dens in the type of substratum
was due to the number of entrances. When a den in the “spruce root system” substratum
(most usual non-breeding den substratum) was extended, surrounding earth could be used
and the substratum became “spruce root system/earth” (most usual breeding den sub-
stratum). We emphasize that the “earth” substratum was never found: entrances were dug
in bare earth, only when a den was made larger.

The observed density of breeding and non-breeding dens was lower than those
observed by Fuchs (1973) in the Swiss Midland (3.5-10.8 dens/km?). It certainly depends
on fox density but also on the possibility for digging. The soils in the Jura Mountains are
generally shallow. The number of breeding dens (0.33/km?) could be qualified as
“medium”: it is lower than in suburban Brussels (1/km*) (BROCHIER 1989) but medium
compared to Great Britain (0.03-1.3/km?) (Hewson 1986).

Hewson (1986) showed that breeding dens in different areas of Scotland were evenly
spaced. NAKAZONoO and Ono (1987) supposed the same situation in Japan. Our results are
different. The difficulty for foxes to find or make an adequate den for breeding could
explain the random distribution; we consider that the distribution of breeding dens was
limited by the number of suitable sites.

The number of breeding dens ıs related to the number of breeding vixens (NAKAZONO
and Ono 1987) and thus it ıs an indication of the number of foxes (Hrwson 1986).
However, the estimation of fox density is difficult because the number of foxes in an area
also depends on the socıal organization of the population: foxes usually live ın pairs or ın
groups according to area and prey availabilıty (Arroıs 1989). With foxes living ın groups,
BROCHIER (1989) counted 3 individuals per breeding den to estimate the number of adult
foxes.

In a stable population, the number of breeding dens should be stable (NAKAZoNoO and
Ono 1987). In our area the number of breeding dens varıed between years, indicating an
unstable population; this fact was confırmed by nıght-lighting counts (WEBER et al. 1991).
Changes in prey availability could explain these differences. In our area, the main prey of
foxes, the water vole Arvicola terrestris, fluctuates consıderably in numbers (WEBER and
AUBRY preliminary information). HEwson (1986) compared different habitats, and sup-
posed that some differences in the number of breeding dens were due to food avaılabiılıty.
However, the cycles of the water vole are pluriannual (4-8 years) and cannot be the only
reason for such substantial differences in the number of dens. Although Hewson (1986)
noticed no change in the number of breeding dens according to the number of foxes killed
during winter, we consider that hunting pressure has an important influence on the
number of breeding dens in the following year, e.g., a strong fox hunting during the winter
of 1987-1988 corresponded to an unusually low number of breeding dens in the following
year (PARATTE 1989). Under such unstable conditions and without having established the

142 J.-S. Meia and J.-M. Weber

social organization of the population, and its possible modification, it is very difficult to
make a reliable estimation of fox number using number of breeding dens.

Regular use of breeding dens over the years has already been reported by NAakAZoNno
and Ono (1987). Some factors could influence the use of breeding dens: number of foxes,
change of the mating individuals, disturbance at the moment of birth. This fact showed
once again the importance of the “pool” of breeding dens in an area. Human permanent
disturbances of these sites or their destruction without doubt will cause changes. A
possible effect will be the decrease in fox numbers. WEBER (1983) assumed that the number
of dens can possibly become a limiting factor in areas with unsuitable soil. But more
probably, foxes would find other sites certainly closer to houses and that would cause
problems to both humans and foxes.

Acknowledgements

The authors are very grateful to $. Augry who took an active part in the search and survey of the dens,
as well as P. Desıeve and A. PARATTE who established the first map of the dens in our study area. We
are also very thanktul to Prof. C. MERMOD for allowing us to study the red fox in his team, and to Dr.
R. Hewson for his critical and very helpful comments on the manuscript. This study was supported
by the Swiss National Foundation (grant 31-27766.89/2).

Zusammenfassung

Kennzeichen und Verteilung von Aufzuchtbauen beim Rotfuchs (Vulpes vulpes) in einem gebirgigen
Habitat

Fuchsbaue wurden seit 1986 in einem 30 km? großen Gebiet des Schweizer Jura gesucht und
überwacht. Im Jahre 1990 wurden Lage und Verteilung der Baue untersucht, um Aufzuchtbaue mit
den übrigen, anderweitig genutzten Bauen vergleichen zu können. Es wurden 62 Baue gefunden
(0,33/km?). Die Aufzuchtbaue machen 19,4% der Gesamtzahl vorhandener Baue aus (1,88/km?). Ein
Vergleich der Lage von Aufzuchtbauen mit der anderer Baue zeigt nur eine Besonderheit: die
Aufzuchtbaue hatten deutlich mehr Eingänge. Von Menschen geschaffene Strukturen und von
Dachsen gegrabene Baue wurden als Aufzuchtbaue genutzt.

Die Aufzuchtbaue waren von Straßen und Häusern nicht weiter entfernt als die übrigen Baue, und
sie waren nicht regelmäßig über das Untersuchungsgebiet verteilt. Dieselben Aufzuchtbaue wurden
über mehrere Jahre benutzt. Die Benutzung und Verteilung der Aufzuchtbaue waren begrenzt von der
Zahl günstig gelegener vorhandener Baue. Die Anzahl der Aufzuchtbaue kann grundsätzlich genutzt
werden, um die Anzahl von Füchsen in einem Gebiet abzuschätzen. Dazu muß jedoch die soziale
Organisation der betroffenen Population bekannt sein.

References

ArTOI1s, M. (1989): Le Renard roux (Vulpes vulpes Linnaeus, 1758). In: Encyclopedie des carnıvores
de France. Nort s/Erdre (F): Societe frangaise pour l’Etude et la protection des mammiferes. Vol. 3,
1-R.

BROCHIER, B. (1989): Emplacement et densite des terriers de mise-bas du renard roux (Vulpes vulpes
L.) en peripherie bruxelloise. Cahiers d’Ethologie appliquee 9, 495-508.

EIBERLE, K. (1975): Zur Anlage und Benützung der Fuchsbaue im jagdlichen Versuchsrevier der ETH
Zürich. Schweiz. Z. Forstwesen 126, 41-46.

Fuchs, F. (1973): Untersuchungen über die Baue von Rotfüchsen (Vxlpes vulpes L.) im bernischen
Hügelland. Mitt. Natforsch. Ges. Bern 30, 39-50.

Hans, $. (1977): Distribution, habitat utilization and age structure of a suburban fox (Vulpes vulpes)
population. Mamm. Rev. 7, 25-29.

Hewson, R. (1986): Distribution and density of fox breeding dens and the effects of management.
J. Appl. Ecol. 23, 531-538.

IokEm, A. (1985): Eco-Ethologie du renard roux (Vulpes vulpes L.) en Lorraine belge. 2. Choix de
l’habitat. Ann. Med. Vet. 129, 319-328.

NARAZONO, T.; Ono, Y. (1987): Den distribution and den use by the Red fox Vulpes vulpes japonica
in Kyushu. Ecol. Res. 2, 265-277.

PAQuoT, A.; Lısoıs, R. M. (1986): Etude des criteres d’implantation du terrier chez le renard roux
(Vulpes vulpes L.) au Pays de Liege. Cahiers d’Ethologie appliquee 6, 7-26.

Characteristics and distribution of breeding dens of the Red fox 143

PARATTE, A. (1989): Etude d’une population de renards dans le Jura. Travail de licence non publig,
Universite de Neuchätel.

Roman, G. (1984): The burrow construction strategy of foxes ın the Bialowieza primeval forest. Acta
Theriol. 29, 425-430. |

WEBER, D. (1983): Lage und Verteilung der Fuchsbaue in verschiedenen Landschaften des Saarlandes.
Zool. Anz. 211, 237-263.

WEBER, J.-M.; Augry, S.; LACHAT, N.; MEIA, J.-S.; MERMOD, C.; PARATTE, A. (1991): Fluctuations
and behaviour of foxes determined by nightlighting: Preliminary results. Acta Theriol. (in press.)

Authors’ address: JEAN-STEVE MEIA and Dr. JEAN-MARC WEBER, Institut de Zoologie, Chantemerle
22, CH-2000 Neuchätel 7, Switzerland

Z. Säugetierkunde 57 (1992) 144-154
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Zur Zytologie eines hochspezialisierten Sebozyten am Beispiel
der holokrinen Analbeuteldrüsen der Hauskatze,
Felis silvestris f. catus

Von M. F. FLACHSBARTH und R. SCHWARZ

Anatomisches Institut, Abt. für Histologie, Tierärztliche Hochschule Hannover, FRG

Eingang des Ms. 13. 1. 1992
Annahme des Ms. 18. 2. 1992

Abstract

The cytology of a highly specialized sebocyte, as demonstrated in the holocrine glands of anal sacs in the
domestic cat, Fels sılvestris f. catus

Studied seasonal changes ın organell equipment of holocrine glands of anal sacs in the female domestic

cat with regard to specific glandular functions in pheromone production. Similar observations from

scent marking organs ın other mammals are discussed. The cytological dynamics observed are

particularly connected with mitochondria and the endoplasmatic reticulum and could be related to

lıpogenesıis.

Einleitung

Bei vielen Säugetiergruppen besitzen speziell die von den Drüsenorganen der Analregion
produzierten Sekrete, denen Pheromoneigenschaften zugeschrieben werden (ALBONE
1984), eine große Bedeutung für soziale Interaktionen. Zu nennen sind z.B. das Fortpflan-
zungs- oder Territorialverhalten (EISENBERG und KLEIMAN 1972), aber auch die Spezies-,
Gruppen- und Individualerkennung (MykyTowycz 1972; STuBBE 1970). Dem Sekret der
Analbeutel kann neben den genannten Funktionen auch die Aufgabe als Detensivwaffe
(KruskaA 1988), wie beim Stinktier (Mephitis mephitis) und beim Iltıs (Mustela putorins),
zufallen.

Bei der Hauskatze entspricht der Aufbau der Analbeutel und ihrer Drüsen dem
typischen Strukturtypus von Markierungsorganen bei Karnıvoren als eine Kombination
spezialisierter Talg- und Schlauchdrüsen (FLACHSBARTH 1990; GORMAN und TROWBRIDGE
1989; GREER und CALHOUN 1966; KrörLLıng 1927). Beide Drüsentypen geben ıhr
Sekretionsprodukt über eigene Drüsengänge in die Analbeutelhöhle ab, wo das Mischse-
kret durch mikrobielle Tätigkeit (ALBONE und EGLINTON 1974) zum reiten Analbeutelse-
kret modifiziert wird. Dieses kann mittels Kontraktion der den Analbeutel umgebenden
Abspaltung des M. sphincter anı externus (Marrın et al. 1974) willkürlich über den
Analbeutelgang, der in der Zona cutanea anı mündet, auf die Körperoberfläche abgegeben
werden.

Die holokrinen und die apokrinen Drüsen des Analbeutels der Katze lassen ım
Jahresverlauf strukturelle Veränderungen erkennen, die dem jahreszeitlichen Reproduk-
tionszyklus dieser Tiere zugeordnet sind. Bei der weiblichen Katze ist zudem in der
Gravidität eine charakteristische Strukturänderung der Analbeuteldrüsen zu beobachten
(FLACHSBARTH et al. 1992a). In der vorliegenden Arbeit soll ausschließlich über die
Ultramorphologie der holokrinen Analbeuteldrüsenzellen weiblicher, unkastrierter, nicht
trächtiger Katzen unter besonderer Berücksichtigung ihrer Funktion als hochspezialisierte
Sebozyten berichtet werden. Die Morphologie der apokrinen Analbeuteldrüsen wird an
anderer Stelle vorgestellt (FLACHSBARTH et al. 1992b).

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5703-144 $ 02.50/0

Zur Zytologie eines hochspezialisierten Sebozyten 145

Material und Methode

Das Probenmaterial entstammt zu euthanasierenden Patienten oder Versuchstieren tierärztlicher
Einrichtungen. Es sind sieben unkastrierte, nicht trächtige weibliche Katzen aus den Monaten Januar,
Februar, April, Mai, August, Oktober und Dezember untersucht worden.

Die unmittelbar nach Eintritt des Todes exstirpierten Analbeutel wurden für die elektronenmikro-
skopische Präparation in einem Gemisch nach Karnovsky (1965) bei 4°C für mindestens 24 h fixiert,
in 1%iger Osmiumtetroxidlösung nachfixiert, über Ethanol dehydriert und in Epon 812 (Serva)
eingebettet. Die lichtmikroskopische Vororientierung erfolgte an mit Toluidin-Blau gefärbten 0,5 bis
1,0 um dicken Semidünnschnitten; die 60 bis 100 nm dicken Ultradünnschnitte wurden mit Uranyl-
azetat und Bleizitrat (VENABLE und CoGGESHALL 1965) kontrastiert und mit einem Zeiss EM 10 bei 60
kV ausgewertet.

Für den allgemeinen Nachweis von Lipiden wurden von in 4%igem neutralem Formalın mit
2,5%ıgem Kalzıumzusatz (LiLLIE und FuULLMER 1976) bei 4°C für mindestens 24 h fixierten Proben
Kryostatschnitte hergestellt. Ihre Färbung erfolgte mit gesättigter Sudan-Schwarz-B-Lösung in
70%igem Ethanol bei 4°C nach BAarRKA und AnDERsoN (1963) mit Kontrollen an azetonbehandeltem
Material. Zum Nachweis von Phospholipiden und Cholesterol wurde zusätzlich eine vorausgehende
lipidstabilisierende Bromierung durch Inkubation in 2,5%ıigem wäfßrigen Brom und Spülung mit
0,5%igem Natriumdisulfit (Bayrıss-HıcH 1981), ebenfalls mit Kontrollen an azetonbehandeltem
Material, vorgenommen.

Ergebnisse

Bei den holokrinen Analbeuteldrüsen handelt es sich um zusammengesetzte verzweigt-
azınöse Drüsen, deren Azinı periphere Rand- und zentrale Binnenzellen enthalten.
Aufgrund der morphologisch erkennbaren Sekretionsaktivität sowie von Vorgängen des
Drüsenauf- und -abbaues können die holokrinen Drüsen den Stadien der ansteigenden
Sekretion ım Frühjahr, der Hauptsekretion mit je einem Sekretionsmaximum ım Früh-
und Spätsommer und der abklingenden Sekretion im Herbst und Winter zugeordnet
werden.

Die Drüsenmorphologie im Stadium der ansteigenden Sekretion und im Übergang
zum Stadium der Hauptsekretion

Der Drüsenaufbau ım Frühjahr nimmt seinen Ausgang von den Basalzellen des Drüsen-
gangepithels, die Zellknospen (Abb. 1), als Vorläufer der Drüsenazini, ın das grundsub-
stanzreiche interstitielle Bindegewebe vorschieben. Die so entstandenen Zellen besitzen
anfangs nur ein saumartiges Zytoplasma mit zarten, gegen die Basalmembran gerichteten
Ausläufern (Abb. 2). Die zunächst stark aufgefaltete Zellmembran glättet sich mit zuneh-
mender Zellgröße und bildet gegenüber der Basalmembran Hemidesmosomen, zu den
Nachbarzellen Desmosomen aus. Massıve Filamentbündel verlaufen parallel zum Kern;
mit zunehmendem Zellwachstum verteilen sıe sıch als zarte Fädchen über das ganze
Zytoplasma. Dieses ist reich an Glykogenschollen sowie Ribosomen; sekretorisch bedeut-
same Organellen wie glattes und rauhes Endoplasmatisches Retikulum (ER) oder der
Golgiapparat sind nur spärlich ausgeprägt. Entsprechend sınd auch osmiophile Sekretgra-
nula nur selten zu finden. Ihr hoher Lipidgehalt ist durch eine intensive Schwärzung nach
Sudan-Schwarz-B-Färbung deutlich nachweisbar; mit vorausgehender Bromierung erhöht
sich ihre Anfärbbarkeit noch. Die polymorphen Mitochondrien lassen sich dem Crista-
Typ zuordnen (Abb. 2). Die Zellkerne sind euchromatinreich mit einem oft randständigen
oder doppelten Nukleolus; z. T. lassen sich Mitosefiguren beobachten.

Zur Sekretproduktion übergehende Zellen kennzeichnet eine veränderte Organellen-
ausstattung. Rauhes ER ist als lokal geringfügig dilatiertes, weit verzweigtes Netzwerk
anzutreffen. Es bildet zudem aus vielen konzentrisch gelagerten Röhren wirbelartige
Strukturen (Abb. 3) aus. Kleine Gebilde dieser Art weisen zentral zahlreiche Rıbosomen
auf, die aber auch im übrigen Zytoplasma neben Polyribosomen in großen Mengen zu

146 M. F. Flachsbarth und R. Schwarz

Abb. 1. Ausbildung von Zellknospen ım Stadium der ansteigenden Sekretion (Vergrößerung 4000fach)

finden sind. Einige Wirbelformationen sind kombiniert aus rauhem und glattem ER
aufgebaut; vorwiegend aus glattem ER bestehende Strukturen können ein vesikelartig
gekammertes Zentrum aufweisen (Abb. 3). Die Masse dieser Organelle verteilt sich jedoch
in Form von Vesikeln, die strukturell denen des wohl ausgebildeten Golgiapparates
gleichen, über das gesamte Zytoplasma. Die zahlreichen, polymorphen Mitochondrien
haben eine sehr dichte Matrix, die eine sichere Klassifizierung in Crista- oder Tubulustyp
nicht immer zuläßt (Abb. 4); das Auftreten des letzteren häuft sich jedoch bei zunehmen-
dem Gehalt der Zellen an Sekretgranula. Diese erreichen zunächst die halbe bis dreifache
Größe der Mitochondrien, zu denen sie oft eine enge Lagebeziehung zeigen. Die Mito-
chondrien schmiegen sich halbmondförmig und z.T. in diese übergehend um die Lipid-
tröpichen (Abb. 5). Einige von ihnen scheinen von einer membranähnlichen Abgrenzung
umgeben zu sein (Abb. 5): ein Eindruck, der durch das sternförmig auf sie zulaufende und
um sie einen feinkörnigen Kranz bildende rauhe ER (Abb. 4) unterstützt wird. Die
Sekretgranula können, als vermutlich eine Möglichkeit ihres Wachstums, konfluieren,
jedoch nicht unkontrolliert. Prall mit Sekretionsprodukt gefüllte Zellen schmelzen im
Sinne holokriner Sekretion ein.

Zur Zytologie eines hochspezialisierten Sebozyten 147

Abb. 3. Sekret bildende Drüsenzellen im Stadium der ansteigenden Sekretion mit spiralig angeordne-
tem ER (Vergrößerung 10 000fach)

148 M. F. Flachsbarth und R. Schwarz

Abb. 4. Sekret bildende Drüsenzelle im Stadıum der ansteigenden Sekretion mit sternförmig auf die
Sekretgranula zulaufendem rauhen ER und nicht eindeutig typisierbaren Mitochondrien (Vergröße-
rung 19 500fach)

Die Drüsenmorphologie im Stadium der Hauptsekretion und im Übergang zum
Stadium der abklingenden Sekretion

Bei Erreichen des ersten Sekretionsmaximums zeigt sich wiederum eine Modifikation der
Ultrastruktur des Drüsenepithels. Das Zytoplasma der Drüsenzellen wird auch elektro-
nenoptisch undurchdringlich dicht; nur wie ins Zytoplasma eingestreut wirkende Desmo-
somen markieren den Verlauf der Zellgrenzen. Sekretorisch bedeutsame Organellen sind
drastisch reduziert, vom rauhen ER sind nur noch einige kurze Abschnitte erkennbar. Die
Größe der Sekretgranula hat auf das zehn- bis zwanzigfache der durchschnittlichen
Mitochondriengröße zugenommen. Die sehr dichte Matrıx der zahlreichen, polymorphen
Mitochondrien erschwert ıhre Typisierung; es überwiegen jedoch Tubuli. In der Nähe von
Lipidtröpfchen scheinen die Mitochondrien zu kondensieren, sie werden kleiner und
dichter und besitzen z. T. osmiophile Einschlüsse.

Im Spätsommer zeigen die holokrinen Analbeuteldrüsen neben einem zweiten, kleine-
ren Sekretionspeak auch Anzeichen der Drüsenrückbildung, was sich in ihrer Zytologie
dokumentiert. Die Zellen weisen eine von der Azinusperipherie zum Zentrum hin deutlich
zunehmende Dichte ihres Zytoplasmas auf (Abb. 6), die solche mit dichtem, weniger
dichtem und transparentem Zytoplasma unterscheidbar macht und mit dem Differenzie-
rungsgrad der Zellen positiv korreliert ist. Die unterschiedlichen Zytoplasmadichten lassen
die Zellkonturen deutlich erkennbar werden. In den zentral gelegenen Binnenzellen
entsprechen rauhes und glattes ER sowie der Golgiapparat der im Frühjahr beschriebenen
Situation, nur ihre Ausprägung ist geringer. In den Zellen mit weniger dichtem Zyto-

Zur Zytologie eines hochspezialisierten Sebozyten 149

Abb. 5. a-Lipidtröpfchen von Doppelmembranen des ER zirkulär umgeben; b-Lipidtröpfchen stern-
förmig von rauhem ER umgeben und in unmittelbarer Nähe zu einem Mitochondrium vom

Tubulustyp (Vergrößerung 62 500fach)

plasma besitzen die wirbelartigen Strukturen z.T. keine Membransysteme (Abb. 7),
sondern zeichnen sich als konzentrische Anordnungen von Ribosomen ab, die auch im
übrigen Zytoplasma zahlreich vertreten sind. In den Azinusrandzellen finden sich nur
vereinzelt längere Schläuche des rauhen und kurze Tubuli des glatten ER sowie einige
Strukturen des Golgisystems. Die von diesen Organellen abstammenden und nur in den
zentralen Zellen noch häufiger auftretenden Vesikel sind vermehrt mit feingranulärem
Inhalt gefüllt. Die Mitochondrien weisen in den Zentralzellen sowohl Cristae als auch
Tubuli auf; Azinusrandzellen besitzen ausschließlich Mitochondrien vom Crista-Typ.
Unregelmäßig konfluierende, mit einer wenig elektronendichten Substanz gefüllte Räume,
in denen kondensierte Membrananteile liegen können, fallen häufiger in den zentralen
Zellen auf (Abb. 6). Diese besitzen auch die meisten Sekretgranula, die jedoch ım Vergleich
zum ersten Sekretionsmaximum in Anzahl und Größe deutlich abgenommen haben.

150 M. F. Flachsbarth und R. Schwarz

Abb. 6. Drüsenazinus im Stadium der abklingenden Sekretion, von peripher nach zentral zunehmende
Dichte des Zytoplasmas (Vergrößerung 5000fach)

Letztgenannte Charakteristika der Sekretgranula nehmen in den peripheren Azinuszellen
stark ab; die Randzellen zeigen nur sehr selten kleine Sekretgranula. Einige dieser Zellen
scheinen zu verdämmern: ıhr Zytoplasma wird durchscheinend, der Kern schrumpft und
bekommt eine ungleichmäßige Kontur und die Zellen verschwinden, ohne daß ein
holokriner Einschmelzungsprozeß3 oder eine Nekrose beobachtet werden könnte.

Diskussion

Die Zellen der holokrinen Analbeuteldrüse der Katze sind als hochaktive, spezialisierte
Sebozyten anzusprechen. Ihre Zytologie erfährt unter dem Einfluß des Zeitpunktes der
Probennahme und des Reproduktionsstatus des untersuchten Tieres große Änderungen,
die das unterschiedliche und aus ıhrer Funktion als Pheromonproduzenten (ALBONE 1984)
bedingte Aktivitätsniveau widerspiegeln.

Ihre konstante Ausstattung mit reichlich Rıbosomen und Polyrıbosomen gewährleistet
zu jedem Zeitpunkt die Versorgung der hochaktiven Zellen mit zellintern verbleibenden
Substanzen, z.B. Enzymen. |

Beispielhaft für die funktionell bedingten Änderungen der Morphologie sind die
Mitochondrien zu nennen. In den Basalzellen des Drüsengangepithels sowie in aus diesen
hervorgegangenen jungen Azıni sind vielgestaltige Mitochondrien vom Crista-Typ vor-
handen. Mit Einsetzen der Sekretproduktion zeigen die Mitochondrien eine verdichtete
Matrix und zunehmendes Auftreten tubulärer Innenstrukturen. Eine eindeutige Typisie-
rung ıst deshalb, ebenso wie bei den von KayanjJa und SCHLIEMANN (1981) für die

Zur Zytologie eines hochspezialisierten Sebozyten 154

ER le 3
OT ee
Bi & Ü 2.0 2

Abb. 7. Ausschnitt einer zentralen Drüsenzelle im Stadium der abklingenden Sekretion mit wirbelartig
gelagerten Ribosomen, Mitochondrien nicht eindeutig typisierbar (Vergrößerung 10 000fach)

holokrinen Analbeuteldrüsen der Großtleck-Ginsterkatze (Genetta tigrina) beschriebenen
Befunde, nicht mehr möglich. Die Mitochondrien vom Tubulus-Typ, die zur Zeit des
ersten Sekretionsmaximums am zahlreichsten vorhanden sind, mögen auf eine Beteiligung
dieser Zellen am Steroidstoffwechsel hinweisen (GHapIarıy 1988). Die Produktion von
Steroidderivaten, die als mögliche Pheromone diskutiert werden (ALBONE 1977), verläuft
demnach weitgehend parallel zum disaisonalen Fortpflanzungszyklus der Hauskatze
(STRAuss 1986).

Auch die direkt an der Sekretbereitung beteiligten Organellen wie glattes und rauhes
ER und der Golgiapparat zeigen ihre größte Ausprägung und Aktivität ım späten Frühjahr
bzw. Frühsommer. Das ER liegt, wie auch von KayanJa und SCHLIEMANN (1981) für die
holokrinen Analbeuteldrüsen der Gloßfleck-Ginsterkatze (Genetta tıgrina) beschrieben,
in wirbelartiger Anordnung vor, die von anderen Autoren (GAssE und PEUKERT-ADAM
1985; GHADIALLY 1988) in unterschiedlichen, hochaktıven Zellen als Aktivitätshypertro-
phie interpretiert wird.

Primäre Lysosomen konnten aufgrund ihrer unscheinbaren Morphologie nicht aus der
Gruppe der Vesikel-Strukturen differenziert werden. Die Notwendigkeit ıhres Vorhan-
denseins für die Zytolyse im Rahmen der holokrinen Sekretion wird jedoch von BRANDES
und BerTIn1 (1965) hervorgehoben. Peroxisomen, die in modifizierten Talgdrüsenorganen
regelmäßig gezeigt werden konnten (GoRGAs und VÖLKL 1984; GoORGAS und ZAaar 1984;
ZaAaR und GoRGas 1985), ließen sich hier ohne histochemische Untersuchungstechniken
ebenfalls nicht darstellen.

Das vornehmliche Sekretionsprodukt der holokrinen Analbeuteldrüsen stellt sich ın
Form der beschriebenen Sekretgranula dar. Mittels der Sudan-Schwarz-B-Färbung läßt

152 M. F. Flachsbarth und R. Schwarz

sich ihr hoher Lipidgehalt nachweisen; eine Intensivierung der Anfärbbarkeit nach einer
Behandlung mit Brom spricht für das Vorkommen von Cholesterolabkömmlingen (Bay-
Lıss-HıGH 1981). Die genaue Lokalisation der Lipogenese ın der Zelle ist umstritten und
steht in unmittelbarem Zusammenhang mit der Frage nach einer das fettige Zellprodukt
umgebenden Membran. KreıniG und SITTE (1986) bezeichnen Fetttröpfchen, die am ER
entstehen und sich mit einer elektronendichten Schicht amphiphiler Moleküle, einer half-
unit-membrane, umgeben, als Oleosomen. JENKINSON et al. (1985) zeigen in Hauttalgdrü-
sen das Entstehen von Fettsubstanzen am glatten ER, das Fetttröpfchen hufeisenförmig
umgeben und so eine Membran vortäuschen kann. Für NıızumA (1981) entstehen mem-
branumgebene Lipide ım Golgiapparat reitender Zellen in menschlichen Talgdrüsen.
Unter Beteiligung des glatten ER konfluieren die Tröpfchen, die ursprüngliche Membran
geht verloren. Lipogenese durch mitochondriale Enzyme und nachfolgende Umwandlung
von Mitochondrien ın Fetttröpfchen wird von JENKINsoN et al. (1979) in apokrinen
Hautdrüsen von Rindern, von GHADIALLY (1988) im Herzmuskel des Rindes und von
Aropı et al. (1989a) in der Präputialdrüse des japanischen Seraus (Capricornis crispus)
beschrieben. In den Infraorbitaldrüsen derselben Tierart wird die Lipogenese den Mito-
chondrien sowie dem glatten und rauhen ER zugeordnet (Arojı et al. 1989b). In den
holokrinen Analbeuteldrüsen der Hauskatze scheinen einige Lipidgranula frei im Zyto-
plasma zu liegen; andere, besonders in unmittelbarer Nähe von Mitochondrien oder des
rauhen ER, sind scheinbar von einer Membran umgeben. Es ist denkbar, daf Fettsubstan-
zen alternatıv von verschiedenen Organellen erstellt werden können. Die holokrinen
Analbeuteldrüsen der Katze, besonders ım Stadium der ansteigenden Sekretion, könnten
sich daher für weitere Untersuchungen zur Lipogenese anbieten.

Die Zellkerne der Drüsenzellen imponieren durch ihren Euchromatinreichtum, der ın
Verbindung mit den ausgeprägten Nucleoli für große Kernaktivität spricht. Die Lokalısa-
tion der Kernkörperchen am Kernrand ıst nach GHADIALLY (1988) ebenfalls als Aktıvitäts-
merkmal zu werten. Der hohe Euchromatingehalt unterscheidet diese holokrinen Zellen
von den Talgdrüsenzellen der allgemeinen Körperdecke, deren Kerne einen größeren
Anteil von Heterochromatin aufweisen (JENKINSON et al. 1985).

Die Hauskatze (Fels sılvestris t. catus) zeigt im Vergleich zu ıhrer Stammform, der
Falbkatze (Felis silvestris libica), eine für die Haustiere typische Steigerung der Fertilität
(Haase 1985; HERRE und RÖHRs 1990) mit einem zweiten Fortpflanzungszeitraum ım
Spätsommer (STRAuss 1986). Zu diesem parallel verläuft ein zweites Sekretionsmaximum
der holokrinen Analbeuteldrüsen, allerdings wesentlich moderater als das erste (FLACHs-
BARTH 1990). Während dıe Tubulusstruktur der Mitochondrien der zentralen Binnenzellen
auch eine forcierte Sekretionsaktivität von Cholesterolabkömmlingen vermuten läßt, so
weist der Crista-ITyp der Mitochondrien in den zum Azinusrand orientierten Binnenzellen
sowie den Randzellen auf eine verzögerte oder ausbleibende Zelldifferenzierung und
herabgesetzte Sekretionstätigkeit hin. Auch die kleiner bleibenden Wirbelstrukturen des
ER bzw. die fehlende Ausbildung von Tubulusstrukturen in ihnen sowie die herabgesetzte
Anzahl von Golgikomplexen deuten auf eine verminderte Zellaktivität hın. Insgesamt
lassen das teilweise Ausbleiben der Zelldifferenzierung bzw. das Verdämmern der Rand-
zellen eine drastische Reduzierung der Sekretionstätigkeit erkennen.

Die holokrinen Analbeuteldrüsen der Hauskatze zeigen somit Charakteristika, die in
verschiedenster Kombination als typische Eigenschaften bei Markierungsorganen von
Säugetieren gefunden werden können: Sie weisen eine deutliche Saisonalıtät auf, die sich an
den Zeiten sexueller Aktivität der Tiere orientiert (BAKER 1988; Jomnson 1973). Ihre
Sekretionsintensität wird außerdem durch Reproduktionsstatus und Geschlecht maßgeb-
lich beeinflußt (FLACHSBARTH 1990; JOHNSTON 1983; KODERA et al. 1982; STARCK und
PopuscHka 1982). Der sekretionsfördernde Einfluß von Androgenen auf Talgdrüsen ist
dabei unbestritten (Esrıng 1974; LUDERSCHMIDT 1985). Die Beteiligung weiblicher
Geschlechtshormone an der Steuerung modifizierter Sebozyten in hochspezialisierten

Zur Zytologie eines hochspezialisierten Sebozyten 153

Duftdrüsenorganen wird jedoch diskutiert (Arojı et al. 1989a; Heymann et al. 1989;
Kopera et al. 1982). Die holokrinen Analbeuteldrüsen der Katze sind nach unseren
Untersuchungen — anders als von BECKER (1991) es - nicht als ausschließlich
androgengesteuerte Drüsen anzusprechen.

Das Sekretionsprodukt der holokrinen Analbeuteldrüsen wird durch das der apokrinen
Drüsen und die abschilfernden Massen des Analbeutelepithels zum vollständigen Mischse-
kret kompletiert (ALsoneE 1984). Dabei dürfte die stark fetthaltige Komponente der
holokrinen Drüsen für eine recht lange Haftdauer des zur territorialen Markierung
genutzten Sekretes sorgen, während die leichter flüchtige Komponente aus den apokrinen
Drüsen eine Kurzzeitinformation liefert, die über die Luft schnell im Umkreis verteilt wird
(GORMAN und TROWBRIDGE 1989). Die dem Analbeutel eigene Mikroflora und -fauna mag
über ihre spezielle Zusammensetzung Individuen (Gorman et al. 1974) oder zumindest
Angehörige verschiedener Tiergruppen (Mykyrowycz 1970) voneinander unterscheidbar
machen.

Zusammenfassung

Die sich saisonal ändernde Organellenausstattung der Sebozyten holokriner Analbeuteldrüsen von
weiblichen Hauskatzen wird aufgezeigt und ım Hinblick auf die Funktion dieser Drüsen als
Pheromonproduzenten diskutiert. Dabeı wird auf parallele Erscheinungen bei diversen Markierungs-
organen von Säugetieren hingewiesen. Die der zytologischen Dynamik besonders stark unterworfe-
nen Organellen (Mitochondrien und Endoplasmatisches Retikulum) werden hinsichtlich ihrer Bedeu-
tung für die Lipogenese hinterfragt.

Literatur

ALBONE, E. S. (1977): Ecology of mammals - a new focus for chemical research. Chemistry in Britain
13, 92-100.

ALBONE, E. $. (1984): Mammalıan semiochemistry. The Investigation of Chemical Signals Between
Mammals. New York, Chichester: Wiley.

ALBONE, E. $.; EGLINTON, G. (1974): The anal sac secretion of the red fox (Vulpes vulpes); its
chemistry and microbiology. A comparison with the anal sac secretion of the lion (Panthera leo).
Life Sci. 14, 387400.

Aroyı, Y.; SUZUKI, Y.; SUGIMURA, M. (1989a): The preputial gland of the Japanese serow Capricornis
crıspus; ulerastrueture and lecuin histochemistry. Acta anat. 134, 245-252.

ATojJı, Y.; SUGIMURA, M.; Suzukı, Y. (1989b): Sebaceous glands of the infraorbital gland of the
Japanese serow Capricormas crıspus. J. submicrosc. Cytol. Pathol. 21, 375-383.

BAKER, C. M. (1988): Scent markıng behaviour ın captıve Water mongooses (Atılax paludinosus). Z.
Säugetierkunde 53, 358-364.

BARKA, T.; ANDERSON, P. J. (1963): Histochemistry. Theory, Practice and Bibliography. New York:
Harper and Row.

Bayrıss-HıcH, ©. B. (1981): The histochemical versality of Sudan Black B. Acta histochem., Suppl.
24, 247-255.

BECKER, K. (1991): Untersuchungen zur Entwicklung und Struktur des Analbeutels der Katze (Felis
catus) unter Berücksichtigung seiner Funktion und phylogenetischen Stellung als Hautduftorgan.
Diss. Freie Univ., Berlin.

BRANDES, B.; BERTINI, F. (1965): Role of lysosomes in cellular lytic process. II. Cell death during
holocrine secretion in sebaceous glands. Exp. Molecul. Pathol. 4, 245-265.

EsLing, F. J. (1974): Hormonal control and methods of measuring sebaceous gland actıvity. ].
Investig. Dermatol. 62, 161-171.

EISENBERG, J. F.; KLEıman, D. G. (1972): Olfactory communication in mammals. Ann. Rev. Ecol.
Syst. 3, 1-32.

FLACHSBARTH, M. (1990): Untersuchungen zur funktionellen Morphologie des Analbeutels und seiner
Drüsen bei der Hauskatze, Felis silvestris f. catus. Diss. Tierärztl. Hochsch., Hannover.

FLACHSBARTH, M. F.; SCHWARZ, R.; GERISCH, D. (1992a): Die Analbeutel der Hauskatze. Ein Beitrag
zur funktionellen Morphologie eines Chemokommunikationsorgans. Kleintier. Prax. (im Druck).

FLACHSBARTH, M. F.; MEYER, W.; SCHwaRZ, R. (1992b): Zur funktionellen Zytologie apokriner
Amalbeuteldrüsen der Hauskatze, Ts silloassr si er Nas einen (im Druck).

Gasse, H.; PEUKERT-ADAM, 1. (1985): Ultrastrukturuntersuchungen am bovinen Trächtigkeitsgelb-
körper im Hinblick auf eine mögliche Relaxin- und Oxytocinsekretion der Luteinzellen. Z.
mikrosk.-anat. Forsch. 99, 593-602.

GHapIALLy, F. N. (1988): Ultrastructural Pathology of the Cell and Matrix. 3. Aufl. London,
Boston: Butterworth.

154 M. F. Flachsbarth und R. Schwarz

Gorcas, K.; VöLkı, A. (1984): Peroxisomes ın sebaceous glands. VI. Aggregates of tubular
peroxisomes in the mouse Meıbomian gland. Histochem. J. 16, 1079-1098.

GoRrGas, K.; Zaar, K. (1984): Peroxisomes ın sebaceous glands. III. Morphological similarities of
peroxisomes with smooth endoplasmatie reticulum and Golgi stacks in the circumanal gland of the
dog. Anat. Embryol. 169, 9-20.

GORMAN, M. L.; NEDWELL, D. B.; SMITH, R. M. (1974): An analysıs of the contents of the anal scent
pockets of Herpestes auropunctatus (Carnıvora: Viverridae). J. Zool., London 172, 389-399.

GORMAN, M. L.; TROWBRIDGE, J. B. (1989): The role of odor in social lives in carnıvores. In:
Carnivore Behavior, Ecology, and Evolution. Ed. by J. L. GirrLeman. London: Chapman and
Hall. Pp. 57-88.

GREER, M. B.; CarHoun, M.L. (1966): Anal sacs of the cat (Felis domesticus). Am. J. vet. Res. 27,
713-783.

Haase, E. (1985): Domestikation und Biorhythmik - Implikationen für den Tierschutz. Natur und
Landschaft 60, 297-302.

HERRE, W.; RÖHRs, M. (1990): Haustiere - zoologisch gesehen. 2. Aufl. Stuttgart, New York: G.
Fischer.

HEYMAnN, E. W.; ZELLER, U.; SCHWIBBE, M. H. (1989): Muzzle rubbing ın the moustached tamarın
(Sanuinus mystax) (Primates: Callitrichidae) — behavioural and histological aspects. Z. Säugetier-
kunde 54, 265-336.

JENKINSON, D. McEwan; ELDER, H. Y.; MONTGOMERY, 1.; Moss, V. A. (1985): Comparative studies
of the ultrastructure of the sebaceous gland. Tiss. Cell 17, 683-698.

JEnkınson, D. McEwan; MONTGOMERY, 1.; ELDER, H. Y. (1979): The ultrastructure of the sweat
glands of the ox, sheep, and goat during sweating and recovery. J. anat. 129, 117-140.

JoHnson, R. P. (1973): Scent marking in mammals. Anım. Behav. 21, 521-535.

JoHnsTton, R. E. (1983): Chemical sıgnals and reproductive behavior. In: Pheromones and Reproduc-
tion in Mammals. Ed. by J. G. VANDENBERG. New York: Academic Press. Pp. 1-37.

Karnovsky, M. J. (1965): A formaldehyde-glutaraldehyde fixative of high osmolality for use in
electron microscopy. J. Cell. Biol. 27, 137a-138a.

Kayanja, F. I. B.; SCHLIEMAnN, H. (1981): Sebaceous glands of the anal sacs of Genetta tigrina
(Schreber, 1778). Z. Säugetierkunde 46, 26-35.

Kreinıc, H.; SITTE, P. (1986): Zellbiologie. Ein Lehrbuch. 2. Aufl. Stuttgart, New York: Fischer.

KODERA, $.; SUZUKI, Y.; SUGIMURA, M. (1982): Postnatal Development and Histology of the
Infraorbital Glands in the Japanese Serow, Capricornis crispus. Jpn. J. Vet. Scı. 44, 839-843.

Kröuuing, ©. (1927): Entwicklung, Bau und biologische Bedeutung der Analbeuteldrüsen bei der
Hauskatze. Z. Anat. Entw. gesch. 82, 22-69.

Kruska, D. (1988): Marderartige. In: Grzimeks Enzyklopädie — Säugetiere. München: Kindler.
Bd. 3, 388-446.

LiLLieE, R. D.; FuLLMER, H. M. (1976): Histopathologice Technic and Practical Histochemistry. New
York: McGraw-Hill.

LUDERSCHMIDT, C. (1985): Hormonelle Kontrolle der Talgdrüsenfunktion. Med. Klin. 80, 628-633.

Marrın, W. D.; FLETCHER, T. F.; BRADLEY, W. E. (1974): Perianal musculature in the cat. Anat. Rec.
180, 3-14.

Mykyrowycz, R. (1970): The role of skin glands in mammalian communication. In: Advances ın
Chemoreception. Vol. 1: Communication by Chemical Signals. Ed. by J. W. Jonnston; D. G.
Mourrton; A. TuURK. New York: Appleton-Century-Crofts. Pp. 327-360.

Mvkyrowxcz, R. (1972): The behavioural role of the mammalıan skin glands. Naturwissenschaften
59, 193-139.

Nirzuma, K. (1981): An electron microscopic study of lipid droplets in the normal human sebaceous
gland. J. Dermatol. 8, 391-400. _

STARCK, D.; PoDuscHkA, W. (1982): Über die Ventraldrüse von Solenodon paradoxus Brandt, 1833
(Mammalıa: Insectivora). Z. Säugetierkunde 47, 1-12.

Strauss, F. (1986): Der weibliche Sexualzyklus. In: Handbuch der Zoologie. Bd. 8: Mammalıa,
Teilband 55. Hrsg. von J. NIETHAMMER; H. SCHLIEMANN; D. STARCK. Berlin, New York: De
Gruyter.

an (1970): Zur Evolution der analen Markierungsorgane bei Musteliden. Biol. Zbl. 89,
213-223.

VENABLE, J. H.; CoGGEsHauL, R. (1965): A simplified lead citrate stain for use ın electron micro-
scopy. J. Cell. Biol. 25, 407-408.

ZaaR, K.; GorRGAas, K. (1985): Peroxisome — endoplasmatic reticulum aggregates in duck uropygial
gland. Europ. J. Cell. Biol. 38, 322-327.

Anschrift der Verfasser: Dr. M. F. FLACHSBARTH und Prof. Dr. R. SCHwARZ, Anatomisches Institut,
Tierärztliche Hochschule Hannover, Bischofsholer Damm 15, W-3000 Han-
nover 1, FRG

Z. Säugetierkunde 57 (1992) 155-162
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Cytogenetics and karyosystematics of phyllotine rodents
(Cricetidae, Sigmodontinae)

III. New data on the distribution and variability of karyomorphs of the genus
Eligmodontia

By A. ZaMBELLI, F. DyzZEncHAUZ, A. Ramos, N. DE Rosa, R. WAINBERG,
and ©. A. REıc

Catedra de Biologia General, Departamento de Ciencias Biolögicas, Facultad de Ciencıas Exactas,

Universidad Nacional de La Plata, Argentina, Grupo de Investigacion de Biologia Evolutiva,

Departamento de Ciencias Biologicas, Facultad de Ciencias Exactas y Naturales, Universidad de
Buenos Aires, Argentina, and Museo Nacional de Ciencias Naturales, Madrid, Espana

Receipt of Ms. 25.6. 1991
Acceptance of Ms. 6.11. 1991

Abstract

Studied bone-marrow banded and Ag-NORs karyotypes of the South American phyllotine Elhg-
modontia ın three populations of northern Patagonıa (Argentina): south of Nahuel Huapı Lake and
Los Menucos (Rio Negro Province), and Junin de los Andes (Neuquen Province). In the first localıty,
two polymorphic varıants (2n = 34 and 2n = 32) were found; in the other two localıties the 2n = 44
karyomorph previously reported as belonging to Eligmodontia typus, was dominant, but it was found
in sympatry with two polymorphic varıants (2n = 33-34) corresponding to the Nahuel Huapı
karyotype, thus confirming that these karyomorphs belong to different, probably synmorphic
species. The 2n = 34 variant was found for the first time in the Nahuel Huapi and ın Junin de los
Andes populations. G-banding and Ag-NORSs proved that 2n = 44 and the polymorphic variants 2n =
32-33-34 karyomorphs are strikingly different, thus confirming a full species status for each of them.

Introduction

The desertic long-tailed phyllotine mice of the genus Eligmodontia are wıdely distributed
in the southern cone of South America, from south of Perü to Tierra del Fuego. Several.
species have been named (according to review ın TATE 1932), but after HERSHKOVTTZ’s
revision (1962), ıt was currently considered that the genus comprises only one species with
. two subspecies: E. typus typus and E. typus puerulus (CABRERA 1961; Honackt et al.
1982). However, in a recent paper on the karyosystematics of several Argentinian
populations (ORTELLS et al. 1989), three different allopatric karyomorphs (2n = 44, 2n =
32-33 and 2n = 50) have been reported, stressing the view that Eligmodontia ıs a polytypic
genus. The 2n = 44 form was ascrıbed to the type species E. typus, and that of 2n = 50
(previously described by PEArson and PATTon 1976) to E. typus puerulus, whereas the
polymorphic 2n = 32-33 form was of no definite ıdentification, being assigned to Ehg-
modontia sp.

New and recent collecting in northern Patagonia allowed us to gain new knowledge on
the distribution of 2n = 44 and 2n = 32-33 chromosomal species, finding that the two
karyomorphs occur ın sympatry, and that they are strikingly different in the Ag-NOR and
in G-banding pattern. It also allowed us to find the so far unknown 2n = 34 variant of the
polymorphic form, and to study the meiotic behavior of the heterozygous 2n = 33 variant.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5703-155 $ 02.50/0

156 A. Zambell, F. Dyzenchauz, A. Ramos, N. de Rosa, R. Wainberg, and O. A. Reig

Material and methods

Thirty-one animals from three different localities in northern Patagonia (Argentina) have been
processed in this study. Two females were obtained by OLivEr PEARsoN (University of California,
Berkeley) in the steppe biome 13 km south of Nahuel Huapı Lake (Rio Negro Province, Fig. 1). Four
females and nine males were caught by ArLan DICKERMAN (University of Wisconsin) and ADRIAN
MonjJEau (University of Comahue, San Carlos de Bariloche), 15 km S.E. of Los Menucos (Rio Negro
Province). Ten females and sıx males were collected at Estancıa Quenquetren, 110 km southeast of
Junin de los Andes (Neuquen Province) by Anpr£s NovaroO and ANGEL CAPURRO (University of
Buenos Aires). Anımals were captured ın the field with Sherman live traps and processed in the
laboratory.

<

R\g 25 100

0 50

Fig. 1. Map showing where samples of Eligmodontia were collected and localities. 1 = Chasicö, 2 =
Puerto Madryn, 3 = 28 de Julio, 4 = Pampa Salamanca, 5 = Paso de Indios, 6 = Los Lagos, 7 = Junin de
los Andes, 8 = Los Menucos, 9 = Nahuel Huapı

Bone-marrow metaphases were obtained following a modified technique of ROTHFELS and
SIMINOVICH (1958). Testicular material was treated according to some modifications of Evans et al.
(1964). Some specimens were also previously treated with yeast following LEE and ELDER (1980). Ag-
NOR identification was performed according to HowWELL and BLack (1980). Buffered Giemsa stain at
10% was used to stain mitotic and meiotic preparations, but a 3% concentration was used in Ag-
NOBRSs staining. G- and C-banding was obtained in a few specimens following SEABRIGHT (1971) and
SuUMNER (1972), respectively. Voucher specimens were deposited in the collection of mammals at the
Municipal Museum of Natural History of Mar del Plata and the Museum of Zoology, University of
Michigan. Chromosomal lengths were expressed as a percentage of the female haploid set (FHS) and
calculated from a minımum of 10 metaphases. Chromosome size classes followed ReıG and KısLısky
(1969), calling “large” those chromosomes >9 FSH, “medium-sized” those between 9 and 5.5 FHS,
“small” those between 5.5 and 2 FHS and “minute” those <2 FHS. Chromosome nomenclature
according to centromere position followed LEvan et al. (1964). FNa values are autosomal arm
numbers.

Results

Fifteen anımals from Junin de los Andes and twelve from Los Menucos showed equally the
2n = 44, FNa = 44 karyotype. A male from Los Menucos presented a 2n = 33, FNa = 32
karyotype; a female from Junin de los Andes and a female from Nahuel Huapı showed a
2n = 32, FNa = 32 karyotype. A female from Junin de los Andes and another from Nahuel
Huapı had an identical karyotype of 2n = 34, FNa = 32.

Distribution and variabılity of karyomorphs of the genus Eligmodontia 157

The 2n = 44, FNa = 44 karyomorph
Karyotype

This karyotype agrees with that previously described as belonging to E. typus (ÖRTELLS et
al. 1989). It comprises one very large pair of metacentric (m) and twenty pairs of
acrocentric (t) autosomes gradually decreasing in size. Autosomes of pair one are very large
and almost fully metacentric (m); their total length ıs 2.5 times the length of autosomes of
pair 2, and each of their arms ıs larger than the total size of pair 2 autosomes. The
remaining autosomal pairs are distributed according to their size: those of 2 and 3 are large;
those of pairs 4, 5 and 6 are medium-sized; those of pairs 7 to 20 are small, whereas those
of pair 21 are minute. The XY sexual pair comprises the X chromosome, which ıs
metacentric (m) and has the same size as autosomes of pairs 2 and 3. The Y chromosome is
subtelocentric (st) and as small as the autosomes of pair 12.

Ag-NOßRS localization

In the 2n = 44 karyotype the Ag-NOBRs are located in two large and three medium-sized
acrocentric autosomal pairs and in the 21 pair, the smallest autosome of the complement;
this one has a low staining frequency. Although the theoretical value is twelve, in most of
the plates we found from 5 to 8 chromosomes with Ag-NOBßRs (Fig. 2a). A high frequency
of association was found between two of those elements, and occasionally, between three

otsthemillıen2e).

10U

Fıg. 2. a: Ag-NOR labeled 2n = 44 karyomorph chromosomes. b: NOR association between 2n = 44
karyomorph chromosomes. c: Ag-NOR labeled 2n = 33 and 34 karyomorph chromosomes

Complexes of 2n = 32-33-34, FNa = 32
Karyotype 2n = 32

An Elıgmodontia female from Nahuel Huapı had a 2n = 32 karyotype; it agrees with that
of the specimen previously studied as belonging to Eligmodontia sp. collected from Los
Lagos (Junin de los Andes) (ORTELLS et al. 1989). Pairs 1 to 6 comprise large acrocentric (t)
autosomes; pair 7 is made of medium-sized metacentric (m) autosomes, and pairs 8 to 15
are acrocentric (t) chromosomes, decreasing gradually in size from medium to small. The
fundamental autosomal number (FNa) is 32. The X chromosomes are of medium size and
acrocentric (t) similar to the autosomes of pair 8.

158 A. Zambellı, F. Dyzenchauz, A. Ramos, N. de Rosa, R. Wainberg, and O. A. Reig

Karyotype 2n = 33

A male from Los Menucos showed a 2n = 33 karyotype, in which the sexual and fifteen
autosomal pairs were acrocentric (t), plus an odd metacentric (m) autosome. The funda-
mental number ıs FNa = 32 (ORTELLS et al. 1989). Autosomes of pairs 1 to 6 are large,
decreasing gradually ın size; the seventh position is occupied by the odd medium-sized
metacentric (m); pairs 8 to 15 decrease gradually in sıze from medium to small. There is an
evident size gap between the first sıx pairs and the remaining set of autosomes. The X
chromosome ıs medıum-sized and acrocentric (t) similar to autosomes of pair 8; the Y
chromosome is comparable to chromosomes of pair 14. We have been unsuccessful in
obtaining good C- and G-banding in this specimen. Pairs 4 and 9 have prominent
secondary constrictions located in a medial position, but in pair 4 they are closer to the
telomeric end, whereas in pair 9 they are closer to the centromere.

Karyotype 2n = 34

A female from Estancia Quenquetren and another one from Nahuel Huapi presented a
2n = 34 karyotype ın which all 34 elements are acrocentric (t) keeping the FNa of 32.
Comparing the 2n = 32 and 33 karyomorphs with that of 2n = 34, the latter does not
present a medium-sized metacentric (m) autosome, but instead one additional small
acrocentric autosomic pair (Fig. 3).

14 15 16

Fig. 3. Bone marrow standard Giemsa staining karyotype of Eligmodontia sp. from Estancıa
Quenquetren (Junin de los Andes), Neuquen Province, Argentina. 2n = 34; FNa = 32

Ag-NOßRs localızation

In the complexes of 2n = 33 and 34, Ag-NOßRs staining was identical. The rRNA cistrons
of pairs 4 and 9 are in the same morphological position as the secondary constriction. One
of the pairs from the group 12 to 15 (where all the autosomes have sımilar size) carrıes
NORSs, which are located in a distal pericentromeric position (Fig. 2b). Pair 9 shows the
highest frequency and intensity of staining and the two homologues are usually dyed. Pair
4, which presents a lower intensity of silver staining, is usually stained in the two
homologues. Silver was fixed only in a few times on the smallest pair and only one

homologous showed Ag-NOR.

Distribution and variability of karyomorphs of the genus Eligmodontia 159

Meiosis

Meiosis was studied in the 2n = 33 male. In diplotene, diakinesis and metaphase I, fourteen
autosomic bivalents and the XY pair with the classic end-to-end association were observed.
Moreover, a characteristic autosomic trivalent was found. It was constituted by two
acrocentric elements and the metacentric, which corresponds to the odd biarmed chromo-
some found in somatic cells (Fig. 4). Sıx bivalents corresponding to the first six pairs of
somatic autosomes are noticeable due to their larger sıze. The largest pairs form two or
three chıasmata. Two chiasmata are regularly shown in three large bivalents, and one or
two chıasmata occur in two large bivalents. The remaining bivalents show only a bridge.

Fıg. 4. Diakinesis of the male Eligmodontia sp. from Los Menucos, Rıo Negro Province, Argentina.
2n = 33; FNa = 32. The arrow points to the trivalent

G- and C-banding

G- and C-bands were obtained in the 2n = 32 and 2n = 34 metaphases from Nahuel Huapı
and compared with the 2n = 44 bands previously obtained (ORTELLS et al. 1989). The two
karyomorphs of Nahuel Huapı fully match ın arm-to-arm G-bands comparisons, allowing
to confirm that metacentric pair 7 of the 2n = 32 karyotype was the result of a Robertso-
nıan fusion of acrocentrics of the 2n = 34 karyotype (Fig. 5a, b).

C-banding of the 2n = 32 karyotype showed pericentromeric positive staining in
autosomal pairs 1, 5 to 8 and 11 to 15, as well as in the sex chromosomes. C-banding of
2n = 34 specimen fully matches the pattern found in the 2n = 32 karyotype.

When comparing the 2n = 34 G-bands with those of the 2n = 44 karyotype, few arm-to-
arm correspondence was found (Fig. 5c). The metacentric autosomes of the fırst pair of the
2n =44 karyotype match the banding pattern of autosomes 2 and 3 ofthe 2n = 34 karyotype.
We found an apparent lack of two bands, one pericentromeric and another telomeric in the
long arm of the 2n = 44 metacentric, and another band which is present ın the short arm but
absent ın autosomal pair 3 of the 2n = 34 karyotype. Complete homology was also found in
four other autosomal pairs between the two karyotypes (Fig. 5c).

Moreover, regarding the remaining chromosomes, the 2n = 34 karyotype showed 10
autosomes and the X which are not found in the 2n = 44 karyotype, and the latter shows 16
non-shared autosomal pairs.

160 A. Zambellı, F. Dyzenchauz, A. Ramos, N. de Rosa, R. Wainberg, and O. A. Reig

9

”.,

nn I

N
w

>

e})

SS

nn’

u
w

“-

“oe ‘s a;
10 11 12 13 14 15 x

104

zz 8

99 13 10 14 14

Fig. 5. G-banded karyotypes of Eligmodontia sp. from south of Nahuel Huapı Lake, Rio Negro
Province, Argentina. a: 2n = 32; FNa = 32. b: 2n = 34; FNa = 32. c: G-banding pattern comparison
between Ehgmodontia typus (left) and Ehgmodontia sp. (right). The numbers correspond to their
position in each species’ karyotype

Distribution and varıabılıty of karyomorphs of the genus Eligmodontia 161
Discussion

The 2n = 44 karyotype found in Los Menucos and Junin de los Andes was identical to the
one previously reported from Chasic6ö (Buenos Aires Province) (HURTADO and WAINBERG
1977) and from the same localıty and central Chubut Province and referred to as E. typus
(ORTELLS et al. 1989). This allows us to extend the distribution of this species 750 km to
the west and 800 km to the north of previous chromosomally based records. The 2n = 43
varıant found in Chasıcö was not found in our new material.

The previously reported 2n = 32-33 karyomorphs from Los Lagos, south of Neuquen
Province (ÖRTELLS et al. 1989) were found to occur in three new localities: in northern Rıo
Negro (Nahuel Huapi), south-west of Neuqu£en (Junin de los Andes) and north-central
Rio Negro (Los Menucos), thus confirming the widespread occurrence of this form in
northwestern Patagonıa. The new samples also allowed to find a 2n = 34 varıant of the
same polymorphic system which was previously unknown. The study of meiosis of the
2n= 33 heterokaryotype and G-banding comparisons between 2n= 32 and 2n= 34
varıants confirmed that all these chromosomal forms belong to one polymorphic system
involving a Robertsonian fusion.

The present study also showed a frequent association between two NOR-bearing
chromosomes, and an occasıonal one among three Ag-NOR-marked chromosomes in the
2n = 44 karyotype. This could be related with a tendency toward centric fusions.
However, it ıs evident that ıt accounts for a part of the chromosomal differences between
these two karyomorphs.

The placement of the Ag-NOBRs in different autosomal pairs and the scarce arm-to-arm
homology found between the 2n = 43-44 and the 2n = 32-33-34 karyotypes confirm that a
large amount of chromosomal repatterning was involved in the evolution of these two
forms, bolstering the previous claim that they belong to two different, albeit probably
synmorphic species (ORTELLS et al. 1989). This conclusion ıs further confirmed by the
finding of sympatry of the two karyomorphs in Los Menucos and Junin de los Andes.

Thus, there is sufficient evidence to confirm that two species of Eligmodontia inhabit
northern Patagonıia. The name to apply to the 2n = 32-33-34 form is still obscure, and this
problem must be solved by a thorough taxonomic revision of the entire genus.

Acknowledgements

We thank TERESA GENTILE DE FRONZA for her scientific and technical collaboration and ANDREA
Corussı for help during the laboratory work. JouHn A. W. KırscH, ALLAN DICKERMANN, OLIVER
PEARSON, ADRIAN MONJEAU, ANDRES NOVARO and JORGE CAPURRO are acknowledged for providing
the specimens included in this study.

This paper was partially financed by CONICET grant PID No. 3079700/85 and BID-CONICET
program 515/OC-AR given to R.L. WAINBERG, and by CONICET grant PID No. 3085300/85 given
to O.A. Reıc.

Zusammenfassung

Cytogenetik und Karyosystematik von phyllotinen Rodentia (Cricetidae, Sigmodontinae). III. Nene
Daten über Verbreitung und Variabilität von Karyotype der Gattung Eligmodontia

Karyotypen der südamerikanischen Rodentia-Gattung Ehigmodontia von 3 Populationen aus Nordpa-
tagonien wurden untersucht. Tiere einer Population entstammten der Region südlich des Sees Nahuel
Huapi, die einer anderen waren von Los Menucos (Provinz Rio Negro) und die der dritten von Junin
de los Andes (Provinz Neuquen). In der ersten Population wurden zwei polymorphe Varianten (2n =
34 und 2n = 32) gefunden. In den beiden anderen war der bislang Eligmodontia typus zugeordnete
Karyotyp (2n = 44) dominant. Sympatrisch zusätzlich gefunden wurden jedoch auch zwei polymor-
phe Varianten (2n = 33; 2n = 34), die dem Typus der Nahuel Huapi-Population glichen. Die Variante
2n = 34 wurde erstmalig für die Nahuel Huapi Region und die Population von Junin de los Andes
belegt. G-Bandenmuster und vergleichende Untersuchungen am Nucleolus-Organisator nach Dar-

162 A. Zambelli, F. Dyzenchauz, A. Ramos, N. de Rosa, R. Wainberg, and O. A. Reig

stellung mit Silbernitrat bestätigen, daß die Karyotypen 2n = 44 und die polymorphen Varianten 2n =
32-33-34 auffallend verschieden voneinander sind. Beiden muß sehr wahrscheinlich ein eigener
Species-Status zuerkannt werden.

References

CABRERA, A. (1961): Catälogo de los mamiferos de America del Sur. Rev. Mus. Argent. Cienc. Nat.
B. Rivadavia 4, 451.

Evans, E.; BRECKTON, G.; FORD, C. (1964): An air-drying method for meiotic preparation from
mammalıan testes. Cytogenetics 3, 289-294.

GARDNER, A.; PATTON, J. (1976): Karyotypic varıatıion in oryzomyne rodents (Cricetinae) with
comments on chromosomal evolution in the Neotropical cricetine complex. Occas. Papers
Museum Zool. 49, 1-48.

HERSHKOVITZ, P. (1962): Evolution of Neotropical cricetine rodents (Muridae), with special reference
to the phyllotine group. Fieldiana Zoology 46, 1-524.

Honackı, J. H.; Kınman, K. E.; KoeppL, J. W. (1982): Mammal species of the World. Lawrence,
Kansas: Allen Press.

Howeıı, W. M.; Brack, D. (1980): Controlled silver staining of nucleolus organizer regions with
protective colloidal developer: a one step method. Experimentia 36, 1014-1015.

HURTADO DE CATALFO, G.; WAINBERG, R. (1977): Cytogenetics of rodents of genus Ehgmodontia
(Cricetidae). In: Joint Seminar and Workshop: Aspects of Chromosome Organization and
Function. III Latin American Congress of Genetics. Ed. by M. DrETZ, N. BRUM-ZORRILLA and
G. Forte. Montevideo.

LEE, M.; ELDER, F. (1980): Yeast stimulation of bone marrow mitosis for cytogenetic investigations.
Cytogenet. Cell Genet. 26, 36-40.

LEvan, A.; FREDGA, K.; SANDBERG, A. (1964): Nomenclature for centromeric position on
chromosomes. Hereditas 52, 201-220.

ORTELLS, M.; REIG, O.; WAINBERG, R.; HURTADO, G.; GENTILE DE FRONZA, T. (1989): Cytogenetics
and karyosystematics of phyllotine rodents (Cricetidae, Sigmodontinae). II. Chromosome mul-
tiformity and autosomal polymorphism in Ehgmodontia. Z. Säugetierkunde 54, 129-140.

PEARsoN, O.; PATTON, J. (1976): Relationships among South American phyllotine rodents based on
chromosome analysıs. J. Mammalogy 57, 339-350.

Reıc, O.; Kısrısky, P. (1969): Chromosome multiformity in the genus Ctenomys (Rodentia,
Octodontinae). Chromosoma 28, 211-244.

ROTHFELS, K.; SIMINOVICH, L. (1958): An air-drying technique for flattening chromosomes in
mammalıan cells grown in vitro. Stain Technol. 33, 73-77.

SEABRIGHT, M. (1971): A rapıd banding technique for human chromosomes. Lancet 2, 971-972.

SUMNER, A. (1972): A simple technique for demonstrating centromeric heterochromatin. Exp. Cell
Res. 75, 304-306.

Tate, G. H. H. (1932): The taxonomic history of the South American cricetid genera Euneomys
(subgenera Euneomys) and Galenomys, Auliscomys, Chelemyscus, Chinchillula, Phyllotis, Para-
lomys, Graomys, Elıgmodontia and Hesperomys. Amer. Mus. Novitates 541, 1-21.

Authors’ addresses: ANDRES ZAMBELLI, ANIBAL RAMOS, NOEM{ DE Rosa and RICARDO WAINBERG,
Cätedra de Biologia General, Departamento de Ciencias Biolögicas, Facultad de
Ciencias Exactas (47 y 115), Universidad Nacional de La Plata, RA-1900 La
Plata, Argentina; FERNANDO DYZEncHAUZ and OsvAaLDo Reıc, GIBE, Depar-
tamento de Ciencias Biolögicas, Facultad de Ciencias Exactas y Naturales,
Universidad de Buenos Aires, Pabellön 2, Ciudad Universitaria Nunez, RA-1428
Buenos Aıres, Argentina

Z. Säugetierkunde 57 (1992) 163-168
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Burrow structure in the subterranean rodent Ctenomys talarum
By C. D. AntinucHI and CRISTINA BUSCH

Departamento de Biologia, FCEyN, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina

Receipt of Ms. 4.6. 1991
Acceptance of Ms. 30.10. 1991

Abstract

Analysed the structure of completely excavated burrow systems of Tuco-tuco (Ctenomys talarum).
Burrow systems of males and females show the same basıc design. The main tunnel occupies 48 % of a
burrow ın total length and is formed by basıc units (interfork distances) of 0.9 # 0.4 m. Subterranean
plant biomass was correlated with burrow length and with the number of branches. Soil granulometry
affected the diameter and depth of tunnels and soil humidity was correlated with the main tunnel
length.

Introduction

South-American caviomorph rodents of the genus Ctenomys, called Tuco-tucos are the
most numerous ın species number ot all fossorıal rodents (Reıc et al. 1990). Tuco-tucos
spend most of their lives within plugged burrows, evident by the mounds that result from
pushing loosened soil out of the tunnels.

Burrow structure is of main importance in terms of energy costs or burrowing. As a
consequence, foraging efficiency and escape from predators are the ultimate factors
shaping burrowing behavior (AnDERSENn 1988). Thus, burrows of different mammalian
taxa have evolved into broadly convergent structures.

Studies on burrow architecture of North American geomyd rodents suggest that
subterranean rodents maximize the energy expended per meter of burrow (VLEck 1981)
and that architecture of burrow systems is not adaptive to resource availability (CAMERON
et al. 1988). REICHMman et al. (1982) reported that total length of the burrow and the
average number of branches are ınversely related to plant productivity. Furthermore, these
authors suggest that any spacing rule involves basic building units of the burrow system.
This unit can be combined ın such a way as to increase overall burrow length in response to
resource availabiılity.

The literature contains little information concerning the structure of Tuco-tuco burrow
systems, although numerous studies have centered on those of the northern pocket-
gopher. For a review on subterranean burrow structures, see HıckMAn (1990).

The present report offers information based on field observations on the structure of
completely excavated burrow systems of the Tuco-tuco, Ctenomys talarum, and relates the
major features of the burrow with characteristics of the surrounding habiıtat.

Material and methods

This study was conducted from January to December 1989 at the sandy dune belt from Mar del Cobo
(Pdo. Mar Chiquita, Prov. Buenos Aires). Plastic live traps were set at fresh surface mounds. Weight
and sex of the Tuco-tuco trapped were recorded. Burrow systems were excavated with a shovel.
Tunnels, chambers and mounds were mapped on graph paper. The length of all tunnels in the entire
burrow system of each individual Tuco-tuco was measured from the maps and the total above area
covered by each individual was also measured from the maps using the minimum convex polygon

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5703-163 $ 02.50/0

164 C©. D. Antinuchi and Cristina Busch

method. The degree of convolution of each burrow system was quantified by dividing the total length
of tunnels in the burrow system by its total above-ground area (CAMERON et al. 1988).

We arbitrarily designated the longest continuous segment of a burrow as the main tunnel. Any
tunnel comming off this segment was considered a branch. Tunnels ending at the surface were named
feeding tunnels. Branch angle was measured as the smallest angle between two intersecting segments.

Plant biomass and soıl characteristics were measured from samples taken near burrows. Vegetation
was collected from a circle around the burrow in five 0.24 m? and 30 cm depth samples. Biomass was
estimated by separation on aerıial and subterranean portions of vegetation that were dried at 80°C for
24 h. Soil samples were collected at the depth of burrow tunnels. Moisture was determined by
differential readings before and after drying soil samples at 80°C to constant weight. Silt-loam
fractions were separated using a sieve set. R

Numerical results are given as mean + S.D. Student’s tand X tests were used to test for significant
differences between mean values and proportions, respectively. Discriminant analysis was performed
between male and female burrows. Correlations among burrow variables as well as between these
variables and soıl and vegetation varıables were established.

Results

Major features of a male and a female excavated burrow system are shown ın Figure 1. Data
for 12 female- and 10 male-excavated burrow systems are presented ın Table 1.

Table 1. Body mass and burrow system characteristics of Ctenomys talarum from Mar del Cobo,
Buenos Aires, Argentina

Values are given as x + SD. Numbers in parentheses are sample sizes

Characteristic Male (n=10) Female (n=12) Total (n=22)

Body mass (g) 13325715 104 + 13 1177 == 20
Burrow length (m) 77
Burrow area (m?) NOE=R8

Degree of convolution 2087
Main tunnel length (m) 8 +4
Branch length (m) 9+4
Number of branches 8+6
Interfork distance (m) 1+ 0.4

Table 2. Soil humidity and granulometry in mass percent at the excavated burrow location

Data are given as x # SD

Soil characteristic Male (n=10) Female (n=12) Total (n=22)

Humidity Seet| = Harz
Silt
(>2 mm) 0203 7=0. 0.5+0.38
Very coarse sand
(<2 mm >1 mm)
Coarse sand
(<1 mm >0.5 mm)
Medium sand
(<0.5 mm >0.25 mm)
Fine sand
(<0.25 mm > 0.125 mm)
Very fine sand
(<0.125 mm > 0.058 mm)
Loam-clay
(<0.058 mm)

Burrow structure in the subterranean rodent Ctenomys talarum 165

Fig. 1. Left: Burrow design of
a mature female Ctenomys
talarum; right: Burrow design
of a mature male Ctenomys
talarım. B = branch, BU =
basic unit, C = chamber, FT =
feeding tunnel, MT = maın
tunnel

The burrow system of Ctenomys talarum has a branching structure, consisting primar-
ily of a main axial tunnel that occupies 48 % of the total length and a varıable number of
lateral branches and feeding tunnels. All tunnels to the surface are plugged and systems
never interconnected.

Male and female burrow systems have the same basic design (0.10 > P>0.05). The
main tunnel is formed by basic unit buildings (interfork distances) of 0.9 # 0.4 m. About
48% of the branching angles were >40° and clustered around 75° and 90° (Fig. 2). The
construction of left- and right-directed segments is statistically different (P < 0.05).

Average body weight was significantly different between sexes (P <0.001). Male
burrows occupied greater above-ground areas than female burrows (0.1 < P <0.05). We

166 ©. D. Antinuchi and Cristina Busch

0 10 20 30 40 50 60 70 80 9
ANGLE (degrees)

Fıg. 2. Frequency distribution of burrow branch angles

FREQUENCY (%)

did not detect a significant difference in the total length of tunnels, degree of convolution
or diameter between burrow systems of male and female Tuco-tuco (P >0.1).

A single nest chamber, packed with dry grasses, was found at the main tunnel ın
females, and ın a blind lateral branch (0.5 + 0.4 m) ın males. Chamber mean diameter was
21 # 7cm and was built in deeper tunnels (P < 0.02) in males (45.62 + 6.07 cm) than in
females (35.5 # 8.32 cm).

Table 3. Plant biomass in g at excavated burrow location
Data are given as x + SD

Biomass Male (n=10) Female (n=12) Total (n=22)

Subterranean BISEEN6S 249 + 148 27.821009
Aerıal 2D=EAIIS 30) El RL Ze 202
Total 527.189 647 + 255 SIDEEDBH

Soil characteristics and plant biomass at the excavated burrow location are shown ın
Tables 2 and 3, respectively. Statistically significant correlations exist between a number of
burrow parameters and between burrow parameters and habitat characteristics:

Burrow total length is correlated with: number of branches, number of feeding tunnels,
anımal weight and subterranean plant biomass (P < 0.05, n = 22).

Main tunnel length is correlated with: number of feeding tunnels, soil humidity and
subterranean plant bıiomass (P < 0.05, n = 22).

Main tunnel depth is correlated with: number of branches, coarse grain sand, medıum
grain sand and subterranean plant biomass (P < 0.05, n = 22).

Tunnel diameter is correlated with: coarse grain sand and medium grain sand (P < 0.05,
n= 22).

The number of branches of the system is correlated with the subterranean plant biomass
(P <0.05, n = 22),

Features of Ctenomys talarum compared to those of other subterranean rodents are
reported ın Table 4.

Burrow structure in the subterranean rodent Ctenomys talarum 167

Table 4. Burrow system characteristics of Ctenomys talarum, Cryptomys hottentotus and
Pappogeomys castanops

Species Ctenomys talarum Cryptomys hottentotus Pappogeomys castanops
Characteristic

Surface (m?) 14.4 + 6.7 74.0 449.7
mounds

Total do E76 LSROZEITEO 79.8)=2,27.0
Length (m)

Tunnel 3722] 22,22 22 0,8 19.8 37:0

Depth (cm) 39.9 + 9.2 49.5 + 17.1 81.8 + 32.8

Tunnel mean Salr=1089 4.523.0:6 110,2 Se 1155)
diameter (cm)

Nest chamber 39.9 + 9.3 Sale==2829 u, SB
deep (cm)

Occupants (n) 0-=0:0 2.2=210:5 2,0) 22 11.0
Reference this study Hıckman (1978) Hıckman (1977)

Discussion

As reported for other species of Ctenomys (HıckmAan 1990; Reıc et al. 1990) our study
shows that burrows of Tuco-tuco are convergent in their main features to those of other
unrelated subterranean rodents. ANDERSEN (1988) found that burrow systems of Geomys
are linked segments of tunnels, and REICHMAaN et al. (1982) suggested that burrow length
of Thomomys are attained by incorporating burrow segments (one interfork distance and
its associated branch). Furthermore, VLEcCK (1981), examining the energetics of foraging of
geomyds, estimated a mınımum-cost segment length between 0.6 and 2.4 m. The mean
segment length (interfork distance) for Tuco-tuco lies within this interval and was 0.91 +
0.31 m. Optimal foraging theory predicts the tendency for burrow branches to be
orthogonal to the originating tunnel (ANDERSEN 1988). We found that Tuco-tuco branch
angles were variable, and greater than 60° (Fig. 2).

Moreover, in concurrence with studies ın the famıly Geomyidae (Hıckman 1990),
gender did not affect architecture of burrow systems of Ctenomys. Although there are only
statistically significant differences between male and female burrow areas, there is a
tendency for males to occupy more elongated, branched burrow systems.

Position of the nest was reported to be adaptıve, multiple entrances increased air
circulation and less traffic congestion near the nest when occupied by young, while a
central position allows equal foraging and territorial defense (HrckmAn 1990). Tuco-tuco
males placed their nests on a central blind branch, while females have them in the main
tunnel. Nest position was more central in heavier females, probably reflecting the
burrowing pattern.

Soil type may influence burrow architecture as a mechanism to compensate for
differences in the cost of excavating and rate of diffusion of gases. In our study, soil
granulometry affected the diameter and depth of the tunnels. Similarly, soil humidity was
correlated with main tunnel length of burrow.

REICHMAN et al. (1982) suggested that elongated, branched burrow systems may be
required for resource acquisition in less productive areas. Although we did not find a
correlation of burrow parameters to total above-ground biomass, both the length of the
burrow and the number of branches were negatively correlated with subterranean biomass.

168 C. D. Antinuchi and Cristina Busch

Field research throughout the year ıs needed to assess seasonal and reproductive
influence on burrow parameters, as well as laboratory studies to estimate the cost of
construction.

Acknowledgement

Financial support was provided by the CONICET; grant-Pid No. 3-104900/88.

Zusammenfassung

Die Struktur der Baue von Ctenomys talarum, einer unterirdisch lebenden Nagerart

Untersucht wurden 22 vollständig ausgegrabene Baue von Tuko Tukos (Ctenomys talarum). Die
Gangsysteme der Männchen sind ım Durchschintt größer und haben die Nestkammer am Ende eines
Seitentunnels, wogegen die Weibchen ıhr Nest im Hauptgang anlegen. Sonst sind die Baue bei
Männchen und Weibchen ähnlich. Sie bestehen aus einem Hauptgang von durchschnittlich 48% des
Gesamtsystems, von dem ım Abstand von im Mittel 0,9 + 0,4 m Seitengänge abzweigen. Die
unterirdische Pflanzenmasse pro Volumeneinheit war mit der Baulänge und der Anzahl von Abzwei-
gungen negatıv korreliert. Die Korngröße des Bodens beeinflußte den Durchmesser und die Tiefe der
Gänge, und die Bodenfeuchtigkeit war mit der mittleren Tunnellänge korreliert.

Literature

ANDERSEN, D. C. (1988): Tunnel-construction methods and foraging path of a fossorial herbivore,
Geomys bursarius. J. Mammalogy 69, 565-582.

CAMERON, G. N.; SPENCER, $. R.; ESHELMAN, B. D.; WıLLıams, L. R.; GrREGoRY, M. ]J. (1988):
Activity and burrow structure of Attwater’s pocket gopher (Geomys attwateri). ]. Mammalogy 69,
667-677.

Hıckman, G. C. (1977): Burrow system structure of Pappogeomys castanops (Geomydae) in Lubbock
County, Texas. Am. Midland. Nat. Pp. 50-58.

— (1978): Burrow system structure of the Bathyergid Cryptomys hottentotus ın Natal, South Africa.
Z. Säugetierkunde 44, 153-162.

— (1990): Adaptive of tunnel system features in subterranean mammal burrows. In: Evolution of
subterranean mammals at the organısmal and molecular levels. Ed. by E. Nevo and O.A. Reıc.
New York: Alan R. Liss. Pp. 185-210.

REICHMAN, O. J.; WHITHAM, T. G.; RUFFNER, G. A. (1982): Adaptive geometry of burrow spacing in
two pocket gopher populations. Ecology 63, 687-695.

Reıc, OÖ. A.; Busch, C.; ORTELLS, M. O.; CoNTRERAS, J. R. (1990): An overview of evolution,
systematics, population biology, cytogenetics, molecular biology and speciation in Ctenomys. In:
Evolution of Subterranean Mammals at the Organısmal and Molecular Levels. Ed. by E. Nevo
and O.A. Reıc. New York: Alan R. Liss. Pp. 71-96.

VLEcK, D. (1981): Burrow structure and foraging cost in the fossorial rodent Thomomys bottae.
Oecologia, Berlin, 49, 391-396.

Authors’ address: Lic. CARLOS DANIEL ANTINUCHI and Dra. Cristina BuscH, Departamento de
Biologia, Universidad Nacional de Mar del Plata, C.C.1245, Mar del Plata (7600),

Argentina

Z. Säugetierkunde 57 (1992) 169-175
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Distribution patterns of small mammal fauna along gradients of
latitude and altitude in Northern Spain

By EuLALIA MoRENoO and A. BARBOSA

Museo Nacional de Ciencias Naturales, Departamento de Ecologia Evolutiva, Madrid, Spain

Receipt of Ms. 19. 8. 1991
Acceptance of Ms. 5. 12. 1991

Investigated the influence of geographical factors (latitude and altitude) on the distribution of small
mammal fauna. We analysed approximately 3000 Barn Owl pellets collected from 20 different
localities in Northern Spain. These pellets contained the remains of 9744 small mammals belonging to
17 species. Three groups of species were found: 1. one group associated with latitude (Sorex coronatus,
Neomys fodiens, Clethrionomys glareolus, Microtus pyrenaicus, Apodemus sylvaticus, Mus spretus), 2.
another group related to altitude (Suncus etruscus, Crocidura russula, Microtus agrestis), and 3. a third
group whose distribution was not affected by latitude or altitude (Sorex minutus, Eliomys quercinns,
Microtus cabrerae, M. nivalıs, M. duodecimcostatus, Arvicola sapidus, Rattus rattus, R. norvegicus).

The distribution of these species is discussed ın relation to geographical and climatic factors. Our
data demonstrate that latitude is the most important factor in determining the presence of a species at
the southern limit of their range.

Introduction

Distribution and diversity of small mammals are affected by geographical factors of which
latitude and altitude are the main varıables used in zoogeographical studies (PIANKA 1966;
Bono et al. 1980; Fons et al. 1980; BRUNET-LECOMTE and DeLiBes 1984; DELIBES 1985;
ALCANTARA 1989; BRÜNNER and NEET 1991).

In Western Europe the number of small mammalıan species decreases from north to
south (HERRERA 1974). It has also been demonstrated that when altıtude increases the
diversity of small mammals decreases (Age 1982; DeLıBEs 1985; ALCANTARA 1989).
Variation in altitude may reproduce varıatıon in latitude, so that ın this study both
gradients are investigated. The aim of the present study was to determine, within amedıum
altitudinal range, the influence of these two geographical varıables on the distribution of
small mammals, and at the southern limit the presence of certain species (CORBET 1978).

Material and methods

The study was conducted ın the province of Huesca (42°45’-42°05’ N, 00°45’-00°17’ W). Although
the latitudinal range is restricted, the orography varıes markedly. Altitude ranges from 420 and 987 m
above sea level with three distincet geographical regions (see Figure): Ebro Valley (Mediterranean
lowlands), pre-Pyrenees (Atlantic lower montane area), and Pyrenees (alpine high mountain area).

The sampling method was the analysis of Barn Owl pellets. In spite of the limitations of this
sampling procedure (SAINT-GIRONS and SpıTz 1966), ıt is valid for biogeographical studies of small
mammals (HEIM DE Barsac and BEAUFORT 1966; HERRERA 1974; BRUNET-LECOMTE and DELIBES
1984). We analysed about 3000 Barn Owl pellets collected from 20 different localities (Fig. and Tab. 1)
which contained 9744 small mammals. The data gathered are most likely heterogeneous since pellets
were collected at different times of the year and pooled together, and although the Barn Owl’s diet
shows monthly changes (SAINT-GIRONS 1968; MarTI 1973; WEBSTER 1973; HERRERA 1973), the effect
of seasonal changes on the results should be buffered since, of the 20 analyses studied, 12 exceeded 300
prey items (see HERRERA 1974 for a similar approach).

Temperature and precipitation data were taken from ELfas and Rufz (1977) for the points nearest
to samplıing sites.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5703-169 $ 02.50/0

170 Eulalıa Moreno and A. Barbosa

X x
X a S
So x Ü, 0, YARR Ar
Ar
} I
BE
70,09
De] SS Ss
IN 5 RSS
o''%e F
oe 19
18 17”o
20

Situation of the localities from which Barn Owl pellets were taken. Numbers correspond to the
localities as numbered in Table 1

Simple correlation analysis was performed to test for an effect of latitude, altitude, temperature,
and precipitation on the geographical distribution of small mammals in the study area. Stepwise
multiple regression analyses (SOoKAL and ROHLF 1981), with the relative abundance of the different
taxa as dependent variables, were performed to show which geographical variable (latitude, altırude)
primarily affected the distribution of small mammals. Small mammal diversity was calculated using the
Shannon-Weaver Index and richness was taken as the number of species in each locality.

Results

In the study area latırude and altitude are highly correlated (r = 0.767, p < 0.001) however,
they do not show the same relation to small mammal distribution, with latitude being more
highly correlated for most species.

The raw data are shown in Table 1 where the richness index for each localıty is also
included. Five insectivorous and 12 rodent species were found. Stepwise multiple regres-
sıon analyses distinguished three groups of species (Table 2):

1. Species whose distribution ıs primarily related to latitude (Sorex coronatus, Neomys
fodiens, Clethrionomys glareolus, Microtus (Pitymys) pyrenaicus, Apodemus sylvaticus,
and Mus spretus).

2. Species whose distribution is primarily related to altıtude (Suncus etruscus, Crocidura
russula, and Microtus agrestis).

3. Species whose distribution ıs not related to either altıtude or latiıtude (Sorex minutus,
Eliomys quercinus, Microtus cabrerae, M. nivalıs, Microtus (Pitymys) duodecimcostatus,
Arvicola sapidus, Rattus rattus, and R. norvegicus).

When species were grouped in Orders, latitude was the first variable selected by the

stepwise regression analysis (Table 2), being positively correlated with the abundance of

Insectivora and inversely correlated with the abundance of Rodentıa.

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Distribution patterns of small mammal fauna along gradients of latitude and altitude

72 Eulalıa Moreno and A. Barbosa

Table 2. Stepwise multiple regression analyses of species distribution showing the first selected
variable, the partial correlation coefficient (r) and the significance level (p)

Species Variable

S. minutus —
S. coronatus latitude
N. fodiens latitude
S. etruscus altiıtude
C. russula altitude
E. quercinus _
C. glareolus latitude
M. agrestis altitude
M. cabrerae _
M. nivalıs _
M. pyrenaicus latitude
M. duodecimcostatus —
A. sapidus -
A. sylvaticus latıtude
R. rattus —
R. norvegicus _
Mus spretus latıtude
Insectivora latitude
Rodentia latitude
Richness latitude
BU altıtude

Richness and diversity (H’) were positively correlated with both geographical variables,
but the former was primarıly related to latitude and the latter to altıtude.

Discussion

In the present study three geographical zones could be differentiated: Pyrenees, pre-
Pyrenees, and Ebro Valley. These important physiographic variations are accompanied by
parallel variation in temperature, precipitation (ELfas and Ruiz 1977), and vegetation
(PErnADoO and Rıvas-MARTiNEZ 1987). All of these factors highly affected the distribution
of small mammals in thıs area.

The distributions of $. coronatus, N. fodiens, C. glareolus, M. pyrenaicus, A. sylvaticus
and Mus spretus are primarıly related to latitude. All these species, except A. sylvaticus and
Mus spretus, have Eurosiberian distributions (SAINT-GIRONS 1973; AMOoRI et al. 1984;
Hausser et al. 1985) and the south slope of the Pyrenees constitutes the southern limit of
their distribution. As expected, they show a positive correlation with latitude, increasing ın
abundance from the Mediterranean to the Eurosiberian region. In spite of the few
individuals found for some species (1.e., N. fodiens and C. glareolus), the positive
correlation with precipitation (p < 0.01 in all cases) and negative with temperature (p
<.0.01 in N. fodiens and C. glareolus; p = 0.06 in $. coronatus) seems to indicate that a
general trend exists in these species for inhabiting areas with a balanced Atlantic climate.

The distributions of A. sylvaticus and Mus spretus are also primarıly related to latitude,
the former being directly correlated and the latter inversely. In France and Spain Mus
spretus shows an increase in abundance to the south (SAINT-GIRONS and VEsco 1974;
BRUNET-LECOMTE and DELIBES 1984). It appears from thıs study that Mus spretus requires
Mediterranean conditions, as its distribution is positively correlated with temperature and
negatively correlated with precipitation (p < 0.01 ın both cases; see also THALER et al.
1981). A. sylvaticus, however, shows a clear positive gradient northwards, with its

Distribution patterns of small mammal fauna along gradients of latitude and altitude 173

distribution directly correlated with precipitation (p < 0.01) but unrelated to temperature
(p = 0.2). ALCANTARA (1989) pointed out that the distribution of this species is related to
habitat structural features. Given the latitudinal varıation of vegetation in the study area
(PEınaDo and Rıvas-MARTINEZ 1987), our results may reflect such variatıon in habıtats.

The distribution of ©. russula, S. etruscus, and M. agrestis ıs related to altitude.
Crocidura russula increases with altıtude. The general trend for Crocidurinae is, on the
contrary, to inhabit temperate lowland areas (Age 1982; ALCANTARA 1989; BRÜNNER and
NEET 1991). This apparent contradiction to general findings might be explained by
considering the unusual kind of habitat preference exhibited by ©. russula ın the mountain
areas of western Europe, where its presence is restricted to the vicinity of human dwellings
(CHURCHFIELD 1990) rather than being influenced by any geographical factors. $. etruscus
decreases with altitude, in accordance with the general distribution of European
Crocidurinae (CHURCHFIELD 1990). M. agrestıs increases at higher altitudes, following the
general trend shown for this species ın Spain (DUENas and PErıs 1985; DELIBEsS 1985).

The distributions of S. minutus, E. quercinus, M. cabrerae, M. nivalıs, A. sapidus, M.
duodecimcostatus, R. rattns, and R. norvegicus are not affected by either altitude or
latitude. S. minutus has been shown as a species inhabiting altırtudes above 1000 m a.s.l. ın
the Pyrenees (VERICAD 1970; GoSALBEZ and LÖPEZ-FUSTER 1985); however, in our study
area, where all sıtes are lower, ıts distribution is not affected by altitude. DELıBEs (1981)
did not find any correlation between altitude and the distribution of this species in the
eastern Cantabric Mountains (North of Spain). In spite of the small number of individuals
found in our study, the results seem to suggest that the main factor affecting the
distribution of this species ıs humidity, rather than altıtude, since its distribution is
positively correlated with precipitation (p = 0.02; see GoSALBEZ 1976 for a similar result).

Arvicola sapidus, E. quercinus, R. rattus, and R. norvegicus are wıidely distributed in
Spain. Their distribution does not seem to be related to geographical factors, but (with the
exception of E. quercinus) to the presence of water-bodies or human habitation (GOSALBEZ
and LöPEZ-FusTErR 1985).

In Spain, M. duodecimcostatus has a typical Mediterranean distribution (SANS-CoMA et
al. 1973). Absence of relatedness with all varıables considered ın this study supports the
suggestion of GOSALBEZ et al. (1985) that M. duodecimcostatus ıs distributed according to
the nature of the ground rather than on any geographical factor.

The distribution of M. cabrerae and M. nivalıs ıs not related to latitude or altitude, but
is likely to be restricted to localısed habiıtats in Spain (GosALBEZ and LÖPEZ-FUSTER 1985),
e.g. rockslides for M. nıvalıs and rush for M. cabrerae.

Insectivora increase with latıtude while Rodentia decrease. These results agree with
those by HERRERA (1973), CHEYLAN (1976), and BRUNET-LECOMTE and Derises (1984),
who found a decline in the proportion of Insectivora southwards in Europe. This trend
may be explained by the boreal orıgin of most of these species (Hausser et al. 1985).

Generally, diversity decreases with altitude (e.g. MArTIn and VERICAD 1977; BLONDEL
et al. 1978; ABE 1982; ALcANnTARA 1989) since high mountains have an island effect
(McARTHUR 1972). Our results, however, are in contradiction to this general trend ın that
diversity increases with altitude. Such disagreement may be explained by the altıtudinal
range of the study area, which probably represents an ecotone (HoFFmann 1984); i. e., the
lowest limit for high altitude species and the highest limit for low altitude species (see
DueEnas and Perıs 1985 for a sımilar result).

Latitudinal gradients in richness are well known, with species numbers decreasing as
latitude increases (HERRERA 1974; McCoy and Connor 1980). Our results, however,
show an increase ın richness as latitude increases. Similar to the trend in diversity, ıt could
be argued that such an increase is the consequence of the border effect (MCARTHUR 1972),
due to the Eurosiberian distribution of the species.

174 Eulalıa Moreno and A. Barbosa

Acknowledgements

The authors thank M. ALcAnTara for helpful comments on the manuscript. R. JoHNSToN corrected
the language.

Zusammenfassung

Verteilung der Kleinsäugerfauna entlang von Breiten- und Höhen-Gradienten in Nordspanien

Es wurde der Einfluß der geographischen Breite und der Höhe über NN auf die Verbreitung von
Kleinsäugern untersucht. Annähernd 3000 Schleiereulengewölle von 20 verschiedenen Orten Nord-
spaniens wurden untersucht. Diese Gewölle enthielten Überreste von 9744 Kleinsäugern aus 17
Arten. Diese Arten konnten drei Gruppen zugeordnet werden: 1. Beziehung zur geographischen
Breite (Sorex coronatus, Neomys fodiens, Clethrionomys glareolus, Microtus pyrenaicus, Apodemus
sylvaticus, Mus spretus), 2. Beziehung zur Höhe über NN (Suncus etruscus, Crocidura russula,
Microtus agrestis), 3. Keine Beziehungen zu geographischer Breite und Höhe über NN (Sorex
minutus, Eliomys quercinus, Microtus cabrerae, M. nıvalıs, M. dondecimcostatus, Arvicola sapidus,
Rattus rattus, R. norvegicus).

Die Verteilung der Arten wird in Beziehung zu geographischen und klimatischen Faktoren
gesetzt. Unsere Daten zeigen, daß die geographische Breite der für das Auftreten von Arten nahe ihrer
südlichen Verbreitungsgrenze bedeutendste Faktor ist.

References

Age, H. (1982): Ecological distribution and faunal structure of small mammals in central Nepal.
Mammalıa 46, 477-502.

ALCANTARA, M. (1989): Analısis de la distribuciön altitudinal de la fauna de micromamiferos de la
Sierra de Guadarrama. Acta Biol. Mont. 9, 85-92.

AMORI, G.; CRISTALDI, M.; ConToLi, L. (1984): Sui rodentori (Gliridae, Arvicolidae, Muridae)
dell’Italia peninsulare ed insulare in rapporto all’ambiente bioclimatico mediterraneo. Anımalia 11,
217-269.

BLONDEL, ]J.; Davıp, P.; LEPART, J.; ROMANE, F. (1978): L’avifaunae du Mont-Ventous. Essai de
synthese biogeographique et ecologique. Terre et Vie 32, 111-145.

Bond, W.; FERGUSON, M.; ForRsyYTH, G. (1980): Small mammals and habitat structure along
altitudinal gradients in the Southern Cape Mountains. S. Afr. J. Zool. 15, 34-43.

BRUNET-LECOMTE, P.; DELIBES, M. (1984): Alimentaciön de la Lechuza Comün Tyto alba en la
cuenca del Duero, Espana. Donana Acta Vertebrata 11, 213-229.

BRÜNNER, H.; NEET, C. R. (1991): A parapatric scenery: the distribution and ecology of Sorex
araneus and S. coronatus (Insectivora, Soricidae) in southwestern Germany. Z. Säugetierkunde 56,
1-9.

CHEYLAN, G. (1976): Le regime alımentaire de la Chouette effraie Tyto alba en Europe Mediter-
raneenne. Terre et Vıe 30, 565-579.

CHURCHFIELD, $. (1990): Shrews of the British Isles. Aylesbury: Shire Publ. Ltd.

CoRBET, G. B. (1978): The Mammals of the Palaeartic Region: A Taxonomic Review. London:
Cornell Univ. Press.

Deriges, J. (1981): Distribuciön en cuanto a altitud y biotopos de los micromamiferos de la parte
oriental de la Cordillera Cantäbrica. Universidad de Oviedo.

— (1985): Distribution and abundance of small mammals in a gradient of altitude. Acta Zool. Fennica
173, 53-56.

DueEnas, M. E.; Perıs, $. J. (1985) Analisis de egagröpilas de Tyto alba en la Sierra de Gata (W de
Espana). Alytes 3, 109-144.

Erfas, F.; Rufz, L. (1977): Agroclimatologfa de Espana. Madrid: Publ. del Ministerio de Agricultura.

Fons, R.; LıBors, R.; Saınt-GiRrons, M. C. (1980): Les micromammiferes dans le departement des
Pyrenees-Orientales. Essai de repartition altitudinal en liason avec les etages de vegetation. Vie et
Milieu 30, 285-299.

GOSALBEZ, J. (1976): Sorex minnutus en las Montanas de Prades (Cataluna, Espana). Misc. Zool. 3,
213-216.
GOSALBEZ, ]J.; LÖPEZ-FUSTER, M. ]J. (1985): The natural communities of small mammals (Insectivores

and Rodents) of Catalonıa (Spain). Misc. Zool. 9, 375-387.

GOSÄALBEZ, J.; VENTURA, J.; GÖTZENS, G.; EscoLA, A. (1985): Microtus pyrenaicus (Rodentia:
Arvicolidae) en el noreste ıberico. P. Dept. Zool. Barcelona 11, 83-91.

HAUSSER, J.; CATZEFLIS, A.; MEYLAN, A.; VoGEL, P. (1985): Speciation in the Sorex araneus complex
(Mammalıa: Insectivora). Acta Zool. Fennica 170, 125-130.

Heim DE Bausac, H.; BEAUFORT, F. (1966): Regime alimentaire de l’Effraie dans le Bas-Dauphine:
Aplications A l’eEtude des Vertebres. Alauda 4, 309-324.

Distribution patterns of small mammal fauna along gradients of latitude and altitude 175

HERRERA, C. M. (1973): Regimen alımenticio de Tyto alba en Espana suroccidental. Ardeola 19,
999-394:

— (1974): Trophic diversity of the Barn Owl Tyto alba in continental Europe. Ornis Scand. 5,
181-191.

Marrı, C. D. (1973): Ten years of Barn Owl prey data from a Colorado nest site. Wilson Bull. 85,
85-86.

MARTIN, J.; VERICAD, J. R. (1977): Datos sobre la alimentaciön de la Lechuza (Tyto alba) en Valencia.
Mediterränea 2, 35-47.

MCARTHUR, R. H. (1972): Geographical ecology: Pattern in the distribution of species. New York:
Harper and Row.

McCory, E. D.; Connor, E. F. (1980): Latitudinal gradients in the species diversity of North
American mammals. Evolution 34, 193-203.

PEINADO, M.; Rıvas-MARTfNEZ, $. (1987): La vegetaciön de Espana. Madrid: Publ. Univ. Alcalä de
Henares.

Pranka, E. R. (1966): Latitudinal gradients in species diversity: A review of concepts. Amer. Nat.
10055346.

SAINT-GIRONS, M. C. (1968): Analyse de fluctuations du regime de l’Effraie Tyto alba dans le
departement de la Somme (Nord de la France) pendant une population de Microtus arvalıs. Act.
Soc. Zool. Bohemoslov. 32, 185-198.

— (1973): Les mammiferes de France et de Benelux. Parıs: Doin.

SAINT-GIRONS, M. C.; Spitz, E. C. (1966): A propos de l’etude des micromammiferes par l’analyse
des pelotes des rapaces: Interet et limites de la methode. Terre et Vie 1, 3-18.

SAINT-GIRONS, M. C.; VEsco, J. P. (1974): Notes sur les mammiferes de France. XIII: Repartition et
densite de micromammiferes dans le couloir Sequano-Rodhanien. Mammalıa 38, 244-264.

SoKAL, R. R.; RoHLF, F. J. (1981): Biometry. San Francisco: Freeman.

VERICAD, J. R. (1970): Estudio faunistico y biolögico de los mamiferos del Pirineo. P. Cent. pir. Biol.
Expgdn1729:

WEBSTER, J. A. (1973): Seasonal varıations in mammal contents of Barn Owl castings. Bird Study 20,
185-196.

Authors’ address: EuULALIA MORENO and AnDRES BARBOSA, Departamento de Ecologia Evolutiva,
Museo Nacional de Ciencias Naturales, Jose Gutierrez Abascal, 2, E-28006 Ma-
drid, Spain

Z. Säugetierkunde 57 (1992) 176-178
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

WISSEINSEHENETSLETEREZERSURTZIN TITTEN EHEN

The use of fur colour characters to distinguish the sibling species
Sorex araneus and Sorex coronatus (Insectivora, Soricidae):
a field test in a zone of parapatric contact

By ©. R. NEET

Institut de Zoologie et d’Ecologie Animale, Batiment de Biologie, Universite de Lausanne,
Lausanne, Switzerland

Receipt of Ms. 20. 12. 1991
Acceptance of Ms. 27. 1. 1992

In their description of Sorex coronatus Millet, 1828, MEyLAn and Hausser (1978) showed
that this species, previously named S. gemellus by Ort (1968), ıs distinguished from the
closely related sıbling species Sorex aranens on the basıs of its karyotype (see HAUssER
1990; Hausser et al. 1990, for a detailed review of the literature on these two species).
Although very clear differences in mandible morphology have been found between
S. araneus and S. coronatus (e.g. Hausser and JamMmoT 1974; HANDWERK 1987) and
although several biochemical characters may be used to separate many of the chromosomal
races of $. araneus from the unique chromosomal race of $. coronatus (CATZEFLIS et al.
1982; CATzErLIS 1984; HAussER and ZUBER 1983; NEET and Hausser 1989, 1991), the
only absolute difference between these sibling species that permits to distinguish them
throughout their whole biogeographical range remains the karyotype.

However, for field ıidentifications, morphological characters are necessary. Some
possible characters such as taıl and hindfoot lengths have been discussed by OTT (1968),
Orr and OLert (1970) and HAnDwERK (1987), but these characters are not clearcut
enough to provide a useful field ıdentification criterion.

Differences in fur colour patterns of $. araneus and S. coronatus were first noticed by
voN LEHMANN (1955) and OLERT (1969). A consistent description of these patterns was
given by OTT and OLerr (1970) and OLErT (1973a, b), who defined $. araneus as a darker
species with a broad dark back band, while $. coronatus has a narrow dark back band, with
lighter flanks and a tricolorous aspect. OLERT used techniques such as optic densitometry
to demonstrate that these fur colour differences can be quantified (OLERT 1973a).
Differences were actually quite obvious ın some localities, enabling OTT and OLerT (1970)
to obtain 100 % correct identifications with n = 8 individuals sampled from the Swiss Alps.
Nevertheless, MEyrLan and Hausser (1978) have considered that fur colour characters are
probably too variable to be of any general value to discriminate $. araneus from S.
coronatus. Our own observations have shown that when one gains some experience and
practice in identifying these two species frequently by use of karyological or biochemical
techniques, fur differences can be observed and some individuals appear to be clearly
ıdentifiable, especially when dealing with typically tricolorous $. coronatus specimens.

In order to assess to what extent fur colour characters can be considered to be reliable
for field identifications, we undertook a test in a zone of parapatric contact between the
two species during the summer 1987. The contact zone is sıtuated on the border of the lake
of Neuchätel (Switzerland) and has been described by NEET and Hausser (1990). The test

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5703-176 $ 02.50/0

Fur colour characters to distinguish Sorex araneus and Sorex coronatus 1727.

Percentages of individuals of Sorex araneus and S. coronatus correctly identified during field tests
using fur colour characters, and tests of the deviation of the numbers of correctly (I.) and
erroneously (I,) identified individuals from a null hypothesis of randomness

Field test period % of correct
identifications

15.-16. 9. 1987 84.6 36 0.0002 ***
22.-23. 9. 1987 66.7 8 0.31 N.S.
28.-29. 9. 1987 73.2 27 0.03 *

Mean 74.8

n, = number of $. araneus ın the test, n. = number of $. coronatus in the test, N.S. =
nonsignificant, * =p < 0.05, *** = p < 0.001.

simply consisted of identifying individuals at night, during trap controls, with a torch
lamp. The tests were carried out in trapping areas that had not been visited more than once
before the onset of testing and thus, there was no particular knowledge of the individuals
encoutered. The fur colour characters mentioned above were used for these identifications.
As individuals were systematically marked and ıdentified by serum albumin elec-
trophoresis (NEET and HaAusser 1989), the field ıdentifications could be controlled a
posteriori. As shown in the Table, a mean correct identification rate of about 75 % was
obtained over three independent tests. This rate indicates that differences are detected in
field conditions since the mean correct ıidentification rate clearly exceeds the 50 % level that
would be expected under a random rate of species attrıbution. However, results in the
Table also show that only two out of three tests gave significant deviations from a null
hypothesis of random species attrıbution, and the maximal proportion of correct identifi-
cations obtained still left 15 % erroneously identified specimens.

Thus, we conclude that fur colour characters are not very efficient and are only of
limited value to distinguish $. araneus and S. coronatns under usual field conditions.

Literature

CATZEFLIS, F. (1984): Systematique biochimique, taxonomiıe et phylog£nie des Musaraignes d’Europe
(Soricidae, Mammalia). PhD Thesis, Univ. Lausanne.

CATZEFLIS, F.; GRAF, J.-D.; HAUSSER, J.; VOGEL, P. (1982): Comparaison biochimique des Musarai-
gnes du genre Sorex en Europe occidentale (Soricidae, Mammalıa). Z. zool. Syst. Evolut.-forsch.
20, 223-233.

HANDWERK, ]. (1987): Neue Daten zur Morphologie, Verbreitung und Ökologie der Spitzmäuse
Sorex araneus und S$. coronatus im Rheinland. Bonn. zool. Beitr. 38, 273-297.

Hausser, J. (1990): Sorex coronatus Millet, 1828. In: Handbuch der Säugetiere Europas. Ed. by. ].
NIETHAMMER and F. Krapp. Wiesbaden: Aula Verlag.

FHHAUSSER, J.; HHUTTERER, R.; VOGEL, P. (1990): Sorex araneus Linnaeus, 1758. In: Handbuch der
Säugetiere Europas. Ed. by J. NIETHAMMER and F. Krapp. Wiesbaden: Aula Verlag.

HAussER, ]J.; JAMMOT, D. (1974): Etude biometrique des mächoires chez les Sorex du groupe araneus
en Europe continentale (Mammalıa, Insectivora). Mammalia 38, 324-343.

HAUSSER, J.; ZUBER, N. (1983): Determination specifique d’individus vivants des deux especes
jumelles Sorex araneus et S. coronatns, par deux techniques biochimiques (Insectivora, Soricidae).
Rev. suisse Zool. 90, 857-862.

LEHMANN, E. von (1955): Über die Untergrundmaus und Waldspitzmaus in NW-Europa. Bonn.
Zool. Beitr. 6, 8-27.

MEYLAN, A.; Hausser, J. (1978): Le type chromosomique A des Sorex du groupe araneus: Sorex
coronatus Millet, 1828 (Mammalia, Insectivora). Mammalia 42, 115-122.

NEET, C. R.; HaAusser, J. (1989): Chromosomal rearrangements, speciation and reproductive isola-
tion: the example of two karyotypic species of the genus Sorex. J. evol. Biol. 2, 373-378.

— ; — (1990): Habitat selection in zones of parapatrıc contact between the common shrew Sorex
araneus and Millet’s shrew S. coronatus. J. Anım. Ecol. 59, 235-250.

178 C. R. Neet

— ; — (1991): Biochemical analysıs and determination of living individuals of the Alpine karyotypic
races and species of the Sorex araneus group. Mem. Soc. vaud. Sc. nat. 19, 97-106.

OLERT, J. (1969): Fellzeichnung und Größe rheinischer Waldspitzmäuse (Sorex araneus). (Mamm.,
Insectivora). Decheniana 132, 123-127.

— (1973a): Cytologisch-morphologische Untersuchungen an der Waldspitzmaus (Sorex araneus
Linne 1758) und der Schabrackenspitzmaus (Sorex gemellus Ott 1968). (Mammalıa, Insectivora).
Veröffentl. Univ. Innsbruck 76, 1-73.

— (1973b): Schädelmessungen an rheinischen Wald- und Schabrackenspitzmäusen. Bonn. zool.
Beitr. 24, 366-373.

OTT, J. (1968): Nachweis natürlicher reproduktiver Isolation zwischen Sorex gemellus sp. n. und
Sorex aranens Linnaeus, 1758 ın der Schweiz (Mammalıa, Insectivora). Rev. suisse Zool. 75,
53-75.

OTT, J.; OLERT, J. (1970): Färbungsunterschiede zwischen Sorex araneus Linnaeus 1758 und Sorex
gemellus Ott 1968 (Mammalia, Insectivora). Rev. suisse Zool. 77, 283-291.

Author’saddress: Dr. CoRNELIS R. NEET, Centre de conservation de la faune, 1, chemin du
Marquisat, CH-1025 St-Sulpice, Switzerland

Z. Säugetierkunde 57 (1992) 179-180
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

On a Fishing cat, Felis (Prionailurus) viverrina Bennett, 1833,
from continental Malaysia

By P. J. H. van BREE and MoHD KHan BIN MOMIN KHAnN

Receipt of Ms. 2. 12. 1991
Acceptance of Ms. 28. 1. 1992

In 1967 the aborigines ın Bahau Negeri Sembilan (about 2°40’ N, 102°36’ E) captured a
spotted cat about the size of a large domestic cat. The anımal was given to the Melaca Zoo
where it arrıved on 9 June 1967 and where it died on 25 April 1977. Then the cat was
mounted and sent to the Wildlife Training Centre at Bukit Rengit, Lancang, Pahang,
where it still can be found (see figure).

The specimen had a rather course earthy-grey fur with body markings consisting of a
series of elongate spots arranged in more or less longitudinal rows. The taıl was less than
50% of the head and body length. The total length of the mounted anımal was about 770
mm, the tail length about 280 mm. The general build was rather stocky with comparatively
short legs and a rather elongated head.

From the description and the photograph it ıs evident that the anımal is a fishing cat,
Felis (Prionailurus) viverrina Bennett, 1833. So far, the species has not been mentioned for
the fauna of continental Malaysıa (see e.g. MEpwAy 1969, 1978; HARRISON 1966) and thus
the Bahau Negeri Sembilan specimen is the fırst one known from the Malay Peninsula.

Is the fishing cat a new faunal element for the Malay Peninsula or has the species always
been present ın small numbers but has gone unnoticed or are we dealing with escaped
specimens kept as pets or in Zoos? These are questions which cannot be answered with
certainty.

It is, however, clear that the species has a rather unusual distribution. It occurs with
isolated populations in southern India and Sri Lanka. The major distribution ıs from Nepal
through western India and Burma to the northern half of Thailand and Indo-China

Mounted fishing cat, Felis viverrina Bennett, 1833, caught in Bahau Negeri Sembilan in 1967

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5703-179 $ 02.50/0

180 P. J. H. van Bree and Mohd Khan bin Momin Khan

(Pocock 1939; U Tun Yın 1967; LEKAGUL and McNEELY 1977; Van PEENEN 1969).
Furthermore, it is found ın northern and western Java, Indonesia. It is said to occur also on
Sumatra but no museum specimens are known from that island.

The isolated occurrence on Java has been explained as an introduction during the
Middle Ages, when there was an important cultural and religious invasion to the islands of
Sumatra, Java and Balı from India. A large number of buildings (mostly temples) on the
islands are still proof of that invasıon. It has been argued that the leopard, Panthera pardus,
the fishing cat, the black-naped rabbit, Lepus nigricollis, and the green peafowl, Pavo
muticus, were then brought to Java for religious and/or cultural reasons.

Another explanation might be that the species originally had a much larger distribution
and that we at present only observe relict populations. In the National Natural History
Museum at Leiden, the Netherlands, there ıs a fishing cat collected by P. DıarD in
Singapore ın 1819 (BRONGERSMA 1935), and in the Zoological Reference Collection ın
Singapore there is a mounted fishing cat, said to be collected at Pontianak, Kalimantan
(Borneo), Indonesia ın 1880. Till now the Leiden and Singapore specimens were thought to
be wrongly labeled but it cannot be excluded that they came from (small) populations that
exist no longer. Also must be mentioned a fishing cat said to be shot at Megaran, Bali,
Indonesia, some time before 1957 (MEıssner 1958). The remains of the specimen,
however, have not been studied by a zoologist, so this remains a doubtful record.

Whatever the correct explanation might be, it is worthwhile to pay attention to the
occurrence of fishing cats ın the Malay Peninsula and ın Indonesia (Borneo and Sumatra).

References

BRONGERSMA, L. D. (1935): Notes on some recent and fossil cats, chiefly from the Malay
Archipelago. Zool Mededel. 18, 1-89.

HARRISON, J. (1966): An introduction to mammals of Singapore and Malaya. Singapore: Singapore
Branch Malayan Nature Soc.

LEkrAGUL, B.; McNEELY, J. A., (1977): Mammals of Thailand. Bangkok: Association for the
conservation of Wildlife.

Mepway, LorD (1969). The wild mammals of Malaya and offshore islands including Singapore. Kuala
Lumpur, Singapore: Oxford Univ. Press.

— (1978): The wild mammals of Malaya (Peninsular Malaysıa) and Singapore. Kuala Lumpur,
Singapore: Oxford Univ. Press.

MEISSNER, H. ©. (1958): Der Balı Tiger -— ein Märchen? Säugetierkde. Mitt. 6, 13-17.

PEEnEn, P. F. D. van (1969): Preliminary identification manual for mammals of South Vietnam. City
of Washington: U. S. National Museum.

Pocock, R. I. (1939): Mammalıa. Vol. I: Primates and Carnivora (in part). The fauna of British India,
including Ceylon and Burma. London: Taylor & Francis Ltd.

U Tun Yın (1967): Wild anımals of Burma. Rangoon: Rangoon Gazette Ltd.

Authors’ address: Dr. PETER J. H. van BREE and MoHD KHan BIN MomiIn Khan, Institute of
Taxonomic Zoology (Zool. Museum), Mauritskade 61, NL 1092 AD Amsterdam,
The Netherlands

Z. Säugetierkunde 57 (1992) 181-182
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Occurrence of a melanistic Common vole, Microtus arvalıs
(Pallas, 1779) in Slovakia

By L. Kocıan and D. Zıak

Department of Zoology, Faculty of Natural Sciences, Comenius University,
Bratislava, Czecho-Slovakia

Receipt of Ms. 7. 11. 1991
Acceptance of Ms. 3. 2. 1992

On September 23, 1989 we succeeded in capturing a melanistic specimen of the common
vole (Microtus arvalıs) in a potato field near the village Matejovce (near Poprad, in
northern Slovakia) at an elevation of 700 m a. s. 1. The specimen was caught accıdentally
during voluntary works of students on potato fields. It is stored ın deposit of the
Department of Zoology, Faculty of Sciences, Comenius University, Bratislava as a skin
preparation and the skull (damaged). On the basis of the body length ($eBex 1959) its age is
estimated at about 3 months.

Description of colouring: dorsal hair - upper part dark, lower part grey-black; ventral
hair —- grey. Colouring on the head partially changes from dark to dark-grey-brownish.

NIETHAMMER and Krapr (1982) describe 10 colour mutations of Microtus arvalıs
including a melanıstic one. Its description was originally given by REICHSTEIN (1957) and
FRANK and ZIMMERMANN (1957) who also made a follow-up study of the progeny of
melanistic voles under laboratory conditions. The latter manifested decreased reactivity,
biting, vitality and growth rate and increased mortality rate in the young. A similarly
coloured melanistic specimen of Microtus arvalıs has been described lately by DorcH and
JAscHkE (1991) from Germany.

The present specimen is to our knowledge the fourth melanıstic Microtus arvalıs
mentioned from Central European areas. From Czecho-Slovakıa, only its albinotic
anomalies have been described so far (HERAN and MazAk 1976; StusAk 1987) and no
melanistic Microtus arvalıs has been reported. The same is true for Poland (Pucek pers.
comm.), Hungary (CsoRBA, pers. comm.), and Austria (SPITZENBERGER, pers. comm.).

Colour anomalies in small mammals are explained in connection with effects of
ecological factors (particularly humidity) (e.g. SIMROTH 1905; HanAk 1957; BLossoMm
1942), but also as being genetically determined (e.g. REICHSTEIN 1957; FRANK and
ZIMMERMANN 1957; SEARLE 1968). Here, the symbol “a” (recessive) accounts for the
melanistic colouring.

References

Brossom, P. M. (1942): Total melanısm in Microtus from Michigan. J. Mammalogy 23, 214.

DoıchH, D.; JascHkE, M. (1991): Farbanomalien bei einigen Kleinsäugern. Säugetierkdl. Inf. 3,
313-320.

FRANK, F.; ZIMMERMANN, K. (1957): Färbungs-Mutationen der Feldmaus. Z. Säugetierkunde 22,
87-100.

Hanäkx, V. (1957): Colour anomalies in small mammals. Cas. när. mus. 126, 144-147 (in Czech).

HERAN, 1.; MAZAR, V. (1976): Proceedings - Zool. Department of the National Museum in Prague. 11.
Colour anomalies. Lynx 18, 109-112 (in Czech).

NIETHAMMER, ]J.; Krapp, F. (1982): Handbuch der Säugetiere Europas. Bd. 2/I. Rodentia II.
Wiesbaden: Akad. Verlagsges.

REICHSTEIN, H. (1957): „Schwarz“, eine neue Mutation bei Microtus arvalıs Pall. Z. Säugetierkunde
22, 102-103.

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182 L. Kocian and D. Ziak

SEARLE, A. G. (1968): Comparative genetics of coat colour in mammals. New York, London:
AcademierBress u

SIMROTH, H. (1905): Über einige Folgen des letzten Sommers für die Färbung von Tieren. Biol.
Zentralblatt 26, 334-340.

SEBER, Z. (1959): The body length. In: The Common vole, Microtus arvalıis, Ed. by J. KrartocHvır.
Prague: Publ. House CSAV. Pp. 63-64 (in Czech).

STusäk, J. M. (1987): Flavism in Apodemus sylvaticus, albinism in Microtus arvalis and notes on colour
anomalies in mammals. Lynx 23, 105-109 (in Czech).

Authors’ address: Lupovır Kocıan and Davın Zıar, Department of Zoology, Faculty of Natural
Sciences, Comenius University, Mlynskä dolına B-1, CS-842 15 Bratislava,
Czecho-Slovakia

Z. Säugetierkunde 57 (1992) 183-185
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Faecal pellet size differences as a field criterion to distinguish
between the two Ctenodactylus species (Mammalia, Rodentia)

By P. GouvaAr

Laboratoire Ethologie Experimentale et Comparee, URA 667, Universite Paris Nord,
Villetaneuse, France

Receipt of Ms. 5. 9. 1991
Acceptance of Ms. 17. 2. 1992

The Ctenodactylidae are among the oldest rodent families (BEINTEMA et al. 1991). They are
an ecological enigma as well as being a phylogenetic curiosity. The five living species are
diurnal although they are to be found ın desert or semi-desert conditions in Africa
(GEORGE 1974). Ctenodactylus gundi and C. valı inhabiıt the rocky districts of the northern
part of the Sahara. A preliminary study of their range in Algeria has shown that they
occupy the Saharan Atlas from Tunisia to Morocco and the wadi Saoura basın to Kerzaz in
the south. This range shows no discontinuity and, at first, we were unable to distinguish
boundaries between the two species (GouAT and Gouar 1984). More recently, using the
method described below, the two species were shown to be parapatric in Algerıia (GOUAT
1988).

Several criteria for species ıdentification have been proposed in the literature (see
GEORGE 1982, for review) but none of them ıs easy to use in the field. One of these criteria
is based on the difference ın size between the two species, C. gundi being slightly larger
than C. valı. Though these species are diurnal, the difference ın size is too small to be
clearly identified by direct observation. In addition, gundis are very difficult to trap and
body measurements are difficult to obtaın.

A gundi sıte ıs often ıdentified by numerous piles of droppings left by the annımals at
the entrance of their rocky shelters. Fresh droppings are black cylinders 3.5 to 4.2 mm in
diameter. They become white with age. In captivity a ©. valı fed ad libitum on fresh
vegetables produces 100 to 250 droppings per day in groups of 10 to 30. According to the
difference in body size between the two species, a difference in the size of the droppings
was to be expected.

To test this hypothesis, samples of fresh droppings were collected in different sites
distributed throughout the range in Algerıa (see Table). The species occupying each site
was identified according to one or several of the criteria as described by GEORGE (1982).

In order to study the influence of the water content of vegetation which decreases from
north to south, three ©. gundi sites (Ferkous, Djemina and Aures 3) were located ın the
Aures mountains at different latitudes. For similar reasons, samples were collected at
different periods of the year on a specific site for each species (Djemina for C. gundi and
Djeniene Bou Rezg for C. valı).

The results are summarized in the Figure. C. gundi droppings are longer than the C.
valı ones. In all the cases but one, the standard error intervals of samples of each species,
do not overlap. The only exception is between the C. gundi Aures 3 sample (mean length:
9.62 mm + 0.50) and the C. valı Djeniene Bou Rezg 1 (Bl) sample (mean length: 8.90 mm
+ 0.27). The difference between these two samples is, nevertheless, significant (t = 2.30,
df = 88, p < 0.05),

This study demonstrates that even if there are intra-specific varıations in the length of
droppings, according to the season or to the site, coprometry is a good criterion for field

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5703-183 $ 02.50/0

184 P. Gonat

Mean Length + S.E. in mm
[o)}

NAURRRARTIRNNNNNNNNNNNN AN NN NN NN NN NN NN NNN NN
DSITTSTSTTTT TTS TTS TS TI TS TTS SS I II ITS III III III
KURRNIUNNNNNNINNNINNNNNN NN NNNNNNNNNNNNNNNNNNN

O9 KSSSSSSSSSSSSSSCSIICISCIIICICIIICCEIETETTCETEEETEEEEETTD

TI KSSSSSSSSSISSSSIIIIIIIIICIICIIIIEEITETTEEEEETTTTT

FALO D1D2D3D4 Z TBO

Fig. 1. Mean length (+ S. E.) of different samples of droppings of C. gundi and C. vali. Each sample is
identified by a code name (see Tab. 1 for legend)

diagnosis between the two Ctenodactylus species. The samples must be large enough (at
least 30 droppings) to be representative but they may be comprised of old white droppings.
Droppings are very dry when emitted and their length does not seem to be significantly
affected by age. This quality allows us to identify the species which has occupied an
abandoned site, and is of great interest when the fluctuations of geographic distribution are
studied. The above method might be very efficient in assessing the exact boundaries
between these two species ın Morocco and in Libya.

Table 1. Geographic distribution of the collecting sites

For each sample are given the name of the site, the date of collecting of the sample, the sample size, the
geographic coordinates of the site, ıts altitude and an identification code

Date of Sample size Long. North ; Alt. in m
sampling

C. gundi

Les Oglats ol; 32023, 0°37' W
Ferkous . 04. 30.107 © 227E
Aures 3 03% 34° 50’ 672305
Djemina 12. 34° 54' 62308

C. valı

Zeghamra oe 39710) 233. NW
Taghıt 3 01 312. 05% ZEIGEN.
Beni Ounif ol, 320 1° 14° W
Djeniene 05. 218% 0°53’ W
Bou Rezg

Coprometry in Ctenodactylus 185

References

BEINTEMA, ]J. J.; RODEWALD, K.; BRAUNITZER, G.; CZELUNIAK, J.; GOODMAN, M. (1991): Studies on
the phylogenetic position of the Ctenodactylidae. Mol. Biol. Evol. 8, 151-154.

GEORGE, W. (1974): Notes on the ecology of gundis (F. Ctenodactylidae). Symp. Zool. Soc. London
34, 143-160.

GEORGE, W. (1982): Ctenodactylus (Ctenodactylidae, Rodentia): one species or two? Mammalıa 46,
375-380.

Gouar, ]J.; GouAT, P. (1984): Repartition et habitat des goundis en Algerie (Rongeurs, Ctenodacty-
lides). Mammalıa 48, 227-238.

Gouar, P. (1988): Competition interspecifique et utilisation de l’escape, etude chez deux especes de
rongeurs ctenodactylides d’Algerie. Sci. Tech. Anım. Lab. 13, 123-127.

Author’s address: PATRICK GOUAT, Laboratoire Ethologie experimentale et comparee, Universite
Parıs Nord, Avenue J-B Clement, F-93430 Villetaneuse, France

Z. Säugetierkunde 57 (1992) 186-189
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

One-year tracking data and behaviour of a released hand-reared
Moose (Alces alces) in Forest Lapland

By E. PuULLIAINEN

Department of Zoology, University of Oulu and Värriö Subarctic Research Station, University of
Helsinki, Helsinki, Finland

Receipt of Ms. 18. 11. 1991
Acceptance of Ms. 13. 2. 1992

It is evident that moose (Alces alces) perform seasonal return migrations between winter
and summer habitats which can be 15 km or more apart (ZHırnov 1969; PULLIAINEN
1974). Atthe same time, the moose provides evidence for the basıc concepts of the familiar
area hypothesis (see PULLIAINEN 1974; BAKER 1978). In this context the natural behaviour
ot moose which have not learned the traditional migration patterns from their mothers are
of special interest.

An opportunity arose in the spring of 1989 to carry out an experiment of this kind by
releasing into the wild conditions of Finnish Forest Lapland a moose which had lost its
mother as anewly born calf in a traffic accıdent and had been raised in captivity at the zoo
attached to the Department of Zoology at the University of Oulu. The anımal had been
hand-reared to the extent that ıt had totally lost ıts shyness towards human beings.

The moose, a female called Suvi, was taken to the northernmost part of the district of
Salla in southeastern Finnish Forest Lapland adjacent to the Soviet frontier on October 4,
1990 and released, furnished with a radio transmitter on a collar. This area ıs characterized
by coniferous, mixed and birch forests of the taiga type and isolated fells and marshes of
varyıng sıze. The release site is one of the overwintering centers for moose in this region
(PuLLiamnen 1974). Suvi was followed as closely as possible after her release. She
occasıonally disappeared, but always reappeared. The one-year tracking data are shown in
the figure. The most interesting observations were as follows:

5-7.10. 1990: Moved in a very restricted area, was lame ın her right fore-leg, was
probably feeding on willows; 18. 10.-1. 12.: Was seen wıth a herd of semi-domestic
reindeer on 22. 10. and with a herd of three male moose six days later. Suvi allowed the
observer to touch her, but the others escaped to a distance of about 30 m. These moose
soon left Suvi, and she then moved about alone, although she was seen with an adult female
moose on 1. 12. She had been feeding on juniper. Suvi came to greet both our technicians
and a group of hunters (who did not kill her), and eventually all of them ran away;
10. 12. 1990-15. 3.1991: At the beginning of this period Suvi was together with the
female mentioned above, but after the turn of the year she was seen together with three and
then four other moose. They had been feeding on juniper and birch. All the moose escaped
to a distance of some tens of metres (the technicians were travelling by snow scooter). In
late January-early March Suvi was alone, feeding on pine, birch and juniper. For some
time she had difficulties with snow which had frozen on her head and kept at a distance of
9-10 m; 22.-26. 3.: Suvi was alone and had been feeding mainly on pine (also some birch);
4.-18. 4.: Suvi was seen three times together with an adult female and her calf. All of them
ran away from the snow scooter. They had been feeding on pine and birch; 30. 4.-28. 5.:
Suvi was still with the adult female and her calf. They had been feeding on pine and
juniper; 5.-25. 6. Suvi was found alone (the adult female had probably given birth to a new
calf). Suvi now followed our technicians in the forest and was seen feeding on willows,

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One-year tracking data and behaviour of a released hand-reared Moose 187

birch leaves and cowberries. She was ın a rather poor condition; 5.-16. 7.: Suvi was still
alone and was seen feeding on birch leaves. She did not come near the technicıans; 25. 7.:
A frontier guard saw Suvi alone at a point about 100 km away from the previous
observation site. Suvi had covered this distance in 9 days at the most; 6. 8.: Again a frontier
guard sited Suvi alone; 17. 8.-15. 9.: On the 17th ot August Suvi was together with sıx
male and one female moose, but she was alone again on the 20th of August and came to
greet the technicıan and followed him for 300 m. She was feeding on willows and fireweed,
Epilobium angustifolium. On 23rd of August she was together with an adult male, and now
ran away to a distance of 150 m. Three days later the number of her companions had
increased to three, the flight distance remained the same. One of them was a male. On the
31st of August she was again seen with three other moose (two adult males and a yearling),
and three days later with four adult male moose, all of which ran away. On the 19th of
September Suvi was alone and came to look at the technician, allowing him to touch her.

Suvi’s life in the wild began in an interesting way, since she fırst joined a herd of semi-
domestic reindeer, having seen reindeer previously in the nearby enclosures in the zoo but
no other moose. She soon discovered her real conspecifics, however, and later on sought
only the companionship of other moose, although large numbers of reindeer were grazing
in the same area. She tended to join all kinds of groups of moose and then leave them again
(or be rejected for some reason). This also means that wild moose accepted Suvi into their
group, at least for a time.

Suvi was faced with a difficult decision when accompanying other moose, as a human
being approached. Usually an anımal such as a moose will either flee or attack when
approached by a wolf, for ınstance, but here the choice was between escape and
approaching the human being, to which she had been conditioned in her early life. Usually
Suviı ran away with the wild moose, but soon afterwards, when alone, she would come to
greet the technicıan. It ıs significant that one year of life in the wild did not change her
attıtude towards human beings to any extent. She remembered their habits, and all her
associations acted in favour of continuous companionship with human beings. It ıs also
noteworthy that the other moose associated with Suvi also showed a surprising short flıght
distance, even as short as 30 m. CEDERLUND et al. (1981), among others, recorded flight
distances varying between 200 and 300 m depending on the approach pattern of human
beings. Perhaps in the case of Suvi her presence and behaviour towards human beings
shortened the flight distance of the other moose.

Our earlier research has shown that the local moose can be classified into two ecological
groups, residents and migrants (PuULLIAINEN and Lo1sA 1967; Lo1sa and PULLIAINEN 1968;
PuLLIAINEN 1974). The releasing site, at Tuntsa, has long been a typical overwintering area
for moose (VESTERINEN 1940; PULLIAINEN 1974), and moose were overwintering there on
this occasıon as well. The majority of the local moose migrate to the south or southwest in
the spring, however (VESTERINEN 1940; PULLIAINEN 1974), and Suvi spent the summer
alone in the area to the west, which also is a typical overwintering area. In late July she
suddenly moved a hundred kilometres further south to an area where many moose spend
their summers, to return to Tuntsa in August, meeting a group of moose which had either
spent their summer there or migrated to the overwintering area. We had found earlier that
the autumn migration can commence before there is any snow on the ground (PULLIAINEN
1974).

We have carried out many investigations into the food biology of the moose ın this area
(PuLLiaınen and Loısa 1967; Loısa and PuLLiaınen 1968; PULLIAINEN et al. 1968;
TAnHUANPÄA and PULLIAINEN 1975), and the present observations support our previous
findings on the diet of the moose during different seasons.

188 E. Pulliainen

.
..,
°o
°..,
..,
..
®o
....
DO
°o

28] 30’ 22.3.-26.3.

One-year tracking data and behaviour of a released hand-reared Moose 189

Acknowledgements

I wish to express my sincere gratitude to the staff of the Zoo of the University of Oulu and Värriö
Subarctic Research Station, University of Helsinki, for rearing Suvi and following her movements in
Lapland.

This paper constitutes Report No. 228 from the Värriö Subarctic Research Station, University of
Helsinki.

References

BAKER, R. R. (1978): The Evolutionary Ecology of Anımal Migration. London: Hodder and
Stoughton.

CEDERLUND, G.; LEMNELL, P. A.; Larsson, K. (1981): Sa olika päverkas rädjur och älg av orientering.
Svensk Jakt 7, 512-516.

Loısa, K.; PuLLIAIEn, E. (1968): Winter Food and Movements of two Moose (Alces alces L.) ın
Northeastern Finland. Ann. Zool. Fenn. 5, 220-223.

PULLIAINEN, E. (1974): Seasonal Movements of Moose in Europe. Naturaliste can. 101, 379-392.

PULLIAINEN, E.; Lo1sa, K. (1967): Koillis-Lapin hirvitutkimuksen tuloksıa. Metsästys ja kalastus 56,
159-162.

PULLIAINEN, E.; Lo1sa, K.; POHJALAINEnN, T. (1968): Winter Food of the Moose (Alces alces L.) in
eastern Lapland. Silva Fenn. 2 (4), 235-247.

TANHUANPÄA, E.; PULLIAINEN, E. (1975): Major Fatty Acıd Composition of some organ Fats in the
Moose (Alces alces) in northeastern Lapland. Ann. Zool. Fenn. 12, 148-155.

VESTERINEN, F. (1940): Muuttaako hirvi määräajoın? Metsästys ja kalastus 20, 148-149.

ZHIRNoOVv, L. V. (1969): Migratsii loseı v Evropeiskoi chastı SSSR. Biologiya ı promysel losya 3,
80-104.

Author’s address: Prof. ERKKI PULLIAINEN, Department of Zoology, University of Oulu, Linnan-
maa, SF-90570 Oulu, Finland

Fig. Movements of the moose Suvi between the 5th of October 1990 and the 19th of September 1991.

Movements are indicated with arrows and dotted lines. Black areas with dates are the minimum areas
in which Suvi lived during the period in question (dates in 1990 underlined). For further details, see

text

BUCHBESERECHIINGEN;

HERHOLDT, ELIZABETH M. (ed.): Natural History Collections: Their Management and
Value. Transvaal Museum Special Publication No.1. Pretoria: Transvaal Museum Book-
shop 1990. 172 pp., US$ 40,-. ISBN 0-907-99011-8

This book, which was edited by the manageress of th mammal collection of Transvaal Museum in
Pretoria, South Africa, contains 15 contributions of South African museologists and two of US
American authors. At least seven of the papers pubished in this book are of relevance to mamma-
logısts.

In her article on vertebrate collections E.M. HERHOLDT gives a personal account of specimen
preservation, storage, fumigation, general security, documentation and policies and procedures that
have to be applied to make the collection available to research.

Very practical aspects are dealt with by F.C. DE Moor, who discusses different types of
containers for wet collection and E. DE WET et al., who address the problem of cleaning and de-
greasing bone material. It is an important aspect of the latter paper that long-term effects of these
techniques are evaluated. The authors also recommend different types of data sheets that help to
document the steps of processing.

Two articles deal with aspects of computerization: L. R. WInGATE balances the advantages of
computerizing data versus the work and time necessary to enter data of specimen records that have
already been placed in a traditional, manual catalogue before computerization (retroactive data
capture). R.D. OwEn emphasizes the possible cooperation (consortium development) between
different museums with the help of computers.

]. MEESTER deals with the necessity of retaining specimens identified by a recognized authority for
the purpose of forming reference collections (voucher specimens). The contribution to nature
conservation in South Africa of research collections of natural history museums and their curators is
discussed by I. L. RAUTENBACH and E. M. HERHOLDT.

This interesting book is certainly of value to all those persons that deal with the management of
biological collections. P. LANGER, Gießen

GENnowaySs, H.H. (ed.): Current mammalogy. Vol. 2. New York and London: Plenum
Press 1990. 577 pp., Abb., Tab. US $ 85,-. ISBN 0-306-43304-4

Der Band enthält zwölf Übersichtsreferate aus verschiedenen Gebieten der Säugetierkunde: WILsON
und EisEnBErG behandeln „Entstehung und Anwendung der Mammalogie in Nordamerika“, spannen
allerdings ihre Betrachtung so weit, daß für speziellere Ausführungen allzu wenig Raum bleibt.
McBeEE und BıckHAM bieten einen außerordentlich inhaltsreichen Überblick über Säugetiere als
Bioindikatoren. So findet man hier nicht nur viele Angaben über die in verschiedenen Säugetierarten
gemessenen mittleren Konzentrationen von Umweltgiften, sondern auch deren Toxizität und Wir-
kungsweise. Über die Bekämpfung von Schadnagern in Kokos-Plantagen auf den Philippinen (fast
ausschließlich Rattus rattus und R. exulans) berichtet P. MıLan. Der Name “rice field rat” sollte
allerdings nicht für die Hausratte, sondern für Rattus argentiventer verwendet werden. Die Popula-
tionsdynamik von Schneeschuhhasen (Lepus americanus) ıst ein viel zitiertes Beispiel für Räuber-
Beute-Beziehungen. L. B. KertH findet, daß ım Norden tatsächlich zehnjährige Häufigkeitszyklen
bestehen, die recht gut synchronisiert sind und offensichtlich durch Nahrungsverknappung ım Winter
mit verringerter Geburtenrate im folgenden Sommer sowie verstärktem Feinddruck zustande kom-
men. Inzwischen ist durch Sendermarkierung gezeigt worden, daß für die hohe Mortalität der
Junghasen nach Dichtemaxima fast ausschließlich Freßfeinde verantwortlich sind. Erdbaue von
Säugetieren, ihre Vor- und Nachteile, Wühltechniken, morphologische und physiologische Anpas-
sungen sind ein reizvolles Thema, das hier allerdings von REICHMANN und SMITH allzu kursorisch
behandelt wird. So reichen nicht nur bei einigen Bathyergiden die Schneidezähne mit ıhren Wurzeln
bis hinter die Molaren — im Unterkiefer gilt das für sehr viele Nager. Unklar ist, warum zwischen
“sensitive hairs” und “sensitive vibrissae” unterschieden wird. Zur Maulwurfschnauze werden nur
„sensory papillae“, nicht aber Eimersche Organe erwähnt. Die Arbeiten von MoRrLok (1983:
Grabanpassungen bei subterranen Nagern), KLEın (1972) und WITTE (verschiedene: Biologie Maul-
wurf) sind nicht zitiert. Die Verteilung zwischen Ruhe, Aktivität und Zeit der Nahrungsaufnahme in
Abhängigkeit von Körpergröße, Nahrungsart und anderen Parametern untersuchen BUNNELL und
HARESTAD. Die neuesten Befunde über Hypophysenvorderlappen und endokrinen Hypothalamus der
Säugetiere faßt E. L. P. ANTHONY zusammen. CoPPINGER und SMITH entwickeln und begründen eine
eigene Hypothese über die Verhaltensontogenese und das Spielverhalten bei Säugetieren. Danach sınd
Neugeborene und Adulte unterschiedlich adaptierte Lebensformen, das Verhaltensrepertoire der
Adulten ersetzt das der Neonaten. Der Übergang zwischen beiden Formen ist mit einer Metamor-
phose zu vergleichen, während der stückweise die ursprünglichen Bewegungskoordinationen und

Buchbesprechungen 194

Motivationen verschwinden, während die Adultelemente ebenso stückweise auftreten. Die varıable
und unterschiedliche Kombination erscheint als Spielverhalten. Srucky analysiert die Evolution der
Landsäugetiere im Kenozoikum Nordamerikas mit dem Ergebnis, daß die Diversität hier seit dem
mittleren Paleozän konstant geblieben ist. Im Alttertiär waren lokale Faunen zwar unterschiedlicher

“als später, stimmten dafür aber zwischen verschiedenen Orten besser überein. Dies kann mit einem
kühleren und trockeneren Klima seit dem Ende des Eozäns erklärt werden. Die Phylogenie der
Marsupialier revidieren MARSCHALL, CASE und WOODBURNE, gestützt auf die Kenntnis der rezenten
und fossilen Formen, die sie bis zur Familie einer kladistischen Analyse unterziehen — eine außeror-
dentlich kenntnisreiche, konzentrierte und durchdachte Arbeit! NovAacEk präsentiert ein Klado-
gramm der Eutheria, das neben einem „Busch“ von neun Stammeslinien, die vom gleichen Punkt
entspringen, folgende speziellere Aussagen enthält, die er jeweils auch mit Synapomorphien begrün-
det: Xenarthren und Pholidoten sind eng verwandt und bilden gemeinsam die Schwestergruppe aller
übrigen Eutheria. Weiterhin faßßt er die Archonta (Primaten, Scandentia, Dermoptera und Chiroptera)
enger zusammen sowie Lagomorpha und Rodentia mit den Macroscelidea als Schwestergruppe. Die
Paenungulata (Proboscidea+Sirenia+ Hyracoidea) behält er bei. CzELusNIaR et al., neun Autoren
insgesamt, versuchen, Vergleiche von Aminosäuresequenzen und DNA taxonomisch zu werten.
Tab. I informiert darüber, welche von acht Proteinen bei 86 Säugertaxa (meist Arten) inzwischen
sequenziert sind. Die aufgrund dieser umfangreichen Datenbasis nach dem Prinzip der Sparsamkeit
konstruierten Beziehungsschemata stimmen vielfach besser mit morphologisch begründeten Stamm-
bäumen überein als frühere und werden zurückhaltend diskutiert.

Der Band ist sorgfältig redigiert und einheitlich, auch wenn hin und wieder noch Druckfehler
vorkommen und z.B. ım Kopf von Tab. I (S. 552) eine Erklärung der Buchstaben-Abkürzungen der
sequenzierten Proteine fehlt. Die Mehrzahl der Beiträge ıst von hoher Qualität und vermittelt den
Zugang zum derzeitigen Stand eines jeweils umfangreichen, kaum noch überschaubaren Forschungs-
gebietes. J. NIETHAMMER, Bonn

LABHARDT, F.: Der Rotfuchs. Naturgeschichte, Ökologie und Verhalten dieses erstaunli-
chen Jagdwildes. Mit einem Beitrag über die Fuchsbejagung von R. KrRÖGER. Hamburg
und Berlin: Verlag Paul Parey 1990. 158 S., 121 Abb. DM 58,-. ISBN 3-490-33812-X

FELIx LABHARDT hat zum einen eine Artmonographie zusammengestellt, die dem Anspruch auf
wissenschaftliche Zuverlässigkeit, Komplexität und Verständlichkeit in einem sehr hohen Maße
gerecht wird, zum anderen hat er einfach ein wunderschönes Buch über Füchse geschrieben,
ausgestattet mit hervorragenden Fotografien, die zudem keine reinen „Schmuckbilder“ sind, sondern
vielfältige Verhaltensweisen treffend darstellen und nicht nur jeden Canidenfreund begeistern müssen!

Dieses neue Buch in der Reihe der Wildmonographien im Verlag Paul Parey ist kein Jagdbuch. Es
behandelt u. a. Forschungsergebnisse zur Ernährung des Fuchses, zu seinem Verhalten in Raum —
Zeit - System und enthält eine Fülle neuer Daten zum Sozialverhalten von Füchsen in unterschiedli-
chen Okosystemen. Überzeugende eigene empirische Befunde werden im sorgsamen, gut recherchier-
ten Literaturvergleich vorgestellt und diskutiert. Somit liefert LABHARDT insgesamt eine sehr solide
erarbeitete, vorbildlich präsentierte Rotfuchs-Biographie. Diese richtet sich an Wildbiologen, Natur-
beobachter — und an Jäger, für die insbesondere eın hoher Bedarf an Informationen zur Lebensweise
dieses Raubtieres bestehen dürfte, werden doch alleın in Westdeutschland etwa 170 000 Füchse pro
Jahr geschossen. Möge diese umfangreiche und genaue Übersicht zu den jüngsten Forschungsergeb-
nissen dem Jäger helfen, verbreitete Vorurteile und Halbwahrheiten über den Fuchs abzubauen, und
die ökologische Bedeutung dieser faszinierenden Caniden, die er nicht selten recht unreflektiert als
„Niederwildfeinde“ und Konkurrenten bejagt, zu erkennen.

Das angefügte Kapitel des Fuchsjägers R. KRÖGER hätte meiner Meinung nach fehlen können, da
es zur LABHARDT-Monographie weder ın Aussage noch ım Stil paßt. Hıer werden die gängigen
Formen der Fuchsjagd beschrieben, wobei es leider nicht selten an Kritik mangelt, was insbesondere
für die Ausführungen über die Fallenjagd und die Baujagd gilt. Der Schlußsatz dieses Kapitels spricht
dafür und für sich: „Den Fuchs scharf bejagen; das macht jägerische Freude und nutzt sowohl der
Wildhege als auch Reinekes Sippe selbst“. DoRrIT FEDDERSEN-PETERSEN, Kiel

FREYE, H.-A.; TEMBROcK, G. (Hrsg.): Humanethologie im Spektrum der Wissenschaf-
ten Noyaracta) Eeopoldina, N. E. Nr. 273, Bd. 63. Leipzig: ]. A. Barth 1990. 113° S., 17
Abb., 5 Tab. DM 48,-. ISBN 0369-5034

Im Rahmen zunehmender Spezialisierung der Wissenschaften hat die Humanbiologie als Synthese
aller Grunddisziplinen, die sich mit der naturwissenschaftlichen Erforschung des Homo sapiens
befassen, heute eine gewisse Figenständigkeit als Grenzwissenschaft zwischen Biologie und Medizin
erreicht. Die Humanethologie nimmt in ıhr eine zentrale Stellung ein. Mit Recht betont H.-A. Freye
in der Einleitung zu vorliegendem Band die Notwendigkeit, die Grenzen des Faches zu beachten. Die

192 Buchbesprechungen

Humanethologie ist nicht in der Lage und beabsichtigt auch nicht, das Wesen des Menschen zu
erklären und verkennt nicht, daß sie nur in der Lage ist, aus einem Blickwinkel, dem naturwissen-
schaftlichen, sich der Problemstellung zu nähern. Das spezifisch Menschliche, Selbst- und Weltbe-
wußtsein, Kulturfähigkeit entzieht sich weitgehend der naturwissenschaftlichen Analyse und bedarf
der Teilnahme von Geistes- und Gesellschaftswissenschaften.

Ergebnisse der vergleichenden Verhaltensforschung sind aber auch für das Problem der Mensch-
werdung aufschlußreich, da auf diesem Weg Wurzeln menschlichen Verhaltens und Vorstufen zu
diesem erkannt werden können.

Der vorliegende Band enthält 9 Beiträge führender Sachkenner aus verschiedenen Disziplinen und
ist zugleich ein gutes Beispiel für die zunehmende Bedeutung interdisziplinärer Forschung. Im
Einzelnen seien folgende Beiträge hervorgehoben. |

G. VOLLMER bringt eine knappe und klare Übersicht über Grundfragen der evolutionären
Erkenntnistheorie als Basıs synthetischen Denkens in der Biologie. Eine sinnvolle Ausweitung dieses
Ansatzes auf weitere Gebiete und grundsätzliche Fragen der Abgrenzung werden erörtert. Soziale
Kognition ın nichtmenschlichen Primatengesellschaften und deren primäre Bedeutung vor Erreichen
des Werkzeuggebrauches sind Thema von CH. VoceEL. Weitere Beiträge behandeln die Evolution
kognitiver Prozesse (Kııx). Es folgt ein Beitrag über Bedeutung hormonal abhängiger Prozesse in der
Hirnentwicklung (G. DÖRNER). Verhaltensprozesse im Bereich der Wechselwirkung von Interaktio-
nen zwischen Organısmus und Umwelt während der perinatalen Lebensphase behandelt G. TEm-
BROCK. Zur Frage nach der Hirnentwicklung und dem Verhalten in der menschlichen Ontogenese
berichtet G. Woır, während P. Proprıng die Abhängigkeit der Hirnfunktion von der genetischen
Variabilität behandelt. ErsL-EiBEsrELD untersucht pathologische Verhaltensweisen beim Menschen
aus der Sicht des vergleichenden Ethologen. Die Schrift bietet eine nützliche Übersicht über
Entwicklungen und Fortschritte auf dem Gebiet der Humanethologie durch kompetente Autoren und
kann zur Lektüre empfohlen werden. D. STARcK, Frankfurt/M.

Emmons, LuIsE H.; FEER, F.: Neotropical Rainforest Mammals. A Field Guide. Chicago
and London: The University of Chicago Press 1990. 281 S., 11 Abb., 29 Farbtafeln, 7
Schwarzweißtafeln, 184 Verbreitungskarten. Kart. US $ 51.75. ISBN 0-226-20718-8

Das Buch behandelt die Säugetiere der unterhalb von 1000 m NN gelegenen Regenwälder Mittel- und
Südamerikas in der für moderne Feldführer üblichen Weise: Englischer und wissenschaftlicher Name,
Merkmale mit Spannweiten der Körpermafße und Gewichte, innerartliche Variabilität, Verwechse-
lungsmöglichkeiten, Lautäußerungen, Lebensweise, Verbreitung, Gefährdungsstatus und eventuell
1-2 Literaturhinweise. Im Anhang finden sich Bestimmungsschlüssel für die Familien und Gattungen,
Erläuterungen zu Taxonomie, Verbreitung und Schutz, Abbildungen von Fährten einiger größerer
Arten und eine komplette Artenliste, durch Fett- und Normaldruck gegliedert ın echte Regenwald-
arten und solche, die nur vom Rande her hineinreichen. Im allgemeinen werden alle Arten, bei den
Fledermäusen und myomorphen Nagern jedoch nur die Gattungen behandelt, und für diese Gruppen
ist die komplette Artenliste im Anhang als Ergänzung besonders wichtig. Der Text stammt von LUISE
H. Emmons, die Abbildungen sind von F. FEER und umfassen für alle behandelten Einheiten
Habitusbilder, bei den Fledermäusen meist nur Kopfporträts und häufiger auch die Gestalt der
Schwanzflughaut. Die Autoren haben sich vor allem auf die neueste Literatur und die Sammlungen
großer amerikanischer und europäischer Museen gestützt. Erstmals wird mit diesem Taschenführer
ein großer Teil Süd- und Mittelamerikas erfaßt, in dem etwa 500 Säugetier-Arten vorkommen. Die
Farbbilder wirken zwar ziemlich grob, dürften aber für den Zweck des Buches ausreichen. Gebißfor-
meln finden sich nur in den Familienbeschreibungen. Merkmale, die nicht äußerlich am lebenden Tier
feststellbar sind, werden sonst nicht erwähnt. Qualität und Grenzen des Führers sind für einen
Europäer am besten zu beurteilen, wenn er Artbeschreibungen wie die für Haus- und Wanderratte
vergleicht. Neben überwiegend zutreffenden Angaben fallen hier allzu subjektive Bemerkungen auf
wie bei Lautäußerungen (Hausratte nagt und läuft geräuschvoll, Wanderratte quiekt und kämpft) oder
Wanderratten sind „very large, robust, ugly rats“. Der Wert des Größenunterschiedes zur Unter-
scheidung der Arten ist überbetont, daß Hausratten außerhalb der Neotropis Regenwaldbewohner
sind, dürfte nicht stimmen.

Die Beschränkung auf Gattungen in einigen artenreichen Familien ist bedauerlich, ebenso das allzu
kurze allgemeine Literaturverzeichnis $. 206, in dem z.B. EISENBERG (1989), CABRERA und YEPES
(1960), Husson (1978) oder MAREs und GENowAays (1982) fehlen. Demgegenüber ist aber hervorzu-
heben, daß die knappe Behandlung eines so umfangreichen Stoffes, die Orientierung ın der vielfach
noch unklaren Taxonomie, die Sammlung allein der zahlreichen Verbreitungskarten und Maße eine
bewundernswerte Leistung darstellt.

Dies Buch dürfte für eine erste Orientierung bei Begegnungen mit Säugetieren in neotropischen
Regenwäldern von großem Nutzen sein. J. NIETHAMMER, Bonn

Fortsetzung von der 1. Umschlagseite

Kocian, L.; Ziak, D.: Occurrence of a melanistic Common vole, Microtus arvalis (Pallas,
1779) in Slovakia. -—- Das Vorkommen einer melanistischen Feldmaus, Microtus arvalis
(Pallas, 1779) in der Slowakei |

Gouat, P.: Faecal pellet size differences as a field criterion to distinguish between the two
Ctenodactylus species (Mammalia, Rodentia). — Größenunterschiede von Kotpillen als
Kriterium zur Unterscheidung zwischen den beiden Ctenodactylus-Arten (Mammalia,
Rodentia) im Freiland

Pulliainen, E.: One-year tracking data and behaviour of a released hand-reared Moose
(Alces alces) in Forest Lapland. — Angaben zu Ortsveränderungen und Verhalten eines
ausgewilderten handaufgezogenen Elches (Alces alces) in der Waldregion von Lappland
während eines Jahres

Buchbesprechungen

181

183

186
190

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213-3798.

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Mitgliedsbeitrages.

Z. Säugetierkunde 57 (1992) 3, 129-192

Grundlagen der Röntgenologie
in der Veterinärmedizin

2., überarbeitete und erweiterte Auflage von Sidney W. Douglas M. A.,
MRCVS, DVR; Michael E. Herrtage M. A., BVSC, MRCVS, DVR; Hamar
D. Williamson M. A., BA, DCR, Department of Clinical Veterinary Medi-
cine, University of Cambridge

Aus dem Englischen übertragen und bearbeitet von Dr. Beate Münzer, unter
Mitarbeit von Prof. Dr. Klaus Hartung, beide Klinische Radiologie an der
Klinik für Pferdekrankheiten, Allgemeine Chirurgie und Radiologie, Freie
Universität Berlin

1991. 204 Seiten mit 166 Abbildungen und 10 Tabellen. 24 x 16,5 cm.
Kart. DM 88,- ISBN 3-489-51916-7

Die rasche Weiterentwicklung der Röntgenologie in der Veterinärmedizin
machte eine gründliche Überarbeitung dieses Buches für die zweite Auflage
erforderlich, die ın allen Kapiteln ihren Niederschlag gefunden hat. Die für
die praktische Anwendung der Röntgenstrahlen unerläßlichen physikalischen
Grundlagen sind ım Teil 1 intensiver aufgeführt und die folgenden Kapitel
über Röntgengeräte, Zusatzgeräte und Filmentwicklungstechniken auf den
neuesten Stand gebracht worden. Dies gilt ebenso für den Abschnitt über
Strahlenschutz, der aufgrund neuerlassener Verordnungen nun dem aktuellen
Stand der notwendigen und gesetzlich erfaßten Strahlenschutzmaßnahmen
entspricht.

Das Buch wendet sich an die Studierenden und an die praktizierenden Tier-
ärzte, um ihre theoretischen und praktischen Kenntnisse in der Radiologie zu
festigen und einen sicheren und effizienten Umgang mit den Röntgenstrahlen
zu gewährleisten. Darüber hinaus werden mit dieser Neuauflage auch die
röntgentechnischen Assistenten angesprochen, die eine wichtige Stütze in der
veterinärmedizinischen Röntgenologie darstellen, sowie die Praktiker, die ein
spezielles Interesse an röntgenologischen Untersuchungsmethoden haben.

PAUL
P/AREYV Berlin und Hamburg

|
‚01. 57 (4). 193-256, August 1992 ISSN 0044-3468 C21274F
l

> ITSCHRIFT FÜR
SAUGETIERKUNDE

NTERNATIONAL JOURNAL
IF MAMMALIAN BIOLOGY

Yrgan der Deutschen Gesellschaft für Säugetierkunde

af, M.; Stutz, H.-P. B.; Ziswiler, V.: Regionale und saisonale Unterschiede in der Nahrungszusammensetzung des
‚Großen Mausohrs Myotis myotis (Chiroptera, Vespertilionidae) in der Schweiz. — Regional and seasonal
differences of the food composition of the Mouse-eared bat Myotis myotis (Chiroptera, Vespertilionidae) in
‚ Switzerland 193
undbacher, Barbara: Nachweis des Baummarders, Martes martes, in der neolithischen Ufersiedlung von Twann
(Kanton Bern, Schweiz) sowie Anmerkungen zur osteometrischen Unterscheidung von Martes martes und
M. foina. — Neolithic remains of the Pine marten, Martes martes from Twann (Switzerland) and osteometrical
methods to distinguish M. martes from M. foina 201
rrero, J.; Canut, J.; Garcia-Ferre, D.; Garcia-Gonzales, R.; Hidalgo, R.: The Alpine marmot (Marmota marmota
L.) in the Spanish Pyrenees. — Die Murmeltiere (Marmota marmota L.) in den spanischen Pyrenäen zu
rez-Zapata, A.; Lew, D.; Aguilera, M.; Reig, O. A.: New data on the systematics and karyology of Podoxymys
‚ roraimae (Rodentia, Cricetidae). - Neue Unterlagen über die Systematik und Karyologie von Podoxymys
‚ roraimae (Rodentia, Cricetidae) 216
jaguedakis-Tsolis, S. E.: Contribution to the study of the wild House mouse, Genus MusL. (Mammalia, Rodentia,

' Muridae) in Greece. Study of three populations based on Iymphocyte antigen analysis. — Beitrag zu Untersuchun-
| gen an der wilden Hausmaus, Gattung MusL. (Mammalia, Rodentia, Muridae) in Griechenland. Untersuchungen
‚an drei Populationen aufgrund von Analysen mit Lymphozyten-Antigenen 225
allardo, M. H.; Araneda, C.; Köhler, Nelida: Genic divergence in Spalacopus cyanus (Rodentia, Octodontidae). —
' Genetische Divergenz bei Spalacopus cyanus (Rodentia, Octodontidae) 231
‚rin, M. R.; Slotow, R. H.; Mendelsohn, J. M.: The population dynamics of rodents at Settlers, Transvaal, South
Africa. — Die Populationsdynamik von Nagetieren in Settlers, Transvaal, Südafrika 238
issenschaftliche Kurzmitteilungen

'tullo, A. D.; Zuleta, G. A.: Cytogenetics and fossil record: confluent evidence for speciation without chromosomal
' change in South American canids. — Zytogenetik und Fossilgeschichte: render Nachweis für Artbildung

‚ ohne Chromosomenänderung bei südamerikanischen Caniden SMITH ISO, Na 248

ılomares, F.; Delibes, M.: Immobilization of Egyptian mongoo&es, Herpestes N: ithn a combination of

‚ ketamine and xylazine. — Immobilisation von Ichneumons, Herpestes ichneumon, mit einet Kombination von
‚Ketamin und Xylazin FD 202 251
ichbesprechungen 3 253

Ir *
A ; 7
IL AN

lerlag Paul Parey Hamburg und Berlin

FIERMA USGE BERYEPDIELORS

P. J. H. van BreE, Amsterdam - W. FIEDLER, Wien - H. Frıck, München — W. HERRE,

Kiel - R. HUTTERER, Bonn - H.-G. Krös, Berlin - H.-J. Kunn, Göttingen - E. KULZER,

Tübingen - W. MAIER, Tübingen - J. NIETHAMMER, Bonn - OÖ. Anne E. Rasa, Bonn -

H. REıcHsTEIn, Kiel - M. Rönrs, Hannover — H. SCHLIEMANN, Hamburg - D. STARcK,
Frankfurt a. M. - E. Tuenıus, Wien - P. VoGEL, Lausanne

SCHERTEIEREFTUNGZEDIEEO RENFORENGE

D. Kruska, Kiel - P. LANGER, Gießen

This journal is covered by Biosciences Information Service of Biological Abstracts, and by Current Con-
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Die Zeitschrift für Säugetierkunde veröffentlicht Originalarbeiten und wissenschaftliche Kurzmittei-
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Zusätzlich erscheint einmal im Jahr ein Heft mit den Abstracts der Vorträge, die auf der jeweiligen
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Fortsetzung 3. Umschlagseite

© 1992 Paul Parey. Verlag: Paul Parey, Hamburg und Berlin. Anschriften: Spitalerstr. 12, D-2000 Hamburg 1;
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Verlagsdruckerei Boyens & Co., Heide/Holst.

Z. Säugetierkunde 57 (1992) 193-200
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Regionale und saisonale Unterschiede in der
Nahrungszusammensetzung des Großen Mausohrs Myotis
myotis (Chiroptera, Vespertilionidae) in der Schweiz

Von M. Grar, H.-P. B. STUTZ und V. ZıswILER

Zoologisches Museum der Universität Zürich, Schweiz

Eingang des Ms. 10. 12. 1991
Annahme des Ms. 17. 2. 1992

Abstract

Regional and seasonal differences of the food composition of the Mouse-eared bat Myotis myotis

(Chiroptera, Vespertilionidae) in Switzerland
Studied the contents of the feces of Myotis myotis, collected in 14 nursery roosts in the central,
northern and eastern parts of Switzerland regionally and seasonally. The taxa, established with
literature and collection-references were quantified with the method of KorscHGEn (1971). In all
colonies Carabidae were the basic food. Other important prey were Orthoptera (Acrıididae, Gryl-
lotalpa gryllotalpa), Diptera (Tipulidae) and Arachnida. The seasonal varıation of the diet of Myotis
myotis seemed to be correlated with the seasonal prey availability. A selection of large prey (> 10 mm)
was supposed. A cluster analysıs revealed 3 regional groups of nursery roosts which were classed
according to landscape and intensity of agricultural land use. The results were discussed with respect
to possible habıtat change.

Einleitung

Viele insektivore Fledermausarten verhalten sich ın ıhrer Ernährung opportunistisch
(FENTON und Morris 1976). Hinweise für eine allfällige selektive Ernährung können
entweder durch den quantitativen Vergleich von Nahrungszusammensetzung und Beute-
angebot am selben Ort oder durch den Vergleich der Nahrungszusammensetzung in
verschiedenen Landschaftsräumen gewonnen werden. Für M. myotis wird einerseits eine
Spezialisierung auf bodenlebende Insekten und andererseits eine selektive Bevorzugung
großer Beutetiere vermutet (Korg 1958; BAUEROVA 1978; ACKERMANN 1984).
Wochenstubenquartiere von M. myotis verteilen sich in der Schweiz auf die Land-
schaftsregionen Jura, Mittelland, Voralpen und Alpen (Sturz und HAFFNER 1984a). Damit
bietet sich die Möglichkeit, durch einen Vergleich der Nahrungszusammensetzung in den
verschiedenen Regionen ein differenzierteres Bild über die Ernährung von M. myotis zu
gewinnen. Von speziellem Interesse ist dabei das Ausmaß der Präferenz für waldbewoh-
nende Carabidae, die bei allen bisherigen Arbeiten festgestellt wurde (Kos 1958; BAUE-
ROVA 1978; ACKERMANN 1984; Pont und MouLin 1985; GEBHARD und HirschHı 1985).

Material und Methode

Aus 14 Wochenstubenquartieren von M. myotis wurden Kotproben (n = 102 Proben) analysiert.
Hierfür wurde der frisch angefallene Kot unter dem Haupthangplatz in 4-Wochen-Intervallen vom
10. 4. 1988 bis 23. 10. 1988 gesammelt. Pro Kolonie ergab dies maximal acht Proben, von denen je 20
Korballen einzeln nach taxonomisch auswertbaren Beuteüberresten untersucht wurden. Diese unver-
dauten Beuteteile wurden anhand von Literaturangaben und mit Hilfe von Vergleichssammlungen
einzelnen Invertebratentaxa zugeordnet.

Die Quantifizierung der qualitativ erfaßbaren Beutekategorien wurde nach KoRscHGEN (1971)

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5704-0193 $ 02.50/0

194 M. Graf, H.-P. B. Stutz und V. Ziswiler

durchgeführt: die Anzahl Kotballen, in denen eine Beutekategorie nachgewiesen wurde, ergab die
Frequenz F, mit einem Wertebereich von 0 bis 20.

Für die Gruppierung der Wochenstubenquartiere aufgrund der ermittelten Beutefrequenzen
wurde eine Cluster-Analyse mit dem Programmpaket MULVA-4 Version 1.02 (WıLpı und OrLocı
1988) durchgeführt. Aus diesem Paket wurden die Programme INIT, CLTR und TABS verwendet.
Die Klassenwerte wurden nicht transformiert. Für die Ahnlichkeitsmatrizen wurde das Kontingenz-
maf3 nach Van den Maarel verwendet. Die Cluster-Analyse wurde mit einem minimum-variance-
clustering durchgeführt (WıLpı 1986). Die Beutefrequenzen wurden in fünf Größenklassen (F =
0-2,4, F = 2,5-7,4; F = 7,5-12,4; F = 12,5-17,4; F = 17,5-20) eingeteilt und für jedes Wochenstuben-
quartier die acht monatlichen Proben in den drei Gruppen Frühling (März-Mai), Sommer (Juni, Juli)
und Herbst (Aug.-Sept.) zusammengefaßt.

Ergebnisse

Aufgrund der festgestellten Häufigkeiten können Coleoptera, Orthoptera, Diptera und
Arachnıda als wichtigste Beutekategorien bezeichnet werden (Abb. 1). Die Ordnung
Coleoptera wurde in allen monatlichen Proben am häufigsten nachgewiesen (Abb. 2). Der
größte Anteil der Nachweise entfällt dabei auf die Familie Carabidae (Abb. 3). Bei der
Familie Scarabaeidae zeigt sich, daß Bruchstücke von Melolontha melolontha/hippocastani

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Abb. 1. Jahresmittelwerte der Nachweishäufigkeiten (F) der verschiedenen Beutekategorien ım Kot
der untersuchten Wochenstubenquartiere von M. myotıs. Die Daten aus sämtlichen Wochenstuben-

quartieren wurden zusammengefaßt

nur im April, Mai und Juni festgestellt werden konnten (Abb. 3). Die Scarabaeıdae-
Nachweise in der zweiten Jahreshälfte entfallen demgegenüber mehrheitlich auf die
Gattungen Aphodinus und Geotrupes. Die Ordnung Orthoptera konnte am häufigsten ım
August, September und Oktober nachgewiesen werden (Abb. 2). Bei den Nachweisen im
Mai und Juni handelt es sich fast ausschließlich um Bruchstücke von Gryllotalpa grylio-
talpa. Die hohen Frequenzen ım August, September und Oktober sind dagegen mehrheit-
lich in Nachweisen von Acrididae begründet (Abb. 3). Die Frequenzen von Diptera weisen
zwei Maxima auf. Das erste ist im Mai und Juni und das zweite im August und September
zu verzeichnen (Abb. 2). Die höchsten Frequenzen für die Klasse Arachnida konnten im
Frühling und Herbst festgestellt werden (Abb. 2).

Die Gruppierung der Wochenstubenquartiere mittels einer Cluster-Analyse aufgrund
der Beutefrequenzen ergab drei Hauptgruppen (Abb. 4, Tab. 1). Diese zeigen eine

Nahrungszusammensetzung von Myotis myotis in der Schweiz 195

F
20
15
Wu Coleoptera
10 Orthoptera
BE Diptera
PA Arachnida
5 z
7 B 7 zu4 Zr
7 A: 71 WAL
ß % 92 en LER E ZuA
A Ar WE 4 A) WA BA

März Aprii Mai Jun. Jul. Aug. Sept. Okt.

Abb. 2. Mittlere monatliche Nachweishäufigkeiten (F) von Coleoptera, Orthoptera, Diptera und
Arachnida. Die Daten aus sämtlichen Wochenstubenquartieren wurden zusammengefaßt

F
20
15
Wi Carabidae
1a Melolontha
74 Acrididae
G. gryllotalpa
5
zZ
2 s
z z
4 zU# ,
(6) 7ER 2 A £ A 2 &

März Apri Mai Jun. Jul. Aug. Sept. Okt.

Abb. 3. Mittlere monatliche Nachweishäufigkeiten (F) von Carabidae, Melolontha, Acrıdidae und
Gryllotalpa gryllotalpa. Daten aus sämtlichen Wochenstubenquartieren wurden zusammengefaßt

Übereinstimmung mit der geographischen Gliederung des Untersuchungsgebietes und mit
den landwirtschaftlichen Eignungsklassen (Bundesamt für Landwirtschaft 1986) (Abb. 5).

Die für die Gruppe 1 charakteristische Nahrungszusammensetzung zeichnet sich durch
sehr hohe Carabidae-Frequenzen in allen Proben aus (Abb. 5, 6). Mit einer Ausnahme
(Wochenstubenquartier in Sachseln, Sa) befinden sich alle Wochenstubenquartiere der
Gruppe 1 im Mittelland sowie ın der landwirtschaftlichen Eignungsklasse „sehr günstig“.

Die Gruppe 2 umfaßt die Wochenstubenquartiere, deren Nahrungszusammensetzung
sich durch tiefere Carabidae-Frequenzen bzw. höhere Frequenzen von Acrididae, Gryllo-
talpa gryllotalpa und Diptera (Tipulidae) auszeichnen (Abb. 5, 6). Diese Quartiere liegen
einerseits im Übergangsbereich zwischen Mittelland und Alpen (in der Folge als Voralpen
bezeichnet) und andererseits in der landwirtschaftlichen Eignungsklasse „günstig“ oder in
den Grenzgebieten der Eignungsklasse „bedingt geeignet“.

Das einzige Wochenstubenquartier der Gruppe 3 zeichnet sich durch die tiefsten
Carabidae-Frequenzen sowie durch hohe Frequenzen für Acrıdidae und Melolontha
melolontha/hippocastani aus (Abb. 5, 6). Dieses Quartier liegt in den Alpen auf 1016 m
ü.M. ın der landwirtschaftlichen Eignungsklasse „bedingt geeignet“.

196 M. Graf, H.-P. B. Stutz und V. Ziswiler

Eg Gruppe 1

Ei Gruppe 2

FT
Gruppe 3
La

USERS USERS WEEENEEFGEEHEEERIEEGE — HERREN LERERUNERNNGER BERHEREHEE BIENEN HERENN: NEN || 0 _____,
0.533 0.607 0.681 062755 0.828 0.902

Abb. 4. Minimum-Variance-Dendrogramm der untersuchten Wochenstubenkolonien aufgrund der
Beutefrequenzen. Ähnlichkeitsmaß: Van den Maarel Koeffizient (nach WıLpı und Orrocı 1988)

Diskussion

Mit der ın der vorliegenden Arbeit verwendeten Methode der Kotanalyse sind Aussagen
über die Ernährung möglich (Kunz und WHITEAKER 1983). Die Wahrscheinlichkeit der
taxonomischen Zuordnung der unverdauten Beuteüberreste ist jedoch von der taxonomi-
schen Relevanz der im Kor aufgefundenen Körperteile abhängig. Die hier verwendete
Methode der Frequenzerfassung hat den Vorteil, daß keine Schätzungen vorgenommen
und keine unbestimmbaren Bruchstücke zugeordnet werden müssen. Die Stichproben-
größe von 20 Kotballen kann aufgrund eigener Erfahrungen (Grar 1990) und aufgrund der
Angaben von Pont und Mourin (1985) als ausreichend angesehen werden. Die Zuord-
nung des Wochenstubenquartieres in Sachseln, Sa durch die Cluster-Analyse ist vermutlich
mit methodischen Fehlern behaftet. So fehlt die Probe September, die allgemein diagnosti-
schen Charakter für die Gruppierung aufweist (Tab. 1). Deshalb wird die Zuordnung zur
Gruppe 1 als nicht stichhaltig erachtet.

Grundsätzlich kann festgehalten werden, daß Carabidae ın allen 14 Wochenstuben-
quartieren während des Sommerhalbjahres 1988 den Hauptbestandteil der Nahrung von
M. myotis ausmachten. Die saisonalen Unterschiede der Nachweishäufigkeiten weisen
zusätzlich aber auf eine Beeinflussung der Nahrungszusammensetzung durch ein saisonal
varıables Beuteangebot hin. Am offensichtlichsten ist dieser Zusammenhang beı Melolon-
tha melolontha/hippocastani, die während ihrer Flugzeit im Mai und Juni auch am
häufigsten im Kot nachgewiesen wurden. Im weiteren wurde die hauptsächlich unterir-
disch lebende Gryllotalpa gryllotalpa fast ausschließlich zur Zeit ihrer Paarungsaktivität ım
Mai und Juni gefressen, wenn diese sich vermehrt an der Oberfläche aufhält. Tipulidae
wurden hauptsächlich im Mai sowie im August und September gefressen. Im Gegensatz zu

Nahrungszusammensetzung von Myotis myotis in der Schweiz 197.

Klassenwerte der für die Cluster-Analyse verwendeten Beutekategorien
1: F= 02,4; 2: F = 2,5-7,4; 3: F = 7,5-12,4; 4: F = 12,5-17,4; 5: F = 17,5-20
Frühling: März, April, Mai; Sommer: Juni, Juli; Herbst: August, September, Oktober

Gruppe 2 Gruppe3

Gruppe1
| Beutetiergruppe _|Mu _ EmMa Ve Eg Sa|lSt _ Ei Ob MI Gr Bu Fl

Heteroptera Sommer
Neuroptera Frühling
Acrididae Frühling
Heteroptera Frühling
Heteroptera Herbst
Neuroptera Herbst
Acrididae Sommer
Hymenoptera Frühling
Chilo-/Diplopoda Sommer
Dermaptera Frühling__
Coleoptera Larven Herbst
Arachnida Sommer
Coleoptera Larven Sommer
Hymenoptera Sommer
Chilo-/Diplopoda Frühling
Gryliotalpidae Herbst
Chilo-/Diplopoda Herbst
Staphylinidae Herbst
Staphylinidae Frühling
Gryliotalpidae Sommer
Gryliotalpidae Frühling
Silphidae Sommer
Silphidae Frühling
Lepidoptera Herbst
Staphylinidae Sommer
Lepidoptera Sommer
Byrrhidae Frühling
Carabidae Sommer
Carabidae Frühling
Carabidae Herbst
Diptera Sommer
Diptera Frühling
Coleoptera Larven Frühling
Arachnida Frühling
Scarabaeidae Herbst
Arachnida Herbst

Diptera Herbst
Acrididae Herbst
Dermaptera Herbst
Hymenoptera Herbst
Scarabaeidae Sommer
Scarabaeidae Frühling

2A
220
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den vorgängig erwähnten Arten sınd Tipulidae jedoch im ganzen Sommerhalbjahr vorhan-
den (Durour 1986), doch scheinen sie im Mai, August und September für M. myotis
optimal verfügbar zu sein. Bemerkenswert ist, daß die für die Tipulidae-Männchen
typischen Büschelfühler nıe festgestellt werden konnten, obwohl diese kaum häufiger
abgebissen werden dürften als die regelmäßig nachgewiesenen Fühler der Weibchen.
Zudem traten Bruchstücke von Tipulidae im Kot sehr häufig zusammen mit einer großen
Zahl von Eiern auf, die große Ähnlichkeit mit Tipulidae-Eiern aufweisen. Vermutlich
handelt es sich beim größten Teil der nachgewiesenen Tipulidae um Weibchen, die sıch
während der Eiablage in Bodennähe aufhielten. Daher ist anzunehmen, daß Tipulidae
wegen des speziellen Verhaltens der Weibchen während der Eiablage gefressen wurden.
Ein weiterer Hinweis für das Ablesen der Beutetiere von einem Substrat läßt sich ebenfalls
von den Nachweishäufigkeiten der Arachnida ableiten. Da bei dieser Beutekategorie eine
genauere Bestimmung nicht möglich war, ist eine eingehendere Diskussion jedoch nicht

möglich.

198 M. Graf, H.-P. B. Stutz und V. Ziswiler

50 km
TE n

Abb. 5. Das Untersuchungsgebiet mit den landwirtschaftlichen Eignungsklassen (Raster) und den
mittels der Cluster-Analyse gruppierten Wochenstubenquartieren (Punktsymbole). Dreiecke =
Gruppe 1; Kreise = Gruppe 2; Quadrate = Gruppe 3. Helles Raster: landwirtschaftliche Eignungs-
klasse „günstig“; mittleres Raster: landwirtschaftliche Eignungsklasse „sehr günstig“; dunkles Raster:
landwirtschaftliche Eignungsklasse „bedingt geeignet“

20

15

N

“

IN

WI Gruppe 1 (n=6)
E3 Gruppe 2 (n=7)
E&J Gruppe 3 (n=1)

10

Carabidae Acrididae G. gryliotaipa Diptera

Abb. 6. Jahresmittelwert der Nachweishäufigkeiten der wichtigsten Beutekategorien ın den drei durch
die Cluster-Analyse gebildeten Gruppen der Wochenstubenquartiere

Nahrungszusammensetzung von Myotis myotis in der Schweiz 199

Die Nahrungszusammensetzung scheint aber nicht nur durch die saisonale Verfügbar-
keit der verschiedenen Beutetiergruppen beeinflußt zu werden, sondern auch durch die
Beutegröße. So zeigen die ın der Literatur (FREUDE et al. 1969, 1976; CHineEry 1984;
BELLMANN 1985) angegebenen Körpergröfßen für alle regelmäßig nachgewiesenen Beute-
tiere, daß diese zu den mittelgroßen bis großen Arthropoden (= 10 mm) gehören. M.
myotis scheint demnach selektiv große Beutetiere zu fressen, was die Vermutung von
BAUEROVvA (1978) und ACcKERMANN (1985) bestätigt.

Die regionale Gruppierung der Wochenstubenquartiere durch die Cluster-Analyse
kommt in erster Linie durch die unterschiedlichen Carabidae-Frequenzen zustande (Tab.
1). Die meisten nachgewiesenen Carabidae sind waldbewohnende Arten, während die beı
gleichzeitig geringeren Carabidae-Frequenzen auftretenden weiteren bedeutenden Beute-
kategorien weniger oder gar nicht in Wäldern leben. Zur Deutung dieser regionalen
Unterschiede bieten sich folgende Erklärungsmöglichkeiten an:

Unter der Voraussetzung, daß M. myotis nach Möglichkeit in Wäldern jagt, könnte die
Verfügbarkeit der Carabidae für M. myotis ın den Voralpen und Alpen bereits zu gering
sein, weshalb Insekten vermehrt auch außerhalb des Waldes erbeutet werden müßten.
Entweder wäre ın diesen Gebieten die Dichte der Carabidae effektiv geringer, oder die
Auffindbarkeit der Carabidae wäre für M. myotis schlechter.

Die Übereinstimmung der Gruppierung der Kolonien mit den landwirtschaftlichen
Eignungsklassen, welche ihrerseits als Intensitätsmaß für die landwirtschaftliche Nutzung
dienen, führt zu einer zweiten Hypothese. Diese basıert darauf, daß M. myotis als
vergleichsweise große Fledermausart auf das Fressen von großen Insekten spezialisiert ist.
Das Angebot an Großinsekten in offenen Habitaten dürfte jedoch vor allem ım Mittelland
durch die erfolgten Landschaftsveränderungen stark zurückgegangen sein. Dies hätte in
der Folge zu einer Verlagerung zum hauptsächlichen Beuteerwerb von waldlebenden
Insekten (v.a. Carabidae) geführt. Unter diesem Gesichtspunkt müßte die ausgeprägte
Nutzung von Wäldern als Jagdhabitate (Auper 1990; RupoLpH 1989; GÜTTINGER mdl.
Mitt.) jedoch als sekundär eingestuft werden.

In diesem Zusammenhang ist auch der Vergleich mit Rhinolophus hipposideros sehr
aufschlußreich. Ähnlich M. myotis erlitt auch diese Fledermausart in der Schweiz in den
letzten Jahrzehnten einen starken Bestandesrückgang. Während R. hipposideros jedoch
gleichzeitig einen Arealverlust im Schweizer Mittelland erfuhr (Sturz und HAFFNER
1984b), konnte sich M. myotis hier zumindest ın Restbeständen halten. Da beide Arten im
Mittelland vermutlich in ähnlichem Ausmaß auf Dachstockquartiere angewiesen sind,
dürften Ursachen für dıe oben aufgezeigten Unterschiede außerhalb der Tagesschlafver-
stecke zu suchen sein. Hier bieten sich die unterschiedliche Ernährung und die unter-
schiedlichen Jagdhabitate als beste Erklärungsmöglichkeiten an. Aufgrund von Nahrungs-
analysen (BEcK et al. 1989; Jones und RAYnErR 1989) kann für R. hipposideros eine stärkere
Bindung an eine kleinräumig strukturierte Kulturlandschaft außerhalb des Waldes ange-
nommen werden. Somit hätte die hauptsächlich durch die zunehmende Intensivierung in
der Landwirtschaft verursachte Ausräumung der offenen Landschaft R. hipposideros in
stärkerem Maße betroffen als M. myotis. Diese hat im Mittelland außerhalb des Waldes
allenfalls einen Teil ihres Beutespektrums verloren, verfügt aber noch immer über eine

gesicherte Nahrungsgrundlage ım Wald.

Danksagung

Für die wissenschaftliche Unterstützung danken wir Dr. M. HaArrner. Bei Prof. Dr. W. SAUTER, Dr.
G. Bächui und A. BEck bedanken wir uns für die Unterstützung bei der taxonomischen Zuordnung
der unverdauten Beuteteile. Im weiteren danken wir R. GÜTTINGER für die vielen anregenden
Diskussionen und allen Quartierbetreuern für die Mithilfe bei der Materialbeschaffung. Die vorlie-
gende Arbeit entstand innerhalb des Forschungsprogrammes des dritten Autors, das vom Schweizeri-
schen Nationalfond unterstützt wurde.

200 M. Graf, H.-P. B. Stutz und V. Ziswiler

Zusammenfassung

Ein Vergleich der Resultate von Kotanalysen in 14 Wochenstubenquartieren von M. myotis ergab, daß
Carabidae in allen Regionen des Untersuchungsgebietes den Hauptbestandteil der Nahrung bildeten.
Es zeigte sich eine Ausrichtung nach dem saisonalen Angebot, wobei allgemein selektiv mittelgroße
und große Beutetiere (> 10 mm) bevorzugt wurden. M. myotis verhält sich somit bei der Wahl der
Beutetaxa opportunistisch, bei der Wahl der Beutegröße hingegen selektiv.

Die mittels einer Cluster-Analyse festgestellte regionalen Unterschiede der Nachweishäufigkeiten
können verschieden gedeutet werden.

Entweder führte eine allgemein geringere Verfügbarkeit der Carabidae in den Voralpen und Alpen
zur vermehrten Nutzung anderer Beutekategorien, oder das Fressen waldlebender Carabidae im
Schweizer Mittelland ist als Folge eines nicht mehr genügenden Angebotes an Großinsekten außerhalb
des Waldes anzusehen. Dies würde bedeuten, daß die Wahl geeigneter Jagdhabitate in starkem Maße
durch das Beuteangebot beeinflußt wird.

Literatur

BUNDESAMT FÜR LANDWIRTSCHAFT (1986): Kulturlandkarte der Schweiz. EDMZ 730.10.

ACKERMANN, G. (1984): Diät, Aktivitätsmuster und Jagdgebiete des Großen Mausohrs Myotis myotis
(Borkhausen, 1797). Dipl. Arbeit Univ. Zürich.

Auper, D. (1990): Foraging behaviour and habitat use by a Gleaning Bat, Myotis myotis (Chiroptera,
Vespertilionidae). J. Mammology 71, 420-427.

BAUEROVA, Z. (1978): Contribution to the trophic ecology of Myotis myotis. Folia Zoologica 27,
305-316.

BEcK, A.; Sturz, H.-P. B.; ZıswiLer, V. (1989): Das Beutespektrum der Kleinen Hufeisennase
Rhinolophus hipposideros (Bechstein, 1800) (Mammalia, Chiroptera). Tev. suisse Zool. 95,
643-650.

BELLMAnN, H. (1985): Heuschrecken beobachten, bestimmen. Melsungen: Verlag J. Neumann
Neudamm.

CHINERY, M. (1984): Insekten Mitteleuropas. Ein Taschenbuch für Zoologen und Naturfreunde.
Hamburg und Berlin: Paul Parey.

Durour, C. (1986): Les Tipulidae de Suisse (Diptera, Nematocera). Documenta Faunistica Helevetiae
Bd 2:

FENTonN, M. B.; Morris, G. K. (1976): Opportunistic feeding by Desert Bats (Myotis spp.) and other
small nocturnal animals. Can. J. Zool. 54, 526-530.

GEBHARD, J.; HirscHt, K. (1985): Analyse des Kotes aus einer Wochenstube von Myotis myotis
(Borkh., 1797) bei Zwingen (Kanton Bern, Schweiz). Mitt. Naturforsch. Ges. Bern 42, 145-155.

GRAF, M. (1990): Regionaler und saisonaler Vergleich der Nahrungszusammensetzung des Großen
Mausohrs Myotis myotiss (Borkhausen, 1797) (Mammalıa, Chiroptera) in der Schweiz. Dipl.-
Arbeit Univ. Zürich.

JONES, G.; RAYNER, J. M. V. (1989): Foraging behavior and echolocation of wild Horsehoe Bats
Rhinolophus ferrumequinum and R. hipposideros (Chiroptera, Rhinolophidae). Behav. Ecol.
Sociobiol 25, 183-191.

Koıs, A. (1958): Nahrung und Nahrungsaufnahme bei Fledermäusen. Z. Säugetierkunde 23, 83-94.

KosscHGen, L. J. (1971): Procedures for food-habits analyses. In: Wildlife management technices.
Washington: The Wildlife Society. Pp. 233-250.

Kunz, T. H.; WHITEAKER, J. ©. (1983): An evolution of fecal analysis for determining food habits of
insectivorous bats. Can. J. Zool. 61, 1317-1321.

Pont, B.; Mourin, J. (1985): Etude du regime alimentaire de Myotis myotis. Methodologie — premiers
resultats. IX. Colloque Francophone de Mammalogie — «Les Chiropteres».

RupoLpH, B. U. (1989): Habitatwahl und Verbreitung des Mausohrs (Myotis myotis) in Nordbayern.
Dipl.-Arbeit Univ. Erlangen-Nürnberg.

Sturz, H. P.; Harrner, M. (1984a): Maternity roosts of the mouse-eared bad Myotıs myotıs
(Borkhausen, 1797) in the central and eastern parts of Switzerland. Myotis 21/22, 180-184.

Sturz, H. P.; HAFFNnER, M. (1984b): Arealverlust und Bestandesrückgang der Kleinen Hufeisennase
Rhinolophus hipposideros (Bechstein, 1800) (Mammalia: Chiroptera) ın der Schweiz. Jber. naturf.
Ges. Graubünden 101, 169-178.

Wırpı, ©. (1986): Analyse vegetationskundlicher Daten. Theorie und Einsatz statistischer Methoden.
Veröff. des Geobot. Inst. ETH Zürich, Stiftung Rübel Heft 90.

Wıroı, O.; Orrocı, L. (1988): MULVA-4, A package for multivariate analysis of vegetation data.

Anschriften der Verfasser: MARTIN GRAF, Limmattalstr. 259, CH-8049 Zürich; Dr. Hans-PETERr B.
Sturz, Benedikt-Fontana-Weg 15, CH-8049 Zürich, und Prof. Dr. Vın-
CENT ZISWILER, Zoologisches Museum, Universität Zürich, Winterthurer
Str. 190, CH-8057 Zürıch, Schweiz

Z. Säugetierkunde 57 (1992) 201-210
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Nachweis des Baummarders, Martes martes, ın der neolithischen
Ufersiedlung von Twann (Kanton Bern, Schweiz) sowie
Anmerkungen zur osteometrischen Unterscheidung von Martes
martes und M. foina

Von BARBARA GRUNDBACHER

Naturhistorisches Museum der Burgergemeinde Bern, Schweiz

Eingang des Ms. 25.9. 1991
Annahme des Ms. 25. 2. 1992

Abstract

Neolhthic remains of the Pine marten, Martes martes from Twann (Switzerland) and osteometrical
methods to distinguish M. martes from M. foına

Studied the bones representing the genus Martes and compared them with those of modern

individuals. From the 200 000 bone fragments excavated at Twann, on the shore of Lake Biel, 149

belong to Martes martes. They represent 25 individuals, making up 1.7 % ot all the wıld anımals from

this site. These pine martens were probably used for food as well as for their fur. Osteometrical
methods to distinguish M. martes from M. foına and also the sexes of each species are discussed.

Einleitung

Anläßlıch des Nationalstraßenbaus in der Schweiz stieß? man Anfang der 70er Jahre beim
Bahnhof Twann am Bieler See (Jura-Südfuß) auf neolithische Siedlungsschichten. Die von
1974-1976 dauernden Ausgrabungen brachten neun Siedlungshorizonte (3838-3532
v. Chr., SUTER und SCHIFFERDECKER 1986) zum Vorschein, in denen über 200 000
Knochen tierischen Ursprungs lagerten. Die knapp 80 000 nach Tierart bestimmbaren
Knochenfragmente stammen zu je ungefähr der Hälfte von Haus- und von Wildtieren.
Eine Gesamtauswertung der Funde erfolgte in den Jahren gleich nach der Grabung
(GRUNDBACHER und STAMPFLI 1977; FURGER 1980; BECKER 1981; BECKER und JOHANS-
son 1981), wobei die Wildcarnivoren späteren Detailuntersuchungen vorbehalten blieben
(GRUNDBACHER 1990; GRUNDBACHER et al. 1990).

Die 149 Marderknochen, welche 0,4 % aller Wildtierknochen entsprechen, sind Gegen-
stand der vorliegenden Arbeit. Sie stammen von mindestens 25 Tieren (= 1,7% aller
Wildtierindividuen).

Material und Methode

Die Twanner Knochenreste

Die Marderknochen stammen meist von adulten Tieren und sind relativ gut, z. T. sogar vollständig
erhalten. Nur wenige Fragmente konnten zu ganzen Knochen zusammengesetzt werden. Von den 149
der Gattung Martes zugeordneten Knochen waren 111 (= 74,5%) vermeßbar (Tab. 1). Nur zwölf
Knochenfunde sind angebrannt oder ganz verkohlt. Rippen und Wirbel (außer 1. und 2. Halswirbel)
wurden nicht artlich bestimmt.

Das Vergleichsmaterial

Schädel und Unterkiefer rezenter Tiere stellten mir die Naturhistorischen Museen von Bern, Basel
und Genf zur Verfügung. Herkunftsgebiet der mehrheitlich in diesem Jahrhundert gesammelten

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5704-0201 $ 02.50/0

202 Barbara Grundbacher

Marderschädel ist vor allem das Berner Mittelland, aber auch die übrige Schweiz und die angrenzende
Haute Savoie (F). Acht Skelette von Martes martes aus Dänemark ergänzten das - keine Langknochen
liefernde — Schweizer Vergleichsmaterial. Sämtliche subfossilen und rezenten Knochen wurden von
der Autorin vermessen.

Artbestimmung

Um am ausgegrabenen Material eine sichere Artbestimmung vornehmen zu können, wurden folgende
Methoden zuerst an artbekannten Vergleichsschädeln geprüft:

Distanz der Foramina mentalia in Abhängigkeit von der Gesamtlänge der Mandibel (SramprLı 1976)
Lage des hinteren Foramen mentale (GAFFREY 1953)

Verhältnis Länge Trigonid zur Gesamtlänge des M, (VAN VALKENBURGH 1989).

Geschlechtsbestimmung

Mittels Clusteranalyse wurde am bekannten rezenten Material geprüft, welche Meßstrecken am
Unterkiefer den deutlichsten Geschlechtsdimorphismus aufweisen (GERASIMoOV 1985). Die Breite des
Processus condyloideus und die mit ıhr korrelierte Länge der Backzahnreihe (P, bis M,, da P, oft nicht
angelegt war), erwiesen sich als brauchbare Größen, um eine Trennung unbekannten Materials in zwei
Gruppen zu erreichen.

Messungen, Auswertung

Gemessen wurden die Knochen nach den Anweisungen VON DEN DRIESCHs (1976) mit einer
Uhrenschieblehre auf 0,1 mm genau. Bei den rezenten Exemplaren wurde jeweils nur eine Seite pro
Schädel gemessen. Die Unterkiefer aus Twann wurden alle vermessen und ausgewertet, unabhängig
davon, ob sie zueinander paßten oder nicht. Die Daten wurden anschließend auf einem Microcompu-
ter mit den Statistikpaketen Systat und Sygraph bearbeitet.

Tabelle 1. Skelettverteilung der Marderreste Ergebnisse
T i
ae Skelettverteilung
Vermessen Nicht meßbar Die Verteilung der Knochen auf Hinter-

und Vorderextremität (Tab. 1) ıst ausgewo-
gen. Mandibeln sind unverhältnismäßig
stark vertreten. Auffällig ıst das vollständi-
ge Fehlen des 1. und 2. Halswirbels sowie
der Knochen des Autopodiums.

Schädelteile
Unterkiefer
Lose Zähne
Scapula
Humerus

Ulna
Radius
Pelvis
Femur

Tıbıa

Schlachtspuren

Om Oov0m +0 W0

NS

An verschiedenen Unterkiefern lassen sich
an der buccalen Seite des Corpus feine
Schnittspuren feststellen (Abb. 1). Sie be-
finden sich meist dort, wo die Haut sehr
eng am Knochen anlıegt. Selbst mit heuti-
gen feinsten Instrumenten können solche Schnittspuren nicht vermieden werden (L.
VINCIGUERRA, pers. Mitt.). Im Ramus von vier Unterkieferhälften befinden sıch offen-
sichtlich absichtlich angebrachte kleine Löcher von 3-5 mm Durchmesser (Abb. 2).

03)
[0,0]

Artbestimmung

Am lebenden oder frischtoten Tier gibt es verschiedene Möglichkeiten, M. martes und M.
foina zu unterscheiden: Form und Farbe des Kehlflecks, Behaarung der Pfoten, Kopfform,
Dichte und Farbe des Felles, Nasenspiegel (BucHALczYk 1981; STUBBE 1988).

Liegen nur Knochen vor, dienen folgende metrische und nichtmetrische Merkmale an

Nachweis des Baummarders in der neolıithischen Ufersiedlung von Twann 203

Abb. 1. Mandibulae von Martes martes mit deutlichen Schnittspuren (Herkunft: neolithische Siedlung
Twann)

Abb. 2. Mandibulae von Martes martes mit Löchern im Ramus mandibulae (Herkunft: neolithische
Siedlung Twann)

204 Barbara Grundbacher

Schädel und Unterkiefer der Artbestimmung: Form und Proportionen des Schädels, Form
der Nasenöffnung, Lage und Distanz der Foramına mentalia, Unterschiede am Gebiß,
Ausformung des knöchernen, äußeren Gehörganges, Ausbildung der Postorbitalregion
(BucHALcZyK 1981; GAFFREY 1953; RODE und DiDIEr 1944; STEINER und STEINER 1986;
STUBBE 1988).

Da die Anwendung subjektiver Kriterien an einem zahlenmäßig beschränkten Material
problematisch ist, wurde versucht, nur mit Hilfe metrischer Merkmale zu arbeiten.

GERASIMOV (1985) unterscheidet verschiedene metrische Systeme, um M. martes und
M. foina zu trennen. Eines davon berücksichtigt die Distanz der normalerweise ın
zweifacher Ausführung vorhandenen Foramina mentalia (manchmal ist nur eines ausgebil-
det, in seltenen Fällen mehr als zwei). Dieses Maß wird zur Kieferlänge (Processus
condyloıdeus bis Vorderrand der Alveole des I,) ın Beziehung gesetzt (STAMPFLI 1976).
Abbildung 3 zeigt die Einzelwerte sowie die 90 %-Ellipsen der erwähnten Maße von M.
martes und M. foina. Ein ? aus der Sammlung Bern wurde in dieser Darstellung nicht
erfaßßt, da eine Fehlbestimmung nicht ganz ausgeschlossen werden kann. Aufgrund der
identischen Lage der Mefßwerte der rezenten Martes martes und der Marder aus Twann
darf mit großer Wahrscheinlichkeit angenommen werden, daß letztere vom Baummarder
stammen.

Nach GarrrEy (1953) sollte das hintere Foramen mentale bei M. martes unterhalb der
hinteren Wurzel von P; liegen. Bei 60 % der Twanner-Unterkiefer liegt es an dieser Stelle.
In neun Fällen (von 25) liegt es zwischen der hinteren und der vorderen Wurzel des P; und
einmal sogar unterhalb dessen vorderer Wurzel.

Die Vermutung, daß sich die beiden Marderarten aufgrund des Anteils von Länge
Trigonid an der Gesamtlänge des M, unterscheiden könnten (wegen unterschiedlich stark
carnıvorer Ernährungsweise, VAN VALKENBURGH 1989; WOoLSsan et al. 1985), bestätigte
sich am rezenten Vergleichsmaterial nicht. Dieses Kriterium wurde daher für eine Artbe-
stimmung im vorliegenden Material nicht herangezogen. Offenbar unterscheiden sich die
beiden Arten in ihren Ernährungsgewohnheiten zu geringfügig, als daß sich das am Gebiß
manifestieren würde. MARcHESsT et al. (1989) finden zwischen M. martes und M. foına der
gleichen Region kleinere Unterschiede im Nahrungsspektrum als zwischen mehreren

7o

Kieferlaenge

Abb. 3. Einzelwerte und 90 %-
Ellipse von Martes foina rezent
(0), Martes martes rezent (©)
und Martes spec. Iwann (A).

Abszisse: Distanz der Foramina

40 mentalia voneinander; Ordina-
2 2 A 5 6 7 8 te: Mandibula-Länge vom Pro-
cessus condyloideus bis zum

FOR ZEISIt Infradentale

Nachweis des Baummarders in der neolithischen Ufersiedlung von Twann 205

M. foina-Populationen aus verschiedenen Gebieten. Die Unterschiede zwischen den bei-
den Arten sind in den wichtigsten Beutegruppen mehr quantitativer als qualitativer Art.
CLuTTon-BRrock (1990) ordnet die Marderunterkiefer der neolithischen Station Yvo-
nand IV ın Anlehnung an die von AnDERSoN (1970) publizierten Daten M. martes zu. Es
gilt jedoch zu beachten, daß ANDERSons Trigonidwerte von M. foina innerhalb der
Variationsbreite derjenigen von M. martes liegen.

Geschlechtsbestimmung

Unter der Annahme, daß das gesamte Marderknochen-Material vom Baummarder stammt,
kann versucht werden, die vorhandenen Mefßwerte den dd oder den ?2 zuzuordnen.
Die Varıationsbreiten der Unterkiefermaße von rezenten Baummarder-Weibchen und
-Männchen zeigen einen großen Überschneidungsbereich. Es können somit nicht ohne
weiteres zwei Gruppen unterschieden werden.
Abbildung 4 zeigt die Werte der Länge des Processus condyloideus korreliert mit der
Backzahnreihe rezenter Baummarder. Innerhalb der untersuchten Meßreihe kann jedes

13

12

le

E

(6)

(6)

6)

Q

DEE I®
Abb. 4. Einzelwerte und 90 %- 9
Ellipse von rezenten Martes
martess d und 2. Abszisse:
Backzahnreihe (P5-M5); Ordi-
nate: Breite des Processus con- 8

dyloideus

Ba M2

Individuum mit einer unterschiedlich hohen Wahrscheinlichkeit dem einen oder anderen
Geschlecht zugewiesen werden. Es zeigte sich, daß die beiden erwähnten Maße die an sie
gestellten Erwartungen erfüllen. In Abbildung 5 sind auf die gleiche Art die Unterkiefer-
maße aus Twann dargestellt (ein Unterkiefer wurde für diese Abbildung nicht mitberück-
sichtigt, da seine Maße extrem außerhalb aller anderen liegen).

Um den Geschlechtsdimorphismus an den Langknochen zu prüfen, muß auf das
dänische Vergleichsmaterial zurückgegriffen werden. Die 4-5 845 und 2-3 ?% unterschei-
den sich ın der Größe recht deutlich voneinander. Bei keiner der gemessenen Strecken
konnte ein Überschneidungsbereich der beiden Geschlechter festgestellt werden. Im
Gegensatz dazu lassen sich die Marder aus Twann nicht eindeutig in zwei Gruppen
aufteilen (statistische Werte der Maße der neolithischen Tiere s. Tab. 2). Untersuchungen
an polnischen (ReıG und RUPRECHT 1989) und an schwedischen Mardern (REINWALDT und

206 Barbara Grundbacher

13 le U ee terre ale

Proc. cond.

Abb. 5. Einzelwerte und 90 %-
Ellipse von Martes martes &
und $ aus Twann. Legende s.

85 AbbA

DON

ERKINARO 1959) zeigen ebenfalls einen ausgeprägten Sexualdimorphismus, der sich am
Schädel deutlicher manifestiert als an den Langknochen.

Größenvergleich

Sämtliche Schädel- und Unterkiefermaße der neolithischen Marder aus Twann liegen
innerhalb der Varıationsbreite derjenigen der rezenten, die Mittelwerte der erstgenannten
sind jedoch höher. Der Vergleich der Langknochenmaße ergibt ein etwas anderes Bild: Die
neolithischen Marder aus Twann waren, verglichen mit den neuzeitlichen Tieren aus
Dänemark, etwas kleiner bis gleich groß. Werden die Baummarder aus Twann mit solchen
aus anderen neolithischen Stationen verglichen (Burgäschisee-Süd, Auvernier, Yvonand),
ergibt sich eine recht einheitliche Größe.

Diskussion
Skelettverteilung

Die grundlegenden Strukturen von Siedlungsschichten und deren Inhalt sollen hier nicht
erörtert werden. Es stellt sich im vorliegenden Zusammenhang jedoch die Frage, wieso
Unterkiefer im Vergleich zu anderen Knochen überrepräsentiert sind. Die relativ feinen,
aber deutlichen Schnittspuren an den Mandibeln sowie das Loch im Processus artıcularıs
lassen eine zweckdienliche Nutzung dieser Unterkiefer vermuten. Die Beschreibung eines
durchbohrten, polierten Marder-Unterkiefers aus der Horgener- Schicht von Eschner-
Lutzengüetle (HARTMANN-FRICK 1960) weist in die gleiche Richtung.

Das Fehlen der entsprechenden Schädel, Wirbel sowie der Knochen des Autopodiums
mag ein Hinweis darauf sein, daß die gefundenen Knochenreste von Mahlzeiten (verkohlte
Knochen) stammen bzw. Zeugen sonstiger Nutzung (Mandibeln) sind. Die Knochen des
Autopodiums blieben vermutlich beim Häuten des Tieres im Fell bzw. wurden als Abfall
weggeworfen.

Nachweis des Baummarders in der neolithischen Ufersiedlung von Twann

207

Tabelle 2. Baummarder (M. martes) aus Twann: Statistische Werte

Schädel

M1: Mediane Gaumenlänge, M2: Prämolarenreihe, M3: Größte Länge des Reißzahnes, M4:
Größte Breite des Reißzahnes, M5: Schädelenge, M6: Stirnbreite, M7: Breite über die Eckzahn-
alveolen, M8: Breite zwischen den Orbitae. n: Anzahl Meßwerte, M: Durchschnitt, SD: Standar-
dabweichung, Min: kleinster Wert, Max: größter Wert

Mi M2
n 1 3
M 42,1 19,80
SD 0,17
Min 197
Max 20,0

M3

3)
8,47
0,76
7,8
3)

M4 M5 M6

3 1 2
DZ 19,6 21,90
0,70
4,9
6,3

Unterkiefer

M7

1
16,3

M8

2
19,45

M1-M5, M8, M9 stimmen mit den entsprechenden Definitionen in VON DEN DRIESCH (1976)
überein; M6: Größte Länge des Reißzahnes, M7: Größte Breite des Reißzahnes, M10: Distanz
zwischen den beiden Foramiına mentalia

Mi M2
n 5 15
M 55 53423
SD 2,82 259
Min 49,4 48,0
Max 59,8 57,4

Scapula

GLP KEG
n 5 6
M 11450 9,45
SD 0,50 0,54
Mın 10,6 8,6
Max 11,8 11.0)

Ulna

GL KTO
n 3 6
M 63,67 7,20
SD 330%. 0,36
Min 61,2 6,8
Max 67,1 7,6

Femur

Se Bp
n 4 9
M 76,68 14,44
SD 4,77 1,02
Mın 72,4 130
Max 81,0 19

M3

i@

10
7,00
0,36
6,6
7,6

M4 M5 M6

18 23 19
46,49 29,96 10,25
BER 19777 0,52
40,7 Pl 9,0
50,8 32,6 ls)
Humerus
GL Tp
4 8
6718212879
4,36 0,90
63,3 119
Zt 14,3
Radius
GE Bp
5 8
54,78 6,69
32977, 0,78
49,4 555
60,3 7,8
Bd
9
AT.
1,36
1251
15,6

Das Fehlen des Steinmarders, Martes foina

M9 M10
28 21
9,86 5,47
0,88 0,56
8,0 4,0
1111874 6,7
Pelvis
LAR LFo
10 3
8,26 11633
0,61 0,70
745 15,6
93 17,0
Bd
10
87
0,65
8,5
10,5

Im untersuchten Knochenmaterial von Twann konnte nur M. martes, nıcht aber M. foına
nachgewiesen werden. Entsprechendes gilt für andere neolithische Siedlungen (Yvonand
IV: CLutron-Brock 1990; Feldmeilen-Vorderfeld: Eısı 1974; Egolzwil 2: HESCHELER
und RÜEGER 1939; Burgäschisee-Süd: JEQUIER 1963; Auvernier: STAMPFLI 1976; Schen-
kon-Trichtermoos: STAMPFLI 1974). Ausnahmsweise finden sıch ın den Listen neoliıthıi-
scher Grabungen auch Knochen von M. foina, allerdings ohne Hinweis auf die Artbestim-
mung (Eschner-Lutzengüetle: HARTMANN-FRICK 1960; Yverdon-Garage Martin: CHAIXx

1976).

208 Barbara Grundbacher

Diese Tatsache wirft Fragen über Verbreitung und Nutzung dieser beiden Tierarten in
der Vergangenheit auf.

EHRET (1964) und PIEHLER (1976) stellen in römerzeitlichen städtischen Siedlungen
noch das Fehlen von M. foına fest. TEICHERT (1989) weist den Steinmarder im Gebiet der
ehemaligen DDR erstmals ın der Slawenzeit nach. Nach AnnpeErson (1970) ist der
Steinmarder in Europa erst „ın late postglacial times“ fester Bestandteil der Fauna. Sie
vermutet sein Eindringen vom mittleren Osten her, wo er in würm- und nacheiszeitlichen
Ablagerungen nachgewiesen werden konnte. Nach seiner nordwestwärts gerichteten Aus-
breitung besetzte er ungenutzte Nischen und entwickelte sich zum Kulturfolger.

Unter der Annahme eines gleichzeitigen Vorkommens der beiden Marderarten stellt
sich jedoch die Frage nach einer möglichen Präferenz durch die ur- und frühgeschicht-
lichen Menschen. Die Felle der Tiere waren sicher ein geschätzter Rohstoff (BUTZECK
1989). Der Baummarder als besser kälteangepaßte Art weist ein deutlich dichteres Fell auf
als der Steinmarder (Mürı 1982; STuBBE 1988). Noch heute werden Baummarderfelle ihrer
besseren Qualität wegen bis doppelt so hoch bezahlt wie diejenigen vom Steinmarder
(GauTscHI 1984).

Da die Marder ihrer nächtlichen Lebensweise wegen wahrscheinlich mit Fallen und
Schlingen erlegt wurden, scheint es fragwürdig, ob die neolithischen Menschen oben
erwähnte bessere Fellqualität auszunutzen wußsten.

Geschlechterverteilung

Verschiedene Gründe können für das Überwiegen von Knochen männlicher Marder im
Material (sowohl Langknochen wie Unterkiefer) verantwortlich sein. Männchen haben
von Natur aus größere Aktionsräume als Weibchen (SCHRÖPFER et al. 1989), laufen also
erhöht Gefahr, gefangen zu werden. Als Vergleich dazu mögen Zahlen aus dem Natur-
historischen Museum Bern dienen: Bei den meisten Carnıvoren - so auch bei den Mardern
- sind bedeutend mehr Schädel männlicher Tiere in den Sammlungen zu finden, da diese
häufiger verunfallen als die weiblichen Artgenossen. Gefangene ?? bzw. ihr Analdrüsen-
sekret können als Köder beim Fang weiterer Tiere dienen, was jedoch wiederum ein
Überwiegen der dd ergibt (diese Fangmethode wird heute noch in Afrika, z.B. für die
Fuchsmanguste, Cynictis penicillata, durch die einheimische Bevölkerung angewendet;
L. VINCIGUERRA, pers. Mitt.).

Größenvergleich

DEGERBOL (1933) stellt für dänische Verhältnisse fest, daß die postglazialen Baummarder
(n = 39) größer und kräftiger gebaut waren als die rezenten Tiere, was sich vor allem ın der
Größe des unteren Reißzahnes manifestiere. Für die Baummarder von Egolzwil (n = 5,
HESCHELER und RÜEGER 1939) gilt das Gegenteil: die heutigen Tiere sind ihnen an Größe
überlegen. Eine dritte Variante beschreibt JEQUIER (1963) für die Baummarder in Burgä-
schisee-Süd (n = 4): Sie sind ungefähr gleich groß wie die rezenten Vergleichstiere.

ANDERsSoN (1970) erwähnt, daß, obwohl die postglazialen Tiere größer sind als die
rezenten, ein Überschneidungsbereich vorhanden sei. Diese Feststellung könnte die vorlie-
gende Untersuchung, die in einzelnen Maßen eine minimale Größenzu-, ın anderen eine
ebenso geringe Größenabnahme ergibt, bestätigen, dürfte möglicherweise auch die unter-
schiedlichen Resultate von DEGERB@L (1933), HESCHELER und RÜEGER (1939) sowie
J£EQUIER (1963) erklären. Bei der Interpretation so kleiner Größenunterschiede darf nıe
vergessen werden, daß evtl. auch klimatische und ökologische Faktoren mitspielen, bzw.
daß bei einem subfossilen Material stets auch die Unsicherheit der Geschlechtsbestimmung
mitspielt (was bei so geringem Material um so stärker ins Gewicht fällt).

Nachweis des Baummarders in der neolithischen Ufersiedlung von Twann 209

Danksagungen

Für die Überlassung des Materials und für die großzügige finanzielle Unterstützung der vorliegenden
Arbeit möchte ich dem archäologischen Dienst des Kantons Bern herzlich danken. Die Bereitstellung
modernen Vergleichsmaterials verdanke ich den Naturhistorischen Museen in Bern, Basel und Gent.
Mein Dank geht ebenfalls an Marc NUSSBAUMER, der mir bei der statistischen Auswertung behilflich
war.

Zusammenfassung

149 Knochen von Martes sp. aus der neolithischen Ufersiedlung von Twann (Bieler See, Schweiz)
waren Gegenstand einer osteometrischen Untersuchung. Schnitt- und Brandspuren lassen vermuten,
daß die Marder ihres Felles, wahrscheinlich aber auch ihres Fleisches wegen gejagt worden waren. Mit
Hilfe rezenter Vergleichsskelette konnte eindeutig festgestellt werden, daß es sich bei den vorliegen-
den Knochen um solche des Baummarders, Martes martes, handelt. Mittels Clusteranalyse gelang es,
die vorhandenen Unterkiefer männlichen bzw. weiblichen Tieren zuzuordnen. Bei den Langknochen
scheint der Überschneidungsbereich der Maße zu groß zu sein, als daß alle vorliegenden Knochen
eindeutig dem einen oder anderen Geschlecht zugewiesen werden könnten.

Der Vergleich mit Baummarderknochen anderer neolithischer Stationen zeigt eine einheitliche
Größe der Tiere. Anhand der Schädel- und Unterkiefermaße kann eine leichte Größenabnahme vom
Neolithikum bis zur heutigen Zeit festgestellt werden.

Literatur

ANDERSON, E. (1970): Quaternary evolution of the Genus Martes (Carnıvora, Mustelidae). Acta
Zool. Fenn. 130, 1-132.

BECKER, C. (1981): Die neolithischen Ufersiedlungen von Twann. Bd. 16: Tierknochenfunde. Dritter
Bericht. Bern: Staatl. Lehrmittelverlag.

BECKER, C.; JOHANSSON, F. (1981): Die neolithischen Ufersiedlungen von Twann. Bd. 11: Tierkno-
chenfunde. Zweiter Bericht. Bern: Staatl. Lehrmittelverlag.

BUCHALCZYK, T. (1981): Order Carnivores - Carnıvora. In: Keys to vertebrates of Poland. Mammals.
Ed. by Z. Pucex. Warszawa: Polish Scientific Publishers. Pp. 260-306.

BUTZECK, $. (1989): Bemerkungen zur historischen Entwicklung des Populationstrends von Baum-
und Steinmarder Martes martes (L.), Martes foına (Erxleben). In: Populationsökologie marderarti-
ger Säugetiere. Hrsg. von M. STuBBE. Wiss. Beitr./Martin-Luther-Univ., Halle/Wittenberg 37
(P39), 371-386.

CHax, L. (1976): La faune de la fouille Yverdon-Garage Martin. Cah. d’archeol. romande 8,
181-233.

CLUTTON-BROcK, J. (1990): Anımal remains from the neolithic lake village site of Yvonand IV,
canton de Vaud, Switzerland. Arch. Sci. Geneve 43, 1-97.

DEGERBOL, M. (1933): Danmarks Pattedyr ı Fortiden ı Sammenligning med recente former I
(Oversigt; Rovdyr [Carnivora]). Vid. Medd. Dansk naturhist. For. Kobenhavn 96, 357-615.
DRIESCH, A., VAN DEN (1976): A guide to the measurement of anımal bones from archaeological sites.

Peabody Mus. Bull. 1. Harvard University.

EHRET, R. (1964): Tierknochenfunde aus der Stadt auf dem Magdalensberg beı Klagenfurt in Kärnten.
II. Carnıvora, Lagomorpha, Rodentia und Equidae. Diss. Univ. München.

Eısr, F. (1974): Die Tierknochenfunde aus der neolithischen Station Feldmeilen-Vorderfeld am
Zürichsee. I. Die Nichtwiederkäuer. Diss. Univ. München.

FURGER, A. R. (1980): Die neolithischen Ufersiedlungen von Twann. Bd. 7: Die Siedlungsreste der
Horgenerkultur. Bern: Staatl. Lehrmittelverlag.

GAFFREY, G. (1953): Die Schädel der mitteleuropäischen Säugetiere. Abh. Ber. Staatl. Mus. Tierkd.
Dresden, Bd. 21.

GAUTSCHI, A. (1984): Vom Edelmarder in der Schweiz. Feld, Wald, Wasser 12/2, 12-17.

GERASIMovV, $. (1985): Species and sex determination of Martes martes and Martes foına by use of
systems of cranıometrical indices developed by stepwise discriminant analysis. Mammalıa 49,
235-248.

GRUNDBACHER, B. (1990): Osteometrische Untersuchungen an Braunbären (Ursus arctos) aus der
neolithischen Ufersiedlung Twann (Bieler See, Kanton Bern, Schweiz). Jahrb. Naturhist. Mus.
Bern 10, 117-130.

GRUNDBACHER, B.; STAMPFLI, H. R. (1977): Die neolithischen Ufersiedlungen von Twann. Bd. 2:
Tierknochenfunde. Erster Bericht. Bern: Staatl. Lehrmittelverlag.

GRUNDBACHER, B.; Lürs, P.; NussBAUMER, M. A. (1990): Osteometrische Untersuchungen an
neolithischen Dachsen (Meles meles) aus Twann (Kanton Bern, Schweiz). In: Festschrift für Hans
R. Stampfli. Hrsg. von J. SCHIBLER, J. SEDLMEIER und H. SpycHEr. Basel: Helbing und
Lichtenhahn. Pp. 101-113.

210 Barbara Grundbacher

HARTMANN-FRICK, H. P. (1960): Die Tierwelt des prähistorischen Sıedlungsplatzes auf dem Eschner
Lutzengüetle Fürstentum Liechtenstein (Neolithikum bis La Tene). Jb. hist. Ver. Fürstent.
Liechtenstein 59, 5-223.

HESCHELER, K.; RÜEGER, J. (1939): Die Wirbeltierreste aus dem Pfahlbaudorf Egolzwil 2 (Wauwiler
See) nach den Grabungen von 1932 bis 1934. Vierteljahrsschr. Naturf. Ges. Zürich 84, 307-330.

JEQUIER, J. P. (1963): Der Baummarder, Martes martes (Linne, 1758). In: Seeberg Burgäschisee-Süd.
Die Tierreste. Hrsg. von J. BOESSNECK, J. P. JEQUIER und H. R. StamprLı. Acta bernensia 11/3,
46-50.

MARCHESsı, P.; LACHAT, N.; LIENHARD, R.; DEBIEVE, P.; MERMOD, C. (1989): Comparaison des
regimes alımentaires de la fouine (Martes foina Erxl.) et de la martre (Martes martes L.) dans une
region du Jura suisse. Rev. suisse Zool. 96, 281-296.

Mürı, H. (1982): Baum- und Steinmarder. Wildbiol. Praxis 1/13, 1-11.

PıieHLER, W. (1976): Die Knochenfunde aus dem spätrömischen Kastell Vemanıa. Diss. Univ.
München.

Reıc, $.; RUPRECHT, A.L. (1989): Skull varıability of Martes martes and Martes foına from Poland.
Acta theriol. 34, 595-624.

REINWALDT, E.; ERKINARO, E. (1959): Zur Taxonomie und Verbreitung des Baummarders, Martes
martes martes (Linne, 1758). Säugetierkdl. Mitt. 7, 97-100.

Rone, P.; Dipier, R. (1944): Differences entre la tete osseuse de la martre et celle de la fouine.
Mammalıa 8, 127-132.

SCHRÖPFER, R.; BIEDERMANN, W.; SZCESNIAK, H. (1989): Saısonale Aktionsraumveränderungen beim
Baummarder Martes martes L., 1758. In: Populationsökologie marderartiger Säugetiere. Hrsg.
von M. STUBBE. Wiss. Beitr./Martin-Luther-Univ., Halle/Wittenberg 37 (P39), 433—441.

STAMPELI, H. R. (1974): Die Tiere aus der neolithischen Ufersiedlung Schenkon-Trichtermoos. Mitt.
Naturf. Ges. Luzern 24, 135-152.

— (1976): Osteo-archäologische Untersuchung des Tierknochen-Materials der spätneolithischen
Ufersiedlung Auvernier La Saunerie nach den Grabungen 1964 und 1965. Solothurn.

STEINER, H. M.; STEINER, F. M. (1986): Die nicht-metrische Unterscheidung von Schädeln mitteleu-
ropäischer Baum- und Steinmarder (Martes martes und Martes foına, Mammalia). Ann. Naturhist.
Mus. Wıen 88/89B, 267-280.

STUBBE, M. (1988): Baum- und Steinmarder Martes martes (L.), Martes foina (Erxleben). In: Buch der
Hege. Hrsg. von H. StuBge. Berlin: Deutscher Landwirtschaftsverlag. Pp. 478-502.

SUTER, P. ]J.; SCHIFFERDECKER, F. (1986): Das Neolithikum im schweizerischen Mittelland. In:
Chronologie, archäologische Daten der Schweiz. Antiqua 15, 34-43. Basel: Verlag Schweiz. Ges.
Ur- und Frühgesch.

TEICHERT, M. (1989): Ur- und frühgeschichtliche Mustelidennachweise vom Territorium der DDR.
In: Populationsökologie marderartiger Säugetiere. Hrsg. von M. STuBBE. Wiss. Beitr./Martin-
Luther-Univ., Halle/Wittenberg 37 (P39), 347-360. |

VALKENBURGH, B. van (1989): Carnıvore dental adaptations and diet: A study of trophic diversity
within guilds. In: Carnivore behavior, ecology and evolution. Ed. by J. L. GITTLEman. London:
Chapman & Hall. Pp. 410-436.

Wowsan, M.; RUPRECHT, A. L.; BUCHALCZYK, T. (1985): Variation and asymmetry in the dentition of
the Pine and Stone martens (Martes martes and M. foina) from Poland. Acta theriol. 30, 79-144.

Anschrift der Verfasserin: BARBARA LÜPS-GRUNDBACHER, Naturhistorisches Museum, Bernastraße
15, CH-3005 Bern, Schweiz

Z. Säugetierkunde 57 (1992) 211-215
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

The Alpine marmot (Marmota marmotaL.) in the Spanish
Pyrenees

By J. HERRERO, J. CANUT, D. GARCIA-FERRE, R. GARCIA-GONZALEZ and R. Hıparco

Instituto Pirenaico de Ecologia, Jaca-Huesca, Spain

Receipt of Ms. 17. 6. 1991
Acceptance of Ms. 9. 10. 1991

Abstract

Studied the distribution and colonization process of Alpine marmot (Marmota marmota L.) ın the
Southern Pyrenees. Marmots became extinct at the end of the Pleistocene in the Pyrenees, and have
been introduced since 1948 on the northern slope of the mountain range (France). More than 350
localızations have been recorded. Results show factors that have affected its expansion, such as:
orographic barriers, mountain passes, habitat selection and human disturbance. Location is given in
2x 2 km of the UTM squares, which indicates the existence of at least one colony. Colonies range
from 1450 to 2900 m, more frequently between 1800 and 2400 m height. A positive correlation exists
between the years of existence in each massıf and the altıtudinal range ( r = 0.89, p < 0.01), and
between the maximal height of the massıf and the maximal height of the colonies (r = 0.80, p < 0.01).

Introduction

The Alpine marmot inhabited the Pyrenees during the Pleistocene (ALTunA 1965; BEssON
1971; VırLaLtA 1972). At the end of this period it only survived in the Alps (Marmota
marmota marmota) and in the Carpatıian mountains (Marmota marmota latirostris). After
1948 (COUTURIER 1955) several deliberate introductions were undertaken either by officıal
organızations such as the Parc National des Pyrenees Occidentales (P. N. P. ©.) or by
hunters, which have continued to date (OLiVIEr 1979; DuBREUIL 1989; NOVvoA, pers.
comm.)

There were varıous motives for these activities. COUTURIER (1955) attempted to reduce
the impact of the golden eagle (Agnıla chrysaetos) preying on the chamoıs (Rupicapra
pyrenaica pyrenaica), while CHimıts (1971) intended the marmot to be an alternative
feeding source for the brown bear (Ursus arctos) and thus to lessen the latters attacks on
livestock (BUFFIERE 1988; CHAUMEIL 1988). The marmot became established in Spain since
at least 1968 and ıs now widely distributed over the entire southern slope of the Pyrenees
(GARCIA-GONZALEZ et al. 1985).

The aim of this paper is to describe the distribution of this species and to outline its
colonising process. From thıs information it ıs expected that factors having conditioned the
spread of this species can be elucidated.

Material and methods

The data for the colonies established on the Spanish slope have been obtained by means of inquiries,
revision of bibliographical sources and mainly systematic investigation of the landscape. The inquiries
were carried out on mountain people, livestock managers and above all the rangers of the various
organizations responsible for wildlife management: Diputaciön General de Aragon (D. G. A.),
Generalitat de Catalunya, Diputaciön Foral de Navarra (D. F. N.).

The surveys have revealed a great deal about the development of the colonizing process (CANUT et
al. 1989; HERRERO et al. 1987). The bibliographical revision of OLiviEr’s (1979) thesis has provided

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5704-0211 $ 02.50/0

2% J. Herrero, J. Canut, D. Garcia-Ferre, R. Garcia-Gonzalez, and R. Hidalgo

information on the French deliberate introductions and on the first marmot localities in the Iberian
Peninsula. Systematic exploration of the land was undertaken to test the validity of these inquiries.
More than two hundred colonies have been visited since 1984, especially systematically in the
summers of 1988 and 1989. In 1990 some new data were added. We have thus been able to gather
information about the ecological features of the habıtat.

On most of these expeditions we were accompanied by the afore-mentioned rangers. Location of
colonies was made easier by the use of a dog. This method has been used with various ground squirrel
species (ZwICKEL 1980) including Marmota vanconverensis. (MUNRO et al. 1985).

Results and discussion
The colonizing process

The analysıs of historical and present-day Alpine marmot distribution on the southern
slope of the Pyrenees enables us to deduce the factors, both physical and human, which
have influenced its expansion (HERRERO et al. 1987). The Spanish locations where
colonisation has taken place most closely correspond to the French areas where the
introduction has been nearest to the border and/or most abundant. In many cases the
marmot has only taken two or three years to establish on the Spanish territory (GONZALEZ-
PRAT et al. 1989).

Dispersion ıs delayed but not prevented by high massifs or steep slopes, as they act as
orographic barrıers. Mountain passes provide passage ways leading to colonization of
other slopes, especially those below 2400 m altitude. Habitat selection ıs also an important
factor in the colonising process and the marmot’s preference for southern slopes is
extremely influential. The features of French northern slope being less suitable, have
favoured the expansıon throughout the Spanish Pyrenees.

Human presence and the construction of infrastructures has made marmot colonızation
difficult, according to what has been discovered by the explorations. Tranquillity having
been restored, however, some previously disturbed areas are quickly reoccupied.

Current distribution

The Figure shows the current distribution of the marmot over the southern Pyrenees,
taken from points superimposed on a UIM grıd of 2 km sıde. Therefore marmots can be
found in at least 190 squares of 4 km? (11% of the area between 1600 and 2400 m). The
height ranges between 1800 and 2400 m altitude, although there are extreme localities at
1450 and 2900 m (HERRERO and GARCIA-SERRANO 1989).

The most westerly point was of a marmot ın spring dispersion. The area between this
one and the nearest localities has not been specifically explored.

The Table shows the first year of marmot presence, the number of colonies and the
altitudinal range occupied by this anımal throughout the southern slope of the Pyrenees
with differentiated geographical sectors. A positive correlation between maximum altıtude
of the massıf and maximum altıtude of marmot colonies can be seen (r = 0.8067, p < 0.01).
Between the maximum height of the massıf and the minimum altitude of colonies,
however, there is no significant relationship (r = 0.375, p < 0.1). There is, therefore, a
natural upper limit conditioned by there being an occupiable habitat that ıs higher in
relation to the height of the massif. The lower limit (tolerance interval of an average of
1813 m #227 m) does not depend on the height of the massif. One conditioning factor
could be human activity (livestock, forestry), which has lowered the natural limit above
tree-line, and has widened the supraforestal pastureland (subalpine alpinized level) and
therefore the ideal habitat for the marmot. This upper forest limit has been established
heterogeneously depending on the specific exploitation of the valley.

The age of the first marmot locality for each massıf is positively correlated to the

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214 J. Herrero, J. Canut, D. Garcıa-Ferre, R. Garcia-Gonzalez, and R. Hidalgo

First observed date, number of colonies and altitudes of marmot colony
recorded in southern Pyrenees

Letters in brackets correspond with the sectors repesented in the figure

Massıfs and 1st date in. Number of
max. height presence colonies

Massıf of Anıe, Alanos, > 1980 29
Pena Forca 2504 m (A)
Massıf of Bisaurin and > 1970 39
Sa of Aısa 2676 m (B)

Aragön-Gällego watershed > 1970 12
2886 m (C)

Gällego-Ara watershed 1968

3144 m (D)

Monte Perdido Massıf 1978

3355 m (E)

Cinca and Cinqueta valleys 1968

3174 m (F)

Posets 1978

3371 m (G)

Maladeta Massıf 1967

3404 m (H)

Pallars 1975

3015 m (I)

Cerdanya 1982

3143 m (J)

Nuria 1984

2910 m (K)

altitudinal range (maximum versus minimum height) occupied at present (r = 0.8941, p <
0.001), although thıs ıs not the case wıth the number of colonies observed ın these ranges
(r = 0.43, p > 0.1), or the altıtudinal range with the number of colonıes (r = 0.59, p > 0.05).

This may indicate that the marmot has tended to increase its expansion, colonising the
whole potentially occupiable altıtudinal range. Some massifs have been shown to be
particularly advantageous, especially the Gällego-Ara watershed, sector D, whereas others
are less suitable for habıtation. This heterogeneous colonisation is most likely the reason
for a lack of correlation between the altitudinal range and the number of colonies. The
colonisation process has not yet finished and there are various massifs which are lıkely to
become occupied soon, such as Cotiella and Turbön.

Acknowledgements

The explorations of Aragonese territory were subsidised by the D.G.A. under its project “Alpine
marmot biology in Aragon”. Additional aid was provided by C.1.C.Y.T. (Interministery Commis-
sıon for Science and Technology) project number PB870 349.

We thank the rangers of the mentioned organızations: D.G.A., Generalitat, D.F.N. who gave us
invaluable help in locating the colonies and who accompained us on many occasions. We were also
accompained by: J. M. AmEzZTOY, A. GARCIA-SERRANO, C. GÖMEZ, A. OTEIZA, and A. VAZQUEZ,
F. GonzALEZ-PRAT and C. NovoA provided us with unpublished information about the marmot in
the Eastern Pyrenees. J. P. BEsson of the P.N.P.O. collaborated with us in obtaining bibliography.

Auıstaır DANnsoN and JOACHIM GRIESINGER did the English and German translations, respec-
tively.

The Alpine marmot in the Spanish Pyrenees 215

Zusammenfassung

Die Murmeltiere (Marmota marmota L.) in den spanischen Pyrenäen

Untersucht wurde die fortschreitende Besiedlung und Ausbreitung des Murmeltieres in den südlichen
Pyrenäen. Murmeltiere starben in den Pyrenäen am Ende des Pleistozäns aus und wurden seit 1948 auf
der nördlichen französischen Seite wieder eingeführt. Uber 350 Beobachtungsdaten gingen in die
Untersuchung ein. Die Ergebnisse zeigen, daß Faktoren wie orografische Barrieren, Gebirgspässe,
Wahl des Lebensraumes und Störungen durch den Menschen die Ausbreitung des Murmeltieres
beeinflußt haben. Die Daten sind in Quadraten von 2x2 km (UTM-Gitter) angegeben, worin sich
mindestens eine Kolonie befindet. Die Kolonien reichen von 1450 m bis 2900 m Höhe, sind jedoch
häufiger zwischen 1800 m und 2400 m Höhe.

Es besteht ein positiver Zusammenhang zwischen Zeitdauer der Anwesenheit der Tiere und ihrer
Besiedelung der Höhenstufen in jedem Bergmassiv (r = 0.89, p < 0.01) sowie zwischen Maximalhöhe
des Massives und Höhe über NN der angesiedelten Kolonien (r = 0.80, p < 0.01).

References

ALTUNA, J. (1965): Las marmotas del yacimiento prehistörico de Letxiki (Guipüzcoa). Munibe 7,
65-71.

Besson, J. P. (1971): Introduction de la Marmotte dans les Pyrenees occidentales. Comptes Rendus du
9%6e Congres National des Societes Savants 3, 397-399.

BUFFIERE, D. (1988): Bilan eco-ethologique de dix huit annes d’attaques d’ours sur le betail
domestique. Acta biol. mont. Ser. Doc. Trav. 2, 45-50.

CANUT, J.; GARCIA-FERRE, D.; MARco, J. (1989): Distribuciön y colonızacıön de la marmota en el
Pirineo central y oriental ıberico. Ecologia 3, 149-156.

CHAUMEIL, D. (1988): Evolution geographique et dynamique de la population d’ours brun dans les
Pyrenees occidentales. Acta biol. mont. Ser. Doc. Trav. 2, 51-60.

CHimIss, P. (1979): La protection de l’ours dans les Pyrenees occidentales. C. R. 96e Congres Nat.
Soc. Sav. Sciences 3, 391-393.

COUTURIER, M. A. J. (1965): Acclimatation et Acclımatement de la Marmotte des Alpes, Marmota
marmota marmota (Linne, 1758), dans les Pyren&es fragaises. Säugetierkdl. Mitt. 3, 105-107.

Dusreuit, D. (1989): La Marmotte des Pyren&es. Chasseur 61, 5-7.

GARCIA-GONZALEZ, R.; CANUT, J.; GARCIA, D.; HERRERO, J.; HIDALGO, R.; JORDAN, G.; NAvazo,
V.; Ruiz-OLmo, J.; Marco, J. (1985): Primeras notas sobre la distribuciön de la marmota (M.
marmota L., 1748) en la Peninsula ıberica. Pirineos 125, 113-115.

GONZALEZ-PRAT, F.; GIL-SANTANO, J.; PuIG-MAIDEU, D. (1989): Notes sobre la presencia de la
marmota al Ripolles. Taleia 2, 15-17.

HERRERO, ]J.; GARCIA-SERRANO, A. (1989): Estudio de la biologia y distribuciön de la Marmota alpına
en el Alto Aragön. Unpubl. report D.G.A. Zaragoza.

HERRERO, H.; HıDALGo, R.; GARCIA-GONZALEZ, R. (1987): Colonization process of the Alpine
marmot (Marmota marmota) ın Spanish Pyrenees. Pirineos 130, 87-94.

Munro, D. W.; Janz, D. W.; HEınsaLu, V.; SMITH, G. W. (1985): The Vancouver Island Marmot:
Status and Management Plan. B. C. Ministry of Environment. Wildlife Bull. B-39, 1-22.

OLIVIER, J. (1979): La marmotte (Marmota marmota Linnee, 1758) dans les Pyrenees. Implantation,
developpement, repartition. These doctorale. Ecole National Veterinaire de Toulouse.

VILLALTA, J. F. (1972): La presencia de la marmota y otros elementos de la fauna esteparia en el
Pleistoceno catalän. Acta Geol. Hispänica 7, 170-173.

ZWICKEL, F. C. (1969): Use of dogs ın Wildlife Management. In: Wildlife Management Techniques
Manual. Ed. by R. H. Gızes. Washington: Wildlife Society. Pp. 319-324.

Authors’ addresses: J. HERRERO, R. GARCIA-GONZALEZ and R. HıDaLco, Instituto Pirenaico de
Ecologia, P.O. Box 64, E-22 700 Jaca (Huesca); J. CANUT, D. GARCIA-FERRE,
Servei de Protecciö ı Gestiö de la Fauna, Direccıiö General del Medi Natural,
c/Cörcega 329 5°, E-08 037 Barcelona, Spain

Z. Säugetierkunde 57 (1992) 216-224
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

New data on the systematics and karyology
of Podoxymys roraimae (Rodentia, Cricetidae)

By A. PEREZ-ZAPATA, D. LEw, M. AGUILERA, and OÖ. A. REıG

Departamento de Estudios Ambientales, Universidad Sımon Bolivar, Caracas, Venezuela; Museo de

Historia Natural La Salle, Fundacion La Salle, Caracas, Venezuela; GIBE, Departamento de Ciencias

Biologicas, FCEyN, Universidad de Buenos Aires, Buenos Aires, Argentina, and Museo Nacional de
Ciencias Naturales, Madrid, Espania

Receipt of Ms. 19. 9. 1991
Acceptance of Ms. 10. 1. 1992

Abstract

Sixty years after ıts first description by H. E. AntHonY, the second record of the monotypic
akodontine cricetid Podoxymys roraimae was obtained at the type localıty, the summit of the Roraima
tepui, Venezuela. It was a juvenile female with little tooth wear. The new specimen permitted an
updated description of the species, and a more precisely characterization of ıts molar teeth, which have
clearly defined bunodont cusps and well developed mesolophids. Podoxymys is more closely related to
Microxus bogotensis than to species of Oxymycterus. The concept of an oxymycterine group is
discussed and rejected on the basis of recent electrophoretic results. Thus, the similarities between
Podoxymys and Oxymycterus are better considered as a result of convergence. Analysıs of standard
metaphase chromosomes of the new individual resulted ın a particularly low-numbered karyotype of
2n = 16. The occurrence of low-numbered karyotypes in different groups of eutherian mammals
indicates that genome condensation in a few chromosome pairs occurred independently in different
phylads. In the Akodontini, two such phylads occur, one involving Brasilian forms, and another
comprising a group of species of Akodon from the northern Andes. Podoxymys is more lıkely to
belong to the latter, both by biogeographical reasons, and because of its close resemblance with the
Venezuelan Microxus bogotensıis.

Introduction

The tepuis are tableland high elevations that rise abruptly interspersed within the forests
and savannas of northeastern South America. They lodge a unique flora and fauna which
has long attracted the attention of naturalists by the high frequency of generic and specific
andemisms (Mayr and PHELPsS 1967; STEYERMARK, 1986; OcHoA and GoRZULA 1992).
Among mammals, one outstanding example of such an endemism ıs Podoxymys roraimae,
a species of a monotypic genus of akodontine cricetid mice only known from the summit
of the Roraima tepui, which rıses up to above 2700 m in the southeastern corner of Bolivar
State (Venezuela). This species was described by AntHonY (1929) on the basıs of 5
specimens. Up to now no additional specimens have been found. Apart from the original
brief description by ANTHONY, those specimens were the basis of further partial descrip-
tions of its anatomy by GYLDENSTOLPE (1932), CARLETON (1973), and HınoJosa et al.
(1987). Recently, one individual was obtained during a brief expedition organızed by the
La Salle Natural History Museum of Caracas (MHNLS) in June, 1989. The new specimen
allowed to advance in the knowledge of the anatomy and systematics of this rare mouse,
and the acceptably successful preparation of chromosomes in the field permitted to report
for the first time ıts standard karyotype.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5704-0216 $ 02.50/0

New data on the systematics and karyology of Podoxymys roraimae 217

Material and methods

The single specimen of P. roraimae reported herein was a young female obtained during the night or
early morning of June 1, 1989. It was captured on a line of 100 Sherman live-traps laid at 2628 m a. s..
at the summit of the Roraima mountain. The trap line was set for sıx nights on a surface covered by a
carpet of the moss Sphagnum sp. in which various small cavities were scattered. The overall yield was
one P. roraimae and four Rhipidomys macconnell. Skins and skulls of all specimens were deposited in
the MHNLS, Caracas, were those of P. roraimae bear catalogue number MHNLS-8860. This
specimen was compared with notes and drawings of original specimens of P. roraimae taken
previously by one of the authors (OAR) at the American Museum of Natural History. Direct
comparisons have also been made with specimens of Akodon, Oxymycterus, Microxus, and other
South American cricetids from different collections. Fur and hair colors follow SMITHE (1975).
Standard body and cranıal measurements were taken with a Vernier calliper (app. 0.1 mm) and the eye
piece of a stereomicroscope (app. 0.01 mm). All measurements are given in mm. Nomenkclature of
enamel components of the molar teeth, follows Reıc (1977). Metaphase chromosomes were obtained
in the field by the bone marrow method (Reıc et al. 1971), and stained with Giemsa. Ten karyotypes
were constructed from enlarged photographic prints, and the lengths of chromosomes and chromo-
some arms were measured, averaged and expressed as a percentage of the total length of the female
haploid set (LHS) (Table) (Reıc et al. 1971). Chromosome nomenclature follows Levan et al. (1964),
Chromosomes were also assorted into size classes as follows: large-sized equal those > 9% of LHS;
medium-sized, those between 5.5 and 9%, and small-sized those between 2 and 5.5 %.

Results
Morphology

The data obtained from the new specimen, combined with our data from the original
specımens and published information on the stomach (CARLETON 1973) allow us to
compose the following description of P. roraimae:

Size small (head and body about or less than 100 mm) Tail long, as long as or a little
longer than head and body. Front claws moderately long (third claw 2.5-3 mm), slender
and pointed: claws of the hind feet as in Akodon. Fur dense, lax and moderately long, back
and sides of head and body, hind feet and tail unıformly dusky-brown (color 19). Hairs
long (10 mm on the back), soft and very abundant, blackish (color 82) in most of the length
from the base and cinnamon (color 123-A) at the tip. Pelage shortest at the head and the
ventral region, where the cinnamon staining is more evident. Eyes very small; ears of small
size but clearly visible, although pinnae are partially covered by the dense pelage. Skull
(Fig. 1) narrow and slender, with long and narrow muzzle, rather broad interorbıtal region
without trace of supraorbital beading, and a long, deep, moderately ınflated and evenly
rounded brain case. Upper profile of skull sloping forward from the frontoparietal suture.
Nasals shorter than frontals and rather narrow, with posterior ends well behind the fronto-
maxillary suture. Anterior borders of nasals and premaxillae moderately projected forward
beyond the incisors. Parietals short, less than half the length of frontals. Interparietal
reduced. Incisive foramına noticeably long, longer than the cheek tooth row and extending
backwards to the hypocone of the first molars. Palate short and broad, extending
backward to the level of last molars; cheek-tooth rows divergent to the front. Pterygoid
region long; mesopterygoid fossa open in front and parellel-sided. Zygomatic plate
reduced, narrow and low and markedly sloping backwards. Zygomatic arches week and
thread-like at the middle, scarcely flarıng beyond brain-case and gradually diverging
backward. Interorbital region broad, smooth and rounded, with supraorbital edges
rounded and moderately convergent backward. Bullae slightly inflated and moderate ın
sıze. Mandible slender, elongate and proodont, though less so than in Oxymycterus, with a
short coronoid process and small capsular projection. Upper incisors opisthodont and
relatively narrow. Molars rather small and broad, bunodont and brachyodont (Fig. 2).
Upper molars with lophs almost completely transverse. In Mi and M2 the main external
cusps are subequal, the para- and metaflexus are oriented backward, and enterostyle is

218 A. Perez-Zapata, D. Lew, M. Aguilera, and O. A. Reıig

Fig. 1. Skull and lower jaw of a juvenile female of Podoxymys
roraimae (MHNLS-8860) from the type localıty (Roraıma moun-
tain, SW of Bolivar State, Venezuela). Above: dorsal view of the
skull; middle: ventral view of the skull; below: lateral view of the
skull and mandible (enlarged x 2.8)

missing. M1 with some-
what reduced procin-
gulum, with visible an-
teromedian flexus and an-
teroflexus in moderately
worn teeth, mesoflexus
very narrow but present,
and mesoloph strongly re-
duced but not fully fused
with paraloph. M2 with
mesoloph well developed
but low, separated from
paraloph by a deep mexo-
flexus; mesostyle absent.
M3 strongly reduced, a-
bout % the length of M2.
Unworn lower molars with
opposing cusps somewhat
oblique in position, the lın-
gual ones more anterior
than the labial ones, tend-
ing to a simple prismatic
pattern wıth wear. Procin-
gulum of mi narrow and
simple, without anterome-
dıan flexid. Mesolophid
and mesoflexid well de-
veloped but low in ml and
m2, and mesostylid absent.
Ectolophid and ectostylid
may be present in ml, but
are absent in m2-m3. Third
lower molar moderately re-
duced, about % the length
of m2. Stomach unilocular-
hemiglandular, with re-
duced area of glandular
epithelium. Caecum well
developed, but very re-
duced, reaching only 4.4 %
of the total intestine length.
Large intestine also short.
Measurements of female

MHNLS-8860 and of the type specimen, female, AMNH 75586 (in parentheses; omitted
when unavailable): Total length 150.0 (196.0); head and body, 72.0 (101.0); taıl, 78.0
(95.0); hind foot 21.5 (23); ear, 13.4; greatest length of skull, 24.7 (27.5); length of nasal,
8.5 (11.0); zygomatic breadth, 11.2 (12.3); interorbital breadth, 5.6 (6.0); breadth of
rostrum at mid-point, 4.1 (4.2); breadth of brain case, 11.4 (12.3); incisive foramen (length
x breadth) 5.8 x 1.7 (7.2 x 2.1); dıastema length, 5.9 (6.9); length upper molar row, 4.14
(4.38); length of lower molar row, 4.50 (4.27); Mi, 1.79 x 1.24 (2.14 x 1.21); M2, 1.32 x
1.10 (1.40 x 1.21); M3, 0.69 x 0.77 (0.83 x 0.91); m1, 1.79 x 1.18 (1.85 x 1.24); m2, 1.24 x
1.10 (1.31 x 1.19); m3, 1.07 x 0.77 (1.07 x 0.94); total length small intestine, 414.0; total

New data on the systematics and karyology of Podoxymys roraimae 21)

>
i
k
3
7

Fıg. 2. Scanning electron microphoto of upper (left), and lower (right) molar teeth of the juvenile
female specimen of Podoxymys roraimae (MHNLS-8860) from the type locality (Roraima mountain,
SW of Bolıvar State, Venezuela)

transverse length, blınd intestine, 22.0; total measured length, large intestine, 53.0 (actual
length must be a little longer, as a small unmeasured cut-off portion must be added); body
weight, 108.

Cytogenetics

The karyotype of P. roraimae ıs strıking by the very low diploid and fundamental
(including sex chromosomes) numbers of 2n = 16 and FN = 26 (Fig. 3). The karyotype ıs
formed by five pairs of large biarmed, and three pairs of teleocentric chromosomes. As
arranged by size, pair 1 ıs made by very large metacentrics (Table) separated from the
following four elements by a sharp sıze gap. Pairs 2 and 3 are similar in sıze, the former
being submetacentric and the other metacentric. Pairs 4 and 5 are sımilarly-sızed sub-
metacentrics. A large size gap separates pair 5 from the medium-sized telocentric pair 6,
whereas pairs. 7 and 8 are small chromosomes. Therefore, each chromosome pair ıs very
distinctive ın size and morphology. As the single studied individual was a female, it ıs only
tentative to identify the X chromosomes. Based on the similarity between the karyotype of
P. roraimae and that of Akodon “arvicnloides” (see later) we tentatively identify the
chromosomes of pair 7 as the female sex chromosomes.

220 A. Perez-Zapata, D. Lew, M. Aguilera, and O. A. Reig

Statistics of mean lengths of entire chromosomes (T.L.) mean lengths their long (L.L.A.) and their
short arms (L.S.A.), and arm ratio (r) and their standard deviations (SD) of Podoxymys roraimae
from Mount Roraima, Bolivar State, Venezuela

The lengths are expressed as a percentage of the total chromosome length of the female haploid set

Chromosome

1
2
3
A
5
6
7
8

5u

Fig. 3. Giemsa-stained bone-marrow karyotype of Podoxymys roraimae, the same specimen of Figs 1
and 2

Discussion

The new specimen matches well enough the holotype and the original description ot P.
roraimae (ANTHONY 1929) as no casting doubts to its species ıidentification. The differences
found in size and morphology reflect the fact that the holotype was an adult with advanced
tooth wear, whereas MHNLS-8860 ıs a juvenile. This allowed us to examine in more detail
the molar structure, which resulted peculiar for akodontine standards by the well-
developed mesoloph-lophids and the bunodont cusps. However, both in the craneo-dental
and digestive system characters, P. roraimae fıts well with the diagnosis of the tribe
Akodontini (REıG 1987).

Of the eleven recognized extant genera of the Akodontini (REıG 1987), Podoxymys was
reported to be alike Oxymycterus (ANTHONY 1929) and Microxus (ELLERMAN 1941).
HERSHKOVvITZ (1966) proposed to distinguish within the akodont rodents an “oxymyc-
terine group”, including Oxymycterus, Podoxymys, Lenoxus, Microxus, and Abrothrix
(HERSHKOVITZ considered Microxus to be a synonym of Abrothrix, but ReEıc, 1987, found
no reasons for such asynonymy). The concept of an oxymycterine group has been recently
discussed by Hınojosa et al. (1987), who concluded that it is unclear. Recent elec-
trophoretic data strongly indicate that Microxus ıs more closely related to Akodon than to

New data on the systematics and karyology of Podoxymys roraimae Do

Oxymycterus, and that the latter is not close to Lenoxus (PaTTon et al. 1989). Besides,
Abrothrix together with Chelemys and Geoxus make a subclade of its own clearly
differentiated in genetic distance from the remaining Akodontini (SPOTORNO 1986;
BARRANTES et al. 1992).

As ELLERMAN (1941) surmised, Podoxymys ıs probably a close relative of Microxus. In
fact a closer relationship of Podoxymys to Microxus than to Oxymycterus is expected by
distribution, as Microxus ıs represented in the Venezuelan Andes, whereas species of
Oxymycterus are mostly distributed in the south of South America. We have for compari-
son specimens referred to M. bogotensis from the Andes of Venezuela. Certainly, M
bogotensis and P. roraimae resemble each other more than any of them resembles species of
Oxymycterus. They are sımilar in the relative forward extension of nasals and premaxillae,
the degree of reduction of the zygomatic plate, the long frontals, the more reduced
interparietal, and the deeper and shorter braincase. However, M. bogotensis has a shorter
pelage, a much shorter incisive foramına that scarcely reaches the front of first upper
molars, parallel cheek teeth rows, and much reduced third molars. Thus, Podoxymys may
well be a close relative of Microxus, but its generic distinction seems to be well warranted.

The karyotype of P. roraimae ıs remarkable by ıts very low diploid number. Karyoty-
pes wıth diploıd numbers lower than 20 are common among marsupials (Hayman 1990),
but they are a rarıty (about 1 %) among placentals (MATTHEY 1973). An extreme case is
that of the muntjak deer Muntjacus muntjak, with 2n = 6 and 2n = 8 ın different subspecies
(WURSTER and BENIRSCHKE 1977; WURSTER and ATkıns 1972). A karyotype of 2n = 14,
with polymorphic varıants anf 2n = 15 and 2n = 16 has been described for a Brasilian
akodontine erroneously referred to Akodon arvicnloides (MaıA and LANGGUTH 1981; for
its nomenclatorial status and references see LıascovicH and ReıG 1989). A monomorphic
2n = 18 karyotype occurs ın the akodontine Akodon urichi (Reıc et al. 1971), and
polymorphic complements of 2n = 16-17 occur ın Nectomys palmipes (BARROS et al. 1992),
whereas karyotypes of 2n = 17-18 with odd sex chromosome systems have been reported
in the arvicolid voles Ellobius Iutescens and Microtus oregoni (MATTHEY 1958), and 2n = 18
was also found in the murid Nannomys (MATTEY 1964). Karyotypes of 2n = 16 are also
known in some species of the leaf-nosed bats (BAKER 1973).

There are good reasons to maintaın that polarıty ın karyotype number among the
Akodontini was from a high-numbered plesiomorphic to a low-numbered apomorphic
state (VITULLO et al. 1986; Reıg 1987). The same trend was found to be most lıkely ın
other trıbes of South American crıcetids (GARDNER and PATTON 1976), and ın arvıcolıds
(MATTHEy 1958; Moopı 1987). Thus, the process of condensing the karyotypes to a low
number of chromosomes occurred independently in unrelated evolutionary phylads.

Karyotypes of Akodontini cover a wide range of diploıd numbers, from 2n = 14 to
2n = 54 (Reıc 1987, 1989; LıaskovicH and Reıc 1989). However, most of the 45
chromosomally known akodontine species have karyotypes within the 2n = 30-44 (42 %)
or the 2n = 52-54 classes (Reıg 1989). Of Microxus, only the karyotype M. bogotensis from
the Venezuelan päramos ıs known (BARRoSs and Reıc 1979), which ıs polymorphic with
2n = 35-37. Actually, among the Akodontini, the karyotype of P. roraimae ıs only com-
parable at the level of chromosome number and gross morphology with the 2n = 14-16
karyotype of Akodon “arviculoides”, and that of 2n = 18 of Akodon urichi. It is remarkably
similar to the 2n = 16 varıant of A. “arviculoides” from Recife (Mara and LANGGUTH
1981). Both share the same fundamental number, and differ mostly in the first autosomal
pair, which is submetacentric in A. “arviculoides”, but metacentric in P. roraımae. As
regards A. uricht, the differences are much greater and may involve several rearrangements.
Unfortunately, we failed to obtain adequate G-banding karyotypes to test how far the
resemblance between P. roraimae and A. “arvicnloides” is due to actual arm sharing.

In fact, a parallel trend towards lower diploid numbers seems to occur within the
Akodontini in two independent phylads. Reıg (1987) recognized a northern Andean

DD A. Perez-Zapata, D. Lew, M. Aguilera, and O. A. Reıg

phylad probably derived from a primitive stock ın the soutern puna region showing diploid
numbers progressively, although irregularly, decreasing northwards. This phylad includes,
among others, species and subspecies of Akodon such as A. aerosus bohiolus (2n = 38),
A. prophilus (2n = 26), A. mollıs (2n = 22-23), A. aerosus ssp. (2n = 22), A. torques (2n = 22)
A. tolimae (2n = 24), and A. urichi (2n = 18) (Reıc 1987; Patron et al. 1990). M. bogotensis
may represent a chromosomally more conservative offshoot of the same branch. As Reıc
(1987) suggested, P. roraimae ıs likely to be derived from the same stock. We now know
that it exemplifies an extreme case of karyotypic reduction consistent with the general
trend observed in the northern Andean phylad. But a trend in karyotypic condensation is
also evident in an independent phylad which dispersed towards Brasil from a postulated
north-central Argentinian dispersal sub-center, as represented by A. cursor of Misiones,
Paraguay, and south of Brasil (2n = 24), and the karyomorphs of 2n = 14-16 referred to
A. “arvicnloides” trom Sao Paulo, Rio de Janeiro and Recife (LrascovicH and Reıc 1989).
The close similarıty found between the karyotype of P. roraimae and the 2n = 16
karyomorph of A. “arviculoides” may be taken as suggesting a closer relation of the tepui
akodont to this phylad. However, besides the general disaprowal of hypotheses on
phylogenetic relations based on similarities among non-differentially stained karyotypes,
there are other reasons to discard this alternative view. There ıs ample evidence that the
tepuian fauna ıs closely linked to the Andean fauna (Mayr and PHELPs 1967). Besides, the
areas of distribution of P. roraimae and A. “arvicnloides” are separated by the Amazonian
Basın, a region thoroughly deprived of representatives of the Akodontinı.

Acknowledgements

EmıLıo HERRERA and Marcı LassIa are acknowledged for comments and suggestions, and ROGER
PEREZ, GABRIEL A. REIG and AnıBaL INVERNÖN for technical help. We also thank the personnel of the
Museo de Historia Natural La Salle expedition, especially GIUSEPPE COLONNELLO and PABLo Lau.
This paper was supported by a Venezuelan (Consejo Nacional de Investigaciones Cientificas y
Tecnolögicas) and Argentinian (Consejo Nacional de Investigaciones Cientificas y TeEcnicas) joint
grant given to M. AGUILERA and ©. A. Reıc.

Zusammenfassung

Neue Unterlagen über die Systematik und Karyologie von Podoxymys roraimae (Rodentia, Cricetidae)

Die akodontine Maus Podoxymys roraimae, von H. E. AnTHony nach fünf Exemplaren beschrieben
und 1929 einer monotypischen Gattung zugeordnet, wurde ım Juni 1989 erstmals wieder an der
Typuslokalität, dem Gipfel des Roraima tepui in Venezuela, gefangen. Anhand des juvenilen
Weibchens und der Originalserie wird eine genauere Beschreibung der Gattung und Art gegeben.
Podoxymys ist Microxus bogotensis ähnlicher als den Arten von Oxymycterus. Das Konzept einer
oxymycterinen Gruppe innerhalb der Akodontini erscheint unwahrscheinlich und wird auf der
Grundlage neuer elektrophoretischer Ergebnisse abgelehnt. Die Ähnlichkeit zwischen Podoxymys
und Oxymycterus ıst eher auf Konvergenz zurückzuführen. Die Analyse standardgefärbter Metapha-
sen des neuen Exemplares ergab eine bemerkenswert niedrige Zahl von 2n = 16 Chromosomen. Eın
Vergleich niedriger Chromosomenzahlen bei Säugetieren zeigte, daß die Konzentration des Genoms
in wenigen Chromosomenpaaren mehrfach in verschiedenen Stammbaumlinien erfolgte. Innerhalb
der Akodontini lassen sich zwei Linien unterscheiden; die eine umfaßt brasilianische Arten, die andere
eine Gruppe von Akodon-Arten der nördlichen Anden. Podoxymys scheint der letzteren nahezuste-
hen, sowohl aus biogeografischen Gründen als auch wegen seiner großen Ähnlichkeit mit dem
venezolanischen Microxus bogotensıis.

References

ANTHONY, H. E. (1929): Two new genera of rodents from South America Amer. Mus. Novitates 383,
1-6.

BAKER, R. J. (1973): Comparative cytogenetics of the New World leaf-nosed bats (Phyllostomatidae).
Periodicum Biologicum 75, 37-45.

New data on the systematics and karyology of Podoxymys roraimae 223

BARRANTES, G.; ORTELLS, M. O.; Reıc, ©. A. (1992): New studies on allozyme genetic distance and
varıiability in Akodontine rodents (Cricetidae), and their systematic implications. Biol. J. Linnean
Soc. London (in press).

BARRoSs, M. A.; Reıs O. A. (1979): Doble polimorfismo robertsoniano en Microxus bogotensis
(Rodentia, Cricetidae) del Paramo de Mucubaji (Merida, Venezuela). Acta Cient. Venezolana 30,
96.

BARROS, M. A.; REıc, ©. A.; PEREZ-ZAPATA, A. (1992): Cytogenetics and karyosystematics of South
American oryzomyine rodents (Cricetidae: Sigmodontinae). IV. Karyotypes of Venezuelan,
Trinidadian, and Argentinian water rats of the genus Nectomys. Cytogen. Cell Genet. 59, 34-38.

CARLETON, M. D. (1973): A survey of gross stomach morphology in New World Cricetinae
(Rodentia, Muroidea), with comments on functional interpretations. Misc. Publ. Mus. Zool.
Univ. of Michigan 146, 1-43.

ELLERMAN, J. R. (1941): The families and genera of living rodents. Volume II. Family Muridae.
London: British Museum.

GARDNER, A.L.; PaTTon, J. L. (1976): Karyotypic varıiation in oryzomyine rodents (Cricetidae) with
comments on chromosomal evolution in the Neotropical cricetine complex. Occ. Pap., Mus.
Zool., Louisiana St. Univ. 49, 1-48.

GYLDENSTOLPE, N. (1932): A manual of Neotropical Sigmodont rodents. Kungl. Svenska Vetensk.
Handl. (3rd. Series) 2, 1-116.

Hayman, D. L. (1990): Marsupial cytogenetics. In: Mammals from pouches to eggs: Genetics,
breeding and evolution of marsupials and monotremes. Ed. by J. A. MARSHALL GRAVES, R. M.
Hope, and D. W. Cooper. Australia, CSIRO (reprinted from Australian J. Zool., 37). pp.
189-207.

HERSHKOVITZ, P. (1966): South American swamp and fossorial rats of the scapteromyine group
(Cricetidae, Muridae) wıth comments on the glans penis in murid taxonomy. Z. Säugetierkunde
31, 81-149.

HınoJosa, P. F.; AnDERSoN, $.; PATTON, J. L. (1987): Two new species of Oxymycterus (Rodentia)
from Peru and Bolivia. Amer. Mus. Novitates 2898, 1-17.

LEvan, A.; FREDGA, K.; SANDBERG, A. A. (1964): Nomenclature for centromeric position on
chromosomes. Hereditas 52, 1-22.

LıAskovIcH, R. C.; Reıc, O. A. (1989): Low chromosomal number ın Akodon cursor montensis
Thomas, and karyologic confirmation of Akodon serrensis Thomas, in Misiones, Argentina.
J. Mammalogy 70, 391-395.

Mara, V.; LANGGUTH, A. (1981): New karyotypes of Brazilian akodont rodents with notes on
taxonomy. Z. Säugetierkunde 46, 241-249.

MATTHEY, R. (1958): Un nouveau type de determination chromosomique du sexe chez les mam-
miferes Ellobius Iutescens Th. et Microtus (Chilotus) gregoni Bachm. (Murides-Microtines).
Experientia 14, 240.

— (1964): La signification des mutations chromosomiques dans les processus d’esp£ciation. Etude
cytogenetique du sous-genre Leggada Gray (Mammalıa, Muridae). Archives de Biologie 75,
169-206.

— (1973): The chromosome formulae of eutherian mammals. In: Cytotaxonomy and vertebrate
evolution. Ed. by A. B. CHIArRELLI and E. Capanna. London, New York: Academic Press. Pp.
350-616.

Mayr, E.; PHELps, W. H. (1967): The origin of the bird fauna of the South Venezuelan highlands.
Bull. Amer. Mus. Nat. Hist. 136, 269-328.

Mopı, W. S. (1987): Phylogenetic analysıs of chromosomal banding patterns among the Nearctic
Arvicolidae (Mammalia, Rodentia). Syst. Zool. 36, 109-136.

OcHOA, J.; GORZULA, $. (1992): Los mamiferos del macızo del Chimantä, con algunas consideracio-
nes sobre la mastofauna de las cumbres tepuyanas. In: Reconocimientodel macızo del Chimanta.
Ed. by ©. Hußer. Caracas: Todman Editions (in press).

PATTon, J. L.; Myers, P.; SmitH, M. F. (1989): Electromorphic varıation in selected South American
akodontine rodents (Muridae, Sigmodontinae) with comments on systematic implications. Z.
Säugetierkunde 54, 347-359.

— — — (1990): Vicariant versus gradient models of diversification: the small mammal fauna of
eastern Andean slopes of Peru. In: Vertebrates in the tropics. Ed. by G. PETERS and R. HUTTERER.
Bonn: Museum Alexander Koenig. Pp. 355-371.

Reıc, ©. A. (1977): A proposed unified nomenclature of the enamelled components of the molar
teeth of the Cricetidae (Rodentia). J. Zool. London 181, 227-241.

— (1987): An assessment of the systematics and evolution of the Akodontini, with the description of
new fossil species of Akodon (Cricetide; Sigmodontinae). In: Studies in Neotropical Mammalogy.
Ed. by B. D. Patterson, and R. M. Tımm. Fieldiana Zoology, NS 39, 347-399.

— (1939). Karyotypic repatterning as one triggering factor in cases of explosive speciation. In:
Evolutionary Biology of Transient, Unstable Populations. Ed. by A. Fontpevıra. Berlin:
Springer Verlag. Pp. 246-289.

224 A. Perez-Zapata, D. Lew, M. Aguilera, and O. A. Reig

Reıc, ©. A.; OLıvo, N.; KısLısky, P. (1971): The ıdiogram of the Venezuelan vole mouse, Akodon
urichi venezuelensis Allen (Rodentia, Cricetidae). Cytogenetics 10, 99-114.

SPOTORNO, A. E. (1986): Systematics and evolutionary relationships of Andean phyllotine and
akodontine rodents. Ph. D. Diss., Univ. California, Berkeley.

SMITHE, F. B. (1975): Naturalist’s Color Guide. New York: American Museum of Natural History.

STEYERMARKR, J. A. (1986): Speciation and endemism in the flora of the Venezuela tepuis. In: High
Altıtude Tropical Biogeography. Ed. by F. VUILLEUMIER and M. MonAsSTERIO. New York:
Oxford University Press. Pp. 317-373.

VITULLO, A. D.; MERANI, M. $.; Reis, O. A.; Kayon, A. E.; ScacLIa, O. A.; Espınosa, M. B.;
PEREZ-ZaPATA, A. (1986): Cytogenetics of South American akodont rodents (Cricetidae). New
karyotypes and chromosomal banding patterns of Argentinian and Uruguayan forms. J. Mammal-
ogy 67, 69-80.

WURSTER, T. H.; Argıms, N. B. (1972): Muntjak chromosomes: a new karyotype for Muntiacus
muntiak. Experientia 28, 972-973.

WURSTER, T. H.; BENIRSCHKE, K. (1970): Indian muntjiac, Muntiacus muntjak: a deer with a low
diploıd number. Science 168, 1364-1366.

Authors’ addresses: ANTONIO PEREZ-ZAPATA and MARISOL AGUILERA, Departamento de Estudios
Ambientales, Universidad Sımön Bolivar, Apartado 8900, Caracas 1080-A, Vene-
zuela; DanıeL Lew, Museo de Historia Natural La Salle, Fundacıön La Salle,
Apartado 1930, Caracas 1010, Venezuela; OsvaLpo A. Reıc, GIBE, Depar-
tamento de Ciencias Biolögicas, FCEyN, Universidad de Buenos Aires. Pabellön
II, 4°. Pıso, Ciudad Universitarıa, 1428 Buenos Aires, Argentina, and Museo
Nacıonal de Ciencias Naturales, Madrid, Espana

Z. Säugetierkunde 57 (1992) 225-230
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Contribution to the study of the wild House mouse,
Genus MusL. (Mammalıa, Rodentia, Muridae) in Greece

Study of three populations based on lymphocyte antigen analysis
By S. E. FRAGUEDAKIS-TsoLIs

Section of Animal Biology, Department of Biology, Patras University, Patras, Greece

Receipt of Ms. 13. 5. 1991
Acceptance of Ms. 24.1. 1992

Abstract

Typed three Robertsonian wild mice populations from southern Greece, using 16 selected Ilymphocyte
antıgens. In all examined mice of the three populations the Thy-1.2 antigen was identified, which is
characteristic for the M. m. domesticus taxon. On the other hand, the Thy-1.1 allele characteristic for
M. m. musculus was not found. Moreover, it was indicated that the Ly-1.2 antigen was fixed in these
populations while the Ly-1.1 allele was absent. It ıs already known that although these two alleles
cannot be used as markers for the different Mus taxa, they can give information about the gene flow
between the populations studied.

A polymorphic distribution of the other antigens examined was noted and compared to other
European M. m. domesticus populations.

It can be concluded from the immunological point of view the studied populations belong to M. m.
domesticus, and confirms the recent opinıons that the Rb populations of Mus almost exclusively
belong to this taxon.

Introduction

According to many investigators, the entire Greek peninsula ıs inhabited by two mor-
phologically and biochemically distinct taxa of wild house mice (BONHOMME et al. 1978;
THALER et al. 1981a, b; BONHOMME et al. 1984). One of them belongs to the biochemical
group Mus-1 and is referred to as Mus musculus domesticus Schwarz and Schwarz, 1943
(DARVICHE and Orsını 1982; AUFFRAY et al. 1990), or as a full species Mus domesticus
Rutty, 1772. The other taxon belongs to the biochemical group Mus-4a, which according
to the recent nomenclatorial opinions (AUFFRAY et al. 1990) is Mus macedonicus Petrov &
Ruzic, 1983.

Many populations of Mus ın Greece are Robertsonian (GIagıa et al. 1987; TıcHy and
Vucak 1987), ı.e., individuals do not have the standard diploid chromosomal number (2n
= 40) known for Mus musculus but rather karyotypes with 2n = 24, 26, 29, 30
chromosomes. All these varıants have occurred by the process of Robertsonian fusion
(ROBERTSON and Rezs 1916). With respect to the phenomenon of chromosomal repattern-
ing where clearcut instances of speciation processes are very often ın progress (CAPANNA et
al. 1977) a clarıfıcation of the taxonomic status and inter- and intra-populational relation-
ships of the Rb populations of Greece is needed. Moreover, there is some discussion
concerning the presence of Robertsonian populations in subspecies other than Mus
musculus domesticus (Zıma et al. 1990).

Since the classification of different taxa of Mus can be undertaken by karyological,
genetical and immunological approaches, in this paper we focussed on the immunogeneti-
cal approach, based on the study of the major histocompatibility complex (MHC). The
MHOC is a large chromosome region containing a giant cluster of genes coding for antigens
(proteins) which are necessary for functions concerned with the immune response. These

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5704-0225 $ 02.50/0

226 S. E. Fraguedakis-Tsolıs

antigens are polymorphic. At least twenty of them are predominantly expressed on
lymphocytes and are therefore referred to as Ly antigens (McKenzie and PoTTER 1979).
KURIHARA et al. (1985) using monoclonal antibodies for Thy-1, Ly-1, and Ly-2 antigens
demonstrated that ın eight Mus musculus subspecies examined each possessed characteristic
phenotype patterns of these antigens. More recently, FIGUEROA et al. (1986) confirmed the
above observations.

Materials and methods

Mice: Wild mice ın this survey belong to three different populations. They were trapped at three
localities in southern Greece: 1) Kastritsı (Patras) 25 individuals with 2n = 29, 30, 2) Olympia 10
individuals with 2n = 24 and 3) Theba 10 individuals with 2n = 26, 30. Some of the animals were
maintained for a certain period ın our laboratory and then transported to Germany (Max-Planck-
Institut für Biologie, Abteilung Immungenetik, Tübingen). The remainder of animals were trans-
ported immediately after trappıng.

Antisera and monoclonal antibodies: The monoclonal antibodies used in this survey were kindly
provided by Dr. J. Kıeın, Max-Planck-Institut für Biologie. These antibodies detect 16 Ilymphocyte
antigens. Most of the antigens are expressed on T cells (Ly 1, Thy 1, L;T,, L, 3) but some are also
expressed on B (Ly 1, Ly5) cells and other cells such as brain cells, epithelial cells and fibroblasts. All
monoclonal antibodies used were obtained from ascites fluid produced by inoculation of inbred cell
lines into mice. Other antibodies were obtained from supernatants of a cell line grown in culture.

For details of the antisera used in this assay, see KrLEıIn (1972), ZALESKA-RUTCZYNsKA and KLEIN
(1977), Duncan and Krein (1980), and FIGUEROA et al. (1986).

Complement-dependent cytotoxic assay: For detection of the antigens in this assay single cell
suspensions prepared from thymus and Iymph nodes were used. Thymus cells were used for the Thy-
1.1, Thy-1.2, Ly-1.1, Ly-1.2, Ly-2.1 and Ly-2.2 antigens and the Iymph node cells for the detection
of Ly-6.2A, Ly-6.2C, Ly-6.2F, Ly-10, Ly-15.2, Ly-18.2, Ly-17.2, Ly-19.2, Ly-28.2. Bm antigens
(Table 1).

Table 1. Antigens tested and antibodies used to detect them

Antigen Antibody Reactivity of Reference
antibody with

Thy- 1.1 HO221 T cells MARSHAK-ROTHSTEIN et al. (1970)
Thy- 1.2 5032-1.3 cells MACKENZIE and POTTER (1979)
Ly - 1.1 7.20.6/3 T cells HOGARTH et al. (1980)

Ly -12 E3P® T cells MARK et al. (1982)

Ly -2.1 49-11-1 T cells HOGAaRTH et al. (1982)

Ly -2.2 19-178 T cells HAMMERLING (unpubl. data)

Ly - 6.2.A 58.106 TandB cells Kımura et al. (1984)

Ly -6.2.C SKIA2.446 T and B cells Kımura et al. (1984)

Ly - 6.2.F TU192.2.10 TandB cells Kreın et al. (unpubl. data)
Ly -10.1 T18/870 T and some B cells Kımura et al. (1980)

Ly -15.2 8.6.2 T cells POTTER et al. (1981)

Ly -18.2 58.261 TandB cells Kımura et al. (1981a)

Ly -17.(20).2 K9-361 TandB cells Kımura et al. (1981b)

Ly -19.2 K 10.6 B cells Tapa et al. (1981)

Ly —28.2 5075-12.1 TandB cells HOGARTH et al. (1984)
B2m S19/8 TandB cells TaDa et al. (1980)

Two different complement mixtures were necessary: One with the Iymph node cells in rabbit
normal serum, guinea pig normal serum, and Hank’s balanced salt solution (1:1:3), and the other
one with thymus cells ın guinea pig normal serum and Hank’s balanced salt solution (1:4).

To detect individual Ly antigens in wild mice, the lymph node and thymus Iymphocytes of these
mice were incubated with monoclonal antibodies in the presence of complement and the percentage of
killer cells was estimated. The microcytotoxicity test was carried out in Terasaki microplates (IC. A.
Greiner and Sohner, Nürtingen, F.R.G.), as previously described (ZaLEskA-RUTCZyNsKA et al. 1983).

The ceytotoxicity was evaluated automatically by the propidium idodide method (Brunıng et al.
1982).

|

Contribution to the study of the wild House mouse, Genus Mus L. in Greece DOT
Results and discussion

As can be seen from Table 2 each population has a different pattern of lymphocyte antigen
frequency. For some of these antigens it is characteristic that either they exist in all
examined individuals of the three populations (e.g. Thy- 1.2) or they are lacking ın all of
them (Thy-1.1 antigen). The Thy-1.2 Ilymphocyte antigen is considered as being charac-
teristic for the individuals belonging to the M. m. domesticus taxon (KURIHARA et al. 1985).
FIGUEROA et al. (1986) confirmed this observations but with one exception. Two of the
eight specimens from Costa Rica, expressed the Thy-1.1 antigen although they belong to
the M. m. domesticns subspecies. The possible explanation for this finding was either that
these two anımals are progeny of a mouse in which recurrent mutation caused the Thy-1.2,
Thy-1.1 conversion [substitution of a single amino acıd at position 89 (WILLIAMS and
GAaGNoN 1982)] or these two mice may indicate the existence of Thy-1 polymorphism,
perhaps present in some populations of M. m. domesticus. The presence of the characteris-
tic Thy-1.2 antigen, in all individuals examined here, verifies their systematic position in
the M. m. domesticus subspecies, a fact that is in agreement with morphological, biochemi-
cal and karyological data (FRAGUEDAKRIS et al. 1986; CHONDROPOULOS et al. 1992; GIAGIA
et al. 1987; Tichy and Vucak 1987). The study of some of the Ly Iymphocyte antigens
(Table 2) showed that the Ly-1.2 antigen ıs fixed ın all the examıned specimens of the

Table 2. Frequency of Ly antigens in different populations of wild mice

Population No. of Antigen frequences
anımals
tested

Thy-1.1 Thy-1.2 Ly-1.1 Ly-1.2 Ly2.1 Ly2.2 Ly-6.2A Ly-6.2C
Kastritsi 0) 1.0 0) 0.96 0.60 0.20 0.36 0.20

Olympia 0) 1.0 0) 1.00 0.60 0.20 0.20 0.10
Theba 0) 150 0) 1.00 0.70 0.40 0.40

OD Ds o yore [ODE 170 16,282
Kastritsi 929 0 0.59 089 4, 020 0,80, 105 0.40
Olympia 0.66 0.80 1.090 + 940... 0:80. 0.80 0.60
Theba 0 Oo oo 70070 0.70

population from Olympia and Theba and almost all specimens from Kastritsı, while the
Ly-1.1 has not been detected in any specimens of these population samples. These results
are ın agreement with those of KuRICHARA et al. (1985) and FIGUEROA et al. (1986) who
also mentioned that for different populations of M. m. domesticus there ıs a characteristic
mode of fixation of the antıgens Ly-1.1, Ly-1.2, ı.e., if the individuals of one M. m.
domesticus population express the Ly-1.1 antigen, the Ly-1.2 is not expressed and vice
versa. From these data, we could conclude that although it ıs not possible to use these
antigens as characteristic markers for the taxonomic possition of the specimens, they could
be used as markers for determining the migration rates between local populations
(FIGUEROA et al. 1986). The situation with regard to the Ly-2.1 and Ly-2.2 antigens ın thıs
study is as follows. The Ly-2.1 allele is very common in the three populations, while
Ly-2.2 only appeared ın low frequency. This ıs one more indication of the homogeneity of
the Greek populations. Rogınson et al. (1984) mentioned that the B5m? allele is charac-
teristic for M. m. musculus, since it ıs present in M. m. musculus and absent ın the M. m.
domesticus taxon. FIGUEROA et al. (1986) reported that half of the wild M. m. domesticus
populations typed by them, reacted with the B>m-specific antibody. As can be seen from
our results, the Bm? allele is absent from the two populations and is present in half of the
examined specimens of the third one. These results combined with those of FIGUEROA et

228 5. E. Fraguedakiıs-Tsolıs

al. (1986) do not confirm the hypothesis that the Bm? allele can be used as a marker for the
M. m. domesticus taxon.

The typing for the remaining Ly antıgen revealed a variability in the frequencies among
the three populations studied. Although for the majority of the Ly antigens, our results are
in agreement with those of FIGUEROA et al. (1986), some are in contrast. For example, the
Ly-28.2 antigen, which the above mentioned authors found to be absent in their collection
of wild mice, ıs present in all our populations. In addition, the Ly-18.2 antıgen, which is
very rare ın the European populations (FIGUEROA et al. 1986), was found frequently in our
populations. The reasons for these fluctuations of Ly antigens among the European M. m.
domesticus populations ıs at present unknown and remain to be elucidated. According to
the present data we can verify that the three examined populations belong to the same
taxon M. m. domesticus, a conclusion that is in agreement with correlative morphological
data. On the other hand, since the three populations are Rb we agree with the opinion of
Zıma etal. (1990) that the Rb populations ın the Mus species are almost exclusively limited
to the range of M. m. domesticus taxon.

Acknowledgements

I am grateful to Prof. Dr. J. Krein, Director of Max-Planck-Institut für Biologie, Abt. Immunogene-
tic, Tübingen, Germany, who kindly hosted me in the Institut and introduced me to the present
research project and also supplied monoclonal antibodies. I would also like to thank Dr. F. FIGSUEROA
for critical comments during the experimental period, Dr. H. Tıchy for providing mice and Prof. Dr.
B. MArmaRas and Prof. B. CHONDROPOULOS for their critical comments on the manuscript.

Zusammenfassung

Beitrag zu Untersuchungen an der wilden Hausmaus, Gattung Mus L. (Mammalıa, Rodentia, Muridae)
in Griechenland. Untersuchungen an drei Populationen aufgrund von Analysen mit Lymphozyten-
Antigenen

In dieser Arbeit werden drei Robertsonsche Wildmaus-Populationen aus Südgriechenland unter
Benutzung von 16 ausgewählten Lymphozyten-Antigenen gekennzeichnet. Bei allen untersuchten
Mäusen der drei Populationen wurde das Antigen Thy-1,2 identifiziert, welches typisch für das Taxon
M. m. domesticus ıst. Ferner zeigte sich, daß das Ly-1.2-Antigen in diesen Populationen vorhanden
war, während das Ly-1.1-Allel fehlte. Wie bereits bekannt, können beide Allele zwar nicht als Marker
für die verschiedenen Mus-Taxa dienen, sie ermöglichen jedoch Informationen über den Genaus-
tausch zwischen Populationen.

Eine polymorphe Verteilung der anderen untersuchten Antigene wurde angegeben und mit
anderen Populationen von europäischen M. m. domesticus verglichen.

Aus immunologischer Sicht kann die systematische Stellung der untersuchten Populationen als M.
m. domesticus bestätigt werden. Das steht in Einklang mit neueren Auffassungen, wonach die Rb-
Populationen von Mus fast ausschließlich zu diesem Taxon gehören.

References

AUFFRAY, J.; MARSHALL, ].; THALER, L.; BONHOMME, F. (1990): Focus on the nomenclature of
European species of Mus. Mouse Genome 88, 7-8.

BONHOMME, F.; BRITTON-DAVIDIAN, ].; THALER, L.; TRIANTAPHYLLIDIS, C. (1978): Sur ]’ existence
en Europe de quatre groupes de Souris (genre Mus L.) du rang espece et semi espece demonstree
par la genetique biochimique. C. R. Acad. Sci. Paris 287, 631-633.

BONHOMME, F.; CATALAN, J.; BRITTON-DAVIDIAN, J.; CHAPMAN, V. M.; MoRIWARI, K.; NEvo, E.;
THALER, L. (1984): Biochemical diversity and evolution in the Genus Mus. Biochem. Genet. 22,
275-303.

BrunIng, W.; CLass, J.; KARDOL, J.; LANSBERGEN, Q.; NaıpL, M.; TAnkE, H. (1982): Automated
reading of HLA-A, B, C, typing and screening. The propidium iodide method. Hum. Immunol.
5, 225-231.

CAPANNA, E.; CIVITELLI, M. V.; CrısTaLDı, M. (1977): Chromosomal rearrangement, reproductive
isolation and speciation in mammals. The case of Mus musculus. Bol. Zool. 44, 213-246.

CHONDROPOULUS, B.; G1IAGIA, E.; FRAGUEDAKIS-TsoL1s, S. (1992): Conbribution to the study of the

Contribution to the study of the wild House mouse, Genus Mus L. in Greece 229

taxonomy and zoogeography of wild house mouse, genus Mus L. (Mammalıa, Rodentia, Muridae)
in Greece. III. Morphological study of five populations from southern Greece. Säugetierkdl. Mitt.
(in press).

DARVICHE, D.; Orsını, P. (1982): Criteres de differentiation morphologique et biometrique de deux
especes de souris sympatriques: Mus spretus et Mus musculus domesticus. Mammalia 46, 205-217.

Duncan, R.; KLein, J. (1980): Histocompatibility-2 system in wild mice. IX. Serological analysis in
13 new congenic lines. Immunogenetics 10, 45-65.

FIGUEROA, F.; Tıchy, H.; McKenzie, 1.; HAMMERLING, U.; Krein, J. (1986): Polymorphism of
Lymphocyte Antigens-Encoding Loci in Wild Mice. Current Topics in Microbiology and
Immunology 127, 229-235.

FRAGUEDAKIS-TSOLIS, $S.; CHONDROPOULOS, B.; GIAGIA, E. (1986): Contribution to the study of the
taxonomy and zoogeography of the wild house mouse, genus Mus L. (Mammalia, Rodentia,
Muridae) in Greece. I. Serological and immunological study of three populations from southern
Greece. Acta veterinarıa 36, 95-106.

GıaGıa, E.; FRAGUEDAKIS-TSOLIS, $.; CHONDROPOULUS, B. (1987). Contribution to the study of the
taxonomy and zoogeography of wild house mouse, genus Mus, L. (Mammalia, Rodentia,
Muridae) in Greece. Il. Karyological study of two populations from southern Greece. Mammalıa
51, 111-116.

HOGARTH, M.; EDWARDS, J.; MCKENZIE, I.; GoDInG, W.; LinwE, F. (1982): Monoclonal antibodies
to murine Ly-2.1 cell surface antigen. Immunology 46, 135-144.

HOoGARTH, M.; HouLpen, A.; LATHAM, E.; SUTTON, R.; McKenzie, I. (1984): Definition of a new
alloantigen encoded by genes in Ly-6 complex. Immunogenetics 20, 57-69.

Kımura, $.; TADA, N.; HAMMERLING, U. (1980): A new lymphocyte alloantıgen (Ly-10) controlled
by a gene linked to the Lyt-1 locus. Immunogenetics 10, 363-372.

Kımura, $.; TapDa, N.; Liv, Y.; HAMMERLING, U. (1981a): A new mouse cell-surface antigen (ly-
m18) defined by a monoclonal antibody. Immunogenetics 13, 547-554.

Kımura, $.; TapDa, N.; Lriu-Lam, Y.; HAMMERLING, U. (1984): Studies of the mouse Ly-6 alloantigen
system. II. Complexities of the Ly-6 region. Immunogenetics 20, 47-56.

Kımura, S.; TaDa, N.; NAKAYAMA, E.; Liv, Y.; HAMMERLING, U. (1981b): A new mouse cell-surface
antigen (Ly-m20) controlled by a gene linked to Mus locus and defined by monoclonal antıbodies.
Immunogenetics 14, 3-14.

Krem, J. (1972): Histocompatibility-2-system in wild mice. I. Identification of five new H-2
chromosomes. Transplantation 13, 291-299.

KURIHARA, Y.; MiyAsHITA, N.; MORIWAKRI, K.; PETRAS, L.; BONHOMME. F.; CHo KonHno, $. (1985):
Serological survey of T-Lympocyte differentiation antigens in wild mice. Immunogenetics 22,
211-218.

MARSHAK-ROTHSTEIN, A.; FINK, P.; GRIDLEY, T.; RAULET, D. H.; BEvan, J.; GEFTER M. L. (1979):
Properties and applications of monoclonal antibodies directed against determinants of the Thy-1
locus. J. Immunol. 122, 2491-2497.

MARSHALL, J.; SAGE, R. (1981): Taxonomy of the house mouse. Symp. Zool. Soc. London 47, 15-25.

McKENZIE, ]. F. C.; POTTER, A. (1979). Murine Iymphocyte surface antigens. Adv. Immunol. 27,
179338.

POTTER, A.; HOGARTH, M.; McKenzie, I. F. C. (1981) Ly-15: A new murine Iymphocyte
alloantigenic locus. Transplantation 31, 339-342.

ROBERTSON, W. M.; Rees, B. (1916): Chromosome studies. I. Taxonomy relationships shown in the
chromosomes of Lettigidae and Acrididae. Chromosomes and varıations. J. Morphol. 27,
179331.

ROBINSON, J.; STEINMETZ, M.; MoRIwAKkI, K.; FISCHER-LINDAHL, K. (1984): Beta-2 microglobulin
types of mice of wild origin. Immunogenetics 20, 655-665.

TApa, N.; Kımura, $.; HATZFELD, A.; HAMMERLING, U. (1980): Ly-m11: The F-3 region of mouse
chromosome 2 controls a new surface alloantigen. Immunogenetics 11, 441-449.

Tapa, N.; Kımura, $.; Liv, Y.; TAyLoR, A.; HAMMERLING, U. (1981): Ly-m19: The Lyb-2 region of
mouse chromosome 4 controls a new surface alloantigen. Immunogenetics 13, 539-546.

THALER, L.; BONHOMME, F.; BRITTON-DAvIDIan, J. (1981a): Processes of speciation and semi-
speciation ın the house mouse. Symp. Zool. Soc. London 47, 2741.

THALER, L.; BONHOMME, F.; BRITTON-DAVIDIAn, ]J.; HAMAR, M. (1981b): The house mouse complex
of species: Sympatric occurrence of biochemical groups Mus-2 and Mus-4 ın Rumanıa. Z.
Säugetierkunde 46, 169-173.

Tıchy, H.; Vucak, I. (1987: Chromosomal polymorphism in the house mouse (Mus domesticus) of
Greece and Yugoslavia. Chromosoma 95, 31-36.

WHITE, D. (1978): Modes of specıation. San Francisco: W. H. Freeman.

WILLIAMS, A. F.; GAGNON, J. (1982): Neuronal cell Thy-1 glicoprotein: homology with immunog-
lobulin. Science, 216, 696-703.

ZALESKA-RUTCZYNSKA, Z.; FIGUEROA, F.; KLEin, J. (1983): Sixteen new H-2 haplotypes derived from
wild mice. Immunogenetics 18, 189-203.

230 S. E. Fraguedakis-Tsolis

ZALESKA-RUTCZYNSKA, Z.; KLEIN, J. (1977): Hıstocompatibility-2 system in wild mice. V. Serological
analysis of sixteen BI OW congenic lines. J. Immunol. 119, 1903-1911.
Zıma, J.; GAICHENKO, A. V.; Mac Horan, M.; RanJapı, I. S.; SABLINA, V. O.; WöjJcık, M. J. (1990):

Are Robertsonian varıations a frequent phenomenon in mouse populations in Eurasia? Biol. ].
Linn. Soc. 41, 229-233.

Author’s address: S. E. FRAGUEDAKIS-TsOLIs, Sect. Anımal Biology, Department of Biology, Patras
University, Patras, Greece

Z. Säugetierkunde 57 (1992) 231-237
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Genic divergence in Spalacopus cyanus
(Rodentia, Octodontidae)

By M. H. GALLARDO, C. ARANEDA, and NELIDA KÖHLER

Instituto de Ecologia y Evoluciöon, Universidad Austral de Chile, Valdivia, Chile

Receipt of Ms. 20. 12. 1991
Acceptance of Ms. 17. 2. 1992

Abstract

Studied electrophoretic varıation of proteins encoded by 23 locı in four populations of Spalacopus
cyanus. Mean polymorphism and heterozygosity were 18.5 % and 5.8 %, respectively. Low levels of
interpopulational genetic differentiation were found ($ = 0.93, D = 0.032). Fixation index indicated a
considerable degree of demic structuration (FST = 0.273), contrary to the inference that Spalacopus
forms extensive interbreeding populations. Levels of interpopulational allozymic differences do not
support the niche-width varıation hypothesis. The amount of genic varıation depends on the degree of
isolation between local populations. Isolation in turn is influenced by physiographic features and
historical chance events, and is not correlated to the geographic distance per se.

Introduction

Allozymic polymorphisms ın subterranean rodents are interpreted as the stochastic
outcome of factors including historical events and population structure (PATTON 1980;
PATTOoN and SMITH 1989), or as an adaptive consequence stemming from natural selection
(Nevo 1990; Nevo and SHAaw 1972). Historical events associated with the breeding
structure (PATTON 1980), and evlutionary constraints imposed by the fossorial way of lıfe
(Nevo 1979; Savıc and NEvo 1990) have been invoked to explain the patterns of genetic
varıatıion in Thomomys bottae (PATTON and Yang 1977), T. umbrinus (PATTON and FEDER
1978), and Geomys bursarıns (PENNEY and ZIMMERMAN 1976; BOHLIN and ZIMMERMAN
1982). Thus, gene flow is thought to be the causative agent responsible for patterns of genic
and chromosomal varıation as reflecting historical biogeography (PATTON and Yanc
1977). Alternatively, an adaptive strategy directed by natural selection operating in a
monotonous subterranean niche has been proposed for Spalax ehrenbergi (NEvo and
SHAw 1972), Thomomys talpoides (NEvo et al. 1974), and for the Bathyergidae (NEvo et
al. 1987).

Subterranean Spalacopus is a monotypic genus of endemic herbivorous rodents (Con-
TRERAS and GUTIERREZ 1991) distributed throughout the western slope of the Andes of
central Chile (REıse and GAaLLAarDo 1989a). Anımals depict the same populational
attributes (REıiG 1970) and physiological adaptive syndrome (CONTRERAS 1986) described
for other underground mammals (NEvo 1979). Preliminary ecological studies in
Spalacopus (REıG 1970) provided a basıs for correlating the inferred wandering nature of
the anımals with karyotypic stability (ReEıc et al. 1972). In this study we examine the
patterns of allozymic varıation and degree of genetic fragmentation in four natural
populations of Spalacopus cyanus from their coastal range. Low levels of interpopulation
genetic differentiation as predicted by the high vagility attrıbuted to Spalacopus are
compared with electrophoretic data to test the consistency of such an ecology-based
proposition.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5704-0231 $ 02.50/0

232 M. H. Gallardo, C. Araneda, and Nelida Köhler

Material and methods

Electrophoretic analysıs was carried out on 76 specimens belonging to four populations of Spalacopus
cyanus. Sample designations, geographic coordinates, and number of specimens examined were as
follows (Fig. 1): Spalacopus cyanus cyanus, Los Vilos (31°55’S, 71°31’W), 28; Los Cristales
(312557S, 71°297W), 7, Hluentelauquen 813575, 71322), 102 Spalacopus eyanusıımanlınıaa
Quirihue (36° 17' S, 72°32' W), 31. Voucher specimens were deposited in the Collection of Mammals,
Institute of Ecology and Evolution, Universidad Austral of Chile.

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zZ
=
zZ
W
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<<

Fig. 1. Map of collecting localities of Spalacopus cyanus

Kidneys and liver were removed from each specimen and stored in liquid nitrogen after sacrifice.
Homogenates, buffer systems, migration conditions, and mixtures for each system were prepared
according to SELANDER et al. (1971). Fifteen enzymes and two non-enzymatic protein (albumin and
transferrin) encoded by 23 presumptive genetic lociı were examined. Details on the enzymes analysed,
their tissue source, and electrophoretic procedures used are given in Table 1. Allozymes were named
alphabetically according to their mobility relative to the commonest allele. A locus was considered
polymorphic if the frequency of the most common allele did not exceed 0.95. D-statistics were
computed to test for deficiency or excess of heterozygosity (SWOFFORD and SELANDER 1989). NEr’s
(1978) unbiased distance (D) and ROGERSs’ similarity (S) coefficients (ROGERS 1972) were calculated to
compare pairs of samples. The genetic relationships among populations were represented by a
dendrogram, using the weighted and the unweighted pair-group cluster algorithm (SNEATH and SOKAL
1963). An analysis of heterogeneity between pairs of populations was conducted by a contingency
table using the Pearson chi-square statistic (SWOFFORD and SELANDER 1989). Spatial correlation ın
allele frequencies was examined by three distribution-free permutational approachs (MANTEL, KEN-
DALL and SPEARMAN) that compare genetic and geographic distance matrices (DIETZ 1983).

Population subdivision was assessed through WRIGHT’s F-statistics (WRIGHT 1965). All computa-
tions were performed in Biosys-1 (SwOFFORD and SELANDER 1989). The criterion of SLATKIN (1981)
for minimum sample size (n = 10) was used to correct sampling bias of FST.

Genic divergence in Spalacopus cyanus 233
Table 1. Enzymes, tissue sources and electrophoretic conditions resolved in Spalacopus cyanus

Enzyme Enzyme Locus Electrophoretic
commiısion abbreviation conditions and
number tissue source!

Isocitrate dehydrogenase ICD-1 4 (K)
ICD-2 4 (K)
MDH-1 4 (K)
MDH-2 4 (K)
Corı 5 (L)
ON 5 (L)
GPD 58)
Gd 6 (K)
LDH-1 3 (K)
LDH-2 3 (K)
xDH 3 (K)
GPI ZU)
PGM-2 Z (08)
PGM-3 7 (L)
PGD ZA UD)
ADH-1 9 (L)
ADH-2 9 (L)
HK 9 (L)
ME-1 5 (L)
ME-2 5 (L)

Malate dehydrogenase

NNNN

Glutamate-oxaloacetate transamınase

Glycerol-3-phosphate dehydrogenase
Glucose 6-phosphate dehydrogenase
Lactate dehydrogenase

NNGO

Xanthine dehydrogenase
Glucose phosphate isomerase
Phosphoglucomutase

A

Phosphogluconate dehydrogenase
Alcohol dehydrogenase

Hexokinase
Malıc enzyme

a1 124
dla,
,
ol)
2.6181
2468. 1
11158
tale
11.12
22
ZA
De
DES
DEN
Nallalla;
ee
Nolaıla
ZLl
elle
Nollollzı

ou®)

from SELANDER et al. (1971). Tissue source (L) = liver, (K) = kidney.

Results

Eight of the 23 locı analyzed (GOT-1, TRFER, PGI-2, PGM-2, PGM-3, ADH-1, ADH-
2, HK) were polymorphic in one or more populations whereas the remainder were
monomorphic across all populations (Tab. 2). Four of the variable locı (GOT-1, PGM-2,
PGM-3, ADH-2) were monomorphic in two or three populations.

The average number of alleles per locus ranged from 1.1 (Quirihue) to 1.3 (Huentelau-
quen and Los Vilos). Polymorphism per population fluctuated from 8.7 % (Quirihue) to
26.1 % (Los Vilos), with 19.6 % for overall polymorphism across all populations. Direct-
count heterozygosity per population ranged from 0.6 % (Quirihue) to 7.3% (Los Vilos),
with an unweighted mean across all samples of 4.5 %.

D-statistics indicated a deficiency of heterozygotes in locı PGM-3 and ADH-1, and
total absence of heterozygotes in locı GOT-1, PGI-2, and ADH-2, suggesting that some
populations are influenced by nonrandom mating and small effective population sizes
(BARROWCLOUGH 1980). Fixation of otherwise polymorphic alleles (GOT-1, TRFER,
PGM-2, PGM-2, ADH-1) was observed in the Quirihue sample.

High values of genetic similarity, ranging from 0.972 (Los Cristales - Los Vilos) to
0.900 (Quirihue — Huentelauquen) were found. The genetic distance (X = 0.032) ranged
from 0.001 (Los Vilos -— Huentelauquen) to 0.074 (Quirihue — Huentelauquen). The non-
significant results (P > 0.079) otained in the tests of association between geographic and
genetic distance matrices indicated a nearly random distribution of genotypes (EPPERSON
and ALLARD 1989).

The UPGMA and the WPGMA phenetic clustering procedures using genetic distances
gave similar results, identifying two genetic subgroups (Fig. 2). The first was formed by
the three northern samples, with Los Vilos and Los Cristales depicting the closest affınıty.
The second group was formed by the Quirihue sample, removed from the rest by the
fixation of specific alleles (TRFER, ADH-1) that were polymorphic in the other samples

234 M. H. Gallardo, C. Araneda, and Nelhida Köhler
Table 2. Allele frequencies of eight variable loci of four populations of Spalacopus cyanus

Population

Quirihue Los Vilos Los Cristales Huentelauquen
(N = 31) (N = 28) (N=7) (N =10)

.000 .036 .000 .000
1.000 964” 1.000 1.000

.300
.700

.300
.300
400”

.100
.900

.000
1.000

.800
.200

.000
1.000

.107 ; .100
.893 : .900

* Significantly different from the Hardy-Weinberg equilibrium.

(Tab. 1). The test for genetic heterogeneity between populations indicated significant
differences between every pair of populations except Los Vilos and Los Cristales (P =
0.37), which were considered homogeneous by the test.

The mean FST was 0.273, indicating extensive genetic subdivision, despite the low
genetic distances recorded. This means that 27 % of the total varıance in allelic frequencies
is expressed between the populations (Zink and WINKLER 1983). If the Quirihue sample is
removed from the analysıs, maximum varıance in allele frequency drops to FST = 0.140.
Since an inverse correlation exists between Nm and FST, this indicates that an average of
one individual every second generation is exchanged among populations (HARTL and
CLARK 1989). The inbreeding coefficient (FIS = 0.307) permitted examination of within-
population breeding structure (VAN DEN BusscHE et al. 1987). Negative FIS values were
obtained for TRFER, PGM-2, and HK, reflecting fewer homozygous than expected under
random mating (CHESSER 1983; RyMan et al. 1980).

Discussion

These samples show levels of genetic varıation typical of fossorial rodents (NEvo 1979).
Mean heterozygosity and polymorphism are within the ranges obtained in Geomys
tropicalis (BOHLIN and ZIMMERMAN 1982), Thomomys umbrinus (HAFNER et al. 1987), and
Thomomys talpoides (NEvo et al. 1974).

|

Genic divergence in Spalacopus cyanus 235

.07 05 .03 .02 00
m 4

QUIRIHUE

LOS VILOS

LOS CRISTALES
HUENTELAUQUEN

el
07 .05 03 .02 .00

DISTANCE

Fig. 2. Distance phenogram between populations of Spalacopus cyanus. The unweighted pair-group
algorıthm was used to cluster NEr’s genetic distances (NEI 1978). Cophenetic correlation coefficient:
0.80

Low H has been invoked to be an adaptive strategy in the relatively uniform subterra-
nean environment (NEvo 1990; NEvo and SHaw 1972). Although a regime of “homoselec-
tion” could be claimed for the excess of monomorphic loci in the Quirihue population,
interpopulation genic differentiation argues against this explanation. If environmental
heterogeneity alone were sufficient to maintain genetic variability, the same alleles under
the niche-width hypothesis should be promoted by directional selection in all populations,
regardless of distance (PATTON and FEDER 1978). High levels of homozygosity and low
levels of polymorphism in the Quirihue sample are better explained as stemming from
founder events affecting a geographical isolate where a decrease ın the frequency of
heterozygotes i is expected to occur. A sımilar effect, but due to a small sample size is
observed in the Huentelauquen sample where extensive inbreeding increases homozygos-
ity while the genus’ colonıal behavior further reduces the effective population sıze (REISE
and GALLARDO 1989b). This results in a pattern that mımics homoselection, especially ın
locı segregating at frequencies close to zero or one (GALLARDO and KÖHLER 1992).

Gregarıous Spalacopus occupies a common burrow, establishing large populations
formed by many small, nomadic colonıes where no less than three generations coexist
(Reıcg 1970). This nomadic behavior is thought to be a consequence of their herbivory,
limited to bulbs of geophytes (ReEıc 1970). From these observations, high vagility has been
inferred, and a concomitant enhancement of gene flow is expected to occur. Accordingly,
chromosome uniformity and low taxonomic diversification are explained by the anımal’s
feeding behavior (Reıc et al. 1972). Nevertheless, diet resources are not depleted by
feeding activities; on the contrary, bulb regeneration seems to be facılitated through seed
germination suggesting coevolution of geophytes and S$. c. cyanus (CONTRERAS and
GUTIERREZ 1991). A sımilar feeding dynamic was observed in $. c. maulinus feeding on
Dioscorea longipes. Here, regermination induces a recurrent pattern of revisiting old
dwelling areas, reversing the anımals’ nomadic habiıtus, thus arguing against high vagılity
(REISE and GALLARDO 1989b). Apparently, genetic drift plays a significant role ın shapıng
the genetic structure of these populations. As the effective population sıze ıs small, local
extinctions and concomitant erosion of the genetic varıation by historical bottlenecks are
likely to occur (MARUYAMmA and FuErsTt 1985; WADE and McCAuLe£y 1988).

These Spalacopus populations occur in descrete patches where the dynamics of finite
populations involve the internal demographic potential (LANDE 1987) and external factors
stemming from habiıtat fragmentation (Hastınas and Woum 1987; Hanskı 1991).
Accordingly, it seems that gene flow is efficient to maintain genetic integrity only ın short
distances where habitat continuity and the distribution of suitable soil types allows ıt. On a
larger geographic scale, interpopulation genetic cohesion is affected by chance events

236 M. H. Gallardo, C. Araneda, and Nelida Köhler

related to physiographic features (REISE and GALLARDO 1989a). Thus, long distance gene
flow ıs affected by stochastic events acting ın a long-term historical scale within finite
populations, and thus may not be correlated at present with actual distances (PATTON and
Yang 1977).

Acknowledgements

We thank Corporacıön Nacional Forestal and Servicio Agricola y Ganadero for providing collecting
permits. Field work assistance was provided by R. Aros, F. Monpaca and D. Reıse. This research
was partially funded by Fondo Nacıonal de Ciencias, Grant 92-178, and Direcciön de Investigaciön y
Desarrollo, Universidad Austral de Chile, Grant S-91-11 to MHG.

Zusammenfassung

Genetische Divergenz bei Spalacopus cyanus (Rodentia, Octodontidae)

Die elektrophoretisch ermittelte Proteinvarıation von 4 Populationen von Spalacopus cyanus ließ sich
in 23 Loci kodifizieren. Mittlerer Polymorphismus und mittlere Heterozygose betrugen 18,5 % bzw.
5,8%. Es wurde ein geringer Grad an interpopulationärer genetischer Differenzierung gefunden ($ =
0,93; D = 0,032). Der Fixierungs-Index zeigte im Gegensatz zur Annahme, daß bei Spalacopus
extensive Durchmischung vorherrscht, ein beträchtliches Ausmaß an demischer Strukturierung (FST
= 0,273). Der Grad allozymischer interpopulationärer Differenzen stützt nicht die Hypothese der
Variation von Nischen-Weiten. Das Ausmaß an genetischer Variation beruht auf dem Isolationsgrad
zwischen lokalen Populationen. Isolierung ist durch physiographische Gegebenheiten und historische
Chancenereignisse beeinflußt und ist nicht mit der geographischen Distanz per se zu korrelieren.

Literature

BARROWCLOUGH, G. F. (1980): Genetic and phenotypic differentiation in a wood warbler (genus
Dendroica) hybrid zone. Auk 97, 655-668.

Bohn, R. G.; ZIMMERMAN, E. G. (1982): Genic differentiation of two chromosome races of the
Geomys bursarins complex. J. Mammalogy 63, 218-228.

CHESSER, R. K. (1983): Genetic varıability within and among populations of the black-tailed prairie
dog. Evolution 37, 310-331.

CoNTRERAs, L. C. (1986): Bioenergetics and distribution of fossorial Spalacopus cyanus (Rodentua):
thermal stress, or cost of burrowing? Physiol. Zool. 59, 20-28

CONTRERAS, L. C.; GUTIERREZ, J. R. (1991): Effects of the subterranean herbivorous rodent
Spalacopus cyanus on herbaceous vegetation in arıd coastal Chile. Oecologia 87, 106-109.

Dietz, E. ]J. (1983): Permutation tests for association between two distance matrices. Syst. Zool. 32,
21-26.

Epperson, B. K.; Arrard, R. W. (1989): Spatial autocorrelation analysıs of the distribution of
genotypes within populations of the lodgepole pine. Genetics 121, 369-377.

GALLARDO, M. H.; KÖHLer, N. (1992): Genetic divergence in Ctenomys (Rodentia, Ctenomyidae)
from the Andes of Chile. J. Mammalogy.

HArFNER, M. S.; HAFNER, ]J. C.; PATTon, J. L.; SMITH, M. F. (1987): Macrogeographic patterns of
genetic differentiation in the pocket gopher Thomomys umbrinus. Syst. Zool. 36, 18-34.

Hanskt, I. (1991): Metapopulation dynamics: brief history and conceptual domain. Biol. J. Linnean
Soc. 42, 3-16.

HarTL, D. L.; CLark, A. G. (1989): Principles of population genetics. Massachusetts: Sinauer.

Hastıincs, A.; Worin, C. L. (1989): Within patch dynamics in a metapopulation. Ecology 70,
1261-1266.

LANDE, R. (1987): Extinction thresholds in demographic models of territorial populations. Am.
Naturalist 130, 624-635.

Mann, G. (1978): Los pequenos mamiferos de Chile. Marsupiales, quiröpteros, edentados y roedores.
Gayana, Zool. 40, 1-342.

ManTEL, N. (1967): The detection of disease clustering and a generalized regression approach. Cancer
Res. 27, 209-220.

MARUYAMA, T.; FUERST, P. A. (1985): Population bottlenecks and nonequilibrium models in
population genetics. II. Number of alleles in a small population that was formed by a recent
bottleneck. Genetics 111, 675-689.

Neı, M. (1978): Estimation of average heterozygosity and genetic distance from a small number of
individuals. Genetics 89, 583-590.

Nevo, E. (1979): Adaptive convergence and divergence of subterranean mammals. Ann. Rev. Ecol.
Syst. 10, 269-368.

Genic divergence in Spalacopus cyanus 237

— (1990): Genetic diversity and its ecological correlates in nature: comparisons between subterra-
nean, fossorial, and aboveground small mammals. In: Evolution of subterranean mammals at the
organısmal and molecular levels. Ed. by E. Nevo and O. A. Reıc. New York: Allan R. Liss.

NEvo, E.; BEN-SHLOMO, R.; BEILES, A.; Jarvıs, J. U. M.; Hıckman, G. C. (1987): Allozyme
differentiation and systematics of the endemic subterranean mole rats of South Africa. Biochem.
Syst. Ecol. 15, 489-502.

NEvo, E.; Kım, Y. ]J.; SHaw, R.; THAELER, C. S. (1974): Genetic varıatıon, selection and speciation in
Thomomys talpoides pocket gophers. Evolution 28, 1-23.

NEvo, E.; SHaw, C. R. (1972). Genetic varıation in a subterranean mammal, Spalax ehrenbergi.
Biochem. Genetics 7, 235-241.

Oscoop, W.H. (1943): The mammals of Chile. Field Mus. Nat. Hist., Zool. Ser. 30, 1-268.

Patron, J. L. (1980): Chromosomal and genic divergence, population structure and speciation
potential in Thomomys bottae pocket gophers. In: Ecologia y Genetica de la Especiaciön Animal.
Ed. by ©. A. Reıc. Caracas: Equinoccio.

PATTon, J. L.; FEDER, J. H. (1978): Genetic divergence between populations of the pocket gopher,
Thomomys umbrinus (Richardson). Z. Säugetierkunde 43, 17-30.

Patron, J. L.; SMITH, M. F. (1989): Population structure and the genetics and morphologic divergence
among pocket gopher species (genus Thomomys). In: Speciation and its consequences. Ed. by D.
OTTE and J. A. ENDLER. Massachusetts: Sinauer Assoc.

PaTTon, J. L.; Yang, S. Y. (1977): Genetic varıation in T’homomys bottae pocket gophers: macrogeog-
raphic patterns. Evolution 31, 697-720.

PENnNEY, D. F.; ZIMMERMANn, E. G. (1976): Genic diverence and local population differentiation by
random drift in the pocket gopher genus Geomys. Evolution 30, 473-483.

Reıc, ©. A. (1970): Ecological notes on the fossorial octodont rodent Spalacopus cyanus (Molina). ].
Mammalogy 51, 592-601.

Reıc, ©. A.; SPOTORNO, A.; FERNANDEZ, R. (1972): A preliminary survey of chromosomes ın
populations of the Chilean burrowing octodont rodent Spalacopus cyanus Molina (Caviomorpha,
Octodontidae). Biol. J. Linn. Soc. 4, 29: 38.

ReIsE, D.; GALLARDO, M. H. (1989a): Intraspecific variation in facıng-water behaviour of Spalacopus
cyanus (Octodontidae, Rodentia). Z. Säugetierkunde 54, 331-333.

Reise, D.; GALLARDO, M. H. (1989b): Biology of the coruro Spalacopus cyanus manlinus Osgood
(Rodentia, Octodontidae) from Chile. V. Int. Theriol. Congress. Abstracts of papers and posters
1, 33-34.

ROoGERs, J. S. (1972): Measures of genetic similarity and genetic distance. Studies in genetics. Univ.
Texas Publ. 7113, 145-153.

Ryman, N. R.; REUTTERALL, C.; NYGREN, K.; NYGREn, T. (1980): Genetic varıatıon and differentia-
tion ın scandinavian moose (Alces alces): are large mammals monomorphic? Evolution 34,
1037-1049.

Savıc, I. R.; NEvo, E. (1990): The spalacidae: evolutionary history, speciation and population
biology. In: Evolution of subterranean mammals at the organısmal and molecular levels. Ed. by E.
Nevo and ©. A. Reıc. New York: Wiley-Riss. Pp. 129-153.

SELANDER, R. K.; SMITH, M. H.; Yang, S. Y.; Jonnson, W. E.; GENTRY, ]J. B. (1971): Biochemical
polymorphism and systematics in the genus Peromyscus. I. Variation ın the old-field mouse
Peromyscus polionotus. Univ. Texas Publ. 7103, 49-9.

SLATKIN, M. (1981): Estimating levels of gene flow ın natural populations. Genetics 99, 323-335.

SNEATH, P. H. A.; SokAL, R. R. (1973): Numerical Taxonomy. San Francisco: W. H. Freeman.

SWOFFORD, D. L.; SELANDER, R. B. (1989): Byosys-l. A computer program for the analysis of allelic
varlation ın population genetics and biochemical systematics. Illinoıs Nat. Hist. Survey.

VAN DEN BusscHE, R. A.; HAMILTON, M. ].; CHESSER, R. K.; SCRIBNER, K. T. (1987): Genetic
differentiation among cottontails from isolated playa basins. Genetica 75, 153-157.

WADE, M. ]J.; McCautry, D. E. (1988): Extinction and recolonization: their effects on the genetic
differentiation of local populations. Evolution 42, 995-1005.

WRIGHT, $. (1965): The interpretation of population structure by F-statistics with special reference to
systems of mating. Evolution 1, 395-420.

ZınK, R. M.; WINKLER, D. W. (1983): Genetic and morphological similarıty of two California gull
populations with different life history traits. Biochem. Syst. Ecol. 11, 397-403.

Authors’ address: MıLTOn H. GALLARDO, NELIDA KÖHLER and CRISTIAN ARANEDA, Instituto de
Ecologia y Evoluciön, Universidad Austral de Chile, Casılla 567, Valdıvia, Chile

Z. Säugetierkunde 57 (1992) 238-247
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

The population dynamics of rodents at Settlers, Transvaal,
South Africa

By M.R. PErrın, R. H. SLOoTow and J. M. MENDELSOHN

Department of Zoology and Entomology, University of Natal, Pietermaritzburg, South Africa,
and State Museum, Windhoek, Namibia

Receipt of Ms. 16. 9. 1991
Acceptance of Ms. 5. 2. 1992

Abstract

Studies of populations of Mastomys natalensis and Rhabdomys pumilio have shown that densities
increased ın late summer and peaked in midwinter. Numbers were low in spring over midsummer.
Small numbers of Otomys angoniensis were caught throughout the year. Breeding in M. natalensis
ended in March-April and recommenced in August-September. Breeding in R. pumilio ended in May
and recommenced in August. Reproductively active adult O. angoniensis individuals were present
throughout the year. There was a small peak in juvenile numbers of M. natalensis and R. pumilio in
spring, but little juvenile recruitment over midsummer. The mean body mass of M. natalensis and R.
pumilio declined from a peak in March to low values throughout the winter, followed by a slight
increase ın spring. The body mass of O. angoniensis was highly varıable. The low numbers of O.
angoniensis caught are ascrıbed to trap-shyness rather than low density in the field. O. angoniensis was
probably present ın faırly high numbers throughout the year.

Introduction

Rodent population census, by trapping, has been done extensively at varıous localıties ın
South Africa, but usually at monthly intervals, or longer. In order to ascertain possible
subtleties in rodent demography, trapping was instituted weekly. A prior study by
MENDELSOHN (1982a) found three common rodent species, the multimammate mouse
Mastomys natalensıis, the fourstriped field mouse Rhabdomys pumilio, and the angoni vlei
rat Otomys angoniensis to be resident on the study area at Settlers. This paper deals with
the demography of the rodent populations in relation to season and body mass dynamics.

Material and methods

The study site was situated near Settlers (24° 57'S, 28° 33’ E) on the Springbok Flats, Transvaal, South
Afrıca. This study area fell inside that of MENDELSOHN (1982a, b). The topography was flat, but
drainage lines produced a gently rolling landscape from East to West. The area was used for mixed
farming, with cultivated fields (72 °5) interspersed with patches of grazed bushveld (27 %). The entire
area was on Springbok Flats Turi ıhornveld (Acocks 1975). The rainfall data (Fig. 1) were obtained
from Deeside farm, on the southern edge of the study area.

Mastomys natalensis has been separated into sıbling species (M. natalensis and M. coucha) based on
chromosome numbers and haemoglobin electrophoresis (BRONNER 1986; GREEN et al. 1980; MEESTER
et al. 1986). MEESTER et al. (1986) do not give the Springbok Flats (Northern Transvaal) in the
distribution of either species. As the M. natalensis population at Settlers was not ıdentified to sıbling-
species level, we will use M. natalensis as referring to M. natalensis sensu lato throughout.

Two live-trap lines were established, the first (Line A) through grazed bushveld on black turf
[MEnDELsoHn’s (1982a) line 2]. This line crossed a dry river bed which was later flooded. The second
(Line B) ran along a fence between a tarred road (5 m away) and a cultivated field (5 m away). This
line incorporated both black turf as well as red clay [MEnDELsoHn’s (1982a) lines 4 and 5]. Trapping
was initiated in February 1986, and in June 1986 the number of traps was increased from 20 to 35 in
line A and from 20 to 40 in line B. Both lines were set weekly, for two trapping nights per week. The

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5704-0238 $ 02.50/0

The population dynamics of rodents at Settlers, Transvaal, South Africa 239

a 150

50 |
M

150

RAINFALL (mm)

o Ss
ars
VE]
=D
|]
Ol rare
SER BRETT ZEN]
ST ss Zee
ei asE Ge

100

sol II

AVERAGE RAINFALL (mm)

0 ia
JE MITA OZZNZID

Fıg. 1. Rainfall figures at Deeside Farm on the southern border of the study area. a: Rainfall during the

study period. b: Average raıinfall from 1978 to 1987

traps were placed 6 m apart, adjacent to runways or other signs of rodent activity (to increase the
capture rate of O. angoniensis). The traps were baited with peanut butter and oats, and left in place
throughout the study period. From February to May 1986 all anımals caught were removed, but from
mid-June 1986 capture-mark-recapture (FLOWERDEW 1976) was instituted, using the toe-clipping
method (Twıcs 1875a).

Additional trappıng was done using snap-traps, placed randomly along a field verge between two
cultivated fields [on black turf (MENDELSOHN 1982a, line 4)]. These traps provided data on population
age and sex structures, and body mass.

All anımals were identified, aged, sexed, weighed, and their reproductive condition noted.
Reproductively active individuals were defined as those that were scrotal (males), or that were
perforated, pregnant or lactating (females) (Twıcc 1975b). Body mass was used to separate individuals
into juvenile and adult age classes, with the separating mass being: M. natalensis - 30 g (Davıp and
Jarvıs 1983); R. pumilio - 30 g (Brooks 1974, 1982; Davıp and Jarvıs 1985) and O. angoniensis —
50 g (Davıs 1973). Individuals which showed reproductive activity although weighing less than the
above values, were considered to be adults.

Two indices of population numbers were obtained: a. the minimum number of mice alive (MNA)
(Davın and Jarvıs 1985) [MNA = the number of mice actually caught + the number of mice marked
before the I" trapping occasion, which were not caught at the I occasion but were captured
subsequently (i.e. mice assumed to have been present at time I)]. b. As the number caught per 100
trap-nıghts (1 trap night = 1 trap set for 24 hours) (CHrpumayo 1984; MENDELSOHN 1982).

Results

Three species dominated the captures: Mastomys natalensis, Rhabdomys pumilio and
Otomys angoniensis. Occasionally shrews (Crocidura spp. n < 20), the striped mouse
Lemniscomys rosalia (n = 2) and the pouched mouse Saccostomus campestris (n = 1) were
caught. The results focus on the first three species.

240 M. R. Perrin, R. H. Slotow, and J. M. Mendelsohn

Population numbers

Numbers of M. natalensıs (Fig. 2a, b) increased from February to the end of June, and
then gradually decreased over late winter. There was a slight peak in late spring, low
numbers over midsummer, and an increase towards the end of summer (Fig. 2.1b). The
MNA showed fairly constant numbers over winter, a slight increase in late spring and a
decrease over midsummer.

Fewer P. pumilio were caught (Fig. 3a, b) than M. natalensis. R. pumilio showed the
same seasonal trend in numbers as M. natalensis, with the exception of the spring peak. No
R. pumilio were trapped after the end of October.

MAR APR MAY JUN JUL AUG SER OCT NOV DEC JAN FEB
0... 4129412341 2341234512341 2341 234 123 AST PSP

BKELELILIELLTEEFLTLTIILITITELEL SEIT LIT EEE 572 52% 2232 2%
MAR APR MAY JUN JUL AUG SEP OCT’ 'NOVTEDECEEITTEEEB

TIME IN WEEKS

Fig. 2. The population demography of Mastomys natalensis at Settlers during the study (see text for
details). a: The minimum number of mice alive (MNA) through the study period. b: The number of
individuals caught per 100 trap nights through the study period. c: Breeding season: the number of
adult individuals in breeding (BR) and non-breeding (N-BR) condition. d: Age structure: the number
of adults (AD) and juveniles (JUV) present, ©—0 = all species trapped; e—@ = M. natalensıs.
Numbers between a and b indicate the number of traps used in each trapping session

u

The population dynamics of rodents at Settlers, Transvaal, South Africa 241

MOREENDRSEENZNSCESJUNT UL ANÜG SER FFIOCTTINONM DECHDANZEEEB
012934123412341234123451294123412341234512341293412

1 TA EARTARTAS TE SUAEIE2E3TAT 4 STaySs WU 3yaTıE2W37AnE2
DIOREENIRE EEMASKTFJ UN FUEL MÜGHEESEBFEOCTEEFNON DEC EAN SEEB

TEENDEZUNZWIEEERS

Fig. 3. The population demography of Rhabdomys pumilio at Settlers during the study (see text for
details). a: The minimum number of mice alive (MNA) through the study period. b: The number of
individuals caught per 100 traps nights through the study period. c: Breeding season: the number of
adult individuals in breeding (BR) and non-breeding (N-BR) condition. d: Age structure: the number
of adults (AD) and juveniles (JUV) present. —0 = all species trapped; e—@ = R. pumilio. Numbers
between a and b indicate the number of traps used in each trapping session

Breeding season

The breeding season of M. natalensis came to an end in March-April, with few reproduc-
tively active anımals caught from June to July (Fig. 2c). Breeding began again in August-
September and reproductives were present throughout spring and summer. Seasonal
changes in recruitment (juveniles present - Fig. 2d) showed a slıght peak in numbers in
November, and an absence of juveniles from December to February.

Although present data for R. pumilio are not as complete as for M. natalensıs,
indications are that reproductive activity ceased in May, and recommenced in August
(Fig. 3c). Juvenile numbers increased over winter, but there were no juveniles trapped in
spring (Fig. 3d).

Reproductively active O. angoniensis adults were present throughout the year, showing
no marked breeding season (Fig. 4c). Very few juveniles were trapped, but indications
were that juveniles were born throughout the year (Fig. 4d).

242 M. R. Perrin, R. H. Slotow, and J. M. Mendelsohn

MARSSAPR FMAXEJUN ZUR NUGEISER FIOSTEENON DECSZIANEEEB
0 Sa 23a TS Tan 2 Ta E23 AS E 2 T Ta BEST PRATER SE

. TEETEEIIIEEIISN TEST
MARSEAPRIEMANZFAIIUN 1UE AUG SEP OCHZENONM DECSEESANGEEB

TIME IN WEEKS

Fig. 4. The population demography of Otomys angoniensis at Settlers during the study (see text for
details). a: The minimum number of mice alive (MNA) through the study period. b: The number of
individuals caught per 100 traps nights through the study period. c: Breeding season: the number of
adult individuals in breeding (BR) and non-breeding (N-BR) condition. d: Age structure: the number
of adults (AD) and juveniles (JUV) present. ©—0 = all species trapped; e—@ = O. angoniensıs.
Numbers between a and b indicate the number of traps used in each trapping session

Body mass

Mean body mass of M. natalensis ıs shown ın Figure 5a, while that of adults and juveniles
are shown separately in Figure 5b. Adult body mass (Fig. 5b) was low over winter, and
then increased from spring onwards to a peak ın January-February. The mass of juveniles
increased through autumn to relatively high levels ın spring, as they matured.

The mean body mass of R. pumilio (Fig. 6b) decreased from a peak ın March to lower
values throughout winter, and then increased slightly in spring. Body mass of O.
angoniensis was highly varıable throughout the period illustrated (Fig. 6a).

Discussion

The correlation between rainfall and the seasonality of reproduction in many African
grassland rodents is generally accepted. LEırs et al. (1989) ın a detailed, three year study of
M. natalensis at Morogoro, Tanzania, have shown that the breeding season starts soon
after the onset of the rainy season in March-April, but if rainfall at the end of the year is
heavy, there ıs a short additional separate breeding period early in the following year.

The population dynamics of rodents at Settlers, Transvaal, South Africa 243

MAR APR MAY JUN IU8 AUG S32 OCT NOW DEC JAN FEB

ZI II FSANEITN ZEN REIN AT DAIIT IN AEG ID ESTER AUT,
De ee nn eye ee ee
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MASS (8)
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Imarsyasım2raranı 4123412345123412341 41723451234 172341 2
NIORZENERT MAY JUN JUL NIGEESERZESOCTZENOV ZZ DECZZIJANT EEB

TIME IN WEEKS

Fig. 5. The body mass of Mastomys natalensis at Settlers during the study. a: The body mass of all
individuals from each trappıng session pooled. b: The body mass of adult and juvenile individuals
shown separately. Horizontal lines indicate means; and vertical lines indicate 1 X SE error

Population numbers

M. natalensis numbers at Settlers follow closely the trend found ın the same area by
MENDELSOHN (1982a). CHiDUMAYoO (1984) also found a small increase in late spring
followed by lower numbers from November to December. Unfortunately his trappıng
ended in December. MENDELSOHN (1981) ascribed the small spring peak in numbers to the
production of juveniles, and the low midsummer numbers to low rates of juvenile
recruitment. This is supported by this study which showed an increase in the number of
juveniles at the time of the spring peak, followed by an absence of juveniles over
midsummer.

MASS (8)

MASS(B)

244 M. R. Perrin, R. H. Slotow, and J. M. Mendelsohn

MAR APR MAY JUN JUL AUG SEPFT oe NOVA DESZTANEEEER
12341 2341234123412345123412341234123451234123412

123412341 23412341 2345123412341 234 1727370551 R2E37AE E27 3742
MAR APR MAY JUN JUL AUG» SEP : "OCT ZNOVZSIDECZZIANEEREB

TIME IN WEEKS

Fig. 6. The body mass of Rhabdomys pumilio and Otomys angoniensis populations at Settlers during
the study. a: The body mass of Otomys angoniensis individuals. b: The body mass of Rhabdomys
pumilio individuals. Horizontal lines indicate means; and vertical lines indicate 1 X SE error

A possible reason for the low numbers over midsummer is the large amount of raın
which fell at Settlers from late October through to the end of January. TAYLOR and GREEN
(1976) suggest that exceptionally heavy or prolonged rainfall results in very successful
reproduction. This would, however, be a longterm effect, the immediate effect perhaps
being a decrease in numbers (because of flooding). Individuals may die from overnight
exposure when wet (PERRIN 1975), or the decrease in numbers may be because anımals
moved out of the flooded areas.

R. pumilio numbers were sımilar to those of MENDELSOHN (1982a), who also found that
population numbers were lowest from November to February. BRooxs (1974) showed an
increase in R. pumilio from May to June, followed by a gradual decrease, wıth lowest
numbers in mid-summer. He trapped in an intensive grid, and the number of anımals

The population dynamics of rodents at Settlers, Transvaal, South Africa 245

trapped per session ranged from a minimum of 40 upward. His results may well be
indicative of the trends in the whole Transvaal population, as corroborated by this study
and MENDELSOHN (1982a). Davıp and Jarvıs (1985), working in the western Cape
(winter-rainfall area) found that numbers began to increase from October to November,
and rose steadily to a peak in February-March; this was followed by a decline during
winter, with lowest numbers in August-September. The general trend was therefore the
same as in the Transvaal, but with the cycle shifted three months earlıer.

Davıs (1973) found that O. angoniensis numbers were constant from March to
December of one year, followed by an increase over the next year to a peak in November.
This was followed by a decrease. ©. angoniensis numbers seem to lack the seasonal
fluctuations shown by of the other two species, and rather display relatively constant
numbers that vary yearly rather than seasonally.

Breeding season

MENDELSOHN (1982a) found a similar breeding season to this study, with reproductives
appearing from July to September, and juveniles showing a slight peak in numbers in
September, before very low numbers over summer. He suggested that this was a result of
an interrupted breeding season, in which young are produced in spring and late summer-
autumn. He found, as in this study, that reproductives were present throughout the
summer, and suggested that the absence of juveniles was because environmental conditions
were not suitable for the production and/or survival of young. The work of CHIDUMAYO
(1984) and TAyLoR and GREEN (1976) agrees with the current results and MENDELSOHN’S
(1982a, b) data. CoETZEE (1965), however, showed that pregnant females are present in
large numbers from September onwards (throughout the summer), with 44 % of the adult
females caught in December being pregnant. It seems therefore that the M. natalensıs
populations attempt to breed continuously from August to March, but juvenile mortality
limits recruitment over midsummer.

The absence of spring recruitment ın R. pumilio could have been because unusually high
rainfall from October to January caused high juvenile mortality. MENDELSOHN (1982a)
showed the R. pumilio breeding season to be sımilar to that of M. natalensıs. PERRIN (1980)
showed a recession in breeding over midsummer, and attributed this to an environmental
factor (drought). ROwE-RowE and MEESTER (1982) found reproductives present from
September to March. Their results also indicated a drop in recruitment in November. The
first young entered the trappable population in October, but no juveniles were captured
during November. No trappıng was done in December, and they trapped juveniles from
January onwards. DavıD and Jarvıs (1985) showed numbers of reproductives increasing in
September, and present until March; juveniles increased from November through to May.
This disagrees with the above findings, but they worked in a winter-rainfall area. Survival
of young would depend on environmental conditions, and in certain areas (e.g. Settlers)
survival may be adversely affected over midsummer, as ıs the case with M. natalensıs.

As in our study, TAyLoR and GREEN (1976) found pregnant OÖ. angoniensis females
throughout the year, with a breeding peak ın the wetter months. They found that the
number of juveniles trapped varied little. O. angoniensis therefore shows little seasonality
in reproduction, other than a slıght peak in wet months (summer).

Body mass

The decrease in M. natalensis adult body mass over winter ıs documented by several
authors (CHIDUMAYO 1984; COETZEE 1965; TAYLOR and GREEN 1976). Growth and
maturation seem therefore to be delayed over winter, juveniles not becoming mature until

spring.

246 M. R. Perrin, R. H. Slotow, and J. M. Mendelsohn

R. pumilio body mass changes were similar to those of M. natalensis. This trend is
supported by HEnscHEL et al. (1982) and TayLor and GREEN (1976) who suggest that
growth and maturation are inhibited during the non-breeding season (winter).

The body mass of ©. angoniensis varıed greatly at each trapping session, and small
sample sizes probably disguised trends. Davıs (1973) found that Otomys irroratus lost
mass over winter.

General

Numbers ot M. natalensis and R. pumilio peaked ın autumn following summertime
breeding, but recruitment occurred after the summer rains, when body masses were high.
Although adults were reproductively active throughout summer, density did not increase.
This apparent paradox has been recorded previously but not adequately explained. It has
been inferred that low juvenile recruitment, or infant mortality, is caused by environ-
mental factors, including heavy rainfall (TAyLoR and GREEN 1976), drought or nutrition
(PERRIN 1980). However, temporal correlations between environmental variables and
demographic events may not be indicative of cause-effect relationships and alternative
explanations should be considered.

Changes in the survival and recruitment of young into natural murid populations have
been explained by intraspecific competition in the form of aggression (SADLEIR 1965;
HEALEyY 1967; Watts 1969). For example, the mortality of young redbacked voles
Clethrionomys grapperi ıs greatest during the summertime breeding season, when levels of
aggression are higher in adults than young (PERRIN 1981) and when diet is optimal and
body growth is greatest (PERRIN 1979). Field experiments, that manipulate density (and
hence aggression) and food resources (independently of climate) while agonistic behaviour
is being monitored and quantified, are necessary to distinguish between alternative
explanations of demographic process. Descriptive studies of the population dynamics of
Afrıcan rodents should now be complemented with experimental investigations.

Acknowledgements

We wish to extend our thanks to A. TUCHSCHERER, M. SLOTOw and W. May for their assistance in the
field. J. CLEvERDON supplied the rainfall data from his farm Deeside. D. WArD and OÖ. WIRMINGHAUS
commented on drafts of the manuscript. OÖ. WIRMINGHAUS and G. MAcLEANn translated the Zusam-
menfassung. Financial aid was obtained from the Council for Industrial and Scientific Research and
the University of Natal.

Zusammenfassung

Die Populationsdynamik von Nagetieren ın Settlers, Transvaal, Südafrika

Studien über Populationen von Mastomys natalensis und Rhabdomys pumilio haben ergeben, daß ihre
Dichte zwischen Februar und Ende Juni zunahm und in der Mitte des Winters wıeder abnahm. Im
Frühling gab es ein Populationsmaximum, das während des Hochsommers abnahm. Otomys ango-
niensis konnte ganzjährig in kleinen Zahlen gefangen werden. Die Wurfzeit von M. natalensis kam ım
März/April zum Abschluß und begann wieder im August/September. Die Wurfzeit von R. pumilıo
endete im Mai und fing im August wieder an. Fortpflanzungsfähige, ausgewachsene ©. angonıensis
kamen das ganze Jahr über vor. Die Zahlen der Jungtiere von M. natalensıs und R. pumilio erreichten
im Frühling ihr Maximum; wenige Jungtiere ergänzten die Populationen während des Sommers.
Karge Umweltbedingungen könnten die Überlebenschancen der Jungtiere im Sommer beeinträchtigt
haben. Das Durchschnittskörpergewicht von M. natalensis und R. pumilio nahm ab von einem
Maximum im März bis zu geringen Werten im Winter. Im Frühling gab es eine kleine Gewichts-
zunahme. Das Körpergewicht von O. angoniensis variierte stark. Die niedrige Zahl von gefangenen
O. angoniensis wird eher der Fallenscheu zugeschrieben, als daß sie die tatsächlichen Populationsver-
hältnisse widerspiegelt.

The population dynamics of rodents at Settlers, Transvaal, South Africa 247

References

Acocks, J. P. H. (1975): Veld types of South Africa. 2nd Ed., Mem. bot. Surv. $. Afr. 40, 1-128.

BRONNER, G. N. (1986): Demography of the multimammate mouse Mastomys natalensis (A. Smith
1934) on Bluff Nature Reserve, Durban. M. Sc. Thesis, Univ. Natal, Durban.

Brooks, P. M. (1974): The ecology of the four striped field mouse, Rhabdomys pumilio (Sparrman,
1784), with particular reference to a population on the Van Riebeek Nature Reserve, Pretoria. Ph.
D. Thesis, Univ. Pretoria, Pretoria.

— (1982): Aspects of the reproduction, growth and development of the Four Striped Field Mouse,
Rhabdomys pumilio (Sparman, 1784). Mammalıa 46, 53-63.

COEITZEE, C. G. (1965): The breeding season of the Multimammate mouse Mastomys (Mastomys)
natalensis (A. Smith) in the Transvaal highveld. Zool. Afr. 1, 29-39.

CHIDUMAYO, E. N. (1984): Observations on populations of multimammate mice at Livingstone,
Zambia. Mammalıa 48, 363-376.

Davıp, J. H. M.; Jarvıs, J. U. M. (1983): Notes on two brief surveys of the small mammal fauna on
the Rooiberg, Ladysmith, southern Cape Province. S. Afr. J. Zool. 18, 370-377.

— — (1985): Population fluctuations, reproduction and survival in the Striped Fieldmouse Rhab-
domys pumilio on the Cape Flats, South Africa. J. Zool., Lond. 207, 251-276.

Davıs, R.M. (1973): The ecology and life history of the Vlei Rat, Otomys irroratus (Brants, 1827), on
the Van Riebeek Nature Reserve, Pretoria. Ph. D. Thesis, Univ. of Pretoria, Pretoria.

FLOWERDEW, J. R. (1976): Ecological methods. Mammal Rev. 6, 123-159.

GREEN, C. A.; KEocH, H.; Gorpon, D. H.; Pınto, M.; Harrtwıc, E. K. (1980): The distribution,
ıdentification and naming of the Mastomys natalensis species complex in southern Africa (Roden-
tıa, Muridae), J. Zool., Lond. 192, 17-23.

HEALEY, M. C. (1967): Aggression and self-regulation of population fluctuations of voles (Microtus).
Ecology 48, 377-392.

HENSCHEL, J. R.; Davıp, J. H. M.; Jarvıs, J. U. M. (1982): Age determination and age structure of a
Striped Fieldmouse, Rhabdomys pumilio, population from the Cape Flats. S. Afr. J. Zool. 17,
136-142.

Leırs, H.; VERHEYEn, W.; MıcCHIELS, M.; VERHEYEN, R.; STUYCK, J. (1989): The relation between
rainfall and the breeding season of Mastomys natalensis (Smith, 1834) in Morogoro, Tanzania.
Annls. Soc. Roy. Zool. Belg. 119, 54-69.

MEESTER, J. A. J.; RAUTENBACH, I. L.; DippEnAAR, N. ]J.; BAKER, C. M. (1986): Classification of
southern Afrıcan mammals. Transvaal Museum Monograph No. 5. Pretoria: Transvaal Museum.

MENDELSOHN, J. (1981): A study of the Blackshouldered Kite Elanus caeruleus. Ph. D. Thesis, Univ.
Natal, Pietermaritzburg.

— (1982a): Notes on small mammals ın the Springbok Flats, Transvaal. $S. Afr. J. Zool. 17, 197-201.

— (1982b): The feeding ecology of the Blackshouldered Kite Elanus caeruleus (Aves, Accipitridae).
Durban Mus. Novit. 13, 75-116.

PERRIN, M.R. (1975): Trap deaths. Acta Theriol. 20, 167-174.

— (1979): Seasonal varıatıon in the growth, body composition, and diet of Clethrionomys gapperi ın
spruce forest. Acta theriol. 24, 299-318.

— (1980): The breeding strategies of two coexisting rodents, Rhabdomys pumilio and Otomys
irroratus, with a brief review of some pertinent life history ideas. Acta Oecologica-Oecol. Gener.
I, Se9-ll0,

— (1981): Seasonal changes in agonistic behaviour of Clethrionomys gapperi ın south eastern
Manıtoba and its possible relation to population regulation. Am. Midl. Nat. 106, 102-110.

ROWE-ROWE, D. T.; MEESTER, ]J. (1982): Population dynamics of small mammals in the Drakensburg
of Natal, South Africa. Z. Säugetierkunde 47, 347-356.

SADLEIR, R. M. F. S. (1965): The relationship between agonistic behaviour and population changes ın
the deermouse, Peromyscus maniculatus (Wagner). J. Anım. Ecol. 34, 331-352.

TAyLoR, K. D.; GrEEn, M. G. (1976): The influence of rainfall on diet and reproduction in four
Afrıcan rodent species. J. Zool., Lond. 180, 367-389.

Twısg, G. J. (1975a): Marking mammals. Mammal Rev. 5, 31-46.

— (1975b): Catching mammals. Mammal Rev. 5, 13-30.

Warts, C. H. S. (1969): The regulation of wood mouse (Apodemus sylvaticus) numbers ın Wytham
Woods, Berkshire. J. Anım. Ecol. 38, 285-304.

Authors’ addresses: Prof. Dr. M. R. PERRIN (for correspondence) and R. H. SLoTow, Department of
Zoology and Entomology, University of Natal, P.O. Box 375, Pietermaritzburg,
South Africa; J. M. MENDELSOHN, State Museum, Windhoek, Namibia

Z. Säugetierkunde 57 (1992) 248-250
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

WISSENS@ELSEIEILCHTEZKTURZIIEEREREUNIG EIN

Cytogenetics and fossil record: confluent evidence for speciation
without chromosomal change in South American canids

By A. D. VıruLro and G. A. ZULETA

Centro de Investigaciones en Reproducciön, Facultad de Medicina, Universidad de Buenos Aires,
Argentina, and Resource Ecology, University of British Columbia, Vancouver, Canada

Receipt of Ms. 7. 10. 1991
Acceptance of Ms. 10. 3. 1992

South American wild dogs and foxes are the most diversified canıds of any other continent,
including seven genera and 11 species distributed in a wide range of habitats of the
Neotropics (BERTA 1987). However, this group is the least known of the Canidae in many
aspects of ıts general biology. The South American fox, Dusicyon (Honackt et al. 1982) or
Pseudalopex (BERTA 1987), ıs the most polytypic genus encompassing five living species
among which the chromosomes have only been reported for D. vetulus from Brazil
(WURSTER and BENIRSCHKE 1968). In this note we describe the karyotypes of two other
species of Dusicyon, the Patagonıian red fox, D. culpaeus, and the Pampean gray fox, D.
gymnocercus. Moreover, we discuss the trends in chromosomal evolution of South
Amerıcan Canidae in conjunction with available information on fossil records.

Cytogenetic analysis was performed in four D. culpaeus from the breeding stock of
PIROS SA, Argentina (1 male and 1 female) and from the Zoo of Buenos Aires City (2
females), and in three D. gymnocercus (1 male and 2 females) maintained at the Zoo of
Buenos Aires City. Chromosomes were obtained from blood culture. In brief, blood
samples were aseptically taken with heparanızed syringes from the cephalic vein of the
foreleg. One ml of whole blood was cultured ın Eagle Minimun Essential medium
supplemented with 20 % fetal calf serum, 2x glutamine, antibiotics (penicillin-streptomy-
cin), and phytohemagglutinin. After 68 h at 37°C, cultures were arrested with colchicine
(1 ug/ml of culture) for 1.5 h. Colchicine-treated cultures were centrifuged at 1,000 rpm,
resuspended in 0.075 M KCI for 15 min at 37°C, and then fixed ın cold 3:1, methanol:ace-
tic acıd. Chromosome spreads were air-dried and stained with Giemsa.

Both D. culpaeus and D. gymnocercus showed a 2n = 74 (NF = 76) karyotype, with an
all-telocentric autosomal complement decreasing gradually ın sıze, a large submetacentric
X, and a small subtelocentric Y chromosome (see Figure). This karyotype is ıdentical to
that previously reported for the hoary fox, D. vetulus (WURSTER and BENIRSCHKE 1968).

The South American canıds evolved along two different lines (LANGGUTH 1975):
invadıng forest habitats and producing specialist forms such as Atelocynus and Speothos;
or, colonizing the open plains as generalized species, e.g. of the genus Dusicyon. Both
evolutionary lines have maintained the same 2n = 74-76 all-telocentric karyotype (Table).

Cerdocyon thous und Urocyon cinereoargentus are exceptions to the chromosomal
homomorphism which characterizes the South American canids. C. thous also shows a 2n
= 74 karyotype, but 36 metacentric and submetacentric autosomes which increase the
number of arms up to 110 (Wurster-Hırr 1973). The origin of this karyotype may be
deduced by the accumulation of pericentric inversions in the all-telocentric karyotype.
However, the required extent of such repatterning and the lack of known intermediate

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5704-0248 $ 02.50/0

ee

Cytogenetics and fossil record 249

IKTIEWIETWTYWTWTWT

aa a8 08 28 20 a8 as Ba
“a a1 aa Ba ap »8 %& 88

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4 a8 88 .. h.
XY

Giemsa stained karyotype of the Patagonian red fox, Dusicyon culpaeus (2n = 74, FN = 76). The same
karyotype is also found in the Pampean gray fox, D. gymnocercus

states between the all-telocentric condition and C. thous-karyotype weaken this assump-
tion. The karyotype of U. cinereoargentus (2n = 66; NF = 70) departs from the all-
telocentric one, and may be derived by means of tandem fusions which reduce the diploid
number without altering the number of arms, plus one pericentric inversion giving rise to
the only metacentric autosome which characterizes this karyotype. Nevertheless, U.
cinereoargentus is mainly distributed in North and Central America, reaching Colombia
and Venezuela, and there are no fossil records in South America. This species probably
represents a North American canıd which reached the north of South America (BERTA
1987).

Available chromosomal data in living species of South American Canidae

Species r Reference

Atelocynus microtıs WURSTER and BENIRSCHKE (1968)
Cerdocyon thous WURSTER-Hirr (1973)
Chrysocyon brachiurus NEWNHAM and Davıpson (1966)
Dusicyon culpaeus This study

D. grisens

D. gymnocercus This study

D. sechurae

D. vetulus WURSTER and BENIRSCHKE (1968)
Speothos venaticus WURSTER and BENIRSCHKE (1968)
Urocyon cinereoargentus WURSTER and BENIRSCHKE (1968)

Fossil records indicate that the open plains of North America seem to have been the
center of evolution of canıds that later dispersed to South America (BERTA 1987). A species
or group of generalized canıds entered South America after the emergence of the Panamian
Land Bridge during the late Pliocene and early Pleistocene, and spread over the grasslands
along the Andes reaching the southern pampas, the Patagonian grasslands, and the
Brazilian highlands (BERTA 1987; LANGGUTH 1975). It is of interest to note that discrepan-
cies in karyotype homomorphism mentioned above, are found in those genera for which
earlier North American fossils are recorded - Cerdocyon and Urocyon - (BERTA 1987). The

250 A.D. Vitullo and G. A. Zuleta

remaining canıd species that radiated in South America — Atelocynus, Dusicyon and
Speothos — display a high chromosomal conservatism. In addition, the all-telocentric
karyotype of 74 chromosomes ıs also found in Chrysocyon, a form early recorded for
North America and now restricted to a South American distribution.

Chromosomal information, in conjunction with fossıl records seems to indicate that:
1. the species recorded early ın North America which later attained South America, show a
low karyological affınıty with the other South American canıds and are more closely
related to the North American ones; this is the case for C. thous and U. cinereoargentus,
2.the 2n = 74 all-telocentric karyotype is most likely the primitive condition for South
American Canıdae, retained without change during diversification which resulted mainly
from an opportunistic feeding strategy (BERTA 1987), and 3. a North American orıgin may
be suspected for this primitive karyotype which is also found in the early North American
recorded genus Chrysocyon.

Acknowledgements

We thank the authorities of the Zoo of Buenos Aires City for permission to collect samples from
foxes, and J. STEIN for his technical assistance in collection of blood samples. This work was partially
supported by PIROS SA, Argentina.

References

BERTA, A. (1987): Origin, diversification, and zoogeography of the South American Canidae. In:
Studies in Neotropical Mammalogy: essays in honor of Philip Hershkovitz. Ed. by B. D.
PATTERson and R. M. Tımm. Fieldiana: Zoology (New Series) 39, 455471.

Honackr, J. H., Kınman, K. E.; Koeppr, J. W. (1982): Mammal species of the world: A taxonomic
and geographic reference. Lawrence, Kansas: Allen Press.

LANGGUTH, A. (1975): Ecology and evolution in the South American canıds. In: The wild canids:
Their systematics, behavioral ecology and evolution. Ed. by M. W. Fox. New York: Van
Nostrand Reinhold Comp.

NEWNHAM, R. E.; BENIRSCHKE, K. (1966): Comparative study of the karyotypes of several species in
Carnivora including the giant panda (Arluropoda melanoleuca). Cytogenetics 5, 152-166.

WURSTER, D. H.; BENIRSCHKE, K. (1968): Comparative cytogenetic studies in the order Carnivora.
Chromosoma (Berlin) 24, 336-382.

WURSTER-Hiur, D. H. (1973): Chromosomes of eight species from the five families of Carnivora.
J. Mammalogy 54, 753-760.

Authors’ addresses: A. D. VıruLLo, Centro de Investigaciones en Reproducciön, Facultad de
Medicina, Universidad de Buenos Aires, Paraguay 2155, piso 10, RA-1121-
Buenos Aires, Argentina, and G. A. ZuULETA, Resource Ecology, 2204 Main
Mall, University of British Columbia, Vancouver, BC, Canada, V6T 1W5

Z. Säugetierkunde 57 (1992) 251-252
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Immobilization of Egyptian mongooses, Herpestes ichneumon,
with a combination of ketamine and xylazine

By F. PALoMAREs and M. DELIBES

Estacion Biolögica Donana, Sevilla, Spain

Receipt of Ms. 21. 1. 1992
Acceptance of Ms. 17. 2. 1992

Based on three immobilizations, BELTRAN et al. (1985) suggested that dosages of 7 mg per
kilogram of body weight of a combination of ketamine hydrochloride (KE) and xylazine
hydrochloride (XY), could be enough to successfully immobilize free-ranging Egyptian
mongooses, Herpestes ichneumon. However, Manvock (1989) needed higher dosages (36
mg/kg on average) of KE to immobilize 22 individuals of this same species. These results
suggest that BELTRAN et al. (1985) could not have actually immobilized their mongooses,
and that higher dosages of anaestetic should be administered for total immobilization.
Here, we report the result of 48 total immobilizations of free-ranging Egyptian mongooses
of different sex and age, using sımilar drugs and dosages to that of BELTRAN et al. (1985).

Mongooses were captured between September 1987 and July 1989 with wire cage traps,
cork double-door box for dens, or padded foothold traps (PALOMARES 1990). After the
capture, mongooses were transported to the laboratory and moved into a box with a
slıding wall that allowed us to inject ıntramuscularly a combination of KE (10 mg/m];
Ketolar) and XY (2%; Rompun) into their hind quarters. An additional dose of KE, or KE
and XY was administered when immobilization was only partial (SEAL and KREEGER
1987).

Induction time (time from injection until total immobilization) and arousal time (time
from injection until first head, leg or mouth movement) were recorded for every indı-
vidual. Rectal temperature records were taken as soon as practical after immobilization,
and successive ones at 8-10 min intervals until handling procedures were completed.

We immobilized 26 different mongooses 48 times. We used mean dosages of 4.2 and
6.5 mg/kg of body weight of KE and XY respectively, irrespective of sex or age classes
(p > 0.05; ANOVA; Table). Mean induction and arousal time were 7 and 74 min respec-
tively (Table). Induction time and arousal time did not differ significatively among sex and
age classes (Table). In 6 individuals, a mean dose of 3.9 mg/kg (SD = 0.7, range = 3.2-5.0)
of KE and 6.0 mg/kg (SD = 0.9, range = 4.0-7.0) of XY was insufficient for total
immobilization and complementary dosages of 2 mg/kg of KE and 2 mg/kg of XY were
needed.

Rectal mean temperatures for the first, second, and third record were very sımilar
(around 37.7°C; Table). No difference was observed among classes of individuals (Table).

Three individuals were immobilized on 4, 4 and 6 occasions at intervals of 4, 8, and 1.6
months, respectively. One was immobilized twice in 24 hours. No anımal died during the
immobilization or recuperation processes, and we never observed spasms or convulsions
with muscular contractions, as were sometimes noted in other carnivores (e.g. BoyD et al.
1990). Vomits were frequent during the recuperation.

We successfully immobilized mongooses using similar and lower dosages of KE than
those used by BELTRAN et al. (1985) and MAappvock (1989), respectively. MAnpock (1989)
sometimes used Acetilpromacine as tranquilizer together wıth KE. Our results proved that
a combination of KE and XY ıs an effective and safe immobilizing agent for Egyptian

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5704-0251 $ 02.50/0

252 F. Palomares and M. Delibes

Ketamine hydrochloride (Ketolar) and tiazine hydrochloride (Xilacine) dosages (mg/kg) adminis-
tered, induction time (Ind. time), arousal time (Arous. time), and three successive records of rectal
body temperature (Temp. 1, Temp. 2, Temp. 3) for adult females, adult males and young (in this

group we included the data of two immatures individuals) of Egyptian mongooses

ANOVA values and probabilities from comparisons among classes of individuals are given as well

Females
Mean (SD)
Range

N

Males
Mean (SD)
Range

N

Young
Mean (S$)
Range

N

Total
Mean (SD)
Range

N

Ketolar

4.2 (0.9)
2.3-6.8
20

4.3 (1.5)
WR
9

4.1 (0.7)
2.3-7.8
13

4.2 (1.0)
288708
42

Xilacine

6.8 (1.6)

6.5 (1.4)
351
42

Ind. time

7.0 (4.3)
N
20

7.4 (3.5)
5-16
9

5.3 (2.3)
0

12

6.8 (3.7)
7
4

Arous. time

67.7 (34.7)
27-151
18

99.0 (36.7)
47-107
9

65.3 (29.7)
16-120
12

74.2 (35.6)
16-170
39

Temp. 1

3727.02)
36.140.0
14

37.7. 01)
36.2-39.8
7

37.9 (1.1)
35.4-39.2
10

37.9 (1.1)
36.140.0
31

Temp. 2

37.2 (2.1)
36.0-39.9
14

37.3 (1.4)
36.1-40.0
7

37.9 (1.2)
35.1-39.2
10

37.6 (1.2)
35.140.0
30

Temp. 3

37.6 (1.4)
35.4-39.9
10

37.4 (1.7)
35.5-39.1
5

38.0 (1.0)
36.3-39.1
8

37.7 (1.3)
35.4-39.9
22

ANOVA (F)
Probability

0.160
0.085

0.941
0329

1.162
0.323

3.185
0.053

0.181
0.835

0.276
0.761

0.760
0.480

mongooses. Some advantages with ketamine use as an anaesthetic in wild carnivores are
described in SmuTs and BrRYDEN (1973).

Acknowledgements

The research was supported by CSIC and DGICYT (project PB87-0405). One of the authors (FP) has
a postdoctoral grant of CSIC. We thank N. BuUSTAMANTE for reviewing the English version.

References

BELTRAN, J. F.; DeLısBEs, M.; IBANEZ, C. (1985): Immobilization and marking of the Egyptian
mongoose, Herpestes ichneumon (L.), ın Spain. Z. Säugetierkunde 50, 243-244.

Bovp, I. L.; Lunn, N. J.; Duck, C. D.; Barton, T. (1990): Response of antarctic fur seals to
immobilization wıth ketamine, a ketamine-diazepam or ketamine-xylazine mixture, and zoletil.
Marine Mammal Science 6, 135-145.

Mappvock, A. H. (1989): Anaesthesia of four species of viverridae with ketamina. $. Afr. Tydskr.
Naturnav. 19, 80-84.

PALOMARES, F. (1990): Ecologia y organizacıön social del meloncillo, Herpestes ichneumon L., en el
Parque Nacional de Donana. Ph. D. Thesis, Univ. Granada, Spain.

SEAL, U.; KREEGER, T. J. (1987): Chemical immobilization of Furbearers. In: Wild furbearer
management and conservation in North America. Ed. by M. Novak, J. A. BAKER, M. E. OBBARD
and B. MarrocH. Toronto: Ministry of Natural Resources. Pp. 191-215.

SMUTS, G. L.; BRYDEN, B. R.; Vos,, V. DE; Young, E. (1973): Some practical advantages of CI-581
(ketamina) for the field immobilization of larger wild felines, with comparative notes on baboons
and ımpala. The Lammergeyer 18, 1-14.

Authors’ address: FrRancısco PALOMARES and MIGUEL DELIBEs, Estacıiön Biolögica de Donana,
CSIC, Apdo. 1056, E-41080 Sevilla, Spain

BUCHBESPRECHUNGEN

PenzLın, H.: Lehrbuch der Tierphysiologie. 5., durchgesehene Auflage. Jena: Gustav
Fischer Verlag 1991. 657 S., 418 Abb., 75 Tab., kartoniert DM 58,-. ISBN 3-334-60363-6

Wenn ein Lehrbuch, welches 1970 erstmals erschien, nach 21 Jahren in der 5. Auflage publiziert wird,
dann haben die Leser bereits ein klares und positives Urteil über die Qualität des Werkes abgegeben.

In der vorliegenden Neuauflage werden zunächst grundsätzliche dynamische und energetische
Probleme sowie die Integration von Teilleistungen besprochen. Es schließen sich Kapitel über
Aufnahme und Verteilung von Substanzen sowie über die Regulation des inneren Körpermilieus an.
Nach Abhandlung der Aufnahme und Verarbeitung von Informationen behandelt der Autor in einem
eigenen Abschnitt die Physiologie der Effektoren, welche das Lebewesen „sinnvoll“ auf Informatio-
nen aus der Umwelt reagieren lassen. Das letzte Kapitel beschäftigt sich mit der Physiologie des
Verhaltens und der Orientierung. A

Im Anhang wird eine Zeittafel zur Geschichte der Tierphysiologie, eine Übersicht über das System
rezenter Tiere, mehrere Tabellen zu Maßeinheiten, eine Auswahl weiterführender Literatur und ein
ausführliches Bildquellenverzeichnis geboten. Ein Register von 27 Seiten und eine Zusammenstellung
der benutzten Abkürzungen und Symbole schließen das Werk ab.

Das „Lehrbuch der Tierphysiologie“ behandelt die Probleme unter vergleichenden Gesichtspunk-
ten und bezieht sich auf ein breites Spektrum zoologischer Lebensformen. Obwohl viele Einzelbei-
spiele dargestellt werden, verfällt der Autor nie in „Detailhuberei“, sondern arbeitet möglichst die für
alle Tiere und den Menschen gleichermaßen gültigen Gesetzmäßigkeiten heraus. Er macht ferner dem
Leser bewußt, daß die Anwendung mathematischer, physikalischer und biochemischer Kenntnisse die
Darstellung tierphysiologischer Zusammenhänge präzisiert. Die zahlreichen Tabellen und die sorgfäl-
tig überarbeiteten Abbildungen erleichtern das Verständnis des im Text vermittelten Stoffes. Der
Autor des Lehrbuches vermeidet unzulässige Simplifizierungen und einseitige Darstellungen, er stellt
auch widerstreitende Theorien dar. P. LAnGeER, Gießen

Dyce, K. M.; Sack, W. O.; WEnsING, C. J. G.: Anatomie der Haustiere. Lehrbuch für
Studium und Praxis. Stuttgart: Ferdinand Enke Verlag 1991. 883 S.; zahlr. Abb.
DM 248,-. ISBN 3-432-98631-9

An vielen Bildungsstätten hat sich in verschiedenen Ländern seit mehreren Jahren die Problematik
ergeben, unter dem Zwang von Studienzeitverkürzungen starke Beschränkungen im fachspezifischen
Lehrangebot hinzunehmen, obwohl Wissensumfang und Spezialisierungen beständig stark zuneh-
men. Diese Tatsache und das Bestreben um internationale Angleichung in der Ausbildungsqualität
haben die Veterinäranatomen K. M. Dyce (Edinburgh), W. ©. Sack (Ithaca) und C. J. G. WENSING
(Utrecht) veranlaßt, eine allgemeine Darstellung über die Anatomie der Haustiere als „Textbook of
Veterinary Anatomy“ zu verfassen. Diese liegt nun auch in deutscher Sprache vor. Es wurde von den
Veterinäranatomen K. D. Bupras und K. D. WeYrRAucH aus Berlin sowie H. GOLLER, R. R.
HoFrFMAnn, G. HuUMMEL und INGRID GOLLER aus Gießen sachkompetent übersetzt.

Dieses einbändige Lehrbuch ist -— dem Untertitel entsprechend - in zwei Teile gegliedert. Im
ersten, allgemeinen Teil werden nach einleitenden Darstellungen von Grundfakten und -begriffen
Bewegungs-, Verdauungs-, Atmungsapparat sowie Urogenitalsystem, endokrine Drüsen, Herz-
Kreislaufsystem, Nervensystem, Sinnesorgane und äußere Haut in einzelnen Kapiteln abgehandelt.
Anschauungsobjekt ist der relativ unspezialisierte Hund, aber es werden vielfach zusätzlich die
anderen Haussäugetiere vergleichend in Wort und Bild erwähnt. Im wesentlichen wird die Situation
beim adulten Tier beschrieben, ontogenetische Lageveränderungen und entwicklungsgeschichtliche
Aspekte werden stellenweise zusätzlich angeführt.

Der zweite Teil ist als spezieller Teil stärker den klinischen Anforderungen an den Praktiker
gewidmet. Hier wird ın 27 Kapiteln die regionale Anatomie des Tierkörpers abgehandelt und
spezieller auf Fleischfresser, Pferd, Wiederkäuer und Schwein eingegangen. Ein letztes Kapitel befaßt
sich mit der Vogelanatomie.

Das Buch ist verständlich und gut lesbar geschrieben. Nur an wenigen Stellen sind Formulierungen
zu bemängeln, weil sie kausale Entwicklungszwänge unterstellen, wie z.B. „Bei Beendigung des
Wachstums sind die Schädelnähte nicht mehr notwendig .. .“ (S. 66); „Der Wandteil, den die Lippen
bilden, hängt von der Ernährungsweise ab, ...“. „Nahrung und Ernährungsweise bestimmen auch
die Form der Lippen.“ ($. 111); „... die Nerven, welche die aus den Urwirbeln hervorgehenden
Kopfmuskeln versorgen...“ ($S. 343); etc. Dem Text zugeordnet sind sehr viele deutliche und
instruktive Schema- und Situationsdarstellungen. Im zweiten Teil fallen besonders mehrere Röntgen-
aufnahmen auf. Eine gute qualitative Aufmachung rechtfertigt den etwas hohen Preis.

Das Kapitel Nervensystem enthält allerdings einige Schwächen und auch Fehler ın wenigen Abb.
(z.B. Abb. 8-10; 8-21).

254 Buchbesprechungen

Abgesehen von diesen wenigen Mängeln, die in weiteren Auflagen leicht zu beheben sind,
erscheint dieses Buch als eine gelungene Alternative ın der Stoffauswahl, die das Anliegen der Autoren
erfüllt. Auch der an Anatomie interessierte Säugetierkundler kann es mit Gewinn nutzen.

D. Kruska, Kiel

CoRBET, G. B.; Hııı, J. E.: A World List of Mammalian Species. 3.ed. Natural History
Museum Publications. Oxford: Oxford University Press 1991. 243 pp., approx. £ 27.50.
ISBN 0-19-854017-5

This treatise is just a list of the scientific names of all mammalıan species of the world, their English
vernacular equivalents, when available, and their distribution. They are ordered according to Orders,
Families and Genera. Some controversies are marked by adding species or generic names in brackets at
the appropriate places. References are given for recent changes ın nomenclature in addition to some
general works. All the remaining complicated accessories of nomenclature and taxonomy (synonym
lists, opinions of different authors, author name and year) are omitted. The increase in net number of
species from the first (1980) to the second (1986) edition (221) is now smaller with only 93 species in
the present book. This is the result of some revisions mainly for Soricidae with 28, Cebidae with 10
and Muridae with 40 more species. Drawings by Ray BuRRows give an idea of some of the species
listed. A list of 27 extinct species is also now including only mammals that have been known “in the
flesh” (e. g. Thylacınus cynocephalus, Equus quagga, but also Pitymys bavaricus which has not been
found again since the description) and a table with species numbers for all Orders in the 6
zoogeographical regions of the world. Much of the decisions in this book are debatable, but the list in
general reflects a sober and serious effort and is also informative concerning the consequences of
recent taxonomic work. It is a good balance between flexibility due to scientific progress and stability
necessary for practical work. J. NIETHAMMER, Bonn

Kurr, F.: Das Reh in der Kulturlandschaft. Sozialverhalten und Ökologie eines Anpas-
sers. Hamburg und Berlin: Paul Parey 1991. 284 S., 126 Abb., 18 Tab. Geb. DM 68,-.
ISBN 3-490-17618-9

In dieser Abhandlung hat der Autor, ein ausgewiesener Rehforscher, die Fülle der wissenschaftlichen
Literatur über das Reh, fußend auf seinen eigenen Untersuchungen und den umfangreichen Studien
von STRANDGAARD (1972) und ELLENBERG (1978), zusammenfassend erarbeitet.

Wesentliche Zielsetzungen sind dem Titel zu entnehmen: Es geht um die Lebensbedingungen und
Lebensmöglichkeiten des Rehs in der Kulturlandschaft, also in der vom Menschen beeinflußten, ja
gestalteten Landschaft. Eine Kulturlandschaft kann reich strukturiert sein durch Wechsel von
artenreichem, durch Lichtungen unterbrochenem Wald mit kleinräumigen Feldern und Wiesenarea-
len, die durch Wallhecken begrenzt sind. Sie kann aber auch aus eintönigen Monokulturen bestehen,
seien es ‚Holzplantagen‘ oder eintönige Agrargebiete. Entsprechend solchen verschiedenen Gegeben-
heiten zeigt das Reh Unterschiede im Sozialverhalten und in seinen Wechselbeziehungen mit seiner
Umwelt. So unterscheiden sich Waldrehe und Feldrehe beträchtlich voneinander: Während z.B.
Weibchensippen und Ein-Mann-Familien in waldreichen Gebieten zu beobachten sind, kommt es
beim Feldreh zur Rudelbildung. Diesem unterschiedlichen Sozialverhalten entsprechend ıst beim
Feldreh ım Unterschied zum Waldreh keine Territorialität zu beobachten.

Anpassungen an eine offene Landschaft sind besonders für die moderne Kulturlandschaft typisch,
in der zudem natürliche Beutegreifer fehlen. So kann es zu beträchtlichen Bestandszunahmen
kommen. Wenn dann nach der Erntezeit das offene Land nicht mehr genügend Nahrung bietet,
wandern die Rehe in großer Zahl in den Wald; dort verursachen sie erhebliche Verbißschäden.
Vielmehr als zu geringe Jagd sind es also Veränderungen der natürlichen Umwelt, denen sich das Reh
anzupassen weiß, die letztendlich zu Waldschäden führen. Kurr plädiert dafür, das Rehwild auf eine
Bestandsgröße zu regulieren, bei der die Artenvielfalt der Lebensgemeinschaft Wald ebensowenig
gefährdet wird wie dessen natürliche Verjüngung. Das ist aber nur möglich, wenn man über das Reh
und seine sozialen und ökologischen Bedürfnisse sowie über seine vielfältigen Anpassungsmöglichkei-
ten Bescheid weiß.

Diese Kenntnisse vermittelt das Buch in umfassender Weise. Es ist in zehn Themen gegliedert: Das
1. Kapitel referiert Stand und Probleme der Rehwildforschung. Das 2. Kapitel vermittelt dem Leser
die wesentlichen ökologischen Ansprüche des Rehs. Die Kapitel 3-8 behandeln die verschiedenen
Aspekte des Sozialverhaltens in seiner Abhängigkeit von ökologischen Gegebenheiten. In den letzten
beiden Abschnitten erläutert der Autor die Bestandszunahmen und die heutige Bestandssituation
sowie daraus abzuleitende Erfordernisse für die Bejagung.

Das Buch ist sehr anschaulich geschrieben und mit zahlreichen Tabellen und Abbildungen
ausgestattet, die der Rezensent allerdings zum Teil als schwer lesbar empfindet. Da der Leserkreis

Buchbesprechungen 255

wohl nicht allein auf Jäger beschränkt sein soll, wäre ein gesondertes Glossar der zahlreichen
jagdlichen Ausdrücke wünschenswert gewesen. Argerlich ist, daß mehrere zitierte Arbeiten unter der
Literatur nicht verzeichnet sind, z. B. HoFmann 1979 (S.262), Maccıo 1988 (S. 261), MEUNIER 1979
(S.243) und noch weitere. Diese Mängel schmälern allerdings nicht den Gesamteindruck: ein sehr
empfehlenswertes Buch. | D. Heinrich, Kiel

Rüsse, I.; SINOwATZ, F.: Lehrbuch der Embryologie der Haustiere. Berlin, Hamburg:
Paul Bareyal991:2473.9.:5318 Abb.; 39 Tab. DM 178,-. ISBN 3-489-57716-7

Dieses Lehrbuch der Münchener Veterinäranatomen ist in neuer und modernisierter Fassung als
Nachfolgewerk der Entwicklungsgeschichte der Haustiere von ZIETZSCHMANN und KRÖLLINg konzi-
piert, vornehmlich für Studierende der Veterinärmedizin, aber auch Humanmedizinern und Biologen
anempfohlen. Der Stoff wird in mehreren Abschnitten in einem allgemeinen und einem speziellen Teil
geboten, vorangestellt ist eine Geschichte der Embryologie der Haustiere von A. VON DEN DRIESCH.
Die beiden Autoren teilen sich die Aufgabe, indem sie für die verschiedenen Abschnitte entweder
einzeln oder gemeinsam verantwortlich zeichnen. Im allgemeinen Teil werden behandelt: Prinzipien
der Entwicklung und Morphogenese; Gametogenese; weiblicher Sexualzyklus; Befruchtung und
Teilung; Gastrulation; Keimblattbildung und Bildung der Körpergrundgestalt; Frühgravidität,
Implantation und Plazentation. Der spezielle Teil befaßt sich mit Herz- und Kreislaufsystem;
Nervensystem; Sinnesorganen; Harn- und Geschlechtsorganen; Verdauungskanal und Anhangsorga-
nen; Atmungsorgan; Körperhöhlen; Bewegungsapparat; Haut- und Anhangsorganen; Gesicht und
Körperform; Mißbildungen. In mehreren Abschnitten stehen die Haustiere Rind, Schaf, Schwein,
Pferd, Hund, Katze, Huhn im Vordergrund, andere Kapitel enthalten allgemeinere Beschreibungen.
Das Buch ist mit zahlreichen Abbildungen von Präparaten sowie Skizzen und Übersichtszeichnungen
eindrucksvoll illustriert. Viele Tabellen kennzeichnen darüber hinaus artspezifische Entwicklungssta-
dien ın zeitlicher Zuordnung.

Der Text liefert grundsätzlich viel Information, vor allem einige neuere Erkenntnisse im Detail.
Allerdings machen sich mehrere Schwächen bemerkbar, vor allem aus zoologischer Sicht, weil der
evolutive Wandel der Ontogenesen im Tierreich nur sporadisch angedeutet bleibt. Die verschiedenen
Abschnitte sind inhaltlich unterschiedlich weit gefaßt und wenig konsequent begrenzt. Die Darstel-
lung der Gametogenese ist z.B. sehr ausführlich, bleibt aber auf placentale Säugetiere und auf Vögel
beschränkt. Im Kapitel über Gastrulation hingegen wird zusätzlich sogar auf Branchiostoma, Seeigel
und Amphibien eingegangen. Der spezielle Teil behandelt fast ausschließlich die Organsysteme der
Säugetiere in der Embryogenese, auf den Vertebraten Vogel wird kaum eingegangen. Zusätzlich sind
die sprachlichen Formulierungen an vielen Stellen ungenau, verwirrend oder mißverständlich, aber
auch komplizierend. Folgende Beispiele mögen das belegen: die Eizelle hat einen „Cortex“; „die
Eizelle ist der Dotter“; „die Spermien wandern um die Ovulation den Eileiter hinauf“; einmal ist von
Replikation, dann wiederum von Reduplikation die Rede; „die Blastocyste enthält ein Blastocoel“;
„das Ei entwickelt sich an der Oberfläche des Dotters“; „das zephale Ende des Primitivstreifens“;
Somite sind „Urwirbel“; „die Erkennung der Gravidität seitens des Muttertieres...“; „zwischen
Amnion und Chorion ist die seroamniotische Platte“; „die Vorniere ist in der Tierreihe bis zu dem
primitiven Fischen funktionstüchtig“; etc. Störend sind ferner häufige Wiederholungen vorher
geschilderter Sachverhalte und neu eingeführte lateinisch-griechische Mischprodukte in der Fachspra-
che, denn es gibt nun Ovogenese, Ovogonie und Ovozyten, aber immer noch einen Cumulus
oophorus. Auch stimmen die Abbildungen nicht immer mit den Ausführungen in Legenden und Text
überein.

Insgesamt liegt damit eine recht heterogene Darstellung vor, die dem Studenten als Lehrbuch den
Zugang zum ohnehin komplexen und komplizierten Wissensstoff wenig erleichtert. D. Kruska, Kiel

Kos, GERTRUD M.H.: Vergleichende Histologie, Cytologie und Mikroanatomie der
Tiere. Berlin, Heidelberg, New York: Springer-Verlag 1991. 352 pp., 201 Abb., 2 Farbtaf.
brosch. DM 48,-. ISBN 3-540-52842-3

Von der Autorin wird ein ‚Springer-Lehrbuch‘ der vergleichenden Histologie der Tiere unter
Berücksichtigung der Cytologie und mikroskopischen Anatomie geboten, welches „für Studenten der
Biologie, Veterinärmedizin und für naturwissenschaftlich Interessierte“ gedacht ist. Dabei wird
bewufßst auf die Darstellung spezieller Details verzichtet. Die Mehrzahl der Abbildungen ist der
Literatur entnommen. Wirbeltiere sind in diesem Buch ausführlicher dargestellt als Wirbellose.

Nach einer kurzen Übersichtsdarstellung der mikroskopischen Technik werden in fünf Kapiteln
die Gewebetypen dargestellt: Epithelien, Drüsen, Binde- und Stützgewebe, Blut und freie Zellen des
Bindegewebes, Muskelgewebe. Anschließend werden unter Berücksichtigung funktionell-anatomi-
scher Gesichtspunkte in sieben Kapiteln Organe im Systemzusammenhang besprochen: Aufnahme
und Weiterleitung von Information, Integument, Zahn- und Zahnentwicklung, Zunge, Transport-,

256 Buchbesprechungen

Speicher- und Resorptionssysteme, Systeme des Stoffaustausches und Permeabilität, Fortpflanzungs-
organe.

Die Gewichtung der besprochenen Systeme ist auffällig ungleichmäßig. So ist beispielsweise der
Zunge von Amphibien und Säugetieren und sehr knappen Hinweisen auf die Verhältnisse bei anderen
Wirbeltiergruppen ein kurzes eignes Kapitel gewidmet, welches typographisch gleichartig dargestellt
wird wie das ausführlichere Kapitel über die Systeme der Aufnahme und Weiterleitung von Informa-
tion, dessen Anfangsabschnitt zunächst eine allgemeine Darstellung der Nervengewebe sowie der
Synapsen und der Glia bietet. Eine anschließende Übersicht stellt jeweils in wenigen Zeilen Nerven-
systeme ım Tierreich für Taxa, wie beispielsweise Cnidaria, Plathelminthes, Echinodermata oder
Polychaeta, dar. Das Nervensystem der Wirbeltiere wird auf anderthalb Seiten abgehandelt.

Die Veröffentlichung macht dem Leser bewußt, daß das Tierreich auch heute noch außerordent-
lich ungleichmäßig intensiv mikroskopisch-anatomisch studiert worden ist. Entsprechend interes-
sierte Zoologen sollten in diesem Buch einen Ansporn zu Untersuchungen bisher wenig berücksich-
tigter Bereiche der vergleichenden Histologie sehen. Insbesondere bei den Wirbellosen und den
Nonmammalia unter den Wirbeltieren bietet sich ein weites Feld möglicher Untersuchungen.

P. LANGER, Gießen

STEPHAN, H.; BARON, G.; FRAHM, H. D.: Comparative Brain Research in Mammals.
Vol. 1: Insectivora. Berlin, Heidelberg, New York, London: Springer-Verlag 1991. 573
pp-, figs. and tables. DM 146,-. ISBN 3-540-97505-5

Over a period of 40 years HEınz STEPHAN from the Max-Planck-Institut für Hirnforschung,
Frankfurt/M. has studied comparative brain anatomy in many mammals. During this time he initiated
appropriate research both natıonally and internationally. This volume is the first in a survey series,
where he together with GEORG Baron (Montreal) and HEıko D. FRAHM (now Köln) characterizes
the brains of insectivores covering the whole of their diversification. Further volumes, dealing with
the brains of Chiroptera, marsupials, and primates are still in progress.

This book is presented in several chapters. Following short introductory remarks, a compilation of
investigated species and a list of abbreviations are presented. The material and methods chapter clearly
describes: fixation and preparation of brains, determination of fresh brain weights, a compilation of
brain and body weights, comparison of linear brain measurements, brain sectioning, determination of
volumes, evaluation of species-specific standards, survey of structures and complexes, varıability, and
methods of comparing brain sıze and volume. Especially under the last heading the interspecific
allometric method of comparing fresh tissue size based on a brain-to-body weight relation is explained
and reviewed critically.

In the following chapter comparative aspects of brain characteristics are highlighted, and data are
documented on an unusually large spectrum of species and number of specimens worldwide in their
distribution. Here, the external appearance of the brains of insectivores ıs described qualiıtatively, and
several parts and components of the brain are characterized with respect to their histology, configura-
tion and sıze. According to calculations of indices clear differences exist in the total brain sızes of the
species investigated independent of a body size influence and thus, all the other structures measured
vary in absolute and relative size. The sub-family Geogalinae with the single representative Geogale
aurıta from Madagaskar shows by far the most primitive brain characteristics and the smallest brain
size. Furthermore, indices calculated for average levels of brain sızes within sub-families result in the
following arrangement from small to large brain size: Tenrecinae, Erinaceinae, Crocidurinae,
Soricinae, Oryzorictinae, Potomogalinae, Chrysochlorinae, Talpınae, Solenodontinae (Solenodon
paradoxus), Echinosoricinae, Desmaninae. The same has been calculated for the classıcal parts of the
brain and certain other components. For the first time data on 20 nuclei of the medulla oblongata are
presented as well as data on several nuclei and structures of the mesencephalon, the cerebellum, the
diencephalon and the telencephalon. A size comparison of some main brain complexes wıth those of
primates (prosimians, non-human simians, F/omo) is additionally included.

The next chapter is devoted to the brain characteristics of the taxonomic units, thus resulting in a
highly diverse and heterogeneous brain composition of the extant species within this order.

These differences are discussed in the following two chapters in connection with phylogenetic and
evolutionary adaptive radıation in general and wıth ecoethological adaptations in particular (surface
dwellers, fossorial species, semi-aquatic species, winter survival).

The final chapter is devoted to brain characteristics related to functional systems, e.g., olfactory
(main and accessory), visual, somatosensory, auditory, vestibular, motor, limbic and the neocortex.
There are 50 pages of references, 74 tables added in the appendix and a very impressive and detailed
stereotaxic atlas of the brain of Atelerix algirus cut in the frontal plane. 108 figures and further tables
are distributed throughout the text.

This book is well written, and the most accurate analysis and documentation on the topic
presented to date. It is a valuable resource book, not only of interest to neuroanatomists but also to
mammalogists in general, due to its high biological significance. D. Kruska, Kiel

Deutsche Gesellschaft
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Z. Säugetierkunde 57 (1992) 4, 193-256

Boar Semen
Preservatiıon II

Proceedings of the Second International Conference on Boar Semen
Preservation, held at Beltsville, August 1990

Edited by Prof. Dr. L. A. Johnson, Beltsville Agricultural Research
Center, USA and Dr. D. Rath, Institut für Tierzucht und Tierverhalten
Mariensee, Bundesforschungsanstalt für Landwirtschaft Neustadt.
Dedicated to the memory of Kjell Larsson.

Supplements to Reproduction in Domestic Animals, No. 1

1991. 424 pages wıth 73 figures and 97 tables. Soft cover DM 58,-
ISBN 3-489-53316-X

These proceedings are the compilation of papers presented at the Sec-
ond International Conference on boar semen preservation held at
Beltsville, Maryland, USA. The Conference, the Second in the series
was devoted to the subjects of deep frozen and liquid stored boar
semen. Iwenty-one papers were presented by outstanding scientists.
Areas covered were: The epididymis, testıs and sperm maturation; fun-
damental cryobiology; an update on the state of the art relative to fro-
zen boar semen; semen evaluation; liquid semen production, preserva-
tion and use; management of semen production and artificial insemina-
tion and new technologies in swine reproduction. In addition there are
updates on the commercial use of swine artificial insemination from 11
different countries of the world. Short papers or abstracts are also in-
cluded from the 33 posters presented at the Conference.

Boar Semen Preservation I is mandatory reading for anyone interested
in Animal Reproduction or the overall field of Animal Science. The
book will be essential to’those interested in sperm preservation and
storage at the basic and the applied level.

PAUL
PAREV Berlin and Hamburg

1.57 (5), 257-320, Oktober 1992 ISSN 0044-3468 @2E7AE

-EITSCHRIFT FÜR
>AUGE TIERKUNDE

rgan der Deutschen Gesellschaft für Säugetierkunde

Brin, M. R.; Hughes, J. J.: Preliminary observations on the comparative gastric morphology of selected Old World
ınd New World bats. — Vorläufige Befunde zur vergleichenden Magenmorphologie von ausgewählten Altwelt-
ınd Neuwelt-Fledermäusen 257,

ker, C.; Höhmann-Kröger, Hella; Doyle, G. A.: Social relations in groups of Black-capped capuchin monkeys,
Cebus apella) in captivity: sibling relations from the second to the fifth year of life. — Soziale Beziehungen in
aruppen des Gehaubten Kapuzineraffen (Cebus apella) in Gefangenschaft: Beziehungen zwischen Geschwi-
itern vom zweiten bis zum fünften Lebensjahr 269

in, E. W.; Knutsen, L. ©.: Satellite-linked radio tracking of Atlantic walruses (Odobenus rosmarus rosmarus) in
ıortheastern Greenland, 1989-1991. — Satelliten-gestützte Telemetrie an Atlantik-Walrossen (Odobenus rosma-
‚us rosmarus) von 1989 bis 1991 im Nordosten Grönlands 275

vers, M. A.; Carr, T. G.: Home range shifts accompanying breeding in the Eastern Chipmunk, Tamias striatus
‚Rodentia: Sciuridae). — Verschiebungen des Aktionsraumes beim Östlichen Streifenhörnchen Tamias striatus
‚Rodentia: Sciuridae) während der Fortpflanzung 288

nett, N. C.: Aspects of the social behaviour in a captive colony of tne Common mole-rat Cryptomys hottentotus
rom South Africa. -— Aspekte des Sozialverhaltens einer in Gefangenschaft gehaltenen Kolonie des südafrikani-
‚chen Graumulls Cryptomys hottentotus 294

senschaftliche Kurzmitteilungen

ison, G. W. H.; Zubaid, A.: Food habits of the Lesser false vampire, Megaderma spasma, from Kuala Lompat,
>eninsular Malaysia. — Ernährungsgewohnheiten der Kleineren Großblattnase, Megaderma spasma, von Kuala

„ompat, Halbinsel Malaysia 310
ınapp, D.; Howroyd,J.: Distribution and local range of the Orinoco dolphin (Inia geoffrensis) in the Rio Apure,
/enezuela. — Verbreitung und Revierverhalten des Orinoco-Delphins (/nia geoffrensis) im Apure, Venezuela 313

oks, D. M.: Reproductive behaviour and development of the young of the Chacoan peccary (Catagonus wagneri
Ausconi, 1930) in the Paraguayan Chaco. — Reproduktionsverhalten und Jugendentwicklung beim Chaco-Pekari

‚Catagonus wagneri Rusconi, 1930) im Chaco von Paraguay 316

hbesprechungen 218

HERAUSGEBERYE DITORS

P. J. H. van BrEE, Amsterdam - W. FIEDLER, Wien — H. Frıck, München - W. HERRE,

Kiel - R. HUTTERER, Bonn - H.-G. Krös, Berlin - H.-J. Kunn, Göttingen —- E. KuLzEr,

Tübingen - W. MAIER, Tübingen - J. NIETHAMMER, Bonn - ©. Anne E. Rasa, Bonn -

H. REıcHsTEIN, Kiel - M. Rönrs, Hannover — H. SCHLIEMANN, Hamburg — D. STARCK,
Frankfurt a. M. - E. THENnIUSs, Wien — P. VOGEL, Lausanne

SCHRIETLE TUN G/ZEDITORTATORFI@E

D. Kruska, Kıel - P. LANGER, Gießen

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Z. Säugetierkunde 57 (1992) 257-268
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Preliminary observations on the comparative gastric
morphology of selected Old World and New World bats

By M.R. Perrın and ]. J. HucHes

Department of Zoology and Entomology, University of Natal, Pietermaritzburg, R.S.A.

Receipt of Ms. 28. 6. 1991
Acceptance of Ms. 3. 3. 1992

Abstract

Stomachs of ten species of bats (eight microchiropteran and two megachiropteran species), represent-
ing nine genera from five families, were examined and compared morphologically and histologically.
All stomachs were wholly glandular but differences in gross morphology were observed between
insectivorous, omnivorous and frugivorous species. Anatomical varıatons ın the gastric mucosa
between species were minor. The insectivorous bats exhibited little variation between species and
possessed a simple tubular gastric stomach. The stomachs of the frugivorous species were more
specialised with increased compartmentalisation. Scanning electron microscopy revealed the presence
of microvilli in the stomachs of both an insectivorous and a frugivorous species.

Introduction

The gastrointestinal morphology of bats approximates that of other mammals in general
organisation (Hırr and SMITH 1984). Most mammals have a single chambered (unilocular)
stomach although ruminants and other foregut fermenters possess a multichambered
(plurilocular) stomach which ıs an adaptatıon to herbivory (MApce 1975). Feeding styles
found among bats include insectivory, piscıvory, omnivory, nectarivory, frugivory and
sanguinivory, and these are reflected ın the anatomy of various regions of the digestive
Grace:

The gross morphology and ultrastructure of the stomach of many microchiropteran
species have been reported (KamıyA and Pırror 1975; FORMAN 1972; RouK and GLass
1970), but little attention has been devoted to the digestive tract of the Megachiroptera
(Oxon 1977; BHIDE 1980; TEpman and Harr 1985a, b). The stomachs of Epomophorus
wahlbergi and Eonycteris spelaea as ın Eidolon helvum (Oxon 1977), Rousettus le-
schenaulti (BHIDE 1980), and Pteropus alecto and P. poliocephalus (TEDMANn and Harr
1985a, b) are large and saccular wıth an expanded cardiac and fundic region and a well
developed pyloric tube. The pyloric sphincter is asymmetrical. These features are also
characteristic of frugivorous microchiropteran species and serve to increase surface area for
digestion.

Kamiıya and Pırror (1975) interpreted stomach structure as plesiomorphic ın insec-
tıvorous bats, transitional in nectar feeders and apomorphic in frugivorous, and especially
sanguinivorous, bats. They noted only minor differences in gastric anatomy between Old
World and New World insectivorous species and also suggest that the Old World
(frugivorous) pteropodids are more specialised for a vegetarian diet than the New World
phyllostomatids. It ıs suggested that the pteropodids followed an independent path of
evolution towards vegetarianism before that of the phyllostomatids, and that similarities
between the two families are likely a result of convergence (STEPHAN and Pırror 1975;
Kamıya and PırLoT 1975).

Gastric histology and histochemistry have been used to reveal systematic relationships
of bats (ForRMmAn 1972; KamıyA and PırroT 1975), particularly in the Phyllostomatidae.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5705-0257 $ 02.50/0

258 M. R. Perrin and J. J. Hughes

This examination was undertaken to determine whether gross gastric anatomy can be
correlated with feeding specialisations (CARLETON 1973; PERRIN and Currıs 1979) and
phylogeny (PERRIN and Currıs 1979).

Material and methods

The African species were euthanised with carbon dioxide. Stomachs used for histological and
morphological studies were fixed in Bouin’s fixative for 18 h after which they were stored in 70 %
alcohol. The stomachs of the non-African species, which had been stored in 10% formalin for up to
three years, were also placed in 70 % alcohol. Gross morphology was first examined by bisecting the
stomach sagittally. Stomachs less than 1 cm in length were photographed with an Olympus B/H2
photomicroscope and larger stomachs wıth a Pentax SP II camera fitted with a Pentax macro lens.
They were than placed into one of the categories defined by Forman (1972). These include: a.
“regular”, b. “tunnelled”, and c. “elongated”. The authors recognise a further two forms, “recurved”
and “tubular” (Table).

Stomachs for histology were embedded in paraffın wax, sectioned at 6-9 u, and stained with
Ehrlich’s haematoxylın and eosin, Periodic Acıd Schiff (PAS) (Humason 1967), or AyouB and
SHKLAR (1983). Light micrographs were taken through a Leitz Laborlux 12 microscope equipped with
a Wild Photoautomat MPS 45/51 camera.

For scanning electron microscopy (SEM) small pieces (3x3 mm) of stomach tissue were fixed in
3% cold butfered glutaraldehyde for a minimum of 12 h. The tissue was subsequently critical point
dried, coated with gold palladıum and viewed with a Hitachi S-570 scanning electron microscope
(Cross 1979).

Results

The terminology used in describing the anatomical form of a hypothetical “generalised”
chiropteran stomach ıs presented ın Figure 1.

Oesophagus

Cardiac
Duodenum

Fundus-fundic glands

Fig. 1. A diagram to represent a generalised chiropteran stomach. BG = Brunner’s glands, CFTZ =
cardiofundic transition zone, PFTZ = pyloric-fundic transition zone

Gross morphology
Insectivorous species

The stomachs of the African insectivorous bats, M. schreibersi, M. fraterculus, R. simulator
and M. tricolor are categorised as “regular” and exhibit the simplified tubular gastric form
(Fig. 2). They are reniform and generally symmetrical with the greater and lesser curvature
nearly parallel. The stomachs are relatively short and the terminal portion (distal to the
gastro-oesophageal junction) is equal in length to that of the fornıx ventricularis. In M.
tricolor, however, the fundus is elongated (Fig. 3). The pyloric sphincters of all these
species are symmertrical.

Comparative gastric morphology of selected Old World and New World bats 259

Fig. 2 (left). Diagrammatic representation of a ‘regular’ chiropteran stomach. BG = Brunner’s glands,
CG = cardiac glands, FG = fundic glands, PG = pyloric glands, TZ = transıtion zone. (Miniopterus
schreibersi x 5,6). - Fig. 3 (right). The bisected stomach of Myotis tricolor showing the sharply angled
oesophagus and elongated fundus. C = corpus, F = fundus, O = oesophagus, PS = pyloric sphincter,
TZ = transition zone

Omnivorous species

In the “elongated” stomach of P. hastatus the cardıac vestibule is reduced to a vestige
(Fig. 4) while in G. soricina it ıs absent (Fig. 5). The fornix ventricularis is dilated and
expanded dorsally in both species. The terminal tubular stomach is extensive in G. soricina

Fıg. 4 (left). The bisected stomach of Phyllostomus hastatus. D = duodenum, F = fundus, O =
oesophagus, PS = pyloric sphincter. — Fig. 5 (right). Diagrammatic representation of an “elongated’
chiropteran stomach. BG = Brunner’s glands, CG = cardiac glands, FC = fundic caecum, FG = fundic
glands, PG = pyloric glands, TZ = transition zone (Glossophaga soricina X 6,3)

260 M. R. Perrin and J. J. Hughes

and P. hastatus, and the pyloric sphincters are asymmertrical (since the valves are larger on
the greater than the lesser curvature).

Nectarıvorous species

Eonycteris spelaea has a markedly sacculated stomach which is extensively elongated,
forming a tubular structure (Fig. 6). It is specialised and is here defined as “tubular”. The
large fornıx ventricularis is separated from the fundus by a fold of the stomach wall. The
cardiac vestibule is narrow while the fundus forms the elongated tubular portion of the
stomach.

Fıg. 6. The bisected stomach of Eonycteris spelaea. D = duodenum, F = fundus, FC = fundic caecum,
O = oesophagus, P = pylorus, PS = pyloric sphincter, TZ = transition zone

Frugivorous specıes

Artibeus sp. has a saccular stomach with an unusually large fornix ventricularis and a long
broad cardiac vestibule (Fig. 7). The pyloric tube ıs relatively long and narrow and has a
pronounced sulcus intermedius. Artibeus exemplifies the “funnelled” stomach condition
(Fig. 8).

The stomach of B. cavernarum ıs tubular and reniform and the terminal fundic area ıs
large and recurved (Fig. 9). It is here defined as the “recurved” stomach type. The fundic
caecum is also recurved and elongate while the oesophagus enters the stomach at a slight
angle. There is a pronounced pyloric constriction and the pyloric sphincter is symmetrical.

E. wahlbergi has a modified ‘recurved’ saccular stomach with an elongated, recurved
fundic caecum (Fig. 10). The fundus, corpus, pyloric antrrum and pyloric canal are
demarcated externally by constrictions in the stomach wall. The pyloric canal is elongated
and the pyloric sphincter is symmerrical.

Comparative gastric morphology of selected Old World and New World bats 261

Fıg. 7. External view of the whole stomach of Artibeus sp. C = corpus, CV = cardia vestibule, D =
duodenum, F = fundus, FC = fundic caecum, O = oesophagus, P = pylorus, SI = sulcus intermedius

eG

CV
FC

(eo)

| PG

7 F G

Fig. 8 (left). Diagrammatic representation of a “funnelled’ chiropteran stomach. BG = Brunner’s
glands, CG = cardiac glands, CV = cardiac vestibule, FC = fundic caecum, FG = fundic glands, PG =
pyloric glands, TZ = transition zone. (Artıbeusf sp. X 6,3). — Fig. 9 (right). Diagrammatic representa-
tion of the ‘recurved’ stomach condition. FG = fundic glands, PG = pyloric glands, FC = fundic
caecum, D = duodenum, (Brachyphylla cavernarum x 3,8)

Musculature

The muscularis externa of the insectivorous bats ıs exceptionally thick throughout the
stomach (Fig. 3), and is approximately twice as thick as that of the frugivorous E.
wahlbergi. In E. wahlbergi (Fig. 10), only the circular muscle throughout the greater
curvature of the pyloric tube appears to be particularly thickened.

262 M. R. Perrin and ]J. J. Hughes

Fig. 10. The bisected stomach of Epomophorus wahlbergi (x 3). F = fundus, FC = fundic caecum, O =
oesophagus, PS = pyloric sphincter, C = corpus

Pyloric sphincter

The pyloric sphincters of each African insectivorous species examined are symmetrical,
and typically possess thick muscle layers. The omnivorous species, P. hastatus and G.
soricina, however, have long asymmerrical valves which are longer on the greater curvature
(Figs 4, 5).

In the nectarivore, E. spelaea, the musculature ıs evenly developed on both sides of the
pyloric valve. A well-developed valve on the greater curvature is present in B. cavernarum.
In contrast to the other frugivorous bats, the pyloric sphincter in E. wahlbergi ıs
asymmetrical. The musculature is thicker in the valve on the lesser curvature, while the
valve on the greater curvature ıs longer and thinner.

Gastric mucosa

The stomachs of all the species examined are wholly glandular. Fundic glands occupy most
of the mucosal surface area, and these are characterised by their long slender appearance,
and the presence of chief and parietal cells wıthin the gland (Fig. 11). Under SEM the
pyloric and fundic regions are characterised by deep intoldings, the gastric pits. The glands
open into these recesses and the columnar epithelial cells show a typical “cobblestone”
surface appearance (Fig. 12).

Microvilli are present in the stomach of M. schreibersi and are short and sparsely
distributed. However, scanning electron microscopy reveals the presence of numerous
elongate microvilli throughout the stomach of E. wahlbergi (Fig. 13). Yeast and fungal
spores (possibly Penicıllıum or Argostinm) are particularly abundant in the megachiropte-
ran fruit bat, E. wahlbergi (Fig. 14), but are also common in the African insectivorous bat
species. No bacteria or other symbiotic organisms were observed in any of the bat
stomachs examined.

Comparative gastric morphology of selected Old World and New World bats

Fig. 11. The fundic glands in
the corpus of Epomorphus
wahlbergi (x 550). Cc = chief
cells, GP = gastric pit, Mc =
mucoid cells, Pc = parietal
cells

Fig. 12. A scannıng electron
micrograph of the “cobbles-
tone” surface of the fundic
glands in Miniopterus
schreibersi (x 480). Ec =
epithelial cells, GP = gastric

pit

263

M. R. Perrin and J. J. Hughes

264

]P> ıse9A = x ‘snanw = MW ‘sa1ods
jedung = SI ‘(00FE x) duagjgvm snaoqdowod7 jo ypewoıs ayı ur sa1ods jeduny pur 1seax (14214) pI 'Zu.] — ad sınsed = 9) ‘snanuı = W
frAOAIU = A 'paorstuı pare3uof> snolsumu ayı Surmoys T4agygrm "7 Fo snpuny ayı Jo ydeı3orsru U01299[9 Zuruueag ‘(1/97) EI "314

Comparative gastric morphology of selected Old World and New World bats 265

Discussion
Gross morphology

Variation in gross gastric morphology is extensive among the bat species examined, but
similar trends exist among closely-related genera and among bat species with similar food
habits. Several broad categories of gastric anatomy are recognised, named and exemplıfied.
These include regular (M. schreibersi), funnelled (Artibeus sp.), elongated (P. hastatus),

recurved (B. cavernarum) and tubular (E. spelaea).

Characteristics of the bat stomachs studied

Species Stomach type Dietary guild Family

Rhinolophus simulator Regular Insectivorous Rhinolophidae

Myotıs trıcolor Regular Insectivorous Vespertilionidae
Miniopterus schreibersi Regular Insectivorous Vespertilionidae
Miniopterus fraterculus Regular Insectivorous Vespertilionidae

Epomophorus wahlbergi Recurved Frugivorous Pteropidae
Artibeus sp. Funnelled Frugivorous Phyllostomatidae
Brachyphylla cavernarum Recurved Frugivorous Phyllostomatidae
Phyllostomus hastatus Elongated Omnivorous Phyllostomatidae
Glossophaga soricina Elongated Omnivorous Phyllostomatidae
Econycteris spelaea Tubular Nectarivorous Pteropidae

The funnelled and elongated stomachs have well developed, or reduced/absent, cardıiac
vestibules respectively, but each has a large fornıx ventricularis. The former characterises
frugivores while the latter exemplifies a condition intermediate between herbivores and
carnıvores.

FORMAN (1972) suggests that the sharply-angled pylorıc tube of the recurved stomach
has a distinctive crook at the point of recurvature, when the stomach ıs distended. This
might serve to retard the rapid transport of food through the stomach and cause foods that
are difficult to digest, to be exposed longer to digestive enzymes.

The tubular stomach of E. spelaea resembles that of Artibeus with respect to the cardıac
vestibule and fornıx ventricularis. In pteropodids, the cardiac vestibule is more evident
than in phyllostomatids (Kamıva and Pırror 1975), while the angled pyloric segment of
the pteropodids is as marked as that observed in Artibeus sp. Sımilarities also exist between
E. spelaea and Rousettus leschenaulti (BHiDE 1980), since the stomachs become progres-
sively narrower from the fornıx ventricularis to the pyloric region, and the tubular
portions reflex sharply.

Musculature

At the gastro-oesophageal junction in E. wahlbergi, there is a sphincter-like development
of the muscularis externa. This resembles similar structures ın E. helvum (Oxon 1977), P.
alecto and P. poliocephalus (TEpman and Harr 1985a, b). It is, however, absent ın R.
leschenaulti (BHiDE 1980). The sphincter may be important in resisting back pressure from
liquid food material contained within the stomach, especially when hanging upside down.

The insectivorous bats reveal a much greater degree of muscular hypertrophy through-
out the stomach than the frugivorous species. The prominent musculature of the insec-
tivorous bats is of great advantage in increasing the area over which large rhythmical
contractions can take place, thereby assisting gastric mıxing (FORMAN 1972).

The musculature of the stomach in frugivorous bats is better developed in the fornıx
ventricularis, cardıac funnel and region of the pyloric sphincter than ın the fundus and

266 M. R. Perrin and ]J. J. Hughes

corpus. The muscularıs externa ıs, however, less developed than in the insectivorous
species. In addition, small grooves are common on the grater curvature, notably in the
megachiropteran E. wahlbergi. The decrease in thickness of the muscle layer in frugivorous
species, and the development of ınvaginations, is probably an adaptation to allow
distension of the stomach to hold large quantities of food.

Pyloric sphincter

Those species possessing a symmetrical pyloric sphincter have a relatively effective closing
mechanism which ıs of greatest advantage to those bats feeding on a diet difficult to
assımilate, such as pulpy plants (Forman 1972). The frugivorous and nectarivorous
species, B. cavernarum and E. spelaea, possess a symmetrical valve, while the omnivorous
species, P. hastatus and G. soricina, possess a very long asymmetrical valve. The
megachiropteran E. wahlbergi, however, has an asymmetrical valve similar to that of R.
leschenaulti (BHIDE 1980).

The African insectivorous bats appear to possess relatively symmetrical valves, and
BHiDe (1980) reported that the aperture of the pyloric sphincter ın M. schreibersi ıs central.
However, many (partially) carnıvorous North American bats exhibit some degree of
asymmetry of the pyloric sphincter (FORMAN 1972).

Scanning electron microscopy

The presence of microvilli in the stomachs of insectivorous and frugivorous bats has not
been reported previously. The microvilli of E. wahlbergi, found throughout the stomach,
are long, slender and very abundant. The microvilli of the small intestine of Rousettus
aegyptiacus have been similarly described (KEEGAn and MoDinGer 1979). Villi in the small
intestine maximise the absorptive surface area (BARRY 1976), and probably account for the
rapid digestive process found ın megachiropteran fruit bats (KEEGAn and MODINGER 1979;
TEDMAN and Harr 1985 a, b). The microvilli in the stomach of M. schreibersi, although
much shorter and less abundant than in E. wahlbergi, likely serve the same function. In the
frugivorous bats, gastric microvilli probably increase the surface area for the absorption of
carbohydrates, but, in the insectivorous bats, ıt ıs likely they function in maximising
absorption of glycogen.

The presence of numerous yeast and fungal spores ın the stomach of E. wahlbergi is not
surprising but their occurrence in all the African insectivorous bats examined is intriguing.
The bats may ingest spores when feeding on insects, which might themselves have fed on
fruit or flowers.

The absence of symbiotic protozoans and bacterıa can be explained by the high food
transit rate observed in bats (THEDMAN and Harr 1985a) and the fact that herbivory ın bats
has not been recorded (YALDEN and MoRrRrıs 1975).

Within the family Phyllostomatidae, a gradatıon exists from insectivorous to OMnivor-
ous (P. hastatus to G. spelaea) to frugivorous habits (Artibeus sp.). Dietary differences
habe caused a progressive alteration of stomach structure, from the simplified condition in
the insectivorous species, to greater elongation and compartmentalisation of the stomach,
culminating in the condition found in Artibeus sp. This sequence suggests that changes ın
food habits from the early insectivorous condition resulted in adaptive modifications to
stomach morphology.

The uniformity of gross stomach morphology in the four insectivorous species
examined in this study lends support to Kamıya and PırLor’s (1975) findings of limited
variation in gastric structure between insect-eating bats. Variations between frugivorous
bats were, however, much greater. The general trend for frugivorous bats, which ingest
large quantities of bulky plant material with reduced protein content, is to increase gastric

Comparative gastric morphology of selected Old World and New World bats 267

volume by elongation and sacculation of the stomach, thereby increasing the exposure of
food to the digestive processes.

The stomach of the pteropodid E. spelaea exhibits the most specialised form ot all the
bat species examined. This supports Kamıya and PırLor’s (1975) hypothesis that the
Pteropodidae followed an independent evolutionary lineage after having diverged from an
ancestral stock at a very early stage. The general hypothesis that insectivorous bats
constitute the more plesiomorphic taxon (by having a simple tubular stomach), and that
the frugivorous species (possessing a complex sacculated gastric structure) represent a more
apomorphic taxon, is supported by this study.

Acknowledgements

We are especially grateful to Prof. G. C. Hıckman for his critical reading of a previous draft of this
paper. Many thanks also go to Mr. M. R. BrUORToN for his ideas, helpfulness in histological
interpretation, and correction of the initial draft; to Mr. ©. WIRMINGHAUS for assisting in the
collection and identification of the insectivorous, cave-dwelling bats; and the staff of the Electron
Microscope Unit for their technical assiıstance and the use of their darkroom. We acknowledge
financial support from the Foundation for Research Development, and the University of Natal’s
Research Fund.

Zusammenfassung

Vorläufige Befunde zur vergleichenden Magenmorphologie von ausgewählten Altwelt- und Neuwelt-
Fledermäusen

Mägen von zehn Fledermausarten (acht Microchiropteren und zwei Megachiropteren) aus neun
Gattungen und fünf Familien wurden morphologisch und histologisch untersucht. Alle Mägen waren
vollständig mit Drüsenepithel ausgekleidet. Es ließen sich aber morphologische Unterschiede zwi-
schen insektenfressenden, allesfressenden und fruchtfressenden Arten nachweisen. Anatomische
Abweichungen der Magenschleimhaut waren unter diesen Arten nur gering. Die insektenfressenden
Fledermäuse wiesen geringfügige zwischenartliche Unterschiede auf und hatten einen einfachen
röhrenförmigen Magen. Die Mägen der Fruchtfresser waren spezialisierter mit stärker voneinander
abgesetzten Abteilungen. Rasterelektronenmikroskopische Untersuchungen wiesen das Auftreten
von Microvilli in den Mägen einer insektenfressenden und auch einer fruchtfressenden Art nach.

References

Ayous, P.; SHKLAR, G. (1983): A modification of the Mallory connective tissue stain as a stain for
keratin. J. Oral. Surg. 16, 580-581.

BARRY, R. E. (1976): Mucosal surface areas and villous morphology of the small intestine of small
mammals: functional interpretations. J. Mammalogy 57, 273-2%.

BHIDE, $. A. (1980): Observations on the stomach of the Indian fruit bat Rousettus leschenaulti
(Desmarest). Mammalıa 4, 571-579.

BLoom, W.; FAwceEtT, D. W. (1975): A textbook of histology. 10th Ed. London: Saunders Co.

CARLETON, M. D. (1973): A survey of gross stomach morphology in New World Cricetinae
(Rodentia, Muroidea), with comments on functional interpretations. Misc. Publ. Mus. Zool.
Univ. Michigan, Ann Arbor 146, 1-43.

Cross, R. H. M. (1979): The preparation of biological material for electron microscopy. Unpubl.
manual, Rhodes University Electron Microscope Unit.

FORMAN, G.L. (1972): Comparative morphological and histochemical studies of stomachs of selected
North American bats. Univ. Kans. Scı. Bull. 26, 591-729.

Hırı, S. E.; SMITH, J. D. (1984): Bats: a natural history. London: British Mus.

Humason, G.L. (1967): Anımal tissue techniques. San Francisco: Freemann.

Kamıya, T.; PırroT, P. (1975): Comparative gastric morphology of Old World bats. I. In light
microscopy. J. Mammalogy Soc. Jpn. 6, 145-154.

KEEGAn, D. ]J.; MODINGER, R. (1979): Microvilli of the intestinal mucosal cells of Rousettus
aegyptiacus. S. Afr. J. Zool. 14, 220-223.

MADGe, D. S. (1975): The mammalıan alimentary system: A functional approach. London: Edward
Arnold.

Oxon, E.. (1977): Functional anatomy of the alımentary canal in the fruit bat Zidolon helvum, and the
insect bat Tadarida nigeriae. Acta. Zool. 58, 83-93.

PERRIN, M. R.; Currıs, B. A. (1979): Comparative morphology of the digestive system of 19 species

268 M. R. Perrin and ]J. J. Hughes

of Southern African myomorph rodents ın relation to diet and evolution. $. Afr. J. Zool. 15,
22-23.

Rouk, C. $.; GLass, B. P. 61970): Comparative gastric histology of five North and Central American
bats. J. Mammalogy 51, 454-472.

STEPHAN, H.; PıRLOT, P. (1970): Volumetric comparisons of brain structures in bats. Z. zool. Syst.
Evolut.-forsch. 8, 200-235.

TEDMAN, R. A.; Harrı, L. $. (1985a): The morphology of the gastrointestinal tract and food transit
time in the fruit bats Pteropus alecto and P. poliocephalus (Megachiroptera). Aust. J. Zool. 33,
625-640.

— — (1985b): The absorptive surface area of the small intestine of Pteropus poliocephalns
(Megachiroptera: Pteropodidae): an important factor ın rapid food transit? Aust. Mammal. 8,
271-278.

YALDENn, D. W.; MoRrrıs, P. A. (1975): The life of bats. New York: Demeter Press.

Authors’ address: M. R. PERRIN and J. J. HucHes, Department of Zoology and Entomology,
University of Natal, P.O. Box 375, Pietermaritzburg, 3200, South Africa

Z. Säugetierkunde 57 (1992) 269-274
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Social relations in groups of Black-capped capuchin monkeys,
(Cebus apella) in captivity: sibling relations from the second to
the fifth year of life

By C. WELKER, HELLA HÖHMANN-KRÖGER, and G. A. DovLe

Zoologie und vergleichende Anatomie —- Primatenethologie -, Universität Kassel, FRG

Receipt of Ms. 15. 8. 1991
Acceptance of Ms. 20. 3. 1992

Abstract

For juvenile black-capped capuchin monkeys brothers and sisters (related through the mother) are,
after the mother herself, the most attractive social partners to one another within the social group.
They approach, are approached, and sit together with their respective brothers or sisters significantly
more often than with other members of the social group, irrespective of age and sex. The same is true
for grooming and social play. In addition juveniles are more interested in their same-sex sıblings than
in their opposite-sex sıblings.

Introduction

Long-term studies of some primate species lıving in large social groups reveal that, after the
mother, juveniles prefer siblings as their social partners. Generally, close kin are more
attractive as social partners than lesser or non-related individuals. This ıs true for Macaca
mulatta (SapE 1965; DRICKAMER 1976; KapLan 1978; CHEPKO-SADE and SADE 1979;
BERMAN 1982), Macaca nemestrina (Massey 1977; WADE 1979), Macaca fuscata (KURLAND
1977; GLick et al. 1986a, b), Macaca arctoıdes (Estrapa and SANDOVAL 1977), Macaca
fascienlaris (DE WaaL 1977; WELKER and LÜHRMAnN 1982a, b; WELKER and WırT 1982),
and Theropithecus gelada (DunBAr 1978, 1980, 1982). It has been suggested that such a
preference is widespread throughout the primate order (WELKER 1985), including prosi-
mians (TAYLOR and SussmanNn 1985). This assumption needs to be tested, particularly ın
New World monkeys, ın which there are no comparable studies to date. Previous reports
on our long-term study of black-capped capuchin monkeys, indicated that, after the
mother, siblings are the most attractive social partners for infants (WELKER et al. 1987,
19903).

Since we have shown that black-capped capuchin young, irrespective of age, prefer their
mothers as social partners (WELKER et al. 1992), we would expect this to apply as well to
their second choice of siblings as preferred social partners. Whether any preference for
sıblings as social partners remains stable or decreases with age, is of particular interest. It ıs
also of importance to establish whether the choice of siblings as social partners is stronger
for same-sexed than for opposite-sexed siblings.

Material and methods

The main subjects of the present study were 18 Cebus apella juveniles, nıne males and nine females,
born into the same social group at the primate station of Kassel University. During the period of time
under consideration, this group consisted of up to 43 individuals. These 18 subjects provided data on
53 dyadic relationships — 12 male-male dyads, 15 female-female dyads and 26 male-female dyads ın
none of which the focal anımal was younger than two or older than 5 years. The data were collected by
focal anımal observations (12 anımals) or group observations (6 anımals). Each focal anımal was

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5705-0269 $ 02.50/0

270 C. Welker, Hella Höhmann-Kröger and G. A. Doyle

observed daily for 15 minutes each minute being a separate entity such that if one behaviour pattern
lasted 10 minutes it was scored 10 times. Group observations were conducted daily for 60 minutes
each two minutes being regarded as a separate unit such that if one behaviour pattern lasted for 10
minutes it was scored 5 times. All observation sessions were conducted randomly during the period
from 1500 to 1900 hours according to an established schedule. As in a previous paper (WELKER et al.
1992) both data sets were combined since comparison between both methods revealed no differences
between the different age/sex groups when frequency scores were converted to percentages.

Three of the 18 main subjects were observed over the whole life span covered in this paper, i.e.,
from year 2 to year 5. All She subjects were observed for from one to three years.

The patterns of social behaviour which occurred regularly and which were scored in terms of their
frequency of occurrence per unit time, by trained observers, were the same as those reported
previously (WELKER et al. 1992). These were: active approach, passive approach (being approached),
contact sitting, active grooming, passive grooming, social play.

The frequency of occurrence of a particular behaviour, in which a given sibling was involved with a
brother or sister, was converted to a percentage for the purpose of statistical comparison with the same
behaviour in which the sıbling was involved with other members of the social group on the basis of an
expected percentage frequency that assumed that all members of the group except the mother are
equally attractive as social partners.

High percentages in the figure should be read with caution since they may represent absolute
frequencies of behaviours that occur very seldom compared to others. To give sample sizes for the
data sets the mean (with standard error) of the absolute frequency of the different behaviour patterns
protocolled within one year ıs added (Tab. 1).

The statistical test used was the Mann-Whitney test with the level of statistical significance set at
p <0.05. The data of one individual collected over one year were taken as one independent sample for
statistical purposes.

Results

Both males and females approach their brothers and sisters significantly more often than
would be expected on the basıs of chance alone (approach - active - ın the Figure). For
males this ıs supported statistically, from year 2 to year 5, for both their brothers (B/B) and
their sısters (B/S) (Year 2, B/B p <0.01 and B/S p < 0.025; Year 3, BB p < 0.005 and B/S
p<0.005; Year 4, B/B p <0.001 and B/S p <0.0055 Xear' 5, DB pr I. 052.200
p < 0.05). For females this is supported statistically for their sisters (S/S) from year 2 and
for their brothers (S/B) from year 3 (Year 2, S/S p < 0.005; Year 3, S/S p <0.005 and S/B
p <0.005; Year 4, S/S p <0.001 and S/B-p <0.001; Mear 5, S/Sup= 00 TER
p < 0.001).

As would be expected both male and female juveniles are approached (approach -
passive — in the Figure) statistically more frequently by their brothers and sisters than
would be expected on the basis of chance. This is true for nearly all possible dyads (for
males: Year 2, B/B p <0.05; Year 3, B/B p <0.025 and B/S p = 05 Fear
p <0.001 and B/S p < 0.05; Year 5, B/S p < 0.05; for temales: Near 2,SSp 200 DC:
3, S/S p <0.005 and S/B p < 0.005; Year 4, S/S p <0.01 and S/B p < 0.001; Year 5, S/S
p <0.001 and S/B p < 0.001).

The tendency for juveniles of either sex to choose their own siblings wıth whom to sit ın
close contact is even stronger than the behaviour patterns of approaching and being
approached. Juvenile males and females sit in close bodily contact (contact sitting, Figure)
with their brothers and sisters more often than would be expected on the basıs of chance
(males: Year 2, B/B p <0.01 and B/S p <0.01; Year 3, B/B p < 0.01 EndB/ Sp 0
Year 4, B/B p < 0.001 and B/S p < 0.005; Year 5, B/B p < 0.05 and B/S p < 0.05: females:
Year 2, S/B p <0.05 and S/S p < 0.005; Year 3, S/B p < 0.005 and S/Sıp OL OU Sea
S/B p <0.01 and $/S p < 0.001; Year 5, S/B p <0.001 and $/S p < 0.001).

The Table clearly shows that the actual incidence of grooming between juvenile
siblings, at least in respect of males, ıs so low that conversion into percentages, as
illustrated in the Figure (grooming — active —), is misleading and statistical tests confirm
that, in males, the choice of siblings as grooming partners, in preference to other members

1

Sibling relations of Cebus apella ın captıvıty 271

[%] [%]
5: % Males ° Females
So 4#
OO > 3
QO 2
ri

—

&

—
12]
oO

- passive

_
oO Oo

—

&

[me
oa
oO

Social play Grooming Grooming Contact sitting Approach
_.. passive -

Year of life Year of life

[Brother DiSister

Mean percentage of the frequency of occurrence of some selected behaviour patterns, together with
the Standard Error of the Mean, of males toward their siblings (on the left hand side) and of females
towards their siblings (on the right hand side), compared to an expected mean frequency based on the
assumption that all members of the group are equally preferrable as social partners

aExpected value

of the social group, is insignificant. In females, on the other hand not only does grooming
become important from Year 3 but male siblings become particularly important as
groomees. Because of high individual differences statistics reveal that for female juveniles,
from year 3 on, only their choice of sisters as groomees is significantly greater than their
choice of other members of the socıal group (Year 3, p <0.05; Year 4, p <0.001: Year 5,
p < 0.05). Male sıblings only become attractive as groomees to female juveniles from Year
5 (p <0.05).

As the data for Active Grooming suggests, both male and female juveniles are groomed
(grooming — passive —, Figure) more frequently by their sıblings, particularly theır sisters,

C. Welker, Hella Höhmann-Kröger and G. A. Doyle

Mean absolute values of the social relations among capuchin monkey mother-related offsprings

Behaviour Year of Sex Brother Sister
Batlern life (number of dyads)
Approach 2% m 134 + 19 (6) I1=E194AO)
active f 50 (1) 13222976)
3, m 130 + 23 (9) 85 +21 (11)
f 64+ 26 (5) 132 + 43 (5)
4. m 111+ 17 (7) 79 + 15 (6)
f 79+ 20 (8) 70 + 24 (8)
5, m 135 + 37 (5) 33+ 66)
f 91+ 10(9) 77 #22 (9)
Approach 2. m 137-2346) 105 # 16 (10)
passive f 13 (1) 91 33246)
3. m 132 + 25 (9) 73 + 15 (11)
f 60+ 21 (5) 112 + 32 (5)
4. m 127 + 25 (7) 82 + 15 (6)
f 92+ 24 (8) 63 + 23 (8)
5. m 122 + 28 (5) 50 +17)
f 100+ 24 (9) 73 + 21 (9)
Contact- 2. m 138 + 42 (6) 116 #34 (11)
sitting f 216 + 141 8) 360 + 89 (6)
3, m 221 57 (9) 178 + 41 (11)
f 141 + 42 (5) 202 + 47 (9)
4. m 488 + 112 (7) 240 + 65 (6)
f 197 + 47 (8) 275 + 63 (10)
5. m 114 + 43 (5) 479 + 54 (3)
f 164 + 40 (9) 252 +45 (9)
Grooming 2% m 3EEgEln (6) a)
active f 9 17,474.8) Se ((ö)
3. m 9+ 4(9) g+ 3 (11)
f 70+ 43 (5) 32 +12 (9)
4. m 1+ 5() 7+ 2(6)
f 73 + 30 (8) 60 + 17 (10)
5. m 18+ 76) 7+ 36)
f 78 + 25 (9) 71 +24 (9)
Grooming DR m 15,227 7626) 38, 9a)
passıve f ee =) 89 +20 (6)
3 m 21+ 80) 30+ 8 (11)
f 6+ 465) 33+ 9 (9)
4. m 233+ 15 (7) 25+ 3 (6)
f 4+ 1(8) 26 +11 (10)
5. m 5+ 2(5) 52 +25 (3)
f 5+ 2(9) 19 + 4 (9)
Social 7 m 168 + 55 (6) 41 +12 (11)
play f 58=20224(8) 87 +39 (6)
3 m 144 + 35 (9) 23+ 8 (11)
f 754 24 (5) 108 + 32 (9)
4. m 207 + 45 (7) 17+ 7(6)
f 98+ 18 (8) 105 + 33 (10)
5. m 91+ 29 (5) 23 +23 (3)
f 43+ 8(9) 70 + 24 (9)

at all ages levels under consideration. Males are groomed by their sisters (Year 2,
p<0.001; Year 3, p <0.025; Year 4, p <0.025) and females by their sisters (Year 2,
p<0.005; Year 3, p <0.01; Year 4, p <0.05; Year 5, p <0.001) significantly more
frequently than by other members of the social group. Only at Year 3 are males groomed
significantly more frequently by their brothers than by other members of the socıal group

Sibling relations of Cebus apella in captivity 273

other than their sisters (p <0.05). In contrast, females are seldom groomed by their
brothers, in fact, significantly less frequently than they are groomed by their sisters (Year
DEE. I: Dean pr 0.025, 5 ean 4, pr 0.005, Near 5, p50. 0).

Finally, with regard to social play (socıal play, Figure), males play with their brothers,
but not with their sisters or other members of the group, more frequently than would be
expected on the basis of chance (Year 2, p <0.005; Year 3, p <0.001; Year 4, p < 0.001;
Year 5, p <0.005). Females, however, play significantly more frequently with their
siblings of either sex than wıth other members of the group (Year 2, S/S p <0.05; Year 3,
SISEPE U005; Mearz4, S/BupE=01025gand S/S7 pr 0.091; Mearı3,, S/Brp,=0.05.and S/S
p <0.005). For both males and females there is a preference for their own sex as play
partners (Table).

Discussion

For male and female black-capped capuchin juveniles brothers and sisters are important
social partners extending even into adulthood. Together with data on sibling relations in
the first year of life (WELKER et al. 1987, 1990a) a social network involving juveniles is
apparent. Males prefer their brothers as play partners while females have an equal
preference for brothers and sisters. Females have more affıliative contacts (contact sitting
and grooming) with their sıblings than do males. Similar results on sex-typical differences
in juveniles are well documented within the primate order as a whole (for a review see
WELKER 1985). Males show a strong preference for their brothers as social partners, while
females show an equally strong preference for brothers and sisters, at all age levels. Data on
one hand-reared female (WELKER et al. 1990b) suggest that precise genetic relatedness is
not the sole criterion for social preference. All group-born, juvenile capuchin monkeys
reared by their own mothers, interact more frequently with their sıblings irrespective of
age and irrespective of paternity. There are no reasons for believing that capuchin monkeys
are able to make socıal distinctions as a function of degree of genetic relatedness.

The above data suggest that kin relationships are important for social cohesion in
capuchin monkeys in the wild, as they are in Old World monkeys, and offer a pointer to
social relationships in other New World monkeys living under similar group conditions.

Acknowledgements

The authors wish to thank K. Bourceois, B. HoLLsTEIn, H. ROLAND, $. SCHULZ, G. WERNER for
participating in the data collection. This study was supported by grants from the Deutsche
Forschungsgemeinschaft (DFG).

Zusammenfassung

Soziale Beziehungen in Gruppen des Gehaubten Kapuzineraffen (Cebus apella) in Gefangenschaft:

Beziehungen zwischen Geschwistern vom zweiten bis zum fünften Lebensjahr

Für Jungtiere des gehaubten Kapuzineraffen sind neben der Mutter (über die Mutter verwandte)
Geschwister die attraktivsten Sozialpartner in der Gruppe. Geschwister suchen sich gegenseitig
häufiger auf und sitzen häufiger in engem Körperkontakt als mit anderen Gruppenmitgliedern,
unabhängig vom Alter und Geschlecht. Entsprechendes gilt für die soziale Körperpflege und das
soziale Spiel. Dabei bevorzugen sie gleichgeschlechtliche Geschwister.

References

BERMAnN, C. M. (1982): The ontogeny of social relationship with group companions among free-
ranging infant rhesus monkeys. I social networks and differentiation. Anım. Behav. 30, 149-162.

CHEPKO-SADE, B. D.; SADE, D. $. (1979): Patterns of group splitting within matrilineal kinship
groups. Behav. Ecol. Sociobiol. 5, 67-86.

DE Waar, F. B. M. (1977): The organization of agonistic relations within two captive groups of Java
monkeys (Macaca fascicularis). Z. Tierpsychol. 44, 225-282.

274 C. Welker, Hella Höhmann-Kröger and G. A. Doyle

DRICKAMER, L. C. (1976): Quantitative observations of grooming behavior in free-ranging Macaca
mulatta. Primates 17, 323-335.

Dunßar, R. I. M. (1978). Oestrus behaviour and social relationships among gelada baboons. In:
Recent advances in primatology. Ed. by D. R. CHivers and J. HERBERT. London: Academic
Press. Vol. 1, 491-492.

— (1980): Demographic and lıfe history varıables of a population of gelada baboons (Theropithecus
gelada). J. Anım. Ecol. 49, 485-506.

— (1982): Structure of social relationships in a captive gelada group: A test of some hypotheses
derived from studies of a wild population. Primates 23, 89-94.

EsTRADA, A.; SANDOVAL, J. M. (1977): Socıal relations ın a free-ranging troop of stumptail macaques
(Macaca arctoides): Male-care behaviour I. Primates 18, 793-813.

GLICK, B. B.; EATON, G. G.; JOHNSON, D. F.; WORLEIN, J. M. (1986a): Social behavior of infant and
mother Japanese macaques (Macaca fuscata): Effects of kinship, partner sex, and infant sex. Int. ]J.
Primat 7, 139-155.

— — — — (1986b): Development of partner preferences in Japanese macaques (Macaca fuscata):
Effects of gender and kinship during the second year of life. Int. J. Primat. 7, 467-479.

Kapran, J. R. (1978): Fight interference and altruism in rhesus monkeys. Amer. J. Phys. Anthrop.
49, 241-250.

KuRrLAND, ]J. A. (1977): Kin selection ın the Japanese monkey. Contr. Primat. 12, 1-145.

Massey, A. (1977): Agonistic aids and kinship in group of pigtail macaques. Behav. Ecol. Sociobiol.
2, 31-40.

SaDE, D. $. (1965): Some aspects of parent-offspring and sibling relations in a group of rhesus
monkeys, with a discussion of grooming. Amer. J. Phys. Anthrop. 23, 1-18.

TAyLoR, L.; Sussman, R. W. (1985): A preliminary study of kinship and social organization in a semi-
free-ranging group of Lemur catta. Int. J. Primat 6, 601-614.

Vessey, $. H.; MORTENsonN, B. K.; MUCKENHIRN, N. A. (1978): Size and characteristics of primate
groups in Guayana. In: Recent advances in primatology. Ed. by D. R. CHivers and J. HERBERT.
London: Academic Press. Vol. 1, 187-188.

WADE, T. D. (1979): Inbreeding, kin selection, and primate social evolution. Primates 20, 355-370.

WELKER, C. (1985) Zur Sozialstruktur der Primates. Anthrop. Anz. 43, 97-164.

WELKER, C.; BECKER, P.; HÖHMANN, H.; SCHÄFER-WITT, C. (1987): Social relations in groups of the
black-capped capuchin Cebus apella in captivity. Interactions of group-born infants during their
first 6 months of life. Folia primatol. 49, 33-47.

— — — — (1990a): Social relations in groups of the black-capped capuchin (Cebus apella) in
captivity. Interactions of group-born infants during their second halt-year of life. Folia primatol.
54, 16-33.

WELKER, C.; HÖHMANN, H.; SCHÄFER-WITT, C. (1990b): Significance of kin relations and individual
preferences in the social behaviour of Cebus apella. Folıa primatol. 54, 166-170.

WELKER, C.; HÖHMANN-KRÖGER, H.; DoyLe, G. A. (1992): Social relations in groups of black-
capped capuchin (Cebus apella) in captıvity: mother-juvenile relations from the second to the fıfth
year of life. Z. Säugetierkunde 57, 70-76.

WELKER, C.; LÜHRMANN, B. (1982a): Zum Sozialverhalten des Javanermakaken Macaca fascıicularis
Raffles, 1821. I. Der Rang als Eigenschaft des Individuums. Zool. Anz. 208, 175-191.

— — (1982b): Zum Sozialverhalten des Javanermakaken Macaca fascicularis Raffles, 1821. II. Zur
Sozialstruktur. Zool. Anz 208, 309-322.

WELKER, C.; WITT, C. (1982): Zum Sozialverhalten des Javanermakaken Macaca fascicularıs Raffles,
1821. III. Zur postnatalen Entwicklung während der ersten sechs Lebensmonate, Zool. Anz. 209,
177-195.

Authors’ addresses: Prof. Dr. CHRISTIAN WELKER, Dr. HELLA HÖHMANN-KRÖGER, Zoologie und
vergleichende Anatomie — Primatenethologie —, Universität Kassel, Heinrich-
Plett-Str. 40, D-3500 Kassel, FRG; Pror. Dr. GERALD A. DoyLe, Primate
Behaviour Research Group, University of the Witwatersrand, 1 Jan Smuts
Avenue, Johannesburg, South Africa

Z. Säugetierkunde 57 (1992) 275-287
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Satellite-linked radio tracking of Atlantic walruses (Odobenus
rosmarus rosmarus) in northeastern Greenland, 1989-1991

By E. W. Born and L. ©. KnuTtsen

Greenland Fisheries Research Institute, Copenhagen, Denmark

Receipt of Ms. 4. 11. 1991
Acceptance of Ms. 26. 3. 1992

Abstract

Determined the feasibility of using satellite telemetry for tracking of walruses in studies of stock
identities by attaching a total of 12 satellite transmitters to the tusks of male Atlantic walruses
(Odobenus rosmarus rosmarus) in Dove Bay (approximately 77° N-20° W), NE Greenland in August
1989 and 1990. In 1989 the Platform Terminal Transmitters (PTT) transmitted for an average of 53
days (SD = 36.3; range: 15-111 days; N = 6). In 1990 four PTTs with similar electronics (two of
which had a different antenna design) transmitted for an average of 125 days (SD = 96.9; range: 4-238
days). Two different PT’Ts worked for 62 and 112 days, respectively. It ıs indicated that the main
reason for premature transmission failure is that the walruses dislodged the units. During August and
September 1989 and 1990, all walruses regularly made excursions to the west and southwest up to a
distance of about 80 km from their terrestrial haul out site on the northern coast of Dove Bay. During
late September and early October the formation of a dense cover of land fast ice forced the walruses
off-shore into the Greenland Sea. The instrumented anımals moved north to winter in leads and cracks
in the pack ice between 80° and 82° N off the coast of NE Greenland.

Introduction

In August 1989 and 1990 satellite transmitters (PT’Is = Plattform Terminal Transmitters)
were attached to Atlantic walruses (Odobenus rosmarus rosmarus) ın Dove Bay, northeast-

“ern Greenland. The objective of the study was to determine the feasibility of using satellite

telemetry to track individual walruses and thereby potentially determine stock ıdentities;
in this case to elucidate whether a connection exists between stocks ın eastern Greenland
and in the Svalbard — Franz Josef Land region.

Walruses occur ın eastern Greenland between approximately 63° N and approximately
81°15’ N, but their main distribution is north of 70° N. Although it has been suggested
that walruses in Northeast Greenland form a relatively small and isolated stock, historical
information on observations of walruses in the Greenland Sea and the Fram Strait indicates
that a connection exists between walruses ın eastern Greenland and at Svalbard further east
(Born 1990).

Walruses were first instrumented with satellite transmitters by U.S. Fish and Wildlife
Service at Round Island in Alaska during the fall of 1987 (Fancy et al. 1988). In Greenland
the only terrestrial walrus haul out sites are found within the borders of the National Park
in northeastern Greenland. Because the same individuals occur on the beach several times
during the open water season, and also in subsequent years (BORN 1990), the remote and
undisturbed haul out site at Lille Snen&s (Dove Bay) ıs an ideal place for testing of satellite
transmitters in free ranging walruses.

In this study the satellite-linked radio transmitters used in NE Greenland, and their
performance, are described. The movements of the instrumented walruses in Dove Bay
and the Greenland Sea in the period August 1989 to late March 1991 are also presented.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5705-0275 $ 02.50/0

276 E. W. Born and L. ©. Knutsen

Material and methods

In the periods 9 to 24 August 1989 and 6 to 19 August 1990, a total of 12 adult male walruses,
Odobenus rosmarus rosmarus (sıx in each season) were immobilized by use of etorphine HCl on the
beach of Lille Snen&s (76°52’ N, 19°38’ W) on the northern coast of Dove Bay in NE Greenland, and
a satellite-linked radio transmitter (PTT) was attached to the tusk of each anımal.

The PTTs transmitted via the ARGOS DCLS system (Fancy et al. 1988; Arcos 1989; KEATING et
al. 1990). At 77°N there are about 28 satellite overpasses during each 24 hour period and the total
cumulative visibility of the two satellites above the horizon is about 5.5 hours, with maximum satellite
coverage employing the longest satellite passes between approximately 12 and 23 GMT (Fancr et al.
1988).

Three types of PTTs differing in shape, material, antenna type and electronics were used. In 1989
and 1990 a total of eight ST-3 PTTs (Telonics, Arızona, USA) with 20 cm long antennas constructed
of multistranded stainless steel cable were attached. Two ST-3 PTTs which were similar in shape and
material but had a 7 cm long helical antenna were used in 1990 (Fig. 1). Additionally, two T-2028
satellite transmitters manufactured by Toyocom Inc. (Tokyo, Japan) were attached in 1990 (Fig. 2).
The antennas of all transmitters used in 1990 were covered along their entire length by a 0.5-1.0 cm
thick layer of urethane (Sikaflex 11 FC) to provide strength.

The PTTs had different duty cycles (Tab. 1). The ST-3 PTTs which had a power output of 1 W had
repetition rates of 70 and 77. Repetition rate of the T-2028 units was 60; power output was 0.5 W.
None of the PTTs transmitted when two external conductivity electrodes (salt water switch, SWS),
positioned on the top of the PTT were connected via sea water (i.e. the walrus was submerged).

In addition to providing locations, the ST-3 PTTs also recorded information on external
temperature, duration of the previous dive before an uplink, average dive time over the past 24 or 6
hours, respectively, and number of dives (based on closures of the SWS) during the same periods of
time. The T-2028 PTTs gave location but had no memory for storing information of the activity of the
SWS.

Fig. 1. The ST-3 satellite transmitter with short helical antenna used in 1990 (A); close up view (B);
scale = 15 cm. The electronic package and the batteries of the transmitter were encased in a tinned
brass housing which was hermetically sealed and backfilled with a polymer material. The housing was
covered with urethane rubber to serve as a shock buffer. The unit weighed 1.5 kg

Satellite-linked tracking of Atlantic walruses in northeastern Greenland DM.

Two 19 mm wide, 316-type stainless steel bandings (Band-It, Houdaille, Denver) were used to
attach the unit to the tusk. Grooves were filed in the tusks where these bands would sit, and the lateral
surface of the tusk was ground with coarse sandpaper and then cleaned with acetaldehyde. In 1990
polyurethane (Sikaflex 11 FC) was used as a glue between the PT'T and the tusk. To ensure that the
SWS was out of the water during surfacing, the transmitters were positioned as far up the tusks as
possible and somewhat latero-caudally so that they did not protrude in front of the leading edge of the
tusks (Figs. 1 and 2). Thereby we hoped to prevent disturbance to the walrus when it was rooting with
its vibrissae in the sea floor during feeding. All units were painted with white road paint or fluorescent
car paint. Places where the paint was worn off during the field season would reveal sites of physical
impact.

mich on ice conditions in the study area was gathered from observations at Lille Snenes,
aerial surveys over Dove Bay during the field periods and extracted from NOAA (thermal infrared)
satellite imageries.

Fıg. 2. The T-2028 satellite transmitter used in 1990 (A); close up view (B); scale = 25 cm. The
transmitter which weighed 0.305 kg was glued into a stainless steel cylinder with polyurethane and
two-component epoxy glue, resulting in a total weight of the unit of 0.750 kg

Treatment of satellite-derived data

Activity of the SWS and temperature sensor data were used to determine whether an instrumented
anımal was hauled out. The software protocol repeated a qualified dive time until updated with a new
dive time. Therefore, when the value for the duration of the ‘last dive’ was repeated in the data stream
the walrus apparently was not swimming (i.e. it was hauled out). The duration of such a haul out
period was defined as the time between the first and the last uplink in a sequence of repeated “last dive’
data. An increase in temperature and reception of locations in the best quality classes (NQ = 1-3)
during the same period were regarded as supportive evidence that the anımal was hauled out.

The precision of the satellite-derived locations was determined for the instrumented walruses when
they were observed on the beach of Lille Snen&s. The exact position (+/-30 m) of the haul out site
(76° 52’ 53” N - 19° 38° 10” W) was determined from a 1:250000 topographic map (Greenland
Geological Survey) based on aerıal photographs and ground control points.

Swimming speed was calculated for instrumented walruses from straight line distances and time
between uplinked locations. Only distances with locations of quality NQ = 1-3 are used for this
analysıs.

278 E. W. Born and L. ©. Knutsen
Results

During the field periods, when
the instrumented anımals were
observed several times on the
beach after feeding excursions,
all PI'Ts stayed in position on
the tusks. We saw no attempts
to remove the PT’Ts, and appa-
rently the animals paid little at-
tention to the presence of the
units. Apart from being less vul-
nerable to wear, the short helical
antenna on two of the ST-3 units
used ın 1990 could not touch the
lateral vibrissae and therefore
was not able to disturb the anı-
mal. During the field season the
paint on the somewhat bulky
ST-3 PTTs was gradually worn
off. The wear began on the fron-
tal side, probably indicating that
the units were in contact with
the substrate during feeding.
Signs of wear were not observed
on the more elongate and slen-
der T-2028 unıts.

During August 1990, five of
the sıx walruses which were in-
strumented ın August 1989 were
recognized and subsequently
seen on the beach several times
during the field period. Walrus
no.4345, which transmitted for
111 daysın 1989, stillhadthe 1989
PTT in sırtu whereas the other
anımal had lost their transmitters.
Walrus no.4345 was immobı-
lized again on 8 August 1990 and
provided with a new PTT
(no.4349; Tab.1). On 28 and
29 August 1991 this walrus was
observed on LilleSnenzs with the
1990-PTT intact on the tusk. On
the same dates walrus no. 3985
was observed with the T-2028
PTT attached in 1990 on the tusk.
The antenna of thıs unit was bro-
ken off. Another anımal (ID
no. ?) instrumented in 1990 was
identified on the beach without
the PTT (SODER, pers. comm.).

% of expected
lifetime

then pause until a single string of
single string of sensor data was

No. of days

1 Dec. 90

(day/month/year)
11 Oct 90

Date of last uplink
30 Nov. 89
2IEOEL., 89

2IOct 39

— P reliable data for 22 consecutive days,

ptember then pause until 1 October when a

Expected lifetime*
instrumentation

Duty cycle
1 week on/1 week off

1 week on/1 week off
1 week on/1 week off
1 week on/1 week off

Continuous
1 week on/1 week off

24 h on/24 h off
1 day on/3 d off
1 day on/3 d off

Continuous
Continuous
Continuous

BE
ID number/ type

4344/ST-3
4347/ST-3
1858/ST-3
1856/ST-3
1859/ST-3
4348/ST-3
4346/ST-3'
4349/ST-3
1857/ST-3
3985/T-2028
3984/T-2028

Table 1. Performance of satellite transmitters attached on the tusks of Atlantic walruses in NE Greenland in August 1989 and 1990
4345/ST-3

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Satellite-hnked tracking of Atlantic walruses in northeastern Greenland 20

The PTTs transmitted between 4 and 238 days after attachment (Tab.1). In the
following analyses PTT no. 4346 (1990) is omitted. It only transmitted for the first four
days after attachment while the walrus was hauled out on the beach and is therefore
considered not to be representative. On average the ST-3 PTTs attached in 1990 functioned
three times longer than those used ın 1989 (1989): x = 53 days, SD = 36.3, N = 6; 1990: x =
165 days, SD = 65.7, N = 3; d = 2.749; P < 0.05).

During August and September, when the walruses occurred inshore and hauled out on
land and ice, at least one location was obtained from the ST-3 transmitters on an average of
77 % (range: 25 % to 100 %) of the PTT-days (i.e. days where the PTT was ın the ‘on duty’
mode). When the walruses moved offshore after September, the number of locations
decreased and at least one location was obtained on an average of only 33% of the PTT-
days (range: 14-58 %) during the remaining period. During August-September the two T-
2028 PTTs gave at least one location on an average of 32% of the PTT-days. The
corresponding value for the period October-December was 35 %.

This shift in distribution of instrumented anımals following a decrease in temperature
and formation of land fast ice in Dove Bay, was also reflected ın the location-performance
index of all transmitters (i.e. number of locations per PTT-day; Tab.2). The index for

Table 2. Location-performance index (locations - PTT-day’') as unweighted averages for two
different periods in 1989 and 1990

(i1.e. inshore period in August and September, and offshore period from October until transmission
stop)

PTT-type/N August-September October-onwards
Index (SD) (PTTs’) Index (SD) (PTTs)

1989 ST-3/6 7.77 (2.37) (6) .49 (3.56) (2)

5.49
1990 SEaya? 2.96 (1.22) (3) 1.25 (0.74) (3)
1.05

T-2028/2 1.67 (0.92) (2) (0.39) (2)

2 no. of active PTTs included in the analysis. — ®

no. 4346 which only transmitted for 4 days at the
beach was omitted.

August-Steptember for the ST-3 PTTs attached in 1990 was significantly lower than that
obtained for the same type of transmitters in 1989 (d = 2.749; P < 0.05). This was also the
case during October and later months (d = 4.018; P< 0.05; Tab.2). The low location-
performance indices obtained from the T-2028 PTTs during both periods in 1990 were not
significantly different from those from the 1990 ST-3 transmitters.

Overall, between 60.3 % and 76.6 % of all locations received from the different PTTs
were of the least precise category (NQ = 0; Tab. 3). The ST-3 PTTs with short antennas
apparently gave relatively more locations in the least precise category (NQ = 0) than the
other two types of PTT (Tab.3). However, this difference was not statistically assured
(Be lex 10521, dt — 9).

The number of locations received, and their quality, was to a large extent influenced by
the behaviour of the walruses, and in particularly by whether they were in the water or
were hauled out on ice or land. The time that instrumented anımals hauled out on the
beach of Lille Snenzs, as determined by SWS activity, was on average 0.65 h later (SD =
0.95; range: 0.05-2.43 h; N = 6) than actual time determined from direct observations. On
average, the recorded time of entering the water was 1.37h (SD = 1.50; range:
0.05-5.10 h; N = 16) late in comparison with direct observations. Thus, the activity of the
SWS can be used to roughly determine haul out activity. For walruses instrumented with
ST-3 PTTs a location-performance index was determined for three “behavioural

280 E. W. Born and L. ®. Knutsen

Table 3. Distribution of locations in four categories of precision (NQ = 0-3) for three different
types of PTTs

PTT-type/No. of PTTs No. of % of locations in four different quality classes
locations NQ =0 n 2 3

ST-3 long antenna/6 1251 60.3 21.4 16.6 114,7

ST-3 long antenna/2 254 60.6 26.8 11.8 0.8
ST-3 short antenna/2 459 76.6 11740 Se 0WZ

T-2028 long antenna/2 56 62.5 26.8 8.9 1.8

categories”: 1. ın water, 2. hauled out on land, and 3. hauled out on ice. In both seasons,
and for all three substrates, there was a tendency for the number of locations per hour to
decrease during the period. These trends were, however, not statistically significant and
the data were therefore pooled for the two years (Tab. 4). The location-performance index
for anımals on ice was higher than for anımals which hauled out on land. A relatively larger
fraction of the locations was of the least precise category (NQ = 0) when the animals were
in the water (Tab.4). Although the location-performance indices of the two “short
antenna” PTTs were lower than those obtained from the eight ‘long-antenna’ ST-3 PTTs,
the differences were not statistically significant (P > 0.05).

Table 4. Location-performance index (locations - PTT-h"') for three different “substrates’ for ST-3
PTTs on walruses during August-November 1989 and August-December 1990

Substrate Time Location- % of locations in four quality classes
surveyed’? performance (NQ = 0-3)
(h) index (loc./h) 0 1 2 3

1989/6 Water 3234.96 3 5 8.6
Land 649.77 ; ; 28.4

1
Ice 67.93.57. N i DD 2

1990/4 Water 2781.52 Ä i 07
Land 739.40 ! : 28.8
Ice 342.67 S 5 38

* during the period a variable number of PTTs with different duty cycles were monitored.

The satellite-derived locations (NQ = 1-3) of walruses hauled out on Lille Snen&s were
somewhat less precise than specified by the system (Tab. 5). On average, the locations ın
the least accurate category (NQ = 0) were between 10 and 12 km oft Lille Snens.

Satellite derived information on travelling speed indicates that average swimming speed
was 4.0 km/h (SD = 4.03). In this study a maximum travelling speed of 16.7 km/h was
recorded (Tab. 6).

Movements

Satellite derived information on movements revealed that during August and the first half
of September 1989 and 1990, all instrumented walruses made excursions from the beach of
Lille Snenzs, to the shallow water areas in the western and southwestern parts of Dove Bay
(Fig. 3). Locations in the best quality classes indicate that maximum distance from Lille
Snen&s of such excursions was about 80 km. Due to the absence of ice in Dove Bay in
August and September 1990, the animals were not able to haul out on ice floes during their
feeding excursion. For that reason substantially fewer off-shore locations were obtained in
1990, and hence the walruses movements could not be followed in similar detail.

Satellite-hinked tracking of Atlantic walruses in northeastern Greenland

281

Table 5. Precision of locations for three different types of PTTs on walruses which hauled out on
the beach of Lille Snenzs (Dove Bay, NE Greenland) in August 1989 and 1990

ST-3

Long antenna
(N=8)

ST-3

Short antenna
(N =2)
T-2028
(N=2)

NQ=0
Mean (SD)

(range)

12.374 (26.501)
(0.114-170.690)

90

10.211 (15.633)

(0.300-84.959)
43

1
Mean (SD)
(range)
N

0.935 (0.861)
(0.1344.276)
51

1.131 (1.142)
(0.450-4.581)
19

0.748 (0.422)
(0.447-1.231)
3

2
Mean (SD)
(range)
N

1.364 (1.197)
(0.114-5.428)
31

1.089 (0.786)
(0.101-2.387)
11

Precision (km) of locations in four location classes

3
Mean (SD)

(range)

0.795 (0.035)
(0.764-0.832)
3

11010@)
(0.444-2.203)
2

1.034 (-)

1

Swimming speed (km/h)
Min. Max.

0.32
0.44
0.90
1.68

In 1989 the last location from Lille Snen&s was obtained from walrus no.4345 on
19 September. The two anımals (no. 1858 and no.4345) which still had units which
transmitted after the fırst half of September progressively moved south in Dove Bay during
the second half of September. Presumably this happened as a response to fast ice being
formed in the bay. Walrus no.4345 spent some time at the shallow water banks at
Päskenzsset and at the southwestern shore of Store Koldewey before moving otfshore into
the Greenland Sea around 17 October (Fig. 4). The locations ın the best qualıty class (NQ
= 3) from the shores near Päsken&sset and on the southwestern coast of Store Koldewey
indicate that no.4345 hauled out on land on these locations. During the second half of
October and until 29 November, when the last location was received in 1989, walrus
no. 4345 occurred oft-shore in the Greenland Sea south to a straight line distance of about
430 km from Lille Snenzs (Fig. 4). Locations were obtained from the shear zone between
the very dense pack ice over the continental shelf and the more actıve and loose pack ice
further east overlying deeper waters. At the beginning of November the walrus made an
excursion to the shallow water ground at the southern shore of Shannon where there was a
polynya ın 1989. When transmissions ceased at the end of November, walrus no. 4345 had
moved northwards against the East Greenland Current to a shallow water bank.

In 1990 the walruses were able to haul out on Lille Snen&s until the beginning of
October. The last location from the beach was received from walrus no. 4348 on 5 October
1990. During the first half of October 1990 the walruses were forced by the formation of a

282 E. W. Born and L. ©. Knutsen

(6)
BO

O

Ai
\
A|
Fl
sl
50
dl
‚1
t
Oi
“
A
Ol
Bu
I

Qo

Fig. 3. Locations (NQ = 0-3) received between 6 August and 18 October 1989 (0) and 1990 (@) from a
total of 12 male walruses instrumented with satellite transmitters. All locations south of 76° 20’ N
were from after 29 September. For days where only locations in the least accurate category (NQ = 0)
were obtained, an average location calculated on basis of all locations received during that 24 h period
is given as a single point in the Figs. 3-5

Satellite-linked tracking of Atlantic walruses in northeastern Greenland 283

\| Store Koldewiey:. = ur ;

76

gN

29.11

2 ana
: © j N

et 281 7,

e .
IM 15.11 2 7,
29.10 /
12.118 8,20.10/
. /

07 ;

Fig. 4. Movements of walrus “N” (no.4345) in the Greenland Sea between mid-October and late
November 1989. « = NQ =3;e=2;0=1;A=0, (15.10 = day and month)

dense cover of land fast ice in Dove Bay to retreat offshore into the Greenland Sea (Fig. 5).
This emigration occurred both through the straits north and south of the island of Store
Koldewey. During the fall migration in 1990 walrus no. 4349 followed more or less the
same route as ın 1989. In October and November 1990 the instrumented walruses moved
north in the Greenland Sea, against the direction of the East Greenland Current. They
occurred in the shear zone between the dense land fast ice and the more dynamic pack ice
to the east. This zone lies over the edge of the shallow water banks of the continental shelf.
On 16 November 1990 walrus no.4348 occurred at 82° 15’ N and 6° 33’ W (Fig.5).
However, this position represents an average of three locations in the least precise category
ranging between 80° 36'-83° 42’ N and 4° 23’-9° 02’ W. The last location from no. 4349
was received on 27 March 1991 (Fig. 5).

The study showed that walruses winter ın leads and cracks in the dense pack ice off the
coast of NE Greenland and in the polynya off Nordostrundingen (“The Northeast Water’).

284 E. W. Born and L. ©. Knutsen

10°W 16.11

FramStrait „>22. 80°

DD
pLRAAAR

Sfr\%
mE:
>

SVALBARD X

#1857 r
#3985 —
#4348 ———

#4349 ——

Fıg. 5. Movements in the Greenland Sea of four walruses which transmitted after mid-October 1990.
A: edge of pack ice late March 1991

Based on tracking of admittedly few anımals it is indicated that the group of walruses
occurring in eastern Greenland is separate from walruses in the Svalbard and the Franz
Josef Land areas further east.

Discussion

Observations at Lille Snenzs indicate that the weight and the shape of the ST-3 PTTs
attached to the tusks apparently did not affect the walruses. The ST-3 units represented
only about 0.2 % of estimated total body weight of the instrumented anımals and 4 to 5 %
of the weight of the head (Born, unpubl. data). However, the somewhat bulky configura-
tion of this PTT and the unprotected and lateral position of the 20cm whip antenna

e Ze ememnen

Satellite-Iinked tracking of Atlantic walruses in northeastern Greenland 285

apparently caused premature transmission failure in some cases. Transmission failure due
to breakage or manipulation of the long version of the ST-3 antenna was observed in 1989
and 1990. Loss of the unit after we had left the study area may have caused the
transmissions to stop in other cases. This ıs supported by the finding that walrus no. 4345
(= n0.4349 in 1990), which transmitted for 111 days ın 1989 and 238 days in 1990-1991,
still had the unit attached when it reappeared at Lille Snen&s in August 1990 and 1991,
respectively; and that walrus no. 3984, which transmitted for 112 days ın 1990, also had the
T-2028 PTT in August 1991 whereas all others had lost their unit. Evidently, the short
antenna was superior in that it was not able to touch the vibrissae, which are very sensitive
(KASTELEIN and GAALEN 1988) and thereby motivate the walruses to dislodge the unit. The
fact that no wear was observed on the T-2028 PTTs attached in 1990 confirmed our
suspicion that the use of smaller and more elongated PTTs is desirable, in particular for the
tracking of subadults or female walruses which have slender tusks.

Comparatively more off-shore locations were received during August-September 1989
than in 1990. This ıs due to a difference in ice conditions in Dove Bay during the two
seasons. The availability of suitable ice for hauling out influences walrus behaviour and
hence the results of the telemetry. During the field period in 1989 (29 July to 25 August)
the central and deeper parts of Dove Bay were 9/10 covered with a sheet of old fast ice
whereas the shallow water area ın the western part of the bays was 1-5/10 ice covered. In
1990 the sheet of 6-8/10 fast ice which covered the central parts of Dove Bay by 29 July
broke up between 6 and 10 August and was swept away by strong winds coming from the
west. Thereafter there were no ice floes for hauling out in the area.

The number of locations received per hour was greater for anımals on ice than for
animals on land. This ıs presumably because walruses hauling out on land spent pro-
portionally more time doing so during nıght and early morning than those anımals which
hauled out on ice (Born, unpubl. data). Hence, walruses on land spend proportionately
more time hauled out during periods with reduced satellite coverage and when satellite
overpasses occur at low angles. In contrast, walruses which were on ice preferably hauled
out during afternoon and evening when there is better satellite coverage. In some cases the
400 to 800 m high mountains in the surrounding of Lille Snenes may have blocked
transmissions during some satellite passes.

Walruses on ice produced a greater proportion of higher quality locations than those on
land. Presumably this ıs due to the combined effect of a difference in diurnal haul out
rhythm, as indicated above, and the VSWR (voltage standing wave ratio) effect. When
placed on an anımal the performance of a PTT is reduced due to the proximity of the
antenna to the anımal’s body and the resulting effect of the VSWR. The result of the VSWR
effect is a reduction in effective radiated power from the antenna because of detuning and
pattern lobing due to the antenna’s close proximity to a large conductive mass (Fancy et al.
1988). We suspect that the VSWR effect may be relatively large for PTTs that are attached
to walruses where the antenna is close to the massive and often moist head of the anımal.
The comparatively poor location-performance index for walruses which were hauled out
on land can partly be explained by the VSWR effect also originating from the antenna being
in close proximity to the bodies of other walruses. Observations made from Lille Snenzs
showed that walruses which hauled out on ice were either single or in groups of only two
or three individuals (Born, unpubl. data).

The greater location-performance index of the ST-3 PTTs in comparison with the T-
2028 PTTs can likely be ascribed to the greater power output of the ST-3 transmitters.

Our findings are very similar to those reported by STEwART et al. (1989) who ın a study
of free ranging harbour seals (Phoca vitulina richardi), found that about 60% of the
locations obtained at sea were of poorer quality (NQ = 0) and that the overall accuracy of
NQ = 0 locations was about 15 km. Satellite-derived locations obtained for walruses at
Lille Snen&s were somewhat less accurate than specified by the system. A similar

286 E. W. Born and L. ©. Knutsen

discrepancy was also experienced ın a study of white whales (Delphinapterus leucas) by
MARTIN and SMITH (1989) and by STEwART et al. (1989) in harbour seals.

As pointed out by STEWART et al. (1989) the fact that fewer locations are obtained from
diving anımals makes it likely that locations from feeding areas are under represented.
Direct observations showed that walruses which apparently were feeding spent about 85 %
of the time submerged (Born 1992). Only few locations can therefore be expected from
feeding walruses when they do not have an opportunity to haul out on ice between feeding
bouts. This was confirmed when very few locations were obtained from walruses offshore
during August and September 1990 when there was no ice in Dove Bay. This was in
contrast to 1989 when several locations were obtained from walruses which hauled out on
ice at the shallow banks in Dove Bay. Walruses feed on bottom dwelling molluscs (e.g. Fay
1982; Fay and Burns 1988) and must theoretically dive for between 6 and 16 hours per day
to meet their daily food requirement. They therefore spend a lot of time at the mollusc
banks and the probability of ıdentifying such feeding areas via a relatively large number of
locations is greater than in seals which feed pelagically. We believe that the stenophagous
feeding behaviour of the walrus allows satellite telemetry to be used for the identification
of feeding areas and perhaps also of other areas of ecological importance (e.g. mating areas)
in this species.

Satellite derived information on travelling speeds obtained in our study is consistent
with other published data. According to Fay (1982) the normal swimming speed of
walruses is up to 10 km/h. Fay (1981) states that normal cruising speed ıs ao: 7 km/h
while the maximum “spring” speed ıs at least 35 km/h.

Our study indicates that the walruses migrate into Dove Bay during the open water
season for two purposes: 1. to feed intensively on the molluscs banks, and 2. to haul out
on land at Lille Snen&s between feeding excursions to moult.

From tracking a relatively low number of walruses we tentatively conclude that:
1. satellite telemetry ıs a suitable method for studying spatial and behavioural ecology of
walruses, 2. walruses can winter ın small groups ın leads and cracks along the coast of NE
Greenland in areas wıth shallow water and 3. a separate stock of walruses may occur in
these areas.

Acknowledgements

This study was financed by a research grant from Aage V. Jensens Foundation. The logistic support
received from Greenland Environmental Research Institute, Greenland Fisheries Research Institute
and Greenland Geological Survey ıs greatly acknowledged. We are particularly grateful for the help
and encouragement that we received during various phases of this study from $. Hırıs (U.S. Fish and
Wildlife Service, Alaska), S. Tomkıew1cz (Telonics) and M. HasEGawA (Toyocom). RENE SODER is
thanked for providing us with information on walruses at Lille Snen&s in 1991. We wish to thank Drs.
A. R. Martın (Sea Mammal Research Unit, British Antarctic Survey, Cambridge), $S. TOMKIEWICZ
and $. Hırıs for their constructive criticism to an early draft.

Zusammenfassung

Satelliten-gestützte Telemetrie an Atlantik-Walrossen (Odobenus rosmarus rosmarus)
von 1989 bis 1991 im Nordosten Grönlands

Um die Anwendbarkeit von Satelliten-Telemetrie für Studien des Bestandes von Walrossen zu klären,
wurden im August 1989 und 1990 insgesamt 12 satellitengestützte Sender an den Stoßzähnen von
ausgewachsenen, männlichen Atlantik-Walrossen (Odobenus rosmarus rosmarus) angebracht. Die
Walrosse befanden sich in der Dove Bucht (77° N-20° W) in NO Grönland. 1989 funktionierten die
Sender durchschnittlich an 53 Tagen (min.-max.: 15-111 Tage; N = 6), 1990 vier Sender mit ähnlicher
elektronischer Ausstattung im Durchschnitt 125 Tage (min.-max.: 4-238 Tage). Jedoch hatten zwei
dieser Sender ein anderes Antennendesign. Die zweı Sender des anderen Fabrikates arbeiteten an 62
bzw. 112 Tagen. Der frühzeitige Transmissionsabbruch ist sehr wahrscheinlich dadurch begründet,
daß die Walrosse die Sender zerstört und entfernt hatten. Im August und September 1989 und 1990
unternahmen die mit Sendern versehenen Tiere Exkursionen innerhalb der Dove Bucht, und zwar ın

ZT —

Satellite-linked tracking of Atlantic walruses in northeastern Greenland 287

einem Abstand bis zu 80 km von dem Platz, an dem sie an Land gegangen sınd an der Nordküste der
Bucht. Im Laufe des September/Oktober zwang eine neue, dichte Eisschicht in der Dove Bucht die
Walrosse dazu, sich nach Osten ins Grönländische Meer zu begeben. Danach strebten sie in Richtung
Norden, wo sie in Spalten im dichten Packeis zwischen 80° N und 82° N vor der nordostgrönländi-
schen Küste überwintern.

References

Arcos (1989): Guide to ARGOS system, September 1989. Toulouse, France: CLS ARGOS.

Born, E. W. (1990): Distribution and abundance of Atlantic walrus (Odobenus rosmarus rosmarus) ın
Greenland. In: The Ecology and Management of Walrus Populations: Report of an International
Workshop. Ed. by F. H. Fay, B. P. Kerry, and B. A. Fay. Washington, DC: U.S. Marine
Mammal Commission. 95-153.

— (1992): Odobenus rosmarus Linnaeus, 1758 — Walross. In: Handbuch der Säugetiere Europas.
Meeressäuger. Teil III: Robben. Ed. by R. Ducuy and D. Rosıneauv. Wiesbaden: AULA-Verlag.

. 269299.

Each SU@EEPANK 1 5 DOucräs, Di &I@vrey, EC H.; GARNER, EG: W.3 AMSTIRUP, S./E;;
REGELIN, W.L. (1988): Satellite Telemetry: A New Tool for Wildlife Research and Management.
U.S. Fish and Wildlife Service Resource Publ. 172, 1-54.

Fay, F.H. (1981): Walrus Odobenus rosmarus (Linnaeus, 1758). In: Handbook of Marine Mammals.
Vol.1. The Walrus, Sea Lions, Fur Seals and Sea Otter. Ed. by S. H. Rınagway and R. ]J.
Harrıson. London: Academic Press. pp. 1-23.

— (1982): Ecology and Biology of the Pacific Walrus, Odobenus rosmarus divergens Illıger. North
American Fauna 74, 1-279.

Fay, F. H.; Burns, J. J. (1988): Maximal feeding depth of walruses. Arctic 41, 239-240.

TRASUER, R. A.; GAALEn, M. A. van (1988): The sensitivity of the vibrissae of a Pacific walrus
(Odobenus rosmarus divergens) Part 1. Aquatic Mammals 14, 123-133.

Kearıng, K. A.; BREWSTER, W. G.; Key, C. H. (1990): Satellite telemetry: Performance of anımal-
tracking systems. J. Wildl. Manage. 55, 160-171.

Marrın, A. R.; SMITH, T. G. (1989): Tracking of a beluga whale using satellite telemetry. Int. Whal.
Commn Paper SC/41/SM 27, 1-11.

STEWART, B. S.; LEATHERWOOD, $.; YOCHEM, P. K.; HEIDE-JORGENSEN, M. P. (1989): Harbor seal
tracking and telemetry by satellite. Marıne Mammal Scı., 5, 361-375.

Authors’ address: Erık W. Born and Lars QıvinD KnUTsen, Greenland Fisheries Research Insti-
tute, Tagensvej 135, DK-2200 Copenhagen N, Denmark

Z. Säugetierkunde 57 (1992) 288-293
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Home range shifts accompanying breeding in the Eastern
Chipmunk, Tamias striatus (Rodentia: Sciuridae)

By M.A. Bowers and T.G. CARR

Department of Environmental Sciences and Blandy Experimental Farm, University of Virginia, Clark
Hall, Charlottesville, Virginia, USA

Receipt of Ms. 31. 10. 1991
Acceptance of Ms. 20. 3. 1992

Abstract

Capture-recapture techniques were used to study home ranges of 34 breeding and non-breeding male
and female Tamias striatus over a nıne week period. Results showed that reproductive males were of
larger body sıze and had larger home ranges than non-reproductive males. Females attaining oestrus
were also larger than non-reproductive females at the beginning but not at the end of the study. Also,
females in oestrus had smaller home ranges than non-oestrus females and, for females that attained
oestrus, breeding home ranges were smaller than pre- or post-oestrus home ranges. These results
suggest that the breeding behavior of Tamias may involve home range adjustments made by both
males and females.

Introduction

Mating behavior, availability of food and water resources, and local population density
have all been implicated as factors affecting home range size in the eastern chıpmunk,
Tamias striatus (Linnaeus, 1758) (YERGER 1953; DunFrorD 1970; FORSYTH and SMITH
1973; TRyon and SYNDER 1973; MARESs et al. 1976; YAHNER 1978; GETTY 1981a; BOwERS
et al. 1990). For Tamias, permanently located burrows provide a fixed center of activity
around which areas usually less than 1 ha (more typıcally, between 0.08 and 0.60 ha) are
utilized on a periodic basıs (BLaır 1942; Ickes 1974; ELLIoTT 1978). Although substantial
overlap in home ranges is common, central core areas are defended against conspecific
neighbors (WOLFE 1966; DunrorD 1970; Ickes 1974; YAHNER 1978; ELLIOTT 1978;
GETTY 1981b). During the summer breeding period, males usually have home ranges that
overlap with and may totally subsume the smaller ranges of females and non-breeding
males (ForsyTH and SMITH 1973). Like many solitary, ground dwelling sciurids, Tamias
has a polygynous mating system (EMLEn and OrınG 1977), and the expansion of home
ranges by breeding males ıs a way in which multiple females can be mated (YAHNnER 1978;
Dosson 1984). Breeding females are thought to have home ranges that are not different
from that of non-breeding females (e.g., ELLIoTT 1978).

In our studies of T. striatus in Virginia, USA, we have documented shifts in home
ranges that involve both breeding males and females. Here we describe these shifts.
Included are examinations of home range size of breeding and non-breeding individuals,
and changes in home ranges of individual females that occur with the onset of oestrus.

Material and methods

Our study was conducted at the Blandy Experimental Farm, a biological field station of the University
of Virginia located in the northern Shenandoah Valley at an elevation of 190 m in Clarke County,
Virginia, USA (ca. 78°00W, 39°00N). Located in the central portion of the Farm is the 50-60 ha
Orland E. White Arboretum that includes over 7,000 mostly large, mature native and exotic trees.
Specimen plantings are separated by open fields, and running throughout are more than 2 km of loose

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5705-0288 $ 02.50/0

Home range shifts accompanyıng breeding in Tamuas striatus 289

stone walls that were constructed over 100 years ago from rocks and boulders of dolomite origin. The
understory of the Arboretum is mowed regularly. The open, parklike vegetation with a combination
of thick canopy, open understory, and stone walls with numerous crevices affordıng refugia and
burrowsites, creates favorable habıtat for the eastern chipmunk (for further description of the site see
Bowers et al. 1990).

The population of chıpmunks residing in the Arboretum was studied by capture/recapture
techniques for 9 weeks from 1 June to mid-August, 1988. One-hundred eleven folding, Sherman live
traps were placed within 1m of stone walls at 15 m intervals. Traps were set 3-4 successive days
during each of the 9 weeks, using cracked corn as bait, and were checked at dawn and dusk. To lessen
mortality due to heat stress, traps were placed in cardboard shelters and closed during afternoons on
particularly hot days (> 30 °C). Captured anımals were weighed, sexed, fitted wıth a numbered
eartag, and released. Sexual condition of all captured anımals was recorded: males as scrotal or non-
scrotal; females with swollen or non-swollen vulvas (see SMITH and SmITH 1975).

We use two measures of home range size: 1. the average distance between capture locations; and 2.
the maximum distance between all capture locations. Use of linear estimates of home range size was
justified because chipmunks showed strong affınities for the stone walls (i.e., in previous investiga-
tions they were rarely captured at traps > 5 m from the walls), producing home ranges that extended
along walls and were largely one-dimensional (see BowERs et al. 1990).

Results

Over the 9-week study period more than 3,400 trap nights produced over 400 captures of
58 chipmunks. We restrict our analyses here to only those 34 individuals (10 males and 24
females) captured four or more times. These individuals were captured an average of
10.7 # 7.4 times each over the summer. During the study perid four of the 10 males, and
nıne of 24 females attained breeding condition. Females were observed to be ın oestrus
between 5-14 July. Scrotal males weighed more than non-scrotal males, and anımals of
both sexes in breeding condition were captured significantly more often than reproduc-
tively inactive individuals (Tab. 1). Females that attained oestrus in July weighed less ın

Table 1. Mean (+SD) body weights (in August), number of captures, and the average and
maximum distance between trap captures (calculated over the nine-week study period) for
breeding and non-breeding male and female Tamias striatus

Estimate Females Males
Breeding Non-breeding Breeding Non-breeding
(n = 9) (n = 15) (n=4) (n = 6)

Body weight (g) 86.1+ 7.3 86.0 + 12.1 905+ 66 772+ 5.8
Number of captures 129=-576.5 8.0+ 6.9 SE 55 72 E54
Mean distance (m) 35,9, 221140 43.7 £ 36.8 774 40.1 2592122388
Maximum distance (m) 93.2 + 54.6 88.2.3 72.0 160.3 + 40.2 51.852:43,9

June than did females not entering oestrus (61.4 # 18.1 g versus 79.3 + 20.2 g); by August
there were no significant differences in body weights for females in these two groups
(mabı)

A two-way ANOVA testing for differences in home range size for the entire nıne-week
study period indicated no significant (p > 0.10) sex or breeding condition effect, but a
significant sex by reproductive condition interaction (Tab. 2). This interaction is due to
males ın breeding condition having larger, and females who attained oestrus having smaller
home ranges over the summer than sexually inactıve individuals (Fig. 1).

These different responses by males and females could reflect behavioral changes
associated with contrasting mating behaviors, or alternatively, they could reflect individual
differences involving non-breeding factors (quality of home range, etc.; see BOWERS and
SmitH 1979). A more rigorous test would examine changes in home range size for

290 M. A. Bowers and T. G. Carr
L__]Males Females

Mean Distance (m)

100

807

40 -

20T

6 4 59

Inactive Active
Sexual Condition

Fig. 1. Mean distance between capture locations (in meters) for breeding and non-breeding males and
females. Standard errors of the mean are shown. The number of anımals over which averages were
calculated are given in each bar

Table 2. Summary of two-way ANOVA testing for sex by breeding condition differences in the
two estimates of home range size

Source of variation

Mean distance (m)
Sex 196.7 196.7
Breeding condition 772.6 772.6
Sex by condition 6118.9 6118.9

Residual 30282.4 1009.4
Total SMLEXIEIS) 1133.0

Maximum distance (m)
Sex 126.2 126.2
Breeding condition 10358.8 10358.8
Sex by condition 18026.1 18026.1

Residual 110938.1 9609700,
Total 139508.7 4227.5

particular individuals over breeding and non-breeding periods. Such a test is possible for
females who come in and out of oestrus over time periods of between three and nıne days
(SMITH and SmrtH 1975), and is not possible for males who remain scrotal or non-scrotal
for most of the summer months. In our study, nine females bred during the first two weeks
of July, while 15 females failed to breed. Comparing home range estimates for individual
females captured at least three times during pre-breeding, breeding, and post-breeding
periods showed that females attaining oestrus had smaller home ranges during breeding
relative to the home ranges of non-breeding females (Fig. 2, a test of difference between
breeding and non-breeding chipmunks over the three periods using a repeated measures
ANOVA; F,, = 17.2, P = 0.023 for mean capture distance; F,, = 8.8, P = 0.055 for
maxımum distance between captures).

eu

Home range shifts accompanyıng breeding in Tamuas striatus 291

Mean Distance (m)

40

Pre-Breeding Breeding Post-Breeding

Period
BE Oestrus Non-oestrus

Fig. 2. Mean distance between capture sites (m) for females attaining oestrus (bars with dark shading)
versus those that did not (light shading), and broken into three time-periods: ı.e., pre-breeding
(before 5 July), breeding (5-14 July), and post-breeding (after 14 July) periods. Females entering
oestrus had significantly smaller home ranges relative to: 1. non-oestrus females during the breeding
period; and 2. home ranges during pre- and post-breeding periods

Discussion

These results add to what is known about polygynous mating systems in solitary scıurids.
Tamias has two mating periods (i.e. February-April, and early-to-mid July), both which
may involve a varıable proportion of the resident females (Pıppuck and FaLıs 1973; SMITH
and SmıtH 1972; ErLiortt 1978). In our study females attainıng oestrus in July were
significantly smaller in June than females not breeding in July. This suggests that summer
reproduction was performed by females born in the spring, and that larger females, as a
group, may have bred in the spring but not the summer. By August there were no
significant sıze differences between summer breeding and non-breeding females suggesting
significant weight gains made by the summer breeders.

Our results also suggest that the reduction in home range size of females accompanyıng
the onset of breeding, while more subtle, may be as indicative of the mating system of
Tamias as home range expansıon by breeding males. It is generally assumed that males
expand their home ranges during breeding periods so as to achieve multiple matings
(Dogson 1984). During such periods breeding males converge towards home ranges of
females in oestrus. This is accomplished through the use of olfactory cues that advertise the
onset of oestrus (DOBRORUKA 1972; KEkEvIn et al. 1981). Successful mating is assured by
female tolerance of males ın core areas that are usually defended rigorously (YAHNER
1978). Limiting movements to certain portions of the home range would further increase
the likelihood that breeding males could locate and copulate with resident females. Under

292 M. A. Bowers and T. G. Carr

this scenario, reductions in size of home ranges may be a feature of the mating repertoire of
female Tamias that leads to an increase in competition among males for mates, creating an
arena where only the most fit males would breed.

This assumes that the dominant males, ın fact, perform the majority of the breedings.
However, for the eastern chipmunk a single female may copulate 10-30 times, and with
many of the males available (Er1oTT 1978). Similar breeding systems have been reported
for the tassel-eared (FARENTINOS 1972) and gray squirrels (HorwıcH 1972). In the former,
a majority of the early matings were performed by the dominant males but in the latter
there dıd not appear to be any relationship between dominance and breeding success. If, as
FARENTINOS (1972) argues, the first copulations are most likely to result in fertilization,
then reduction in breeding home ranges of females-and the concomitant aggregation of
males-would assure that the most fit males do most of the matings irrespective of the total
number of males that copulate.

As an alternative, home range reduction by breeding females may result from the
harassment by males attempting to copulate. Some authors have noted that up to 12 males
may accompany and actıvely pursue females in oestrus both before and after copulation
(YAHNER 1978; ErLioTT 1978). During such mating bouts females may seek refuge from
suitors under ground, or in structurally complex microhabitats. Therefore, it may be that
reductions in the home ranges of oestrus females result from the aggressiveness of males
attempting to mate, and/or ıs a means by which females in oestrus avoıd large male
aggregates.

The exact cause of the reduction in breeding female home ranges would be important to
the breeding system of the species because in one case females make themselves more
available, and in the other, less available to breeding males. Specifically, female adjust-
ments in home range size could either increase the degree to which Tamaas ıs polygynous
or place severe limits on it. That Tamias have highly synchronized oestrus periods could be
viewed as evidence supporting the male-avoidence scenario because each female makes
herself less available to local males than if oestrus was asynchronous (EMLEN and ORING
1977). Further study of the behavior of oestrus females in the presence and absence of
breeding males, and the mating success of dominant and subdominant males is needed to
distinguish between these alternatives.

Acknowledgements

This work was partially funded by a Summer Research Fellowship from the Blandy Experimental
Farm to T.G. Carr. We acknowledge the assistance of R. TALLEY ın the field, and to E.F. ConNoR
who provided comments on an earlier version of this manuscript.

Zusammenfassung

Verschiebungen des Aktionsraumes beim Östlichen Streifenhörnchen Tamias striatus
(Rodentia: Scinridae) während der Fortpflanzung

Die Aktionsräume von 34 reproduktiven und nichtreproduktiven Männchen und Weibchen von
Tamias striatus wurden über einen Zeitraum von 9 Wochen anhand markierter Wiederfänge bestimmt.
Reproduktive Männchen waren größer und hatten größere Aktionsräume als Männchen, die nıcht an
der Fortpflanzung teilnahmen. Zu Beginn, aber nicht am Ende des Untersuchungszeitraumes waren
östrale Weibchen ebenfalls größer als anöstrale. Die Aktionsräume östraler Weibchen waren kleiner
als die anöstraler Weibchen, und während des OÖstrus waren die Aktionsräume kleiner als davor und
danach. Die Resultate lassen vermuten, daß Verschiebungen in der Aktionsraumgröße beı beiden
Geschlechtern von Tamias zur Fortpflanzungsbiologie gehören.

Home range shifts accompanying breeding in Tamias striatus 298

References

BLAIR, W. F. (1942): Size of home range and notes on the life history of the woodland deer mouse and
eastern chipmunk in northern Michigan. J. Mammalogy 23, 27-36.

Bowers, M. A.; Smit#, H. D. (1979): Differential habıtat utilization by sexes of the deermouse,
Peromyscus maniculatus. Ecology 60, 869-875.

Bowers, M. A.; WELCH, D. N.; CARR, T. G. (1990): Home range size adjustments in response to
natural and manipulated water availability in the Eastern Chipmunk, Tamias striatus. Can. J. Zool.
68, 2016-2020.

DoBRORUKkA, L. J., (1972): Scent marking and courtship in Siberian chipmunks, Tamias sibiricus
lineatus (Siebold, 1824), with notes on the taxonomic relations of chipmunks (Mammalıia). Vestn.
€s. spol. zool. 36, 12-16.

Dosson, F. $. (1984): Environmental influences on sciurid mating systems. In: The Biology of
Ground-Dwelling Squirrels. Ed. by J. ©. MurıE and G. R. MIiCHENER. Lincoln: University of
Nebraska Press. Pp. 227-249.

Dunrorp, C. (1970): Behavioral aspects of spatial organızation in the chipmunk, Tamias striatus.
Behavior 36, 215-231.

ELLIOTT, L. (1978): Social behavior and foraging ecology of the eastern chipmunk (Tamias striatus) ın
the Adirondack Mountains. Smithsonian Cont. Zool. 265, 1-107.

Emren, $. T.; Orınc, L. W. (1977): Ecology, sexual selection, and the evolution of mating systems.
Science 197, 215-223.

FARENTINOS, R. C. (1972): Social dominance and mating activity in the Tassel-Eared Squirrel (Sciurus
aberti ferreus). Anımal Behav. 20, 316-326.

FoRsYTH, D. J.; SMITH, D. A. (1973): Temporal varıability in home ranges of Eastern Chipmunks
(Tamias striatus). Amer. Midl. Natur. 90, 107-117.

GETTY, T. (1981a): Structure and dynamics of chipmunk home rangs. J. Mammalogy 62, 726-737.

— (1981b): Territorial behavior of eastern chipmunks (Tamias striatus): encounter avoidence and
spatial time sharing. Ecology 62, 915-921.

HorwiıcH, R.H. (1972): The ontogeny of social behavior in the Gray Squirrel (Sciuris carolinensis). Z.
Tierpsychol. Supp. 8, 1-103.

Ickes, R. A. (1974): Agonistic behavior and use of space in the eastern chipmunk, Tamias striatus.
Unpubl. Ph. D. Thesis, Univ. Pittsburgh.

Kevin, T. M.; Harpın, Z. T.; McCurpy, N. (1981): Individual and sex-specific odors ın male and
female eastern chipmunks (Tamias striatus). Biol. Behav. 6, 329-338.

KRAMER, D. L.; NowEır, W. (1980): Central place foraging in the Eastern Chipmunk. Anım. Behav.
28, 772-778.

MAREs, M. A.; Watson, M. D.; LACHER, T. E. JR. (1976): Home range perturbations in Tamias
striatus: Food supply as a determinant of home range and density. Oecologia 25, 1-12.

Pınpuck, E. R.; Farıs, J. B. (1973): Reproduction and emergence of juveniles in Tamaas striatus
(Rodentia: Sciuridae) at two localıties ın Ontario, Canada. J. Mammalogy 54, 693-707.

SMITH, D. A.; SMITH, L. C. (1975): Oestrus, copulation, and related aspects of reproduction ın female
eastern chipmunks, Tamaas striatus (Rodentia: Sciuridae). Can. J. Zool. 53, 756-767.

Tryvon, C. A.; SYNnDER, D. P. (1973): Biology of the Eastern Chipmunk, Tamias striatus: life tables,
age distribution, and trends in population numbers. J. Mammalogy 54, 145-186.

WISHNER, L. (1982): Eastern Chipmunks: Secrets of their solitary lives. Washington, D.D.: Smithso-
nıan Inst. Press.

WOLFE, J. L. (1966): Agonistic behavior and dominance relationships of the eastern chipmunk,
Tamias striatus. Amer. Midl. Natur. 76, 190-200.

YAHNER, R. A. (1978): Burrow system and home range use by Eastern Chipmunks: ecological and
behavioral considerations. J. Mammalogy 59, 324-329.

YERGER, R. W. (1953): Home range, territoriality, and populations of the chipmunk in central New
York. J. Mammalogy 34, 448-458.

Authors’ addresses: Prof. MicHAEL A. BowERs, Department of Environmental Sciences and Blandy
Experimental Farm, Clark Hall, University of Virginia, Charlottesville, VA
22903, USA; TIMOTHy G. CARR, Department of Biological Sciences, Northern
Arızona University, Flagstaff, AZ 86011, USA

Z. Säugetierkunde 57 (1992) 294-309
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Aspects of the social behaviour in a captive colony of the
Common mole-rat Cryptomys hottentotus from South Africa

By N. C. BENNETT

Department of Zoology, University of Cape Town, Rondebosch, South Africa

Receipt of Ms. 30. 08. 1991
Acceptance of Ms. 14. 02. 1992

Abstract

Qualitative and quantitative behavioural studies on a captıve colony of the social mole-rat Cryptomys
hottentotus are reported. The colony consisted of two castes: reproductives and non-reproductives.
The non-reproductives were divisible into “casual workers” and “workers”. The amount of work
performed was not related to body mass.

Behavioural acts were subdivided into three major categories: Burrow maintenance, interactive
and auto behavioural acts. Social interactions were analysed by age and work category. Many of the
behaviours appear to be linked to age and not work grouping. Worker groups did not differ
significantly in the amount of digging and soil movement undertaken. Juveniles carried food more
frequently than adults.

There was a positive correlation between anımals initiating and receiving the following inter-
actions: genital allogrooming, sparring, naso-anal interaction and urino-genital sniffing. Juveniles
allogroomed the pelage and genitalia of other colony members more frequently than adults. Juveniles
sparred and initiated naso-anal interactions significantly more than adults.

There is a distinct toılet area in which the reproductive anımals smear-mark significantly more than
the other colony members. Smearing of organically derived chemicals may be the mechanısm by
which chemo-suppression of reproduction is imposed upon other colony members by the reproduc-
tives.

Introduction

Cryptomys hottentotus occurs in mesic and semi-arıd regions of South Africa (SMITHERS
1983). The colonies are famılial groups comprised of parents and at least two litters and can
vary ın size from 4 to 18 individuals (BENNETT 1988, 1989; ROSENTHAL et al. 1992). Non-
breeding colony members show co-operative and altruistic behaviour in the foragıng,
storage and subsequent harvesting of geophytes.

Cryptomys hottentotus has a colony structure which lacks working groups based on the
relationship between body mass and the amount of work performed.

Studies on the behaviour of the southern African mole-rats were pioneered by ELOFF
(1951, 1952) who described the basic general behaviour of Cryptomys hottentotus. In
particular, reference was made to the orientation of the mole-rats within the burrow
system and the utilisation of the kinaesthetic senses of these mole-rats in orientation wıthin
the burrow system. Generalised behaviours involving digging, feeding and threat postures
have been described for C. hottentotus and C. damarensis (DE GRAAFF 1964, 1972;
GENELLY 1965). The general behaviour for incomplete colonies of C. hottentotus from the
Transvaal have been described by KınrocH (1982), but quantitative analysıs of the
behaviour were not given.

This paper describes, both qualitatively and quantitatively, the behaviours exhibited by
a captive colony of field-captured C. hottentotus. The various types of social interaction
resulting from each behaviour are analysed where possible with respect to the anımals’ age
and work grouping. Where particular actions were uncommon, qualitative behaviour only
is reported.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5705-0294 $ 02.50/0

Aspects of social behaviour in Cryptomys hottentotus 295

Material and methods

A colony of 11 mole-rats was captured in May, 1984 at Darling (33°22’S, 15°25’E) S. W. Cape,
South Africa. From the colony of 11, three non-reproductive males were accıidently killed on capture
leaving only eight mole-rats. |

The mole-rats were captured with Hickman live traps (Hıckman 1979), or by cutting off their
retreat with a hoe when they come to seal opened sections of their burrow system (Jarvıs and SALE
1971). They were captured over four consecutive days.

The colony was housed in a transparent Perspex burrow system consisting of three I-m covered
runs (65 mm x 60 mm) linking three transparent chambers which served as nests, toilet areas and food
stores. Wood shavings were placed in the chambers, paper towelling and dry grass were provided as
nesting material. The mole-rats were fed on a variety of root and green vegetables, apples, grapes and a
commercially prepared nutritionally balanced breakfast cereal. The mole-rats drank no free water.
The room ranged between 26-28°C in summer and 18-21°C in winter. These temperatures were
comparable to field temperatures recorded in the superficial foraging burrows (BENNETT et al. 1988).
The nest chamber was warmed with a lamp to approximately 25°C, a temperature similar to that
recorded in the field, in a burrow leading to the nest in a C. damarensis burrow system.

The room was illuminated from a window and consequently received a natural photoperiod.
Bathyergids have reduced eyes (CEı 1946; ELOFF 1958; REEs 1968) and visual centres in the brain
(Hırı et al. 1957; PıLrerı 1960). Cryptomys hottentotus have very small eyes which they keep closed
except when alarmed. Erorr (1958) claımed Bathyergus and Cryptomys could not see, but could
detect air currents on the cornea. In the C. hottentotus colony under observation, no obvious
behavioural response was detected to bright flashes of light or to movement by an observer as long as
it was not accompanied by sound or by an air current.

The behaviours of the 8 C. hottentotus (2 males and 6 females) trapped at Darling in April 1984
were observed for a total of 240 hours between 15th May and 2nd August, 1984. Colony behaviour
was observed daily by means of continuous scans for durations of 2 to 6 hours. The roles of the indivi-
duals within the colony were determined over the period 15th May to 2nd August.

All statistics were carried out with the aid of SIEGEL (1956) and Zar (1984).

The results obtained for many of the behavioural acts were tested statistically to determine if there
were significant differences for the age and role of the mole-rats in the colony Darling 1. Sexual
differences are not recorded here because there were only two males.

Results
Burrow maintenance behaviours

Four behaviours fall under this heading a) digging and gnawıng, b) sweeping and transport
of wood shavings ın the burrow excluding near the toilet, c) nestbuilding and the carrying
of nesting material and d) food carrying. These behaviours are readily quantifiable and are
believed to approximate behaviours that occur in the wild (BENNETT 1988). In the wild,
nest building and the carrying of nesting material involve transporting stripped husks and
root epidermis from harvested bulbs, tubers and rootstocks etc. to the nest chamber. These
were the only materials found in the nests of wıld colonies. In captivity wood-wool was
provided for this purpose. In the wild, bulbs, corms and other small food items are carried
to the food store and in captivity small ıtems of food were also transported to one clearly
identifiable section of the system. The food items were carrıed between the incisors, the
head being held high and the mole-rat moved backwards or forwards with its load.

Based on the type and amount of work performed by individuals and on their
reproductive role, the mole-rates ın the colony of eight anımals were placed into three
categories. A reproductive caste and a non-reproductive caste composed of two work-
related groups, “workers” and “casual workers” (see Table) (BENNETT 1989).

The three workers (w) were the younger, smaller sızed mole-rats. They were involved
in 12.3 to 22.3 % of the total work done by the colony.

The three casual workers (cw) were usually the larger mole-rats, although a juvenile was
ranked within this group. They were involved in 5.5 to 6.8 % of the total work undertaken
by the colony.

The two reproductive mole-rats (RF, RM) could not be distinguished from workers or

296 N. C. Bennett

Analysis of the amount of work performed by members of the Darling 1 colony
Data were collected over four months May to August, 1984. (After BENNETT 1989)

Animal I.D. Weight Weight Frequency of
capture August digging and
April soil transport

No.
No.
No.
No.
No.
No.
No.
No.

EEJEETIETIE STE rer

W = worker; C.W. = casual worker; R.F. = reproductive female; R.M. = reproductive male;
F = female; M = male.

casual workers on the basıs of the amount of work undertaken (U = 3, p = 1.20 and p =
1.20, Mann Whitney U-test p = 0.05 level of rejection) but clearly differed from the others
in being the only reproductive anımals ın the colony. The male did little work (3.4 %), but
the reproductive female undertook 30.4 %, especially that associated with nestbuilding and
sweeping.

There was a significant tendency for workers to maintain the burrows and work more
frequently than casual workers (U = 0, p = 0.05 Mann Whitney U-test, 1 tailed test).

Using the Kruskal-Walliıs test ıt was found that the three groups did not differ
significantly in the amount of digging and soil movement undertaken (p = > 0.05).

There was a significant difference in the frequency of food carrying by the mole-rats
(X’7 = 22.45, N = 89; p = <0.01). This was linked to the age of the mole-rat; juveniles
carried food significantly more frequently than adults (U = 1.5, p = 0.028, Mann Whitney
U-test).

Interactive behaviours
Naso-anal interaction

Naso-anal interactions involve contact between the nasal region and anal region of two
animals, lying side by side, head to tail. The behaviour does not lead to sexual activity and
is undertaken by all colony members. The animals appear very excited during the actıvity
and vocalısation may occur.

There was a positive correlation (rs = +0.55) between the number of naso-anal
interactions initiated by particular animals and those in turn received (Fig. 1). Juveniles
initiated significantly more naso-anal interactions than did adults (Mann Whitney U = 0;
p = 0.028). Reproductives were rarely involved in naso-anal interactions.

Urino-genital sniffing

One mole-rat sniffs the anal region of another individual which raises its taıl and
simultaneously emits a series of high pitched squeals whilst jumping with its hind legs with
each squeal.

There was a positive correlation (rs = +0.55) between the number of urino-genital
sniffing sequences undertaken by particular individuals and the frequency with which they
inturn received these ınteractions (Fig. 1).

Aspects of social behaviour ın Cryptomys hottentotus DIN,

NASO-ANAL URINO-GENITAL SNIFFING
15 30
)
25
5 o
S 0)

c 10 o 20
wu
2
m 15 ®
® o o A
[a

[e)}
a
o°

5
h 2 rs = +0,55 * fg =+0,55
GB nern ie Bee ae
10) 5 10 15 20 0 5 ı0 ı5 20 25 30
rn SPARRING GENITAL-ALLOGROOMING
50
®
®
"r 40
il
>
= 30 o
6)
u
c 20 ®
©
©
10 .
A ls = +0.76
— EL ae
0 10 20 30 40 50 60 10) 5 10 15 20
INITIATOR INITIATOR

Fıg. 1. The Spearman Rank correlations between the frequency of ınitiating and receiving naso-anal,
urıino-genital sniffing, sparring and genital-allogrooming behavioural interactions

There was no correlation with the age of the mole-rat (Mann Whitney U = 5; p =
0.486).

Sparring

Sparring consists of 3 types of interactions: Adult-adult, adult-sibling, sıbling-sibling
interactions. In sparring, two animals gently lock their incisors and then have a tug-of-war.
During the tugs-of-war the individuals brace themselves in the burrow with their forefeet
and try to pull one another. This may be interspersed with nose-butting and pushing at
each others faces with their forefeet. The skin ıs never bitten and interactions are
terminated either by one anımal rolling over onto ıts back and exposing its belly and
genitalia or by one anımal reversing at high speed along the tunnel system. Adult-sibling
and sibling-sibling interactions are common. Whereas adult-adult interactions are infre-
quent.

A significant positive correlation (rs = +0.76) was found between the number of
sparring episodes initiated by particular animals and the frequency with which these
animals inturn received sparring interactions (Fig. 1). Juveniles sparred significantly more

frequently than dıd adults (Mann Whitney U = 0; p = 0.028).

298 N. ©. Bennett

Juvenile-juvenile sparring constituted 64 %, adult-adult 7% and adult-juvenile 29% of
all observed sparring interactions (n = 183). These data suggest that sparring is important in
pup development and the subsequent incorporation of pups into the colony.

Tail-pulling

When two anımals are moving in the same direction within the burrow, and the anterior
male-rat then stops to feed or rest, the posterior male-rat may pull the obstructing
individual back along the burrow by ıts taıl. The towed anımal usually turns on its back
and attempts to brace itself against the sides of the burrow. Once released the mole-rat will
often return to the place from which it was initially towed from and tail-pulling may be
initiated again.

Passıng over

Mole-rats usually passed each other by flattening their bodies and pulling against the mole-
rat that they were passing. The mole-rat on top was usually the faster moving individual
(unquantified). Before passıng, mole-rats would often chirp, especially when passing
anımals dominant to themselves. Small mole-rats passed side-by-side in the tunnel system.

Passing under

This occurred when one mole-rat passed another by moving underneath it.

Passing side-by-side

This behaviour occurred in the tunnels and ıs self explanatory.

Bıtıng
Biting occurred when one mole-rat encountered another in the nest, when one anımal

blocked the path of another, or during a tussle over food. It involved the biting of the taıl,
leg or rump. The bites varıed in intensity from nibbling to a severe bite.

Rump chewing

This behavioural act involves one mole-rat mouthing the fur on a conspecific’s rump and
then taking the rear between the incisors. The incisors were moved ın a gentle chewing
action.

Mouthing
When mouthing, one anımal would take another’s head between its incisors, sometimes

moving the mouth in a chewing motion. The aggressor would then often drag the victim
along by its head.

Pushing

This behaviour involved a mole-rat pushing its hindlegs against a conspecific whilst bracing
itself with the fore legs and raising the head. In this position the mole-rat would move
backwards while pushing the other down the tunnel.

Allogrooming

Allogrooming consists of nibbling and ano-genital licking. In “nibbling”, the groomer
bites gently at the groomee’s head, neck, shoulders, flanks or back. In “ano-genital

Aspects of social behaviour in Cryptomys hottentotus 299

licking” one anımal licks the ano-genital region of another, this may also involve some
nibbling of the fur in the ano-genital area. Allogrooming occurs in the nest and usually
occurs when a mole-rat has just entered the nest. Grooming is inıtiated when the groomee
is lying ın a relaxed position. The groomer moves to the head and thoracic region of the
groomee and nibbles at its fur, occasionally another region of the body will be groomed.
The groomee responds by moving the part of ıts body being nibbled towards the groomer
it rarely responds by immediately reciprocating the groom. The groomee may however
reciprocate-groom the groomer after a short time lapse.

In ano-genital grooming, the groomer usually approaches the groomee from the rear
and pushes its nose between the hind legs of the groomee. During ano-genital grooming
the groomee gives out a high pitched sıbilant twitter and may on occasion thrust its hind
legs into the face of the groomer. The fur around the ano-genital area may also be nibbled,
but licking occurs 90 % of the time. Ano-genital licking is a short-lıved behaviour lasting
only a few seconds. Allogrooming around the groomee’s mouth and nasal area also occurs
frequently.

The two reproductive anımals and a casual worker (Nos. 1040, 1007, 1008) auto-
groomed significantly more frequently than they allogroomed (p < 0.05, N = 299; S.E. =
0.026, binomial test rejecting at p = <0.05 level). Two workers and a casual worker (Nos.
1001, 1002, 1003) allogroomed more frequently than they autogroomed, whereas one
worker and one casual worker (Nos. 1004, 1070) autogroomed and allogroomed with
equal frequency. Juveniles allogroom significantly more frequently than adults (Mann
Whitney U = 0; p = 0.028).

There was no significant difference in autogrooming between adults and juveniles
(Mann Whitney U = 6.5; p = 0.486).

With genital allogrooming, however, there was a strong direct correlation (rs = +0.82)
between those mole-rats ınitiating and those ın turn receiving grooming to the genitalia
(Fig. 1).

There was a significant trend for juveniles to genital allogroom more frequently than
adults (p = 0.0170, N = 64; S.E. = 0.058; Binomial test p = <0.05 level of rejection).

Allocoprophagy

Allocoprophagy is rarely undertaken except by young or juvenile mole-rats. These anımals
beg faeces from an adult engaged in autocoprophagy. The begging individual approaches
the rear or side of the donor, while giving a high pitched mewing noise resembling Sue-
Sue-Sue. The mole-rat then pushes its nose between the hind legs of the donor, probes the
anus of the donor with its teeth and pulls out faecal material. While this ıs taking place, the
donor produces a high-pitched sibilant cry, similar to that produced by an individual who
is being allogroomed ın the ano-genital area. Adult mole-rats have been seen eating faeces
previously voided by another colony member in the toilet area.

Autobehaviours
Autogroomiıng

There are three methods of cleaning the coat, namely, scratching with the hind leg, licking
and nıbbling with the incisors.

Scratching i iS usually applied to the head, neck, shoulders and flank region, the hind leg
moving in a rapid series of arcs and combing the fur on the downbeat. When the head or
neck is being groomed the head ıs tilted to the side of the body with the hind foot being
used to scratch. The forefeet brace the mole-rat as it grooms itself.

Licking is used to clean the paws, lower belly and ano-genital area. The anımal either

300 N. C. Bennett

first licks and moistens its paws which are then combed through the fur, or it directly licks
its fur using small sweeping movements. In the case of ano-genital licking, slight lapping
movements are utilised. When cleanıng the belly, the ano-genital region or the toes of the
hind feet, the animal rolls backwards and supports its body on the sacral region, its hind
legs are splayed out and its forelegs may be used to balance the body. Incisors are groomed
by the mole-rat inıtially licking its paws and subsequently grooming its incisors and nose
with the paws. The digits of the hind feet are nıbbled and groomed with the incisors.

Tooth-sharpening

The incisors of the bathyergids grow continuously and in the natural environment are
worn down as they chisel-tooth-dig through the soil. In captive animals the incisors are
worn down and sharpened by tooth-sharpening. Tooth-sharpening usually occurs (96 %
of the time) in the nest area. The mole-rat initially braces itself with its forepaws while
adopting the normal tooth-sharpening posture. Forward and backward and side to side
actions of the lower jaw are then used to file the upper and lower incisors against one
another. Squeaky hling noises are produced during these movements. Short forward
thrusts of the lower ıincisors against the upper ones sharpen the lower incisors, whereas
longer slower backward movements of the lower incisors across the upper incisors sharpen
the upper. Loose flakes and dust of chipped incisor are periodically flicked out ot the
mouth by the tongue.

There was a highly significant difference ın the frequency of tooth-sharpening episodes
between colony members (x? = 24.56, N = 367; p = <0.001 Chi-square, one tailed test).

However, this was not related to age (Mann Whitney U = 7; p = 0.886). The score of
each individual weighted the statistic, thus anımal No. 1004 tooth-sharpened 44 % more
frequently than the mean frequency obtained for tooth-sharpening, whereas anımal No.
1070 tooth-sharpened 40 % less than average.

Coprophagy

Autocoprophagy commonly follows ano-genital grooming. The anımal rolls backwards
and supports its weight on its sacral region. Its hind legs are splayed laterally and the
anımal doubles up. The forelegs of the anımal are used to balance and brace the anımal. The
incisors are used to probe and pull faecal material from a slightly everted anus. The faeces
are then eaten. The duration of coprophagy may last a few seconds to many minutes.

Some animals practiced autocoprophagy more often than other individuals (x?, = 35.59,
N = 195; p = <0.001 one tailed test), but this was not related to the age of the mole-rat or
its role (Mann Whitney U = 2; p = 0.114). However, the reproductive male engaged in the
least amount of autocoprophagy. In this study anımals No. 1004 and No. 1040 weight the
y? statistic.

Alarm and threat posture

There are essentially two alarm and threat behaviours used in response to disturbances
from outside the colony: head-back threat posture and pumping.

In the head-back threat posture, the anımal stands with its head thrown back, its eyes
open and its mouth fully agape. The forefeet are placed firmly ın front of the mole-rat and
the hind limbs are widely splayed laterally but braced for a rapid advance or retreat.
Periodically the mole-rat snorts and chatters its teeth. The posture is firm and rigid with
the anımal making short jerks or jumps towards the agonistic source.

Aspects of social behaviour in Cryptomys hottentotus 301

Pumping

In pumping, the mole-rat cautiously approaches the source of alarm to threat repeatedly
sniffing the air and holding its taıl out straight. While still 10-20 cm or more from the
source of alarm, the anımal stands with its fore and hind legs splayed laterally, its head is
stretched out forward and its body flattened dorso-ventrally. The mole-rat then pumps its
hind region (legs and sacral area) up and down. This action is quite forcible, especially on
the downstroke. In a very high-level threat situation the whole body posterior to the
shoulders is lifted off the ground with the upstroke.

A pumping sequence may consists of between six and twenty downstrokes, each
sequence is followed by a refractory period, in which the mole-rat first remains very still
and then advances a few centimeters closer to the source of aggravation. The pumping
display is then repeated. The mole-rat is extremely cautious and may rapidly retreat
backwards along the burrow.

General movement in the burrow

Cryptomys hottentotus move backwards and forwards in the burrow system with equal
ease. They walk and run along the burrow with their hind legs held far apart with most of
the sole of the foot held off the ground. The limbs are short giving them a low body
carrıage. The head is usually held straight out, but is occasionally slightly lowered. The
eyes are kept closed except when investigating a new disturbed or damaged area in the
burrow system. The mole-rat then opens its eyes, holds its head held high, sniffs the air
and cautiously approaches the area. During this cautious approach the fore and hind feet
are braced against the perimeter of the burrow to facılıtate rapid retreat.

Ihe mole-rat turns within the burrow system by curving its body and rotating
sideways, using its forefeet to do much of the pushing, however, a final thrust is provided
by the hind feet.

The mole-rats are generally very agıle, the actual speeds with which the animals move in
the natural underground system have not been recorded, but mole-rats kept in the
laboratory are capable of moving both forwards and backwards, at speeds of up to 15 cm/
second.

Cryptomys hottentotus are exceptionally aggressive anımals and will bite on capture,
this being most noticeable in freshly captured specimens. They are extremely sensitive to
air currents which ELoFF (1958) suggests are detected by the cornea of their eyes. A series
of short sharp rapıd jumping movements with the mouth agape accompanıed by grunting
sounds are evoked ıf one blows air into the face of an individual (DE GRAAFF 1964;
BENNETT, pers. obs.).

Toılet behaviour

There is a well defined toilet area within the burrow system, usually a blind ending tube
that is utilised by all the colony. There are essentially three types ot toilet behaviour:
Grooming and smearing, urination and defaecation.

Grooming and smearing

In grooming and smearing, the mole-rats may enter the toilet area and not urinate or
defecate. This is common in C. hottentotus. On entering the toilet area the mole-rat spends
time smelling the area and then vigorously grooms its head region, flanks and belly,
sometimes the genitalia are also groomed. Before leaving the toilet, the anımal kicks back
with its hind legs for a few times, and leaves the toilet while dragging its ano-genital region
along the burrow. A small amount of fluid (urine?) is left ın a traıl along the tunnel. This

302 N. C. Bennett

wet trail is smelt by other colony members as they pass along the marked section of the
burrow.

Some animals groomed and smeared within the toilet area significantly more often than
other colony members (x = 17.41, N = 138; p = <0.01). This was not linked to the age of
the mole-rats (Mann Whitney U = 4; p = 0.342). There appears to be a tendency for the
reproductive pair to groom and smear more frequently than the rest of the colony (Mann
Whitney U = 0, p = 0.072), although not significant at p = < 0.05 level (Fig. 2).

30

25

N _ D
oO o oO

Frequency of grooming and smearing
[0 7}

0
1001 1002 1004 1007 1040 1070 1008 1003 Animall.D.
F F M F M F F F Sex
\W W W RF RM CW CW _CW Group

Fig. 2. The relative frequencies of grooming/smearing sequences in the toilet area of a Cryptomys
hottentotus colony. RM = Reproductive Male; FR = Reproductive Female; CW = Casual Worker;
W = Worker; F = Female; M = Male

Urination

Urination usually occurs after an anımal has roused from rest or after feeding. The anımal
moves its hind legs apart, lowers its rear and raises its taıl. Short jets of urine are voided. At
the end of urination the animal briefly drags ıts rear along the burrow. A conspecific
passıng over the drag-marked region snifts the marked zone and then moves on. Urination
is not restricted to a particular site in the system (vs defaecation) and the site appear to be
randomly selected.

There was no significant difference between colony members in the frequency of
urination (X, = 7.48, N = 170; p <0.3 > 0.2).

Defaecation

Defaecation occurs after awakening from sleep or after feeding. The mole-rat approaches
the toilet area head first and smells it briefly, before reversing out of the toılet area and
turning around. The anımal then backs into the toilet tube. During defaecation, the mole-
rat stands with its hind feet well apart and its tail raised. Its body is held rigid until the
pellets are voided. The faeces then are kicked with the hind legs towards the blind end of
the toilet area. After defaecating, the mole-rat grooms itself thoroughly starting with its
head and finishing at the ano-genital area. In C. hottentotus defaecation follows or precedes
urinatıon but the two occur ın different parts of the burrow system.

Aspects of social behaviour in Cryptomys hottentotus 303

Feeding

When feeding the mole-rat squats on its hind feet and holds the food with its forefeet.
When feeding on bulbs such as Oxalıs sp., Homeria sp. and Romulea sp. the mole-rat grips
the bulb between its forepaws and dehusks it, slowly rotating the bulb as ıt bites off the
scaley outer layer. Once the bulb has been dehusked, the mole-rat cuts off and eats small
portions of it. Food shaking and brushing precede eating and occur at irregular intervals
during feeding. The bulb ıs occasionally shaken with the fore paws or held in the incisors
and brushed with the forefeet. This action dislodges any attached soil.

Discussion

These first in-depth behavioural studies on a captive colony of C. hottentotus have
provided an opportunity to describe basic colony behaviour in this socıal bathyergid. This
study on C. hottentotus provides a comparison with the other social bathyergids which
may help elucidate which features in the behavioural repertoire of the social bathyergids
evolved first.

Maintenance behaviours
Digging and burrowing

Digging behaviour of all the genera of the bathyergids is very sımilar, although there are
differences ın the actual mode of excavation. Digging in all genera is inıtiated by alternate
movements of the forepaws. However when extending the burrow through well packed
substrata, the mole-rats of four genera excavate the soil with both the upper and lower
incisors, whereas the genus Bathyergus utilises its claws and only occasionally its teeth for
digging (GENELLY 1965; Jarvıs 1969; JARvIs, pers. comm.; BENNETT, pers. ob) AINEE:
hottentotus, the two major maintenance behaviours (diese and soil movement) are not
restricted to particular groups. In contrast, these behaviours are performed mainly by the
frequent worker caste ın C. damarensis (BENNETT 1988) and by small-sızed workers ın A.
glaber (Jarvıs 1981; LAcEy and SHERMAN 1991). Thus, in these behaviours there appears to
be a difference between C. hottentotus and the two more highly socıal bathyergids.

Carrying food

In the burrow system much of the food encountered by the mole-rats while digging is
carried to the food chamber. The mode of transportation varies with the sıze and nature of
the food. The social species store food in a common food store the anımals actively
involved in foraging will probably also collect, transport and store the food. In C.
hottentotus, juveniles (workers) carry food sıgnificantly more frequently than adults. In
the colony of C. damarensis the frequent workers (which are often the juveniles) carry
significantly more frequently than infrequent workers (BENNETT 1990), while ın
Heterocephalus glaber there ıs a significant negative correlation between body mass and
carrying food (Jarvıs 1991; LACEy and SHERMAN 1991).

Interactive behaviours
Naso-anal interaction

Naso-anal associations, or mutual smelling of the partner’s anal region, has not been
recorded in ©. damarensis and together with urino-genital snitfing ıllustrates that Cryp-
tomys damarensis and C. hottentotus are behaviourally distinct.

304 N. C. Bennett

In C. hottentotus there was a highly significant tendency for juveniles to initiate naso-
anal interactions. The reproductive pair were involved in only 4% of the interactions,
whilst the juveniles were involved in 80% of the interactions. Juvenile-juvenile interac-
tions constituted 59.5 % of the observed naso-anal associations.

By contrast in A. glaber, the majority of naso-anal interactions occur between the
reproductive anımals. High ranking non-reproductive colony members are less frequently
involved and juveniles rarely or never (Jarvıs 1981, 1991; Lacey et al. 1991). In A. glaber,
the behaviour ıs primarıly important in the pair-bonding between the reproductives and
they rest ın thıs posıtion ın the nest (Jarvıs 1991). In C. hottentotus the function of the
behaviour ıs not apparent, but ıt may be important in maintaining colony cohesion.

Urino-genital snıffing

Urino-genital sniffing was observed in C. hottentotus, and occurred away from the nest.
Although the behaviour was unrelated to gender or age, the reproductive pair tended to
receive few of these behaviours in comparison to the more subordinate individuals. The
function of urino-genital sniffing is unknown. It may possibly serve to identify individuals
as belonging to the colony or to determine which of the two interacting anımals is
dominant.

Sparring

In all species of the Bathyergidae sparring appears to play an important but yet undefined
role in the development of the pups. In both solitary and social genera it begins early in the
life of the pup. In Cryptomys, sparring begins about 10 days after birth (BENNETT and
Jarvıs 1988a; BENNETT 1990), while 7. glaber pups begin to spar when 14-20 days old
(JARVIS pers. comm.). The solitary Bathyergus suillus and Bathyergus janetta begin to spar
13 and 16 days after birth (Jarvıs, pers. comm.), while Georychus capensis begins later (35
days) (BENNETT and Jarvıs 1988b).

In all the solitary genera, sparring is between litter mates and the intensity increases
until injury is inflicted or the pups disperse. It ıs also possible that ın the young mole-rats
the increased frequency of sparring is a consequence of play, but as the solitary pups
develop sparring becomes more intense with escalation into fıghting, this does not take
place ın the social mole-rats. In the socıal bathyergids, sparring ıs inıtially almost entirely
between litter mates, though, the older juveniles also spar wıth adults. The adults appear
tolerant to the young mole-rats and allow the juveniles to spar wıth them very vigorously.
The reproductive anımals in the genus Cryptomys spar throughout their lives. Thus the
reproductive male and female C. hottentotus spar predominantly among themselves and
rarely with the other adults. The reproductive male C. damarensis rarely sparred. The
reproductive female was involved in many interactions but these were mostly wıth young
animals (BENNETT 1990). Injuries were not inflicted during any of the encounters observed.
The frequent worker caste in C. damarensis contains many of the “younger” anımals
within the colony which could explain the tendency for frequent workers to spar more
readily than infrequent workers. Sparring interactions in H. glaber (called tooth fencing
and incisor tussels) continue until the anımals are about 2 years old then become
infrequent.

The significance of sparring in the socıal bathyergids ıs at present open to conjecture.
Two possible roles are, firstly, a training for defence of the colony and secondly
establishing a position within the colony hierarchy.

In both C. hottentotus (thıs study) and C. damarensis (BENNETT 1990) there is a strong
positive correlation between the frequency with which an animal initiates sparring and
allogrooming (rs = +0.7 and rs = +0.5 respectively). This perhaps suggests that both
behaviours play a role ın establishing a young animal within the colony hierarchy. In

Aspects of social behaviour in Cryptomys hottentotus 305

sparring the juveniles interact most with the reproductive pair and with other juveniles,
while in allogrooming the juveniles interact with the reproductive male.

Within the Geomyidae, Spalacıdae and Ctenomyidae, sparring interactions are not
reported to occur amongst either the young or adults, but adult spalacids placed together
do fight (AnDErseEn 1978; PEARson 1959; NEvo 1961, 1969).

Tail-Pulling

Tail-pulling occurs in the social mole-rats Feterocephalus and Cryptomys. The behaviour
occurs during cooperative burrowing (JARVvIS 1969; BENNETT 1988). The act ot tail-pulling
in the genus Cryptomys appears to be associated with the dominance of particular
individuals, the dominant mole-rats pulling the tails of the subordinate mole-rats. In
C. hottentotus, of the eight occasions on which taıl pulling was observed, seven involved
the dominant anımals pulling the taıls of subordinates. In the Damaraland mole-rat,
“frequent workers” used tail-pulling significantly more frequently than infrequent workers
(BENNETT 1990). Tail-pulling in C. damarensıs ıs employed mainly during chain digging
sequences. In such a sequence three mole-rats may be burrowing in a particular sector of
the burrow. However, after a period of time one of the posteriorly directed mole-rats may
pull the tail of an anteriorly positioned anımal in an attempt to exchange digging positions.
Tail-pulling may also be used to remove an individual resting or blocking a particular
entrance or sector of the burrow.

Allogroomıng

In C. hottentotus, juveniles bodily allogroom significantly more frequently than adults.
The juveniles groomed other juveniles and the reproductive male ın preference to other
colony members.

In a colony of C. damarensis containing two litters of known age anımals (BENNETT
1990) allogrooming by the reproductive male was directed towards the reproductive
female. The reproductive temale most frequently allogroomed the reproductive male and
her most recent litter (hereafter called juveniles). All age groups also groomed the
juveniles, while the juveniles themselves groomed the reproductive pair, the most domi-
nant non-reproductive male and a female yearling. The reproductive male was groomed by
all of these age and sex categories of young colony members while the reproductive female
was only groomed by her most recent pups and the reproductive male.

Ano-genital allogrooming ın C. hottentotus dıttered from more generalised allogroom-
ing in that ıt almost always involved juvenile anımals. All the other colony members
(excluding the reproductive male) ano-genital groomed the juveniles.

The juveniles directed much of their ano-genital allogrooming towards the adult female
colony members (in particular the reproductive female) as well as between the juveniles
themselves. Ano-genital allogrooming between adult anımals was uncommon.

Allogrooming in the genus Cryptomys could serve two main roles, to remove external
parasıtes or as an appeasement behaviour.

Information concerning external parasites associated with C. damarensis and C. hotten-
totus is meagre (SHORTRIDGE 1934; DE GRAAFF 1972). Small mites are found ın the pelage
ot the common mole-rat C. hottentotus (BENNETT, unpubl.).

Allogrooming results in close physical contact between individuals and its performance
could therefore have an indirect appeasement action. This interpretation ıs supported by
the fact that the colony members in general tend to groom the dominant reproductive
mole-rats (BENNETT 1988). This has certainly been suggested for social mongooses (Rasa
1977). The dwarf mongoose (Helogale undulata rufula) occurs ın small colonies with a
strict monogamous breeding set up. A high degree of division of labour exists within the
group which is not unlike that of C. damarensis. In such groups there are definite

306 N. C. Bennett

preferences for subordinate mongooses to groom the dominant animal of the opposite sex
(Rasa 1977). Social grooming also occurs in the common marmoset Calhthrix jacchus in
which subordinates groom their peers, the reproductive pair (ROTHE 1971; ABBoTT 1984).
KınrocH (1982), observed allogrooming in groups of C. hottentotus resting in the nest
areas, however, quantitative studies on the frequencies of allogrooming were not reported.
In the naked mole-rat, allogrooming is not apparent between colony members, perhaps
because they lack a pelage (]J. U. M. Jarvıs, pers. comm.).

Autobehaviours
Autogroomıng

In the C. hottentotus colony, no tendency occurred for juveniles to autogroom more
frequently than adults. However, in C. damarensis, juveniles tended to autogroom more
frequently than adult anımals (BENNETT 1990).

In Cryptomys, juvenile anımals tend to autogroom significantly less frequently than
they allogroom (Binomial Test p = < 0.05 probability rejection level).

The problem of maintaining a clean coat is exacerbated by living a totally subterranean
existence. Burrowing and digging movements through the soil result in sand and soil
particles being dislodged and caught within the fur. The pelage is kept clean by regular and
thorough grooming and also by shaking of the fur and twitching of skin. In C. hottentotus,
there was no correlation found betweeen the frequency of excavating and autogrooming (rs
= +0.23). There was, however, a significant correlation between the frequency of moving
soil or sawdust and that of autogrooming (rs = +0.77). Sımilarly, in C. damarensıis there
was no correlation between the frequency of excavating and that of autogrooming (BENNETT
1990). However, in contrast to C. hottentotus there was no correlation between the
frequency of moving sawdust and that of autogrooming (BENNETT 1990). Grooming
sequences within the rodent moles are very similar. Grooming begins with the face, the
slightly cupped paws are used independently as they are rubbed over the incisors, nasal
region and the cranial area. The incisors and forefeet are used synergistically to groom the
abdomen, genitalia and the parts of the hind region which are accessible. The digits are
cleaned using the incisors. The above description is common to Tachyoryctes splendens,
Heliophobins argenteocinereus, C. damarensis, C. hottentotus, G. capensis and A. glaber (
Jarvıs 1969; N. C. BENNETT, pers. obs.).

Autogrooming in the genera Cryptomys and Georychus appears to mainly occur after
awakening from a period of rest, after a visit to the toilet area or after a period of soil
movement. The behaviour pattern occurs similarly in 7. splendens and A. argenteocinereus
(Jarvıs 1969), but in 77. glaber occurs almost exclusively, in the toilet area, prior to, during
and after urination and defaecation.

Tooth-sharpening

Tooth-sharpening is seen in all the bathyergids (Jarvıs 1969; N. C. BENNETT, pers. obs.).
The tooth- sharpening behaviour is essentially the same in all the mole-rats and takes pass
when the animal is drowsy and usually preceeds “sleep”.

In C. hottentotus, there was no anımal which tooth-sharpened more than another.
However, after recruitment had occurred in a C. damarensis colony “frequent workers”
sharpened their teeth significantly more than “infrequent workers” (BENNETT 1988). These
frequent workers were the two recent litters and a small adult animal. It is possible that the
frequent workers, the animals that do most digging, had a greater rate of incisor growth
compared to the rest of the colony or that their activities were blunting their incisors.

Aspects of social behaviour in Cryptomys hottentotus 307

BRETT (1986) noted that when A. glaber dug through very hard soil they had to make
frequent stops to sharpen their incisors.

Coprophagy

Autocoprophagy occurs in all the southern African bathyergids (C. hottentotus: KinLOCH
1982; G. capensis: BENNETT, pers. obs.; B. suillus: J. U. M. Jarvıs, pers. comm.).
Coprophagy is undertaken to enhance the digestion and absorption of food, (particularly
of cellulose) which do not readily yield their nutrients. The available literature on the
subterranean rodent families Geomyidae, Ctenomyidae and Spalacidae make no mention
of these rodents practising coprophagy.

To my knowledge allocoprophagy, ınvolving pups and other colony members, is
unique to the socıal Bathyergidae. Allocoprophagy includes both begging faecal material
directly from the anus of a conspecific and the consumption of a voided pellet, picked up in
the toilet area.

Coprophagy is commonly undertaken in 7. glaber (Jarvıs 1981); weanıng pups beg
faeces from other colony members, begging for them with mewing crıies and tugs of the
donor’s anus. When very gravid, the breeding female of A. glaber has difficulty in
doubling up to reach her anus. She begs faeces from other adults and subadults engaged ın
autocoprophagy in the nest area (Jarvıs 1991). Unlike the gravid FH. glaber, pregnant
reproductive cryptomyids do not appear to beg faeces from other colony members.
However, the pups of C. hottentotus and C. damarensis beg faeces from their mothers after
weaning. Allocoprophagy at this age may allow the transmission of valuable gut fauna
from the parent to the offspring, as well as providing the weaning pups with easıly
assimilable food.

Toılet behaviour

The exact function of grooming ın the toılet area and the subsequent smearing of a fluid on
exit from this region ıs unknown. It appears to occur mainly within the socıal bathyergids
(Jarvıs 1981).

The marking agent may serve as an indicator in the same way as urination within the
burrow ıs believed to act as an orientation marker (KınLocH 1982). The marking of the
section of the burrow leading away from the toılet area and the actual entrance may well act
as a cue for orientation within the particular region of the burrow system. The frequency
of marking may well inform each anımal of the degree of use of this part of the system.

Smear marking may familiarıse each mole-rat with the odour of other colony members.
This would allow members of the colony to differentiate between conspecifics and
intruding individuals. Marking could be of importance ın expressing the internal sexual
status of each anımal, the urine merely reflecting the corresponding plasma hormone
concentration, in this respect the reproductive pair of C. hottentotus were found to smear
mark sıgnificantly more frequently than non-reproductive colony members. In contrast
there was no significant tendency for any one animal to urinate any more frequently than
another. The second focal area in the burrow system which receives frequent visits and
could be involved as a site of the release of a chemical which initiates suppression of
reproduction in the females other than the reproductive females, is the toılet area. Mole-
rats entering the communal toilet area not only urinate and defecate in this area but also
smear mark and groom. This area, as well as the nest therefore exposes colony members to
each others’ semiochemical signals and will serve to inform each other of the sexual status
of colony members and impart a general group odour. If reproductive suppression of
colony members by the reproductive female has a chemical component, then the toiılet area
would be an opportune site in which to effect this control. It ıs possible that chemicals,

308 N. C. Bennett

such as volatile hormones or pheromones, are released at the toilet areas in the urine by the
reproductive female.

The advantages of having colonıes in which reproduction is limited to a single female
seem to mainly relate to inclusive fitness and the associated benefits of altruistic behaviour
(Rasa 1977). For example food sharing, an altruistic behaviour is exhibited by the colony,
despite the unequal involvement of the colony members in the various burrow main-
tenance activities. This ıs a strong indication of differential participation in burrowing and
food harvesting occurring in the natural environment. Cryptomys hottentotus colonies
involve a reduction in individual reproduction to an extent that only one female in the
colony is reproductive. This offers some of the strongest evidence for the phenomenon of
kin selection.

Acknowledgements

I wısh to thank Prof. J. U. M. Jarvıs for helping to trap the mole-rat colony. I thank Mr. F. DuckETT
tor allowıing me to collect mole-rats on his farm “Waylands” at Darling, South western Cape, South
Afrıca. Prof. JEnNY Jarvıs and CAROLINE ROSENTHAL are thanked for critically reviewing the
manuscript, Dr. WALTER LIEBRICH for the German translation of the summary and Mr. JosepH M.
SHASHA and Mr. JOHN Keartıncs for help in maintaining the mole-rats in the laboratory.

This work was supported by research grants from the C.S.I.R. and a J. W. JAGGER Overseas
Postgraduate Scholarship.

Zusammenfassung

Aspekte des Sozialverhaltens einer in Gefangenschaft gehaltenen Kolonie des südafrikanischen
Graumulls Cryptomys hottentotus

Das Verhalten von Graumullen (Cryptomys hottentotus) in einer Laborkolonie wurde qualitativ und
quantitativ untersucht. Die Kolonie bestand aus einer reproduktiven und einer nichtreproduktiven
Kaste. Die nichtreproduktiven Tiere ließen sich in „Arbeiter“ und „Gelegenheitsarbeiter“ einteilen.
Das Ausmaß der geleisteten Arbeit stand in keinem direkten Verhältnis zur Körpermasse der Tiere.

Die beobachteten Verhaltensweisen ließen sich drei Hauptkomplexen zuordnen: Bauinstandhal-
tung, Interaktionen und Individualverhalten. Bei der Analyse sozialer Interaktionen wurden Alter
und Klassenzugehörigkeit berücksichtigt. Arbeitergruppen unterschieden sich in ihrer Grabaktivität
nicht signifikant von anderen. Jungtiere trugen häufiger Nahrung ein als Adulte.

Eine positive Korrelation zwischen den Verhaltensweisen des Initiators und denen des Empfängers
wurde ın folgenden Fällen festgestellt: gegenseitige Genitalpflege; Kampfspiel; naso-anale Kontakte
und Beschnuppern des Urogenitalbereichs. Das reproduktive Paar pflegte sich nur gegenseitig.
Gegenseitige Fell- und Genitalpflege, naso-anale Kontakte sowie Kamptspiele traten bei Jungtieren
häufiger auf als bei Adulten. Viele der Verhaltensweisen scheinen eher vom Alter abhängig zu sein als
von der Klassenzugehörigkeit.

In der Kolonie gab es einen abgegrenzten Toilettenbereich, in dem reproduktive Tiere signifikant
häufiger markierten als andere Koloniemitglieder.

References

ABB0TT, D.H. (1984): Behavioural and physiological suppression ot fertility in subordinate marmoset
monkeys. Am. J. Primatol. 6, 169-186.

ANDERSEN, D. C. (1978): Observations on reproduction, growth and behavior of the Northern pocket
gopher Thomomys talpoıdes. J. Mammalogy 59, 418-422.

BENNETT, N. C. (1988): The trend towards sociality in three species of southern African mole-rats
(Bathyergidae): causes and consequences. Ph.D. thesis, Univ. Cape Town.

— (1989): The social structure and reproductive biology of the Common mole-rat, Cryptomys
hottentotus hottentotus and remarks on the trends in sociality within the Bathyergidae. J. Zool.,
Lond. 219, 45-59.

— (1990): Behaviour and social organization in a colony of the Damaraland mole-rat Cryptomys
damarensis. J. Zool., Lond. 220, 225-248.

BENNETT, N. C.; Jarvıs, J. U. M. (1988a): The social structure and reproductive biology of colonies of
the mole-rat Cryptomys damarensis (Rodentia, Bathyergidae). J. Mammalogy 69, 293-302.

— — (1988b): The reproductive biology of the Cape mole-rat Georychus capensıs (Rodentia,
Bathyergidae) J. Zool., Lond. 214, 95-106.

BENNETT, N. C.; Jarvıs, J. U. M.; Davızs, K. C. (1988): Daily and seasonal temperatures ın the
burrows of African rodent moles. $. Afr. J. Zool. 23, 189-195.

Aspects of social behaviour in Cryptomys hottentotus 309

BRETT, R. A. (1986): The ecology and behaviour of the naked mole-rat (Heterocephalus glaber
Ruppell) (Rodentia: Bathyergidae). Ph.D. thesis, Univ. London.

Cer, G. (1946): L’occhio dı Heterocephalus glaber Ruppell. Note anatomo-descrittive e istologiche.
Monit. Zool. Ital. 55, 89-96.

DE GRAAFF, G. (1964): A systematic revision of the Bathyergidae (Rodentia) of South Africa. Ph.D.
thesis, Univ. Pretoria.

— (1972): On the mole-rat (Cryptomys hottentotus damarensis) Rodentia in the Kalaharı Gemsbok
National Park. Koedoe 15, 25-35.

ELoFF, G. (1951): Orientation in the mole-rat Cryptomys. Brit. J. of Psych. 42, Pts 1, 2, 134-145.

— (1952): Sielkundige aangepastheid van die mol aan onderaardse leefwyse en sielkundige konvergen-
sie. ITydskr. wet. Kuns. October 1952, 210-225.

— (1958): The functional and structural degeneration of the eye of South African rodent moles
Cryptomys bigalkei and Bathyergus marıtimus. S. African. J. Scı. 54, 293-302.

GENELLY, R. E. (1965): Ecology of the common mole-rat (Cryptomys hottentotus) in Rhodesıa. ].
er 46, 647-665.

Hıckman, G. C. (1979): A live-trap and trappıng technique for fossorial mammals. S. Afr. J. Zool. 14,
9-12.

Eee. @20:7PRoRTER, A.; BLooM, R. T.; SEAGO, ].;; SOUTHwIcK, M. D. (1957): Field and
laboratory studies on the naked mole-rat (Heterocephalus glaber). Proc. Zool. Soc. Lond. 128,
455-513.

Jarvıs, J. U. M. (1969): Aspects of the biology of East African mole-rats. Ph.D. thesis, Univ. Nairobi,
Kenya.

— (1981): Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science Wash.
21273721572:

— (1991): Reproduction in Naked mole-rats. In: The Biology of the Naked Mole-rat. Chapter 13.
Ed. by P. W. SHERMAn, J. U. M. Jarvıs and R. D. ALEXANDER. Princeton: University Press.
Jarvıs, J. U. M.; Sare, J. B. (1971): Burrowing and burrow patterns of East African mole-rats

Tachyoryctes, Heliophobius and Heterocephalus. J. Zool., Lond 163, 451-479.

KınLocH, M. A. (1982): Behaviour and activity cycle of the common mole- -rat, Cryptomys hottentotus
Lesson 1826. Unpubl. project Mammal Research Institute, Pretoria University.

Lacey, E. A.; SHERMAN, P. W. (1991): Social organization of Naked mole-rat colonies: evidence for
divisions of labor. In: The Biology of the Naked Mole-rat. Chapter 10. Ed. by P. W. SHERMaN, ].
U. M. Jarvıs and R. D. ALEXANDER. Princeton: University Press.

NeEvo, E. (1961): Observations on Israeli populations of the mole-rat Spalax e. ehrenbergi Nehring
1898. Mammalia 25, 127-144.

— (1969): Mole-rat Spalax ehrenbergi: mating behaviour and its evolutionary significance. Science
Wash. 163, 484-486.

PEARson, O.P. (1959): Biology of the subterranean rodents, Ctenomys ın Peru. Memorıas del Museo
de hustoria natural ° “Javier Prado” N° 9

PiLLert, G. (1960): Über das Zentralnervensystem von Heterocephalus glaber (Rodentia, Bathyer-
gidae). Acta Zool. 41, 101-111.

AS, O5 Au Es (MOZAR The ethology and sociobiology of the Dwarf Mongoose (Helogale undulata
rufula). Z. Tierpsychol. 43, 337-406.

Res, E. L. (1968): A note on the brain of the Cape dune mole-rat Bathyergus snillus. Acta Anat. 71,
147-153.

ROTHE, H. (1971): Some remarks on the spontaneous use of the hand in the common marmoset
(Callıthrıx jacchus). In: Proceedings of the third international congress of primatology Zurich
1970, Vol 3. Basel: Karger. pp. 136-141.

ROSENTHAL, C. M.; BENNETT, N. C.; Jarvıs, J. U. M. (1992): The changes in dominance hierarchy
over time of a complete field captured colony of Cryptomys hottentotus hottentotus. J. Zool.
Lond. (in press).

SHORTRIDGE, G. C. (1934): The mammals of South West Africa. London: W. Heinemann.

SIEGEL, $. (1956): Non parametric statistics for the behavioral sciences. New York: McGraw-Hill.

SMITHERS, R. H. N. (1983): The mammals of the southern Afrıcan subregion. Pretoria: Univ.
Petroria.

ZAR, J. H. (1984): Biostatistical Analysıs. New Jersey: Prentice Hall, Englewood Cliffs.

Author’s address: NıiGEL C. BENNETT, Department of Zoology, University of Cape Town, Ron-
debosch 7700, Cape Town, Republic of South Africa

Z. Säugetierkunde 57 (1992) 310-312
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

WISSENSCHRNETEICHEZKURZMTIIBEIIEIIENIGIEN

Food habits of the Lesser false vampire, Megaderma spasma,
from Kuala Lompat, Peninsular Malaysia

By G. W. H. Davıson and A. ZUBAID

Jabatan Zoologi, Fakulti Sains Hayat, Universiti Kebangsaan Malaysia, Bangi, Selangor, Malaysia

Receipt of Ms. 13. 3. 1992
Acceptance of Ms. 2. 6. 1992

Very little is known of the feeding habits of Malaysıan microchiropterans except for some
detailed studies on Hipposideros pomona (Zugaıp 1988a), Hipposideros armiger (ZUBAID
1988b) and Taphozous melanopogon (Zugaıp 1990). The main problem with the study of
microchiropteran feeding habıts is that bats thoroughly chew their food, making identifica-
tion of most prey remains below the family level practically impossible and thus giving
only an indication of the order of importance of the dominant prey items (WHITAKER
1988). However, the study of microchiropteran feeding habits is important as bats are

Estimated proportions of animal remains col-
lected from the roost of Megaderma spasma

Proportion (%)

Food item

ORTHOPTERA
Tettigonidae
Blattidae
Acrididae
Phasmantidae
Gryllidae
Mantidae

COLEOPTERA
Scarabaeidae

LEPIDOPTERA
Satyridae
Amathuacidae
Danaidae
Geometridae
Papilionidae
Arctidae
Nymphalidae
Noctuidae

=D OoOoOooOo-m--%'
ou nun o0o00o0

HYMENOPTERA
Formicidae

ISOPTERA

HOMOPTERA
Cicadidae

ODONATA

ANURA
Rhacophorus appendiculatus

SB S
vn uuno

thought to play an important role in ın-
fluencing insect populations both in forests
and cultivated lands (HırLr and SMITH 1984;
CouLson and WITTER 1984; BENJAMINI
1987).

This study was carrıed out at Kuala
Lompat, Krau Game Reserve, Pahang, at a
permanent day-time and feeding roost of
between two and fıve Megaderma spasma.
The roost was located under the asbestos
roof of an abandoned room ın an old
wooden rest-house. This was sited ın a
grass clearıng with fruit trees, bordered on
one side by the 500 km? lowland dip-
terocarp rainforest of the Krau Game Re-
serve, and on the other by a small river and
extensive mature rubber estates.

All observed food discards were col-
lected from beneath the roost, at irregular
intervals from March 1988 to September
1990. No attempt was made to determine
prey selection versus prey availability as the
remains were collected in conjunction with
another study.

The table lists the food material col-
lected. The samples from the various
months were pooled due to small sample
sizes (n = 1632). The remains were com-
pared with identified collections in the

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Food habits of Megaderma spasma from Kuala Lompat, Peninsular Malaysia 311

Zoology Museum, University Kebangsaan Malaysıa. The proportions are percentages of
the total collected remains and the procedure used followed that of LaVaAr and LaVaı
(1980). The majority of the remains were wings and wing-cases, with a few legs. These had
evidently been dropped whilst the head, thorax and abdomen of all prey were fully
consumed. Most of the remains were of big insects found typically on foliage. This, and
the presence of a tree-frog, imply that most prey were probably picked from the
vegetation. Orthopterans and coleopterans made up a large proportion of the diet, 72.5 %
and 12% respectively. Only one vertebrate, the frog (only the legs remained), was
recovered from the roost site.

Amongst the lepidopteran remains (12 %), there were equal proportions from typically
diurnal and typically nocturnal families. This again may be evidence that food is picked
from vegetation, rather than caught while the prey ıs in flight.

There is no previous detailed information concerning the food habits of M. spasma.
Mepway (1982) and Payne et al. (1985) only mention that this species eats “large insects”
and “small vertebrates” (including other bats) but did not mention the specific types of
prey that are consumed. The results of this study indicate that M. spasma feeds selectively
on orthopterans (Table) which make up approximately three-quarters of the diet followed
by coleopterans. Although this species is known to eat other small vertebrates, the findings
in this study indicate that they are a mınor component of the diet.

BrossET (1962) noted that M. spasma hunts near its daytime roost and tends to return to
its roost to consume the prey. If this is also true of the species ın Malaysia, then the results
of the dietary analysıs could be considered to be a reasonably accurate reflection of its
feeding habıts.

Most orthopterans are phytophagous while the coleopterans are considered to be
among the most destructive insect pests of forest trees (CouLson and WITTER 1984).
Birds, bats and other small mammals are among the most significant vertebrate predators
of insects (CouLson and WITTER 1984; SPEIGHT and WAINHOUSE 1989) but quantitative
studies concerning bats are lacking. Although M. spasma occurs only in small groups, not
in big roosts (BROSSET 1962; Mepway 1982), and takes only a limited range of insect prey
(this study), it is likely that the cumulative effect of Peninsular Malaysıa’s rainforest bat
species (MEDwAYy 1982), each with it’s own dietary range (ZugAıD 1988a, 1988b, 1990; thıs
study) has a significant influence on the low-density dispersed populations of rainforest
insects (ELTON 1973).

References

BENJaMINT, L. (1987): Management of Kuhl’s bat (Pipistrellus kuhlı kuhli) as an insect pest control
agent. Myotis 25, 65-69.

BrossET, A. (1962): The bats of central and western India. J. Bombay Nat. Hist. Soc. 59, 583-624.

Couson, R. N.; WITTER, J. A. (1984): Forest Entomology: Ecology and Management. New York:
John Wiley and Sons.

Erron, C. (1973): The structure of invertebrate populations inside neotropical rain forests. J. Anım.
Ecol. 42, 55-104.

Hırı, J. E.; SmrtH, J. D. (1984): Bats: A Natural History. London: British Museum Natural History.

LaVar, R. K.; LaVar, M. L. (1980): Prey selection by the slitfaced bat Nycteris thebaica (Chirop-
tera : Nycteridae) in Natal, South Africa. Biaotropica 12, 241-246.

Mepwax, L. (1982): The Wild Mammals of Malaya (Peninsular Malaysia) and Singapore. 2nd ed.
revised. Kuala Lumpur: Oxford University Press.

PAYnE, J.; Francıs, C. M.; PrırLıps, K. (1985): A Field Guide to the Mammals of Borneo. Kuala
Lumpur: The Sabah Society with World Wildlife Fund Malaysıa.

SPEIGHT, M. R.; WAınHousE, D. (1989): Ecology and Management of Forest Insects. Oxford:
Clarendon Press.

WHITARER, J. O., JR. (1988): Food habits analysis of insectivorous bats. In: Ecological and Behavioral
Methods for the Study of Bats. Ed. by T. H. Kunz. Washington: Smithsonian Institution Press.

Zusaıp, A. (1988a): Food habits of Hlipposideros pomona (Chiroptera : Rhinolophidae) from
Peninsular Malaysia. Mammalıa 52, 134-137.

312 G. W. H. Davison and A. Zubaid

Zusaip, A. (1988b): Food habits of Hipposideros armiger (Chiroptera : Rhinolophidae) from
Peninsular Malaysıa. Mammalıa 52, 585-588.
Zusaıpd, A. (1990): Food and roosting habits of the black-bearded Tomb bat, Taphozous melanopogon

from Peninsular Malaysıa. Mammalıa 54, 159-162.

Author’s addresses: Dr. G. W. H. Davıson, World Wide Fund for Nature Malaysıa, Locked Bag
No. 911, Jalan Sultan P.O., 46990 Petaling Jaya, Malaysıa; and Dr. A. Zugaıp,
Jabatan Zoologi, Fak. Sains Hayat, Universiti Kebangsaan Malaysia, 43600
Bangı, Selangor, Malaysıa

Z. Säugetierkunde 57 (1992) 313-315
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Distribution and local range of the Orinoco dolphin
(Inia geoftrensis) in the Rio Apure, Venezuela

By D. SchnapPp and J. HowroyD

St. Hılds’s College and Christ Church, Oxford, Great Britain

Receipt of Ms. 22. 12. 1989
Acceptance of Ms. 20. 3. 1992

Orinoco dolphins (/nia geoffrensis), in Venezuela known as Toninas, occur in the
Orinoco, Rio Negro and tributaries in Venezuela. We intended to investigate: 1. Whether
Inıa ıs solitary and grouping is a result of aggregation in favourable habitats; 2. Whether
there is evidence for migration, possibly ın connection with seasonal movements of fish
(LowE-McConneLL 1964); 3. Whether /nia is territorıal.

We carried out a 17 day survey by boat during the end of the rainy season in 1989.
Between July 27th and 30th, we covered 45 km of the Apure river to the west of San
Fernando de Apure, using a 4.5 m long engine powered aluminium canoe. Between
August 5th and 15th we covered 156 km of the Apure to the east of the town, 27 km of the
Orinoco upstream from the mouth of the Apure and 27 km of the Apurito upstream from
its mouth into the Orinoco using a 10 m long engine powered wooden dugout-canoe.
Hours of observations were between 8:30 and 17:30 every day. Irregular rainfall inter-
rupted the work so observation times could not be further standardized. Cloud cover and
height of ripples on the water surface were noted on a scale from 0 (slight) to 3 (severe).
The distance covered was followed on a map and sıghtings noted every 3 km interval.
Numbers of sıghtings per interval were compared to a Poisson distribution of equal mean,
using the chi square test (for methods refer to Macnusson et al. 1978).

For each sighting, depth of the river and stream velocity were noted: The depth was
found by lowering a 5 kg iron weight attached to a rope with knots at 50 cm intervals to
the bottom of the river. Stream velocity was measured holding the boat steady against the
current with reference to a landmark on shore. A nail attached to a rope was lowered into
the water up to a marked point. The rope was attached above a scale over which it swept as
the current displaced the nail, giving a relative estimate of stream velocity. Measurements
of depth and current speed were compared to the sıze of sighted groups, using Spearman’s
rank correlation coefficient (r,).

The study was complemented by observations by boat and from shore of dolphins
within a 3.5 km long stretch of the Apure. These observations were carried out from
22nd-26th August between 6:00 and 18:00 hours. The position of the anımals was plotted
on a large scale map. Natural markings of individual dolphins helped in this tracking effort.

The average density of Inıa surveyed between August 5th and 15th was 0.56 anımals per
km with an average sighting frequency of 3.91 anımals per hour. Highest densities were
encountered in the Apurito (1.15 anımals per km, 8.6 sightings per hour). Current and
turbulence lead to inconsistency in boat speed, affecting the values for sightings per unit
effort.

Individual /nia were found to be patchily distributed. The distribution of groups did
not differ significantly from the Poisson distribution (Table). 58 % of our sightings were
groups of two or more (Figure).

There was a significant (Spearman’s rank coefficient r, = -0.608; P < 0.01) relationship
between group sıze and stream velocity. Most large groups were encountered in slow

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314 D. Schnapp and J. Howroyd

frequency

1 2 &) 4 3 6 7

group Size

Fig. 1. Frequency distribution of Inia geoffrensis

running sections of the river, vicinity of flooded banks or clearwater trıbutaries. Most of
the sightings occurred ın 10 to 12 m deep water within 50 m from the bank.

During the observations following the boat survey, most groups of Inia were encoun-
tered regularly within defined ranges of approximately 130-800 m along the river. Dol-
phins following the boat repeatedly remained behind at fixed points but ranges overlapped
and interactions between neighbouring groups occurred. No aggressive interactions were
observed.

58 % of our sightings represent groups of two or more individuals compared with 20 %
in the study of Macnusson et al. (1980). In accordance with points 1. and 2. of the
introductory remarks, possible reasons could be:

1. Seasonal migration: /nıa has been reported by TREBBAU and van BrEE (1974) to enter
floodplains and smaller tributaries during the rainy season, though Best and Da SıLva

(1986) do not recognize any seasonal trend in the data, possibly due to lower annual

Distribution of individuals and groups per 3 km interval for each section of the survey as
indicated above the columns

Statistical results Apure West of East of Orinoco Apurito
(201 km) San Fernando San Fernando
(45 km) (156 km)

Individuals

DIR

”x?

Variance Ä 035

X? = I(x-x)?/x es 18.25 NS

Groups
x 0.200
Ix 3
Dixa 3
Variance 5 0.171
x? = 2(x-x)?/x .936* 12.000 NS 36.000 NS 14.789 NS 6.000 NS

The number of intervals in a section is noted as n and average sightings per interval as x. Significant
values for chi squared are marked * for P<0.05, ** for P<0.01 and *** for P<0.001. For these,
it the mean is maller than the varıance, the distribution is patchy.

Distribution and local range of Inia geoffrensis in the Apure river 315

fluctuations in rainfall further south. The tendency of /nia to aggregate may be related
to movements of characids and catfısh into the floodplains to spawn and feed (LowE-
McConneıı 1964, 1975). In the floodplains and the Apurito high densities of young
catfish could be observed skimming the surface. In the fast flowıng Apure, young
catfish were occasionally observed in direct vicinity to the bank (maximum 3 m away).
2. Opportunistic aggregation: Several authors (Best and Da Sırva 1986; GEwALT 1978;
TREBBAU and VAN BREE 1974; TREBBAU 1975) have reported that the anımals aggregate
around anchored boats, areas of turbulence and in the mouths of trıbutaries. Da SıLvA
(pers. com.) suggests that aggregations are not permanent as the anımals may segregate
after short periods. During our observations single anımals and groups were frequently
joined by others and would then separate. Our observations therefore lead to the same
conclusion.
Earlıer studies suggest that /nıa may be a sedentary species occupying localized ranges at
least during part of the year (see Best and Da Sırva 1986, for a review). Similar
observations lead TREBBAU and van BREE (1974) to suggest that Ina may be territorial.
Our observations of resıdent groups and individuals indicated that /nıa occupies a limited
range for at least part of the year. However, we found no evidence for aggressive or
avoidance behaviour. We would therefore support Best and Da Sırva’s (1986) conclusion
that /nıa occupies an undefended homerange.

Acknowledgements

This study was carried out during the Oxford University River Dolphin Expedition 1989. We wish to
thank our sponsors, in particular the Alexander Allen Patton Fund and the Anonymous Biological
Support Fund. Thanks are due to GRAHAM STONE and SuUE Brown for reading the manuscript.

References

Best, R. C.; Da Sırva, V.M. F. (1989): Biology, status and conservation of /nia geoffrensis ın the
Amazon and Orinoco river basıns. Occ. Pap. IUCN SSC 3, 23-34.

GEWALT, W. (1978): Unsere Tonina (Inia geoffrensis Blainville, 1817) — Expedition 1975. Zool.
Garten N. V. Jena 48, 324-384.

LowE McConntELL, R. H. (1964): The fishes of the Rupununi savanna district of British Guyana,
South America. Part 1. Ecological groupings of fish species and effects of the seasonal cycle on the
fish. J. Linn. Soc. (Zool.) 45, 103-144.

Macnusson, W.E.; Best, R. C.; Da Sırva, V.M. F. (1980): Numbers and behaviour of Amazonian
dolphins /Inia geoffrensis and Sotalia fluviatilis flnviatilis in the Rio Solimöes, Brazil. Aquatic
Mammals 8, 27-32.

TREBBAU, P. (1975): Measurements and some observations on the freshwater dolphin, /nia geoffrensis,
in the Apure River, Venezuela. Zool. Garten N. F. Jena 45, 153-167.

TREBBAU, P.; VAN BREE, P. H. (1974): Notes concerning the freshwater dolphin (/nia geoffrensis de
Blainville, 1817) in Venezuela. Z. Säugetierkunde 39, 50-57.

Authors’ addresses: DEnnı SCHNAPP, Division of Biosphere Sciences, King’s College, Campden Hill
Road, London W8 7AH; JoHn HowROoYD, Department of Mathematics, Univer-
sıty College, Gower Place, London EC1, Great Britain

Z. Säugetierkunde 57 (1992) 316-317
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Reproductive behaviour and development of the young of the
chacoan peccary (Catagonus wagneri Rusconi, 1930) in the
Paraguayan Chaco

By D. M. Brooks

Proyecto Tagna, Fıladelfia, Boqueron, Paraguay

Receipt of Ms. 3. 1. 1992
Acceptance of Ms. 15. 5. 1992

Herein, anecdotal information on Tagua reproduction and development is described;
findings are compared to reproduction and development of other Tayassuidae species
where information is available. The study facılıty (Proyecto Taguä), located in the Central
Paraguayan Chaco, has been described ın detail elsewhere (1.e., HANDEN and BENIRSCHKE
1991; Kınaswoop and Brooks 1991), and is part of the natural range of Taguä, as wild
specimens (two adults and a three month old infant) were sighted on the estancia where the
study site was located. Semi-captive Taguä were studied for a year (September 1989 to
August 1990); study times varıed between 0530-2000 hours, though most of the study
durations were from 1400-1800 hours. Observations were made from one of two high-seat
blinds, and complemented by random observations on foot.

Copulation occurred among adults (male = M1, female = F1) on November 1, 1989, at
1510 hours, with a temperature of 34 °C. Actual conception remained unconfirmed, but
Fi gave birth 184 days later. Two days after this copulation (1210 hours, 34 °C), M1 was
observed following Fl next to a taJamar (temporary, manmade pond), exhibiting pre-
copulatory behavior. Another male (who was dominant over M1) approached MI and Fi
with his dorsal hair halfway erected. M1 then declined, and the pair exhibited what was
probably a submissive behaviour, rooting in tajamar mud, side by sıde. Then shortly
thereafter, Mi sniffed the ano-genital region of another Tagua which proceeded with a
head-slice movement against Mi. F1 exhibited precopulatory behaviour with an alternate
male while in the presence of M1; immediately afterwhich, F1 exhibited precopulatory
behaviour with Mi. MI also exhibited precopulation and air-mounting with an alternate
female. From these observations, ıt seems likely that promiscuity was present ın both
sexes. Due to hierarchial rank or ınhibition by the female, some males were unable to
proceed with precopulatory behavior. Social order between sexes in Tagua appears to be
complex, and remains largely unknown. Precopulatory behavior was observed most
frequently from May 9 to June 8, between the hours of 0730-1600, with temperature
varyıng between 16 °C-30 °C.

The earliest recorded age-specific fertility at Proyecto Taguä was a litter of three at a
maternal age of 21 months (n = 1). Mayer and Branpr (1982) estimated the youngest
pregnant Taguä sow (n = 1) in their study to be 13-18 months of age. Comparatively, the
youngest collared peccary sows (n = 2) in Sowıs (1966) study gave birth at 13.5 months.
White-lipped peccary sows become sexually mature at 18 months (EisEnBERG 1989). Litter
sizes at Proyecto Taguä ranged from 1 to 4 (N = 9; SD = 1.1; mode = 3); whether or not
infanticide occurred is unknown. The findings of MAYER and Branpr (1982) are sımilar;
the average litter size at Proyecto Taguä was 2.33, whereas MAyER and BRAnDT (1982) had
an average of 2.46 (N = 10; r = 1-4; mode = 2-3) for neonatal litters sighted live ın the field.
Additionally, a mean litter size of 2.17 (N = 29; r = 1-4; mode = 2) was obtained ın collared

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SZ

peccaries (SowLs 1966). MAYER and BRAnDT (1982) reported 2 fetuses from a pregnant
white-lipped peccary sow (N = 1) collected in the Paraguayan Chaco, and indicated that
litters of 3 were rare. FRÄDRICH (1972) reported that 9 of 10 white-lipped peccary litters at
the Berlin Zoo consisted of twins.

Data were collected daily for specific individuals of the 21 young born at Proyecto
Taguä as of August 9, 1990. Learning processes are summarized hereafter (mean age [days]
with range [r] when a particular learnıng process was first observed for n individuals
appears parenthetically at the end of each account) as follows: Feeding: mouthing food or
maneuvering with nose, but not eating (n = 4; mean = 4.0; r = 2-6); nibbled or chewed
food, but no consumption (n = 3; mean = 13.5; r = 13-15); rubbed at top layer of soıl with
snout (n = 1; mean = 14.0); ate solid food for first time (n = 4; mean = 18.0; r = 17-19);
maneuvering food with foot and mouth (n = 4; mean = 26.5; r = 14-39). Litter cohesion:
litter of three came to feeding area together for first time (n = 2; mean = 6.0; r = 4-8).
Survivorship skills: Taking cover on ground, or behind adult when warning stimulus ıs
elicited (n = 3; mean = 5.1; r = 5-6); eliciting warning stimulus (n = 1; mean = 54.0).
Intraspecific competition: individual pushes a younger nursing infant, in order to nurse
(n = 2; mean = 13.5; r = 8-19); average proportion of days younger infant was than
competitor (n = 2; mean = 0.7; r = 0.6-0.8). Playing: infants play fighting (n = 2; mean =
23.5; r = 22-25). Independence: arriving at feediung area alone, with infants, or staying
behind after others left (n = 6; mean = 192.5; r = 70-248).

The infants were able to run wıthin a couple of hours after birth. The pelage was not
completely dry prior to fırst quadrupedal movement. Nursing was done from the side,
from the rear, standing up, kneeling on front knees, sitting, or kneeling on all four legs.
Standing up from the side was the most frequent position. It was common for infants and
older juveniles to nurture ınfants, much as the adults dıd. Nurturing Tagua were not
always related to the nurtured individual, suggesting that Tagua maintain strong inter-
famılial group cohesion.

Literature

EISENBERG, ]. F. (1989): Mammals of the Neotropics. Vol. 1: The Northern Neotropics. Chicago:
University of Chicago Press.

FRÄDRICH, H. (1972): Swine and peccaries. In: Grzimmek’s Anımal Life Encyclopedia. Ed. by B.
GRZIMEK. New York: Van Nostrand Reinhold. Pp. 76-108.

HANDEN, C. E.; BENIRSCHKE, K. (1991): Giant Chaco peccary: feeding and social behavior of a
captive group in a natural habıtat. Zoo Biol. 10, 209-217.

Kıngswoop, $. C.; BRooxs, D. M. (1991): Captive management of Tagua (Chacoan Peccary) in
Paraguay. Anım. K. Forum 18, 129-132.

MAYER, ]J.; BRANDT, P. (1982): Identity, distribution, and natural history of the peccarıes. Tayas-
suidae. In: Mammalıan biology ın South America. Univ. of Pittsburgh: Spec. Publ. Serv., Pymat.
Lab of Ecol. Vol. 6, 433-455.

Ruscon1, C. (1930): Las especies fosıles Argentinas de pecaries (Tayassuidae) y sus relaciones con las
del Brasil y Norte America. Ann. Mus. Nac. Hist. Nat. “Bernardino Rıvadavia” 36, 121-241.
Sowrs, L. K. (1966): Reproduction in the collared peccary (Tayassu tajacn). In: Comparative biology
of reproduction ın mammals. Ed. by I. W. Rowranns. London: Academic Press. No. 15,

155-172.

Author’s address: DanieL M. BROoks, Department of Biological Sciences, Texas Tech University,
Lubbock, Texas, 79409-3131; USA

BU@CHBESBERESEIIINGEN

BARQUEZ, R. M.; Mares, M. A.; OJEDA, R. A.: Mammals of Tucuman - Mamiferos de
Tucuman. Norman: Oklahoma Museum of Natural History 1991. Illustrated by N.
GIAnNINI. 282 pp. US $ 17.00. (Obtainable from the Oklahoma Museum of Natural
History, Norman, Oklahoma 73019, USA)

This is a bilingual guide to 95 species of mammals known to occur in Tucuman, a small province
which covers only 0.8 % of the territory of Argentina. Nevertheless its fauna is surprisingly rich due
to topographic diversity with a number of high-altitude habitats in the Andes as well as subtropical
forest and Chacoan thorn scrub in the lowlands.

A key to the orders, families and species is provided which is principally based on external features
and measurements which should permit the ıdentification of living animals. However, the authors
correctly warn the reader that many small mammals such as rodents and bats are difficult to identify in
the hand.

For each species the scientific and common names in English and Spanish are given on a left page,
followed by a short description and notes on distribution. Sometimes comments on abundance,
habitat or reproduction are added. On the opposite right page rough distribution map, a drawing of
the anımal and two aspects of the skull are to be found. 10 references of books suggested for further
reading and an index to species conclude the book.

The bilingual concept of the guide is promising and should be taken as a model for other local
faunas. Without doubt ıt will help to raise interest ın the study and conservation of South American
mammals. However, interested laypeople as well as professional users will soon reach the point where
they wish to consult a more detailed book or an expert. For example, not a single word indicates why
Thylamys elegans is used as scientific name for a mouse opossum known as Marmosa elegans for long,
and the same applies to the rather unusual use of Psendalopex instead of Dusicyon. A comment and a
reference would have been helpful for readers without access to a mammal library. Also, a scale for
each skull and a proportional reduction of the illustrations, at least within one genus, would have
facılıtated the identification, aspects to be considered in a future edition. The present book convers a
nearly blank page of South American mammalogy and just for this reason it is a must for readers
interested in neotropical mammals. R. HUTTERER, Bonn

HERRMANN, M.: Säugetiere im Saarland. Verbreitung, Gefährdung, Schutz. Schriften-
reihe des Naturschutzbundes Saarland e.V. (DBV). Ottweiler: Michel Verlag 1991. 166 S.,
19 Verbreitungskarten, 31 Abb. ISBN 3-923755-25-2

Das Anfang 1991 fertiggestellte Buch ist ein erster begrüßenswerter Versuch, die heute ım Saarland
lebenden Säugetierarten zu erfassen (ausgenommen die Fledermäuse), was flächendeckend allerdings
nicht möglich war. Die Angaben zum Vorkommen und zur Verbreitung der verschiedenen Spezies
gründen ım wesentlichen auf Beobachtungen und Hinweisen von 156 namentlich genannten „fach-
kundigen Informanten“, die dem Kreis von Förstern, Biologen, Jägern und im Naturschutz engagier-
ten Personen angehörten. Wie der Untertitel des Buches verrät, gelten die Bemühungen des Autors
aber nicht nur der Klärung von Verbreitungsfragen; sein Engagement ist mindestens ebenso groß,
wenn es gilt, auf die Gefahrenquellen aufmerksam zu machen, denen die Säugetiere in der heutigen
Kulturlandschaft ausgesetzt sind; und wie diesen Gefahren begegnet werden kann. Den einleitenden
Angaben zur methodischen Seite der Erhebungen schließt sich der Hauptteil des Buches an: Die
Autlistung der saarländischen Säugetiere mit Erwähnung auch der inzwischen ausgestorbenen Arten.
Den Anmerkungen zur „Biologie“ der jeweiligen Art folgen Hinweise zum Vorkommen mit
punktueller Verbreitungskarte auf Meßtischblattbasis und Erörterungen zu „Gefährdung und Schutz“
der Spezies. Auch zum Thema Wiederansiedlung (Biber, Bär, Elch, Fischotter, Luchs und Wolf) und
Faunenverfälschung (Damhirsch, Nutria, Waschbär) wird Stellung genommen. Die Säugetierfauna
des südwestlichen Bundeslandes umfaßt (ohne Fledermäuse) 37 Arten einschließlich der Schabracken-
spitzmaus. Bislang nicht sicher belegt sind die Sumpfspitzmaus, die Gartenspitzmaus und die
Kurzohrmaus; für die Feldspitzmaus fehlen neuere Hinweise, ebenso für den Hamster und die
Hausratte. Im Saarland noch nicht aufgetaucht ist offensichtlich der Marderhund, dessen fachliche
Benennung Nyctereutes procyonoides lautet (nicht N. procyonides). Den letzten Teil des Buches
widmet der Autor eingehend dem Problem der Gefährdung von Säugetieren durch Umwelteinflüsse.
Es werden zahlreiche Gefahrenquellen aufgelistet (Gewässerverschmutzung, Flurbereinigung, Trok-
kenlegungen, Pestizide, Schwermetalle, Chlorkohlenwasserstoffe, Dioxine, Straßenverkehr usw.), die
im Grunde genommen nicht nur für die Säugetiere, sondern für die Tierwelt schlechthin eine
Bedrohung darstellen. Im Anhang 1 wird die naturschutzrechtliche Stellung der Arten erläutert,
Anhang 2 enthält informative Tabellen mit Ergebnissen von Gewöllanalysen, Anhang 3 schließlich die
Namen der Mitarbeiter und Beobachter. Am Schluß findet sich ein umfangreiches Literaturverzeich-

Buchbesprechungen 319

nis, das eigentlich die Auffassung des Autors widerlegt, die Säugetierforschung stecke im Vergleich
mit der Ornithologie „noch in den Kinderschuhen“. So begrüßenswert das große Engagement des
Autors bezüglich des Säugetierschutzes auch ist und so wichtig das von ihm initiierte Vorhaben für die
Säugetierfaunistik auch sein mag, so muf man bei alledem auch der deutschen Sprache gerecht
werden, auch oder gerade dann, wenn die anzusprechende Zielgruppe Naturschützer und wissen-
schaftlich interessierte Laien sind. Es würde den Rahmen dieser Rezension sprengen, wollte man all
die Wortneuschöpfungen und Satzungetüme, die lapıdaren Feststellungen und unbeholfenen Formu-
lierungen aufzählen, die einer strengen redaktionellen Bearbeitung eigentlich hätten zum Opfer fallen
müssen. Und so findet sich ein „undokumentierter Bestandsrückgang“ ($.77) neben einer „Feindver-
meidungsstrategie“ (S.51), der „generalistische Beutegreifer“ ($.52) neben „leerstehenden Habitaten“
(S. 60), die „bärische Aktivität“ neben dem „nomadischen Erschöpfungsjäger“ (S. 80), die „Wander-
barrıere“ (S.40) neben den „Extrembiotopen“ (S.42) und die „potentiell wichtige Gefährdungsursa-
che“ ($.78) neben dem „Habitatelement“ (S.42). Adulte Erdmäuse nutzen ihre Streifgebiete weitge-
hend „exklusiv“ (S.50). Der Baummarder kann als „Indikatorart für den Kronenbereich innerhalb des
Okosystems Wald angesehen werden“ (S.85). Beim Rothirsch ist „für die Populationsentwicklung
historisch das wiederholte Eintreten von Ausrottungsphasen wesentlich“ (S. 109). Sein „Gen-Pool“
wird durch künstliche Selektion, die Jagd „verfälscht“, derjenige der einheimischen Population
„dürfte erloschen sein“ ($S.110). Und vom Nutria heißt es, daß er während einer Nacht mehrere
Kilometer „Gewässerlauf abstreifen“ kann (S. 67). Von den von Zwergmäusen ursprünglich besiedel-
ten Lebensräumen sind „nur noch Bruchstücke“ übrig (S.65). Hausmäuse werden „häufig in Fallen
gefangen“ (S.61). Und die Hausratte schließlich hat eine „geringe Ausbreitungsdynamik“ (S. 60). Wer
sich an solchen oder ähnlichen Formulierungen nicht stört, auch nicht an dem Satz, daß Feldhasen
„auch durch Veränderungen der Vegetation hin zu nitriphilen Bedingungen infolge Düngereintrags
durch die Landwirtschaft und der Stickoxyde aus der Luft sowie durch Verlust von strukturreichen
Lebensräumen infolge der Flurbereinigung“ bedroht sind ($.37), dem kann die Lektüre empfohlen
werden. Die Qualität eines Beitrages kann nicht am Inhaltlichen allein, sie muß auch an seiner Form
gemessen werden. H. REıcHsTEin, Kiel

BAYER, SHIRLEY A.; ALTMAN, J.: Neocortical Development. New York: Raven Press
1991. 256 pp., 208 figs., 2 tables. US $ 161.50. ISBN 0-88167-778-7

As one of the most important and most complicated parts of the mammalıan forebrain the neocortex
has been the subject of a variety of scientific investigations with regard to both its structural
appearance and functional importance as well as practical applications and theoretical interpretations.
Nevertheless, phylogenetic origin, ontogenetic development and evolutionary diversification are the
main issues of zoological evaluations. In this sense, the book by SHIRLEy A. BAYER and JOsEPH
ALTMAN fills a certain gap in our knowledge, as ıt ıs devoted to the ontogenetic development of this
portion of the brain. The authors report on own results very accurately and ın detail, mostly obtained
from an impressively large and well-defined sampling of material using normal histological and
experimental methods (labeling, x-irradiation). However, the one drawback of this descriptive book is
that it is based on only one species and a special breed, namely, the laboratory rat of the Wistar strain.

In contrast to the rather misleading title of the book, results are presented on a rather primitive
mammal in its domesticated form possessing a lissencephalic and structurally less complex cortex.
Furthermore, developmental changes during the postnatal period are not included. Despite these
restrictions, there are 17 chapters associated with 4 major sections, of which the first gives a brief
historical review and provides overviews of major morphological and histological changes that occur
from embryonic day 11 (E11) through birth (E22). Daily changes are recorded qualitatively and
quantitatively, and a global “chronoarchitectonic map” is given on the basis of morpho- and
neurogenetic gradients of growth and differentiation.

The second section of the book is concerned with the entire embryonic development of the
neocortex (neuroepithelium, subplate, cortical plate, cell migration, maturation, stratification).
Retlecting on their results the authors hypothesize an early recognition of prospective cell material.
According to their theory, only radıally cleaving cells in the embryonic ventricular zone differentiate
to precursors of neurons, while variably cleaving cells lose their attachment to the ventricular wall and
develop into neuroglial and ependymal elements. Further cell proliferation at first results ın an early
stage of cortex formation consisting of a primordial plexiform layer with cells of the future layers I
(marginal layer) and VII (subplate). A second stage is established later, resulting in the formation of
the cortical plate (future layers VI-II). This process partitions the primordial layer into superficial and
deep parts. Prior to the definitive stratification, a two-tiered construction is postulated, forming a
lower tier (VI/V) and an upper tier (IV/IIV/II). According to neurogenetic development, the neurons
in layers VI-II are generated in three spatio-temporal gradients: 1. the radial gradient (older neurons
are sıtuated in the depth of the cortex, younger more superficially); 2. the transverse gradient (neurons
situated ventrolaterally tend to be older than those situated dorsomedially); 3. the longitudinal
gradient (neurons closer to the frontal pole tend to be older than those closer to the occipital pole).

320 Buchbesprechungen

The third main section of the book describes the intrinsic neurogenetic gradients within specific areas
(visual, auditory, somatosensory, motor, and limbie cortical). It becomes evident that the general
pattern of neurogenetics is modified in some way between various cortical areas, e.g., in the upper
tier. Furthermore, primary sensory areas always contain younger neurons than their respective
secondary sensory areas. The fourth section of the book includes theoretical issues, a summary, and
conclusions. It is followed by appendices with descriptions of the methods applied.

To summarize, most of the results are not new and some theoretical issues seem to overestimate
and generalize the results obtained in Wistar rats to a comprehensive phylogenetic interpretation.
Nevertheless, this ıs a well ıllustrated and excellent compilation of embryonic neocortical develop-
ment of the rat with some interesting and stimulating interpretations. D. Kruska, Kıel

Marrtın, A. R. (Hrsg.): Das große Bestimmungsbuch der Wale und Delphine. Mün-
chen: Mosaik Verlag 1991. 192 S., 200 z. T. farbige Abb. DM 49,80. ISBN 3-576-10003-2

In dem vorliegenden, von ANTHONY R. MarrTın herausgegebenen Band sind sowohl die Abbildungen
als auch der Text von hoher Qualität. Der Herausgeber, welcher im Vorstand der ‘Sea Mammal
Research Unit’ ın Cambridge, England, tätig ist, hat zehn wissenschaftliche Mitarbeiter und zwei
Künstler zur Erstellung des Werkes herangezogen. Gemeinsam haben sie einen höchst informativen,
harmonischen und sachlich wie auch ästhetisch ansprechenden Band ım DIN-A 4-Format gestaltet.

Das Buch ist in zwei Hauptabschnitte gegliedert, einen allgemein biologischen und einen mit den
Artbeschreibungen. Der erste Hauptabschnitt behandelt zunächst die Besonderheiten der Wale als
marıne Säugetiere, dann wird kurz auf ihre Entwicklungsgeschichte eingegangen. Gesonderte kurze
Kapitel beschäftigen sich mit dem Schwimmen und Tauchen, mit den Sinnen, der Intelligenz, der
Nahrungsaufnahme, dem Sozialverhalten der Cetacea und ihrer Ontogenese sowie mit ıhren Lebens-
zyklen. In den abschließenden Kapiteln des ersten Hauptabschnittes werden Strandungen, Walbeob-
achtungen und Walforschungen sowie der Einfluß der Fischerei und der Meeresverschmutzung auf die
Meeressäuger besprochen.

Der zweite Hauptabschnitt des Buches behandelt 11 Bartenwal- und 67 Zahnwal-Arten. Jede
Artbesprechung ist farbig illustriert, meist mit ausgezeichneten Photos. Die Größe jeder Art wird
dadurch anschaulich gemacht, daß ihr Umriß proportionsgerecht neben den eines Tauchers gesetzt
wird. Die Beschreibung jeder Walart bietet klar gegliedert folgende Einzelheiten: 1. Systematik; 2. die
populären Bezeichnungen der Art; 3. Beschreibungen der Form und Farbe, Angaben zur Adult- und
Geburtskörperlänge sowie zum Körpergewicht; 4. Identifikationskriterien ım Lebensraum und
5. dessen Beschreibung; 6. Angaben zur Verbreitung und Wanderung der Art nebst einer Verbrei-
tungskarte; 7. Nahrung und Nahrungsaufnahme; 8. Verhalten; 9. Fortpflanzung und Entwicklung
sowie 10. Angaben zum Weltbestand und 11. zum Einfluß des Menschen auf die Art.

Alle, die sich für die faszinierenden Meeressäuger interessieren, können sich mit Hilfe des sehr
preiswerten Buches sachlich korrekt und spannend informieren lassen. Dieses Buch ist nicht nur als
Nachschlagewerk, sondern auch zum Schmökern sehr zu empfehlen. P. LAnGeERr, Gießen

Deutsche Gesellschaft
für Säugetierkunde: Referate,
Vorträge und Posterdemonstrationen
der 66. Hauptversammlung 1992

in Hauptziel der Deutschen Gesellschaft für Säugetierkunde ist, aufihren
Jahrestagungen über Säugetiere arbeitende Wissenschaftler verschieden-
ster Fachrichtungen zusammenzuführen, den Gedanken- und Erfahrungsaustausch
anzuregen, um so Erkenntnisse aus den einzelnen Forschungsgebieten zu
integrieren. Tagungsort der 66. Hauptversammlung der Deutschen Gesellschaft für
Säugetierkunde 1992 war das Staatliche Museum für Naturkunde in Karlsruhe.
Zu den Traditionen des Hauses gehört die enge Verbindung zum Naturschutz.
Die Tagungsthematik hatte enge Beziehungen zur Arbeit des Museums:
Paläontologie der Säugetiere, Sozialverhalten der Säugetiere und Fledermäuse.
In den Rahmen des Vortragsprogramms gehörten ferner thematisch freie
Beiträge und Posterdemonstrationen. Die Kurzfassungen der Vorträge und
Posterdemonstrationen der Deutschen Gesellschaft für Säugetierkunde sind ab der
58. Hauptversammlung 1984 in Göttingen noch lieferbar. Zu beziehen durch
jede Buchhandlung. % Deutsche Gesellschaft für Säugetierkunde. 66. Haupt-
versammlung in Karlsruhe, 20. bis 25. September 1992. Kurzfassungen der
Vorträge und Posterdemonstrationen. Herausgegeben von Hans G. PAJL
Erkert und Siegfried Rietschel. 1992. 56 Seiten. Kartoniert 24,- DM
Verlag Paul Parey - Spitalerstraße 12 - 2000 Hamburg 1 P/REV

Subscription information for USA, Canada and Mexiko obtainable from Paul Parey Scientific
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Erscheinungsweise und Bezugspreis 1992: 6 Hefte bilden einen Band. Jahresabonnement Inland: 358,-
DM zuzüglich 13,80 DM Versandkosten, Gesamtpreis 371,80 DM einschließlich 7% Mehrwert-
steuer. Jahresabonnement Ausland: 358,- DM zuzüglich 18,— DM Versandkosten. Das Abonne-
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kann bei jeder Buchhandlung oder bei der Verlagsbuchhandlung Paul Parey, Spitalerstraße 12,
W-2000 Hamburg 1, Bundesrepublik Deutschland, bestellt werden. Die Mitglieder der „Deut-
schen Gesellschaft für Säugetierkunde“ erhalten die Zeitschrift unberechnet im Rahmen des
Mitgliedsbeitrages.

Z. Säugetierkunde 57 (1992) 5, 257-320

Pareys Studientexte 66

Walter Pflumm
Biologie

der Säugetiere

Von Prof. Dr. Walter Pflumm, Kaiserslautern. Pareys Studientexte, Bd. 66.
1989. 565 Seiten mit 413 Abbildungen und 4 Tabellen. Kartoniert DM 58.-—.
ISBN 3-489-63534-5.

Im Zeitalter der Molekularbiologie und Biochemie hat die Säugstierkunge nichtanallen
deutschsprachigen akademischen Ausbildungsstätten, aber auch in den Leistungs-
kursen der reformierten Sekundarstufe den Stellenwert, der Ihr gerade in bezug auf
das direkt auf den Menschen übertragbare Wissen, zukommt. Auch fehlte es bisher
an einer geeigneten Darstellung des Stoffgebietes für die Lernenden. Diesem Defizit
will das vorliegende Buch abhelfen. Mit subjektiver Stoffauswahl und guter didak-
tischer Darbietung ist es umfangreicher als die üblichen Hochschultexte und en .
eines der am reichhaltigsten bebilderten Lehrbücher in der Biologie. |

Das Buch behandelt ausführlich die Schlüsselmerkmale der Säugetiere, z. B. die
Struktur und Funktion von Milchdrüsen und Haaren, und zwar von der zellulären
Ebene bis zum Verhalten. Darüber hinaus werden Leistungen, die im übrigen Tier-
reich nur gelegentlich vorkommen, besonders gründlich dargestellt, so die Echo-
Ortung und der Winterschlaf. Weitere Kapitel beschäftigen sich mit ontogenetischen
Problemen. Auf biochemische und biophysikalische Sachverhalte wird dann einge-
gangen, wenn es sich um für Säugetiere spezifische Leistungen handelt. — Ein Ver-
zeichnis mit Erklärungen der zoologischen Fachwörter, besonders wichtig für Leser
ohne Latein- oder Griechischkenntnisse, sowie zwei Tiernamenverzeichnisse, ein
Sachregister und ein Literaturverzeichnis machen das Buch von vielen Fragestellun-
gen her zugänglich für einen großen Leserkreis. Dazu gehören Studierende der Bio-
logie und Oberschüler der Sekundarstufe Il ebenso wie Biologielehrer, Ausbilder von
Tierpflegern und alle Natur- und Tierfreunde, die an einer umfassenden, in Wort und
Bild leichtverständlichen Darstellung von Bau und Leben der Säugetiere interessiert
sind.

Da
P/REY Berlin und Hamburg

u = ; un
NI

2

S
EN
Il

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a

Fr 5), 321-384, Dezember 1992 ISSN 0044-3468 C21274F
n |

ITSCHRIFT FÜR

rgan der Deutschen Gesellschaft für Säugetierkunde

derlund, Elisabeth; Dannelid, E.; Rowcliffe, D. J.: On the hardness of pigmented and unpigmented enamel in
»seth of shrews of the genera Sorex and Crocidura (Mammalia, Soricidae). — Über die Härte von pigmentiertem
(nd unpigmentiertem Zahnschmelz bei Spitzmäusen der Gattungen Sorex und Crocidura (Mammalia, Soricidae)

\tas, T. R. O.; Bogo, M. R.; Christoff, A. U.: G-, C-bands and NOR studies in two species of bats from Southern
3razil (Chiroptera: Vespertilionidae, Molossidae). — G-, C- und NOR-angefärbte Karyotypen von zwei Fleder-
ınausarten aus Südbrasilien (Chiroptera: Vespertilionidae, Molossidae)

«er, Carolyn M.: Observations on the postnatal behavioural development in the Marsh mongoose (Atilax
»aludinosus). - Beobachtungen über die postnatale Verhaltensentwicklung von Sumpfmangusten (Atilax paludi-
1osus)

'ners, P. E.; Roth, Kathrin; Zimmerli, Ruth: Interpreting social behaviour of Wood bison using tail postures. — Das
'nterpretieren sozialen Verhaltens von Waldbisons anhand von Schwanzhaltungen

\hard-Hansen, C.; Campan, R.: Social environment of Isard kids, Rupicapra pyrenaica p., during their ontogeny. —
Soziale Umwelt junger Gemsen (Rupicapra pyrenaica p.) aus den Pyrenäen während der Ontogenese

don, G.; Paradis, E.; Croset, H.: Capture-recapture study of a population of the Mediterranean Pine vole
\Microtus duodecimcostatus) in Southern France. — Markierungsfangstudien an einer Population der Mittelmeer-
\leinwühlmaus (Microtus duodecimcostatus) in Südfrankreich

v0, A.; De le Court, C.; Soriguer, R. C.: Evaluation of hare abundance allowed by their use of attraction points. —
'zrmittlung der Abundanz von Hasen durch Nutzung von Anziehungspunkten

„senschaftliche Kurzmitteilung

‚te, J.; Castroviejo, J.: Unusual record of the Spotted hyena (Crocuta crocuta) in Rio Muni, Equatorial Guinea
Central Africa). - Ungewöhnlicher äne (Crocuta crocuta) in Rio Muni, Aquatorialguinea
'Zentralafrika)

aanntmachungen

!hbesprechungen

erlag Paul Parey Hamburg und Berlin

321

330

335

343

351

364

373

380
382
384

HERAUSGEBERTZEDITORS

P. J. H. van BreE, Amsterdam — W. FIEDLER, Wien — H. Frick, München - W. HERRE,

Kiel - R. HUTTERER, Bonn - H.-G. Krös, Berlin - H.-J. Kunn, Göttingen — E. KuLzEr,

Tübingen - W. MaıErR, Tübingen - J. NIETHAMMER, Bonn — ©. Anne E. Rasa, Bonn -

H. REıcHsTEin, Kiel - M. Rönrs, Hannover — H. SCHLIEMANN, Hamburg — D. STARcK,
Frankfurt a. M. - E. THENnIUs, Wien -— P. VoceL, Lausanne

SCHRIETEBFLUNG /EDITORENIIOLEFL@E

D. Kruska, Kiel - P. LANGER, Gießen

This journal is covered by Biosciences Information Service of Biological Abstracts, and by Current Con-
tents (Series Agriculture, Biology, and Environmental Sciences) of Institute for Scientific Information

Die Zeitschrift für Säugetierkunde veröffentlicht Originalarbeiten und wissenschaftliche Kurzmittei-
lungen aus dem Gesamtgebiet der Säugetierkunde, Besprechungen der wichtigsten internationalen
Literatur sowie die Bekanntmachungen der Deutschen Gesellschaft für Säugetierkunde. Verantwort-
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Z. Säugetierkunde 57 (1992) 321-329
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

On the hardness of pigmented and unpigmented enamel in teeth
of shrews of the genera Sorex and Crocidura
(Mammalıa, Soricidae)

By ELISABETH SÖDERLUND, E. DAnNELID and D. J. ROWCLIFFE

Department of Physical Metallurgy and Ceramics, Royal Institute of Technology, and Department of
Zoology, Stockholm University, Stockholm, Sweden

Receipt of Ms. 15.1. 1992
Acceptance of Ms. 25. 2. 1992

The hardness of the enamel in the incisors of three species of shrew, Sorex araneus, S. minutus and
Crocidura russula, was tested using a special ultra-low load indentation instrument. Two different
measuring areas were selected; the first area was situated in the anterior part of the incisor (covered
with pigmented enamel in the Sorex spp.), the second area was in the posterior unpigmented part of
the same tooth. Large local varıations in the mechanical properties occur, and possible reasons for
these are discussed. The results do not clearly confirm any hypothesis concerning ditferences in
hardness between the pigmented and unpigmented enamel, although there is some tendency showing
the unpigmented enamel to be slıghtly harder than the pigmented.

Introduction

The teeth of most shrews ın the subfamily Soricinae are partly covered with reddish tooth
pigment. The reddish colouring is most prominent on the labial part of the teeth and on the
occlusal part of the molars. This colouring is due to the presence of ıron (DÖTSCH and von
KOoENIGSWALD 1978). The iron is confined to the outermost zone of the enamel. Pıgmented
enamel ıs also known in rodents (Mıres 1963) and also ın this case ıron is present (SELVIG
and Hase 1975). Tooth pigment was present already in some fossil shrews from the
Miocene (CRocHET 1975), but in thıs case we deal with members of another subfamily
(REUMER 1987). It has been postulated that the iron-containing enamel should be harder
than the white enamel (SELvIiG and Hause 1975) and thus function as a protection against
abrasıon (VOGEL 1984; DAnNnELID 1989). However, DÖTscH (1982, pers. comm.) suggests
that the iron-containing enamel is weaker than the unpigmented parts. The pigmented
enamel is also saıd to be more acıd resistant than the white enamel (SELvıG and HALSsE
1975). Acıd resistance was, however, outside the scope of this paper.

To the present authors’ knowledge no direct studies of the mechanical properties, such
as hardness, have been performed. This is certainly due to the difficulties of making
adequate measurements ın small volumes of material. However, a new type of sub-micron
indentation system has recently been developed (PErHıcA et al. 1983), built on the
principle of a continuous and very precise reading of load and displacement. This system ıs
particularily well suited for investigations of small specimens, such as the enamel of shrew
teeth. In this study we have measured the hardness of both types of enamel on shrew teeth
to see whether any distinction ın hardness is apparent.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5706-0321 $ 02.50/0

922 Elisabeth Söderlund, E. Dannelid and D. J. Rowchffe

Material and methods

The hardness of the incisors of the lower left Jaws of three different species of shrews, Sorex araneus,
S. minutus and Crocidura russula, was measured. The two former species have the teeth partly covered
with reddish enamel containing iron. C. russula has a very low content of iron in the enamel (VoceL,
pers. comm.) and was chosen for comparison.

The jaws were from museum specimens and therefore needed a careful treatment. They were
mounted on a specimen holder by water-soluble glue and then indented as-recieved, even though a
conventional specimen preparation wıth embedding and polishing of a cross-section would have been
preferred. Three different specimens of each species were tested. The measurements were performed
at two different positions of each incisor (Fig. 1); on an anterior part of the incisor, in the iron-

Fig. 1. Part of anterior left lower jaw of $. araneus with the measured areas indicated

containing area in the Sorex spp. or the corresponding area in C. russula (A), as well as ın a more
posterior position (B). At each position of the specimens several indentations were done, either in a
line or ın an ordered array.

The tests were performed with a special depth-sensitive indentation instrument (Nano indenter,
Nano Systems Inc., TN, USA). The construction of the equipment and methods of analysıs are
described in detail elsewhere (PETHICA et al. 1983; DOERNER and Nix 1986). A schematic diagram of
the indentation system is shown in Figure 2. The load ıs provided by a magnet and coıl assembly and
the corresponding displacement is continuously measured by the movement of the middle plate of a
three-plate capacıtance system. The depth-sensing mechanism makes optical imaging of the indenta-
tion unnecessary for the determination of the hardness, and in addition information from both the
loading and the unloading sections of the experiment is recorded. The system is computer controlled
and each indentation can be performed in an exact way by setting the approach rate, loading and
unloading rate, time of hold and maximum load or displacement. The load and displacement
resolutions are 0.3 uN and 0.2 nm, respectively.

In this study indentations were made with maximum displacements of 100 and 250 nm, ı.e. the
maximum depth of indentation ıs only a fraction of the expected thickness of the pigmented part of the
enamel of 40-50 um (Mıres 1963; VoGEL 1984). The loading and unloading rates were 10 nm/s. A
30 s hold segment (a segment during which the load is held constant for a certain period of time) was
applied at maximum load and at 90 % of unloading to check the thermal drift. The result from a single
indentation experiment is typically presented as a load-displacement curve (Fig. 3). The hardness is
calculated as the maximum load divided by the area of the indentation after subtraction of elastic
contributions.

The microstructure was studied and a qualitative elemental analysis of the enamel was done using a
scanning electron microscope (SEM - JSM-840, JEOL Ltd, Tokyo, Japan) equipped with an energy
dispersive spectrometer (EDS - LINK AN 10000, Link Analytıcal Systems Ltd, Hıgh Wycombe,
UK).

Results

The nanoindentation system is very sensitive to differences in height across the specimen,
as well as to unevennesses in the specimen surface. Nevertheless, the method of specimen
mounting worked satisfactorily as long as the indentations were placed on nearly horizon-
tal areas close to the highest point of the samples. The surfaces of the teeth at the microlevel

On the hardness of pigmented and unpigmented enamel in teeth of shrews 325

Upper
leaf
spring z-Motor
drive

Air
capacitance
displacement
gauge

Lower
leaf
spring

III NETTE RTUTNUNNUENNN

SS
N
N
N
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Frame

x-,y- Motor drives

Fıg. 2. Schematic diagram of the indentation system (from SÖDERLUND and MAcCMILLAN 1991)

Load (mN)

0 200

Displacement (nm)

Fig. 3. Typical load-displacement curve obtained from a 250 nm indentation in the unpigmented
enamel of a $. araneus specimen

Hardness (GPa)

324 Elisabeth Söderlund, E. Dannelid and D. J. Rowcliffe

are very rough (Fig. 4), but the load-displacement curves reveal any tendency of sliding of
the indenter or other abnormalıty and such indentations were then disregarded. The
thermal drift in the system was measured and was typically less than 0.05 nm/s.

Most of the hardness data lay in the regime 6-9 GPa (hereafter called the high regime)
and in some cases around 0.1-0.4 GPa (henceforth named the low regime) for a 100 nm
deep impression. Values obtained from 250 nm deep indentations were of the order 4-7
GPa or lay in the same low regime of 0.1-0.4 GPa. The hardness data obtained from one of
the $. minutus specimens lay only in the low regime. The data points in Figure 5 are the

>

BD

S. araneus C. russula S. araneus C. russula

3 2

Fig. 5. The average hardness (high regime) obtained from area A of each specimen (filled symbols) and
from area B (unfilled symbols) for the two indentation depths 100 nm (a) and 250 nm (b)

averages of the high regime values obtained at each position of each specimen. The Table
presents the mean high regime values together with one standard deviation and the number
of valid indentations. The percentage of the total number of indentations that lay ın the low
hardness regime for each region is seen in the Table. The values ın the low regime could not
be used for comparative purposes for several reasons, which are discussed in the next
section.

The SEM study revealed that the surface of the enamel was rough (Fig. 4). Commonly,
the enamel was very scratched and cracks could be seen. Occasionally the enamel had
fractured and pieces of the enamel were missing. The $. minutus specimen with hardness
values only in the low regime, seemed to be covered with a thin film. However, no
difference in composition could be detected by EDS, between areas of enamel with or
without the film. By the EDS analysis ıt was confined that the pigmented areas were rich ın
iron. In areas where the iron content was higher than the surroundings, the concentration
of calcıum was correspondingly lower. The oxygen concentration was enhanced in the
same areas as the iron.

Fig. 4. SEM micrographs of a $. araneus specimen showing (a) the microstructure of the pigmented
enamel (position A), (b) the microstructure of the unpigmented enamel (position B), and (c) two of the
indentations made in position A

326 Elisabeth Söderlund, E. Dannelid and D. J. Rowchffe

Average of hardness (high regime), standard deviation and number of indentations for the two
regions tested at each specimen

Specimen Measured Hardness Standard Number of Indentations
and area (in GPa) deviation indentations ın the low
species on tooth (in GPa) regime (% of

total number)

Indentation depth = 100 nm

. araneus 1
. araneus 1
. araneus 2
. araneus 2
. araneus 3
. araneus 3

. minutus 1
. minutus 1
. minutus 2
. minutus 2
. minutus 3
. minutus 3

.russula 1
.russula 1
.russula 2
.russula 2
.russula 3
. russula 3

vpub>u> vbpyu>u> D>u>u»>
NDONO=- DO NL DLR m OL UMIMO

5
5
5
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5
5
5
$
$
5
5
5
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. araneus 1
. araneus 1
. araneus 2
. araneus 2
. araneus 3
. araneus 3

. minutus 1
. minutus 1
. minutus 2
. minutus 2
. minutus 3
. minutus 3

EN
OO: $P$NVOOOO N PRO N

.russula 1
.russula 1
.russula 2
.russula 2
. russula 3
. russula 3

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vbpu>p>u> vb>p>u>u> D> u > ,>

Discussion

The large scatter ın the hardness data indicates a substantial inhomogeneity in the surface
properties. In particular the occurrence of the low and high hardness regimes can only be
interpreted as arısing from different materials. We suggest that the high hardness regime
reflects the hardness of more or less undamaged enamel, whereas the low hardness sites
would occur ıf the enamel was covered with a thın, soft film or locally absent and the
impressions were then being made in the underlying softer structure. For this reason the
low regime values are not considered further in thıs study.

The different mean levels of the high regime hardness values corresponding to the two

ZEITSCHRIFT FÜR
SÄUGETIERKUNDE

INTERNATIONAL JOURNAL
OF MAMMALIAN BIOLOGY

Organ der Deutschen Gesellschaft für Säugetierkunde

Volume 57, 1992 ISSN 0044-3468

Herausgeber / Editors

P. J. H. van Bree, Amsterdam - W. Fiedler, Wien —- H. Frick, München — W. Herre,
Kiel -— R. Hutterer, Bonn — H.-G. Klös, Berlin — H.-J. Kuhn, Göttingen - E. Kulzer,
Tübingen - B. Lanza, Florenz -— W. Maier, Tübingen — J. Niethammer, Bonn — Anne
E. Rasa, Bonn - H. Reichstein, Kiel — M. Röhrs, Hannover —H. Schliemann, Hamburg —
D. Starck, Frankfurt a. M. - E. Thenius, Wien — P. Vogel, Lausanne

Schriftleitung/Editorial Office

D. Kruska, Kiel - P. Langer, Gießen

Mit 136 Abbildungen

Verlag Paul Parey Hamburg und Berlin

Wissenschaftliche Originalarbeiten

ANTINucHI, C. D.; BuscH, CHRISTINA: Burrow structure in the subterranean rodent Ctenomys
talarum. — Die Struktur der Baue von Ctenomys talarum, einer unterirdisch lebenden
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BAKER, CAROLYN M.: Observations on the postnatal behavioural development ın the Marsh
mongoose (Atılax paludinosus). - Beobachtungen über die postnatale Verhaltensentwicklung
ons umpimaneusten Arlaxipalndımosus)y a. un...

BENNETT, N. C.: Aspects of the social behaviour ın a captive colony of the Common mole-rat
Cryptomys hottentotus from South Africa. - Aspekte des Sozialverhaltens einer in Gefangen-
schaft gehaltenen Kolonie des südafrikanischen Graumulls Cryptomys hottentotus ........ .

BLAUSTEIN, SILvIaA A.; LıascovicH, Rosa C.; APFELBAUM, LILIANA 1I.; DALEFFE, LiD1A;
BARQUEZ, R. M.; Reıc, O. A.: Correlates of systematic differentiation between two closely
related allopatric populations of the Akodon boliviensis group from NW Argentina (Ro-
dentia: Cricetidae). - Korrelate von systematischer Differenzierung bei zwei nahe verwand-
ten allopatrischen Populationen von Akodon aus der Boliviensis-Gruppe des Nordwestens
von Argenamen(Nodeneı, Gere eo) ee

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rosmarus rosmarus) ın northeastern Greenland, 1989-1991. - Satelliten-gestützte Telemetrie
an Atlantik-Walrossen (Odobenus rosmarus rosmarus) von 1989 bis 1991 im Nordosten
Gromlands 5 2 Dr NE EN N NEE HERD NERER ES DRRRK SH

Bowers, M. A.; CaARR, T. G.: Home range shifts accompanying breeding in the Eastern
Chipmunk, Tamias striatus (Rodentia: Sciuridae). — Verschiebungen des Aktionsraumes
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Boyz, P.; HUTTERER, R.; LÖöpEz-MARTINEZ, N.; MicHaux, ]J.: A reconstruction of the Lava
mouse (Malpaisomys insularıs), an extinct rodent of the Canary Islands. — Eine Rekonstruk-
tion der Lavamaus (Malpaisomys insularis), einem ausgestorbenen Nager der Kanarischen
Imeela 2 0000100 Pe PER MANS So NEN EEE RE EEE

COMPARATORE, VIVIANA M.; AGNUSDEI, MÖNICA; BUSCH, CRISTINA: Habitat relations in
sympatric populations of Ctenomys australis and Ctenomys talarum (Rodentia, Octodonti-

.dae) in a natural grassland. - Habitatbeziehungen bei sympatrisch lebenden Populationen
von Ctenomys australis und Ctenomys talarum (Rodentia, Octodontidae) in natürlichem
Grasland . » 0 28 ek EEE RE RER REN ER EEE

CUTRERA, R. A.; CARRENO, N. B.; CASTRO-VAZQUEZ, A.: Correlative genital tract morphology
and plasma progesterone levels during the ovarıan cycle in Corn mice (Calomys musculinus).
— Beziehungen zwischen Genitaltraktmorphologie und Plasmaprogesteronspiegel während
des ovariellen Zyklus von Maismäusen (Calomys musculinus) . .... 2.222222...

DEMPSTER, EDITH R.; PERRIN, M. R.; NUTTALL, R. ]J.: Postnatal development of three symparric
small mammal species of southern Africa. - Postnatale Entwicklung bei drei sympatrischen
Kleinsäiugeramtemaus Steine ee ee oe RT

DE OLiIVEIRA, J. A.; LORINI, MARIA Luc1a; PERSSON, VANESssA G.: Pelage varıatıon in Marmosa
incana (Didelphidae, Marsupialia) with notes on taxonomy. — Variatıon des Haarkleides von
Marmosa incana (Didelphidae, Marsupialia) mit Anmerkungen zur Taxonomie... .....

FLACHSBARTH, M. F.; SCHWARZ, R.: Zur Zytologie eines hochspezialisierten Sebozyten am
Beispiel der holokrinen Analbeuteldrüsen der Hauskatze, Felis silvestris f. catus. — The
cytology of a highly specialized sebocyte, as demonstrated in the holocrine glands of anal
Sesint:heXdomestie cat. Kelissilvestms t.catus nen

FRAGUEDAKIS-TSsOLIS, $. E.: Contribution to the study of the wild House mouse, Genus MusL.
(Mammalıa, Rodentia, Muridae) in Greece. Study of three populations based on lymphocyte
antigen analysıs. — Beitrag zu Untersuchungen an der wılden Hausmaus, Gattung Mus L.
(Mammalıa, Rodentia, Muridae) in Griechenland. Untersuchungen an drei Populationen
auferumdsyonFAnalysen mit Lymphozyten Antigenen . .....r een eesnneon.

FREITAs, T. R. ©.; Boco, M. R.; CHRISTOFF, A. U.: G-, C-bands and NOR studies in two
species of bats from Southern Brazil (Chiroptera: Vespertilionidae, Molossidae). —- G-, C-
und NOR-angefärbte Karyotypen von zwei Fledermausarten aus Südbrasilien (Chiroptera:
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GIANNONI, STELLA M.; BoRGHI, C. E.; MARTfNEZ-Rıca, ]. P.: New data on the burrowing
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GRAF, M.; Sturz, H.-P. B.; ZıswiLer, V.: Regionale und saisonale Unterschiede ın der

163

995

294

2

288

29

47

14

103

129

144

225

231

23

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GRUNDBACHER, BARBARA: Nachweis des Baummarders, Martes martes, in der neolithischen
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maärtes irom Mona... an. ee a
GUEDON, G.; PARADIS, E.; CROSET, H.: Capture-recapture study of a population of the
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fangstudien an einer Population der Mittelmeer-Kleinwühlmaus (Microtus duodecimco-
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HERRERO, J.; CANUT, J.; GARCIA-FERRE, D.; GARCIA-GONZALES, R.; HıDALGo, R.: The Alpine
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Komers, P. E.; ROTH, KATHRIN; ZIMMERLI, RUTH: Interpreting social behaviour of Wood
bison using tail postures. —- Das Interpretieren sozialen Verhaltens von Waldbisons anhand
von Schwanzhaltungen". 2.32. 0.2. ar na ee 2
LAzo, A.; DE LE CouRrT, C.; SORIGUER, R. C.: Evaluation of hare abundance allowed by their
use of attraction points. — Ermittlung der Abundanz von Hasen durch Nutzung von
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MEIA, ]J.-S.; WEBER, J.-M.: Characteristics and distribution of breeding dens of the Red fox
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MORENO, EULALIA; BARBOSA, A.: Distribution patterns of small mammal fauna along gradients
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P£REZ-ZAPATA, A.; Lew, D.; AGUILERA, M.; Reıc, ©. A.: New data on the systematics and
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PERRIN, M. R.; HucHes, ]J. J.: Preliminary observations on the comparative gastric morphology
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PERRINn, M. R.; SLoTow, R. H.; MENDELSOHN, J. M.: The population dynamics of rodents at
Settlers, Transvaal, South Africa. -— Die Populationsdynamik von Nagetieren in Settlers,
Transvaal, Sudafrika. . .. ua... cu os
PessöA, LerLa MARIA; DE OLivEIRa, J. A.; Dos Reıs, $. F.: A new species of Spiny rat genus
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PzssöA, Leıta M.; Dos Reıs, $. F.: Bacular varıation in the subgenus Trinomys, genus
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during their ontogeny. — Soziale Umwelt junger Gemsen (Rupicapra pyrenaica p.) aus den
Pyrenäen während der Ontogenese. ..........uu.. 0. el 2 er
SÖDERLUND, ELISABETH; DANNELID, E.; ROWCLIFFE, D. J.: On the hardness of pigmented and
unpigmented enamel in teeth of shrews of the genera Sorex and Crocidura (Mammalıa,
Soricıdae). - Über die Härte von pigmentiertem und unpigmentiertem Zahnschmelz bei
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affen (Cebus apella) in Gefangenschaft: Beziehungen zwischen Mutter und Jungtier vom
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193

201

364

2441

a)

973

1802

169

94

216

2

238

39

100

9

52

70

269

ZAMBELLI, A.; DYZENCHAUZ, F.; Ramos, A.; DE Rosa, N.; WAINBERG, R.; Reıc, ©. A.:
Cytogenetics and karyosystematics of phyllotine rodents (Cricetidae, Siıgmodontinae). Part
III. - Zytogenetik und Karyosystematik von phyllotinen Rodentia (Cricetidae, Sigmodonti-
DAS SOILEL1RTTIER BERESIEITNEED INNEN RE EHE

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(Mustela nivalıs). -— Morphometrische Analyse der Schädelvariation beim holarktischen
NauswaeseliMstelamivahs) en. ene Bere ae nn. ee ER ER INNE.

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155

77

179

316

310

183

380

58

56

181

118

176

25]

186

12

515

founded colony of Grey Seals (Halichoerus grypus) ın the Netherlands. - Weitere Angaben
über die Wurfperiode in einer kürzlich gegründeten Kolonie von Kegelrobben (Halichoerus

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VıruLLo, A. D.; ZuLera, G. A.: Cytogenetics and fossil record: confluent evidence for
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Fossilgeschichte: Konfluierender Nachweis für Artbildung ohne Chromosomenänderung
bei sudamerikanischen Canıdene 1. u 22 2.22 Ve A 248
Bekanntmachungen
Seitens. a ee he ML I Re De u RER 9 a 0 DER, ae ee 60, 382
Buchbesprechungen
Selten. u. BER A AN Tea EI 62, 124,190253 318334

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ISSN 0044-3468 57 (1-6) 1-384 (1992)

On the hardness of pigmented and unpigmented enamel in teeth of shrews 927,

indentation depths, 100 nm and 250 nm, stem from the fact that hardness determined by
an indentation method shows a strong increase with decreasing indentation depth (see tor
example, Burr et al. 1989). Therefore, the 100 nm values are larger than the 250 nm values
and neither of the data sets can be directly compared with micro- or macro-hardness (bulk)
values. Due to the indentation sıze effect only values obtained from indentations with the
same maximum indentation depth should be compared in detail.

In C. russula, which has unpigmented teeth, only ın one test out of six was there any
significant difference in hardness between the two areas investigated. This uniformity is as
expected. In the Sorex spp., however, clear differences occasionally occur. With an
indentation depth of 100 nm, one specimen of Sorex araneus showed a distinctly harder
white enamel. In Sorex minutus there was one specimen with harder unpigmented enamel
and one specimen with harder pigmented enamel.

The third specimen of $. minutus showed a hardness of the pigmented area which was
almost exclusively sıtuated in the low regime (four different positions were investigated
with 39 indents and only 1 showed high regime hardness). When the indentation depth
increased to 250 nm, most Sorex specimens showed a harder white enamel. In all cases
except two, when going from 100 nm deep to 250 nm deep indentations, the region A
showed a relative decrease ın hardness as compared to region B. This might be due to an
increased influence from the softer underlying substrate, or a decreased influence from a
soft film. No obvious difference in hardness between the red enamel of S. araneus and
S. minutus could be seen from out tests though S. araneus has a clearly darker pigment than
S. minutus.

The large varıations in hardness, both within a single specimen (reflected as a substantial
standard deviation) as well as between specimens of the same species, may have several
possible reasons. One is of course that the teeth may be considerably worn at one or more
of the measuring areas. However, all the specimens were first year anımals without
apparent tooth wear (all specimens were checked in a dissecting microscope before
fixation, to avoıd severely worn teeth). Kozawa et al. (1988) have proposed that the iron
may exist in three different forms ın the pigmented enamel]; fırstly, as an amorphous ferric
oxıde around the hydroxyapatıte crystallites, secondly as ıron atoms in the hydroxyapatıte
lattice, and thırdly as crystalline iron oxide on the crystal surface. In the first of these, the
pigmented enamel may well be weaker than the unpigmented; in the second case probably
harder, since the iron ıons are smaller than the calcıum ıons, which (with constant charge)
means denser packing and shorter bond lengths (Vincent 1990). The EDS analysıs
performed by us indicates that some iron probably substitutes for calcıum in the apatıte
structure. The observed higher level of oxygen could indicate that some iron is also present
in the form of iron oxıde. Kozawa et al. (1988) also found a variable Ca/P ratio in the
enamel of the Sorex specimens (compared to human enamel and F-apatite) which suggests a
non-uniform composition of the enamel crystallites. Furthermore, they observed the
existence of carbonate in the unpigmented enamel and in microareas of the pigmented
enamel, which may indicate a low degree of crystallinity in the enamel. This would
possıbly affect the hardness and give rise to local varıations.

Thus the results do not confirm the hypothesis that iron-containing pıgmented enamel
should be harder than unpigmented. The local varıations in enamel hardness within a
specimen as well as the varıations between specimens are larger than any clear ditferentia-
tion in hardness due to presence of iron in the enamel.

Finally, a harder material ıs usually more resistant to abrasion, but for ceramic materials
this ıs not always true. An increased hardness might lower the threshold load above which
cracking (median and lateral) and chipping, and a corresponding severe wear, occur (EvAnS
and MarsHaLL 1980). For loads below the fracture threshold, no cracking occurs and the
ceramic is worn by a plastic cutting mechanism, the volume removal rate of which is about
one order of magnitude lower than that associated with the lateral fracture mechanısm.

328 Elisabeth Söderlund, E. Dannelid and D. J. Rowchffe

Accordingly, a lowered hardness might cause a transformation from a severe wear
mechanism, to a milder wearing. Another important parameter, that will also strongly
affect the threshold load and determine the wear rate, is the fracture toughness (a measure
of the resistance to crackıng). We have not taken the fracture toughness into consideration
in this investigation, however, there might be possible toughening effects due to the three
postulated different occurrences of iron in the pigmented enamel.

Both the pıgmented and the unpigmented enamel of all specimens show large local
variations in hardness. The nanoindentation hardness for a 100 nm deep indent usually is
6-9 GPa or 0.1-0.4 GPa depending on which region measured. The variation in the results
may be explaiıned by different forms of iron in the pigmented enamel, by varying
composition of the apatite crystallites, by a varying degree of crystallinity in the enamel as
well as by the local wear status. However, there ıs no clear difference in hardness between
the pıgmented and the unpigmented enamel, even though there is some tendency showing
that the unpigmented enamel ıs slightly harder than the pigmented.

The nanoindenter system is well suited for this type of investigation since it can obtain
information from near surface regions of the order of 1 um. This particular material shows
variations in the local properties larger than in synthetic hydroxyapatite, and uniformly
polished surfaces and cross-sections would therefore be needed for a more thorough
investigation.

Acknowledgements

We are indebted to the Swedish Museum of Natural History for providing us with specimens. Dr
Kristin BREDER and Dr ANDERS ANGERBJÖRN are gratefully acknowledged for reading through the
manuscript and giving their valuable suggestions. We would like to thank Nırs Lange for comment-
ing on the EDS work. Finally Mrs Bısgr MAYRHOFER has helped us with part of the illustrations.

Zusammenfassung

Über die Härte von pigmentiertem und unpigmentiertem Zahnschmelz bei Spitzmäusen der
Gattungen Sorex und Crocidura (Mammalıa, Soricidae)

Die Härte des Zahnschmelzes ın den Schneidezähnen von drei Spitzmausarten, Sorex araneus, S.
minutus und Crocidura russula, wurde mit einem speziellen Gerät getestet, welches den Zahn einer
äußerst geringen Belastung aussetzt. Zwei verschiedene Regionen wurden vermessen, die erst in dem
vorderen Teil der Schneidezahnes (bei den Sorex-Arten mit pigmentiertem Zahnschmelz überzogen),
die zweite in der hinteren, unpigmentierten Region desselben Zahnes. Es bestehen große lokale
Unterschiede in den mechanischen Eigenschaften und mögliche Ursachen dafür werden diskutiert.
Die Resultate bekräftigen keine Hypothese über Unterschiede in der Härte des pigmentierten
gegenüber dem unpigmentierten Zahnschmelz. Es gibt jedoch eine Tendenz dahin, daß der unpigmen-
tierte Zahnschmelz etwas härter ıst als der pigmentierte.

References

Buus, $. ]J.; PAGE, T. F.; YoFFE, E. H. (1989): An explanation of the indentation size effect. Phil. Mag.
Lett. 59, 281-288.

CROCHET, ].-Y. (1975): Diversit€ des insectivores soricides du miocene inferieur de France. In:
Colloque international C.N.R.S. 218. Probleme actuels de paleontologie. - Evolution des
vertebres. Pp. 631-652.

Dannerip, E. (1989): Medial tines on the upper incisors and other dental features used as identifica-
tion characters in European shrews of the genus Sorex (Mammalıa, Soricidae). Z. Säugetierkunde
54, 205-214.

DoERNER, M. F.; Nıx, W. D. (1986): A method for interpreting the data from depth-sensing
indentation instruments. J. Mater. Res. 1, 601-609.

DörscH, C. (1982): Der Kauapparat der Soricidae (Mammalıa, Insectivora). Funktionsmor-
phologische Untersuchungen zur Kaufunktion bei Spitzmäusen der Gattungen Sorex Linnaeus,
Neomys Kaup und Crocidura Wagler. Zool. Jb. Anat. 108, 421-484.

DörtscH, C.; KoENIGSwALD, W. von (1978): Zur Rotfärbung von Soricidenzähnen. Z. Säugetier-
kunde 43, 65-70.

On the hardness of pigmented and unpigmented enamel in teeth of shrews 929

Evans, A. G.; MARSHALL, D. B. (1980): Wear Mechanısms in Ceramics. In: Fundamentals of Friction
and Wear of Materials. Ed. by D. A. Rıcney. Metals Park, Ohio: American Society for Metals.
Pp. 439-452.

KozawA, Y.; SAKAE, I.; MısHIMA, H.; BARCKHAUS, R. H.; KreErting, E. R.; SCHMIDT, P. F;;
Hönrrıng, H. J. (1988): Electron-microscopic and microprobe analyses on the pigmented and
unpigmented enamel of Sorex (Insectivora). Histochemistry 90, 61-65.

Mırgs, A. E. W. (1963): Pıgmented Enamel. Proc. Roy. Soc. Med. 56, 32-39.

PETHIca, ]J. B.; HurcHincs, R.; OLIVER, W. C. (1983): Hardness measurement at penetration depths
as small as 20 nm. Phil. Mag. A 48, 593-606.

SELVIG, K. A.; Hause, A. (1975): The ultrastructural localızation of iron in rat incisor enamel. Scand.
]. Dent. Res. 83, 88-95.

REUMER, J. W. F. (1987): Redefinition of the Soricidae and the Heterosoricidae (Insectivora,
Mammalia), with the description of the Crocidosoricinae, a new subfamily of Soricidae. Rev.
Palebiol. 6, 189-192.

SÖDERLUND, E.; Macmıtlan, N. H. (1991): Analysıs of the differential (alternating current)
technique for measuring Young’s modulus during ultra-low load indentation. J. Mat. Scı. Lett. 10,
720-722.

VINCENT, J. (1990): Structural Biomaterials. Princeton, New Jersey: Princeton University Press.

VocGeL, P. (1984): Verteilung des roten Zahnschmelzes ım Gebiß der Soricidae (Mammalıa, Insectiv-
ora). Revue suisse Zool. 91, 699-708.

Authors’ addresses: ELISABETH SÖDERLUND, and Davıp J. ROWCLIFFE, Department of Physical
Metallurgy and Ceramics, Royal Institute of Technology, S-100 44 Stockholm;
ERLAND DANNELID, Department of Zoology, University of Stockholm, $-106 91
Stockholm, Sweden

Z. Säugetierkunde 57 (1992) 330-334
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

G-, C-bands and NOR studies in two species of bats from
Southern Brazil (Chiroptera: Vespertilionidae, Molossidae)

By T.R. ©. Frertas, M. R. Boco, and A. U. CHRISTOFF

Departamento de Genetica, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil

Receipt of Ms. 24. 2. 1992
Acceptance of Ms. 16. 6. 1992

Abstract

Described the karyotypes of two species of bats from Southern Brazil, Eptesicus brasiliensis (2n = 50;
AN = 48) and Molossus molossus (2n = 48; AN = 54). The study of E. brasiliensis was based in seven
males and seven females, while that of M. molossus included three males and 13 females. All autosomal
chromosomes of E. brasiliensis are acrocentric, while M. molossus presents four pairs of submetacen-
trıcand 19 pairs of acrocentric chromosomes. Both species present an acrocentric Y chromosome; the
X is submetacentric in E. brasiliensis and metacentric ın M. molossus. The G-bands of E. brasiliensis do
not differ markedly from those reported for other species of Eptesicus. M. molossus, however, presents
a rather different G-pattern from those of other species of the same family. As for the C-bands, the
results for both species are not remarkably different from those of other species of the same families.
E. brasiliensis and M. molossus show a nucleolus organızing region (NOR) in only one pair, the one
that presents a secondary constriction near the centromere.

Introduction

The bats present in the Southern Brazilian state of Rio Grande do Sul inhabıt an area
between two subregions of the Neotropical region, the Brazilian Highlands and Coast, and
Patagonıia. Eleven species of the family Vespertilionidae and eight of the Molossidae have
been reported to live in the state (SıLva 1985). This work deals with Eptesicus brasiliensis
(Vespertilionidae) and Molossus molossus (Molossidae), bats which are distributed over all
South America (KoopmAn 1982). Previous studies on these species report a diploid
number (2n) equal to 50 for E. brasiliensis (Anno et al. 1977; WırLıams 1978; BICKHAM
1979; VOLLETH 1987), and 2n = 48 for M. molossus (BAKER and Lopez 1970; WARNER etal.
1974), but no chromosome bands or NOR observations were made on them. The objective
of this study was to fill this gap in our knowledge.

Material and methods

Fourteen specimens of Eptesicus brasiliensis (Desmarest, 1819) were studied, seven males and seven
females from Fazenda Cagapava, in Taim’s Ecological Station (32° 32’S; 52° 32’W). The sample of M.
molossus (Pallas, 1766) is constituted by 16 specimens, two males and 10 females from this same place,
one male from Porto Alegre (30° 10’S; 51° 15’W), and three females from Torres (29° 21'S; 49° 46'W),
all localities in the Brazilian state of Rio Grande do Sul.

LEE and Erper’s (1980) technique was employed in the bone marrow chromosome preparations.
The G-bands were induced following SEABRIGHT’s (1971) method with the modifications proposed by
Patron and Baker (1978), while the C-band patterns were obtained with Sumner’s (1972) technique.
The NOR observations were made using HowELL and BLack’s (1980) method.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5706-0330 $ 02.50/0

G-, C-bands and NOR studies in two species of bats from Southern Brazil 331
Results

Eptesicus brasiliensis presented 2n = 50 with an autosomal arm number (AN) equal to 48.
Figure 1a shows the standard karyotype of this species. All the autosomes are acrocentric,
roughly classıfiable ın large (pairs 1 to 15), median (pairs 16 to 21), and small (pairs 22 to
24) chromosomes. The X ıs a median submetacentric and the Y is a small acrocentric.
Figure 1b presents the patterns of constitutive heterochromatin for this species. There are
well defined, small C-bands in pairs 3 to 8, 10 to 13, 16, 18, 20 and 21, representing 58 %
of the autosomes with marked centromeres. The X chromosome also has a C-band, while
the Y is totally heterochromatic. G-bands are shown in Figure Ic, while Figure 1d presents
the nucleolar organızer region ın pair 14, which has a secondary constriction near the
centromere (Fig. 1a).

M. molossus has 2n = 48 and AN = 54. Conventional staining (Fig. le) shows four pairs
of submetacentric chromosomes, pair 1 being the larger; the other three are median
submetacentrics, while the remaining autosomes are all acrocentric. Pairs 22 and 23 are
very small compared to the rest of the karyotype. The X chromosome is a median
metacentric, a little larger than pairs 2-4, while the Y is a small acrocentric. C- and G-band
patterns are shown ın Figures If and 1g, respectively. C-bands occur in almost all
autosome pairs, the exception being pair 7, and in the X. The nucleolar organizer region
(Fig. 1h) occurs in pair 8 at the secondary constriction near the centromere.

Discussion
Eptesicus brasiliensis

The genus Eptesicus comprises about 30 species worldwide (Emmons 1990). Approxi-
mately 50% of them present 2n = 50 and AN = 48 (Anno et al. 1977; WıLLıams 1978;
ZımA 1982; VOLLETH 1987; VARELLA-GARCcIA et al. 1989), but others show reduced
chromosome numbers (for instance, E. capensis with 2n = 32, AN = 50; E. zulensis wıth 2n
= 28, AN = 48). Species with different chromosome numbers, however, are morphologi-
cally sımilar (McBee et al. 1986; McBee et al. 1987; MoRALES et al. 1991). We found 2n =
50 and AN = 48 for E. brasıliensis from Rio Grande do Sul, thus agreeing with BICKHAM
(1979) who found the same numbers studying specimens from the Nearctic region.

No remarkable differences were found between the G-bands presented here and those
found by ZımaA (1982) in E. nılssoni. This fact, and the relatıve constancy in chromosome
numbers, demonstrates that this genus is chromosomically conservative. In relation to the
C-bands, we found only 58% of autosome pairs marked, while Anno et al. (1980)
determined low quantities of constitutive heterochromatin for other species of Vesper-
tlionidae. Only pair 12 of E. brasıliensis showed a nucleolar organızer region, ın
accordance with the findings ın E. serotinis (VOLLETH 1987).

Molossus molossus

Five diploid numbers were reported within the family Molossidae: 2n = 34, 38, 40, 42, and
48 (BAKER et al. 1982; VARELLA-GARCIA et al. 1989). The 2n = 48 karyotype ıs the most
frequently found. WARNER et al. (1974) found 2n = 48 and AN = 58, while BAkER and
Lopez (1970) reported 2n = 48 and AN = 56 for M. molossus ot North and Central
America, respectively. We observed 2n = 48, AN = 54. This suggests varıation due to
pericentric ınversions, but since no bandıng was performed ın these earlier studies, we
cannot be sure about that.

For the C-bands, our results are not too different from those reported by MORIELLE-
VERSUTE et al. (1991). These authors studied two species of the genus Molossops: M.

332 T. R. ©. Freitas, M. R. Bogo, and A. U. Christoff

an nn an nannanlÄh xx Ka un

an an an An n0 an IT: an

an 0 n0 an na = an

on an Pr ._ TR
19 21 22 23 24

si; ö“ Mr as u# a
ET a6 TE -ä as

11 12 14 15
an »d sau te as
18 19 20 21 22

‚a

Fig. 1. Chromosomes of E. brasiliensis. A: Standard bone marrow Giemsa stained karyotype; B: C-
bands; C: G-bands; D: NOR identification. E-H: Chromosomes of M. molossus. E: Giemsa stained
karyotype; F: C-bands; G: G-bands; H: NOR identification

G-, C-bands and NOR studies in two species of bats from Southern Brazil 999

abrasus and M. temminckü. Both showed C-bands in all centromeres. Additionaly M.
abrasus presented a C-band in the telomeric region of the short arms of the largest
acrocentric pair, and M. temminckii a C-band in the satellite region of the short arm of a
large acrocentric pair. We found in Molossus molossus blocks of pericentromeric constitu-
tive heterochromatin in 22 of the 23 autosome pairs and in the X. However, this species
presents rather different G-bands from those reported for M. abrasus and M. temmincku.
In addition, nucleolar organızing regions were found in one pair in M. molossus while M.
abrasus presented such regions ın five small chromosomes, and M. temminckü ın three
pairs.

Acknowledgements

We thank Drs. MARGARETE $. MATTEVI, Lu1z F. B. OLıvEira, Rıvo R. FisHER and Francısco M.
SALZANO for valuable comments on the manuscript, ADRIANA GaAva for drawing the figures, and
CARLA FREITAS for revising the English version. Thanks are also due to Instituto Brasileiro do Meio
Ambiente for allowing the work in the Estagäo Ecolögica do Taim. This research has been sponsored
by grant no. 409272/87 of Conselho Nacional de Desenvolvimento Cientifico e Tecnolögico.

Zusammenfassung

G-, C- und NOR-angefärbte Karyotypen von zwei Fledermausarten aus Südbrasilien
(Chiroptera: Vespertilionidae, Molossidae)

Es werden Standardkaryogramme sowie G-, C- und NOR-gefärbte Metaphasen von zwei Fleder-
mausarten aus Südbrasılien beschrieben. Je 7 Männchen und Weibchen von Eptesicus brasiliensis
(Vespertilionidae) und 3 Männchen und 13 Weibchen von Molossus molossus (Molossidae) wurden
untersucht. Die cytogenetische Analyse ergab 2n = 50 and AN = 48 für E. brasiliensis and 2n = 48 and
AN = 54 für M. molossus. Bei E. brasiliensis sınd alle Autosomen akrozentrisch; M. molossus weist 4
Paare submetazentrischer und 19 Paare akrozentrischer Chromosomen auf. Beide Arten haben ein
akrozentrisches Y-Chromosom, das X-Chromosom ist submetazentrisch bei E. brasiliensis and
metazentrisch bei M. molossus. Die Muster der G-Bänder bei E. brasiliensis unterscheiden sich nıcht
von denen anderer Eptesicus-Arten. Dagegen unterscheidet sich M. molossus deutlich von anderen
Arten der Familie. Beı den C-Bändern ergaben sich keine wesentlichen Unterschiede. Bei beiden
Arten ließen sich NORs nur in einem Chromosom anfärben, welches eine sekundäre Einschnürung in
der Nähe des Centromers aufweist.

References

AnDo, K.; TAaGawa, T.; UcHiDa, T. A. (1977): Consideration of karyotypic evolution within
Vespertilionidae. Experientia 33, 877-879.

Anno, K.; TaGawa, T.; UcHIDa, T. A. (1980): The C-banding of Japanese species of vespertilionine
bats (Mammalıa: Chiroptera). Experientia 36, 653-654.

BAKER, R. ].; LoPEz, G. (1970): Karyotypic studies of the insular populations of bats on Puerto Rico.
Caryologia 23, 465-472.

BAKER, R. J.; HAıpur, M. W.; RosBıns, L. W.; CADENA, A.; Koor, B. F. (1982): Chromosomal
studies on South American bats and their systematic implications. In: Mammalıan Biology in
South America. Ed. by M. A. Mares, and H. H. GEenowars. Pittsburgh Special Publication
Series. Pymatuning Laboratory of Ecology, Univ. Pittsburgh. Vol. 4, 303-327.

BicKHAM, J. W. (1979): Chromosomal varıation and evolutionary relationships of vespertiolionid
bats. J. Mammalogy 60, 350-363.

Emmons, L. H. (1990): Neotropical rainforest mammals, a field guide. Chicago: Chicago University
Press.

Howe, W. M.; Brack, D. A. (1980): Controlled silver-staining of nucleolus organızer regions with
a protective colloidal developer: a 1-step method. Experientia 36, 1014-1015.

Koopman, K.F. (1982): Biogeography of bats of South America. In: Mammalian Biology in South
America. Ed. by M. A. Mares and H. H. Genoways. Pittsburgh Special Publication Series.
Pymatuning Laboratory of Ecology, Univ. Pittsburgh. Vol. 4, 327-332.

LEE, M. R.; ELDER, F. F. B. (1980): Yeast stimulation of bone marrow mitosis for cytogenetic
investigation. Cytogenet. Cell Genet. 26, 36-40.

McBe£, K.; BickHaAm, J. W.; YENBUTRA, $.; NABHITABHATA, J.; SCHLITTER, D. A. (1986): Standard
karyology of nine species of vespertilionid bats (Chiroptera: Vespertilionidae) from Thailand.
Ann. Carnegie Mus. 47, 361-383.

McBeE, K.; SCHLITTER, D. A.; Rosgins, R. L. (1987): Systematics of African bats of the genus

334 T. R. ©. Freitas, M. R. Bogo, and A. U. Christoff

Eptesicus (Mammalia: Vespertilionidae). 2. Karyotypes of African species and their generic
relationships. Ann. Carnegie Mus. 56, 361-383.

MORALES, J. C.; BALLINGER, $. W.; BICKHAM, J. W.; GREENBAUM, I. F.; SCHLITTER, D. A. (1991):
Genetic relationships among eight species of Eptesicus and Pıipistrellus (Chiroptera: Vesper-
tilionidae). J. Mammalogy 72, 286-291.

MORIELLE-VERSUTE, E.; VARELLA-GARCIA, M.; TADDEI, V. A. (1991): Variacgäo cromossömica no
genero Molossops (Molossidae, Chiroptera). Rev. Bras. de Genetica 14 (3, suppl.), 60.

PATToN, J. C.; BAKER, R. J. (1987): Chromosomal homology and evolution of phyllostomatoid bats.
Rev. Sys. Zool. 27, 449-462.

SEABRIGHT, M. (1971): A rapıd bandıng technique for human chromosomes. Lancet 2, 971-972.

Sırva, F. (1985): Guia para determinagäo de morcegos: Rio Grande do Sul. Porto Alegre: Martins
Livreiro.

SUMNER, A. T. (1972): A simple technique for demonstrating centromeric heterochromatin. Exp. Cell
Res. 75, 304-306.

VARELLA-GARCIA, M.; MORIELLE-VERSUTE, E.; TADEL, V. A. (1989): A survey of cytogenetic data on
Brazilian bats. Rev. Bras. Genetica 12, 761-794.

VOLLETH, M. (1987): Difference in the location of nucleolus organizer regions in European vesper-
tulionid bats. Cytogenet. Cell Genet. 44, 186-197.

WARNER, J. W.; PATTON, J. L.; GARDNER, A. L.; BAKER, R. J. (1974): Karyotypic analysıs of twenty-
one species of molossid bats (Molossidae:Chiroptera). Can. J. Genet. Cytol. 16, 165-176.

Wiırrıams, D. F. (1978): Taxonomic and karyologic comments on small brows bats, Genus Eptesicns,
from South America. Ann. Carnegie Mus. 47, 361-383.

Zıma, J. (1982): Chromosomal homology in the complements of bats of the family Vespertilionidae.
II. G-band karyotypes of some Myotis, Eptesicus and Pipistrellus species. Folia Zoologica 31,
31-36.

Authors’ address: THALES RENATO ©. FREITAS, MAURICIO R. BoGo, and ALEXANDRE U. CHRISTOFF,
Departamento de Genetica, Universidade Federal do Rio Grande do Sul, Caixa
Postal 15053, 91501 Porto Alegre, RS, Brazil

Z. Säugetierkunde 57 (1992) 335-342
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Observations on the postnatal behavioural development in the
Marsh mongoose (Atılax paludinosus)

By CAROLYN M. BAKER

Zoology Department, University of Durban-Westville, South Africa

Receipt of Ms. 27. 1. 1992
Acceptance of Ms. 27. 3. 1992

Abstract

Marsh mongooses (Atılax paludinosus) are solitary, nocturnal herpestines. This study describes
postnatal behaviour patterns in naturally reared and hand-raised anımals. First appearance of nine
different categories was recorded. Comparisons were made with postnatal behavioural development in
other herpestines, in order to assess to what extent it reflects the phylogeny of the subfamily.

Introduction

Postnatal physical development in marsh mongooses is documented (FREsE 1980; BAKER
and MEESTER 1986), but there ıs no literature on postnatal behavioural development.
Unlike the more sociable Herpestinae, Atılax ıs soliıtary and shows no co-operative
behaviour in raising young. Differences in the development of postnatal behaviour patterns
amongst herpestines may be attributed to their dıvergent rearıng systems. In order to
investigate this suggestion, this study describes postnatal behaviour patterns of both
naturally reared and hand-raised Atılax, and compares ıt with the rate and pattern of
development ın other herpestines.

Material and methods

The thirteen anımals here reported on originated from five captive matings and two wild matings.
Naturally reared mongooses were maintained in outdoor enclosures measuring 1.5 x 3x 1.2 m, while
hand-raised anımals were reared indoors in aroom measuring 2 x 3 m. The milk formula fed to hand-
reared anımals consisted of one part tinned, evaporated, unsweetened milk (brand name Carnation) to
two parts of water. To each 500 mls of constituted milk compound, 5 mls of glucose and 2 mis of
multivitamin syrup (brand name Vi-daylın) were added. Mongooses were bottle-fed, using miniature
(30 ml capacity) glass bottles with rubber teats, at three- or four-hourly intervals for the first 14 days,
and thereafter at four-hourly intervals during daylıght hours only, untıl weaning commenced. During
weanıng feeds were spaced at five-hourly intervals. First solids offered to the mongooses were finely
chopped oxheart and chicken. Naturally reared anımals were undisturbed and entirely raised by their
mother.

First appearance of behaviour patterns were recorded and descriptions of the patterns were made.

Results

Table 1 provides details of the mongooses described in this study. Concern over the
survival of the young in the presence of the father prompted removal of two of the four
male mongooses from the females as soon as pregnancy was established (BAKER and
MEESTER 1986). As a result these lıtters (Al and E2) were exclusively reared by the mother.
On three other occasıons the males had access to the females during parturition. Firstly

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5706-0335 $ 02.50/0

336 Carolyn M. Baker

(litter B1), the male remained ın the enclosure for three days after parturition but was
excluded from the “nursery nestbox” by the female and played no role in rearing the
offspring. Secondly (litter E1), three young were born, one of which was killed and eaten
by the mother who was agitated by the presence of a male and female. The remaining two
offspring survived as a result of hand-rearing. On the third occasion (litter G1) two young
were removed for hand-raising when their littermate was found dead.

Table 1. Details of the animals from which data were gathered

Litters Mating Offspring Natural (N)/
Hand-reared (H)

Al Captıve
Bl Captive

El Captive
2 Captive
Gl Captive
- Wild
- Wild

Parturition occurred at nıght (between 18.30 h and 03.00 h), and in one instance (litter
El) ıt lasted 4.5 hours. The mother ate little or nothing of the normal food provided on the
nıght of parturition. While activity patterns were normal until the evening of parturition,
the female remained comparatively inactive during the birth, and remained within the
nestbox. Nesting material was not used and on the completion of the birth the female
remained with the young.

Maternal care involved suckling, stimulating excretion, protection and transmitting
skills to the young. In the first few weeks the mother prompted elimination by licking the
ano-genital region of her young, and then consumed the products. If the mother became
agitated or was disturbed when she had a very young litter, she usually picked up a single
youngster in a neck-grip or scruft-hold, and ran about the cage as if attempting to escape
from the source of “danger’.

In naturally reared litters, young became mobile outside the nestbox on day 23 at the
earliest, but more commonly this happened only by day 28. As soon as exploration began,
the mother kept a close watch over the young and, in the event of ‘danger’, she retrieved
them by means of a scruff-hold, transporting them to the safety of the nestbox. As the
young matured they became less docile and attempted to re-emerge as soon as the mother
had retrieved them. On these occasıons she simply blocked the nestbox entrance or held
the young by the scruff until the “danger’ had passed. By day 61 the young avoıded
retrieval by the scruff-hold, and the mother attempted to ‘herd’ them back to safety. When
‘herding’ the mother directed the young by moving quickly beside them and nudging them
forwards.

Table 2 provides details of the onset of behaviour patterns exhibited by both naturally
reared and hand-reared mongooses. Apart from sucking and attention vocalizations (the
attention call and grizzling), crawling and inefficient scratching, the alarm response was the
earliest behaviour pattern to emerge. The feeding growl coincided with the development of
weaning. Play became apparent as locomotory capacities improved, while the development
of scent-marking was closely followed by the onset of cackle vocalizations. Sıbling fighting
and copulatory behaviour were the last behaviour patterns to develop.

While crawling was the first locomotory activity recorded, it was inefficient for the fırst
few days. Young mongooses were scarcely able to lift the belly off the ground, and
movement was shaky. Direction was random and only short distances were traversed. The
grizzle vocalization accompanied all early forms of locomotion.

Behavioural development in the Marsh mongoose 337

Table 2. Average age (in days) of first appearance of postnatal behaviour patterns in Atilax
paludinosus

Behaviour Naturally-reared Hand-reared Significance
Mean age (days) Mean age (days) (p = 0.05)

Vocalizations
Attention 0-38
Grizzle )
Food 5 9353
Cackle 59
Humph
Bray

I
DAN

BBDB 5

Locomotion
Crawl
Run
High-sit

Grooming
Scratch
Fleaing
Lick

Alarm

Feeding
Wean
Throw
Prey kill (rodent)
(crab)

N a w

BBBB
u |

Marking
Urination A SD=0; no t-test
Defaecatıon

Anal marking
Cheek marking

Play
Biting
Dyadic
Object
Mounting

t=0 NS
t=-0.29 NS

NN

SBsB255B

Copulation

Sıbling fightng > SD=0; no t-test

In hand-raised mongooses grooming developed early, but scratching was inefficient
during the first few days. By day 29 scratching was well co-ordinated. The fleaing response
(EWER 1963) resulted from rubbing the mongooses on either the tail base or the shoulder/
neck area. Grooming was deemed effective from day 36 when the mongooses began
tending to their pelage more carefully. Data regarding the development of grooming in
naturally reared animals are lacking due to their confinement in the nestbox during the first
few weeks.

The fear response involved several behavioural components, including mouth opening,
a harsh abrupt expiration, and freezing (tonic immobility). One or more of these patterns
occurred when the young were suddenly disturbed. The onset of the alarm response
coincident with eye opening indicated that the stimulus was visual.

The beginning of weanıng varıed from day 29 to day 40 ın naturally raised mongooses,
and was not significantly different from the onset in hand-raised anımals (Tab. 2). It was
followed by a rapid increase in solid food intake. Suckling did not stop at the commence-
ment of weaning, but was phased out over a long period, with some young still sucking the

338 Carolyn M. Baker

mother’s teats until day 108. The sucking response was particularly well-developed, as
shown by a pair of hand-raised mongooses (EA and EB) that sucked on each other’s
genitalia in the absence of the mother’s teats. This continued well beyound weaning, and
was still observed when the pair (a male and a female) were ten months old.

When presented with live small mammal prey at 67 days of age (white mice) naturally
raised young (AA, AB, AC) seemed unaware of the method of prey capture. The mother
initially caught and killed the prey wıthin view of her oftspring, and then encouraged them
to take it from her by shaking her head and drawing attention to the food. She relinquished
the prey as soon as the young showed interest, and even appeared to encourage food envy
by pulling away if interest in ıt waned. When live prey were introduced 30 days later, the
mother held back and allowed the young to investigate it, and also attempt killing. Killing
was not immediately achieved, and the young were more interested ın playing with the
injured anımal. After approximately 20 min the mother dispatched the prey, and by virtue
ot her interference promoted food envy and consumption. Prey capture and killing was
only achieved on day 135 ın these mongooses. While naturally raised EC and ED captured
their first prey at 102 days, killing was achieved incidentally over a long time by shaking
and injuring the mice. Hand-raised mongooses (EA and EB) were given live prey at 140
days. The mice were bitten in the head region and killed ın approxımately 30 seconds, and
then played with prior to consumption. Both hand-raised and naturally reared young
began to eat from the anterior end. First encounters with Xenopus were different in that
both naturally reared and hand-raised young encountered frogs in the ponds between 80
and 89 days, and immediately began to search for them by feeling over the pond substrate.
When the frog was captured, possession was maintained by “hip-slamming’ and growling.
Although a killing bite was not administered, the young dealt with the prey in adult
fashion (BAKER 1989).

The throwing response relates to the method used by some mongooses in immobilising
crabs, as well as ın egg-breaking. Throwing matured over approximately one month. It
began with holding and fiddling with an object between the forefeet, with the mongoose
lying either on its side or on its ventral surface; it progressed to lifting the object in the
bipedal stance; then to dropping it often accıdentally; and finally the intention of
downward throwing developed. The discovery of the food content of the eggs was revealed
by accidental egg-breaking in hand-raised mongooses, and by the mother breaking them
open for her young in natural circumstances.

Discussion

Mortality in marsh mongoose litters has been recorded at Berlin Zoo by Frese (1980).
Factors contributing to the deaths were suggested to be the presence of a conspecific of the
same sex or lack of experience of the mother. While the effect of the presence of a male
during parturition and the subsequent early development of the young was a cause for
concern, it appeared that from eight weeks onwards the young and their mother suffered
no ill-effects from the re-introduction of the male. The present study confirmed the
adverse effects of the presence of more than one conspecific other than the mother (i.e. a
male and a female) on the survival of a litter during parturition. On the other hand the
presence of a single male during parturition and the following few days appeared to have
no ill-effects. The male clearly did not participate in rearing the young, however, and it is
unlikely that a male marsh mongoose which was actively avoided in the natural environ-
ment would remain in the vicinity of a mate with young. Exclusively maternal care seems
more likely. The solitary nature of marsh mongooses, and the general lack of co-operative
behaviour patterns, suggest that females habitually rear young in the absence of a partner.
This contrasts strongly with the “helper” system which predomination in the more social

Behavioural development in the Marsh mongoose 339

mongooses (dwarf mongooses — Rasa 1989; suricates — EwER 1963; banded mongooses —
Roop 1974).

In the nocturnal marsh mongoose the adaptıveness of parturition at night is clear, ın
that it would allow the mother to remain with her young for the daylight period following
birth and perhaps longer, as the nourishment provided by the placental material is adequate
to her needs for the first day. Further, the presence of the mother provides both security
and nourishment for the young, so that when she does leave to forage the following
evening the young are nutritionally satisfied and quiet. Hand-raised young which are not
hungry remained asleep and quiet when new-born. When hungry, however, they vocalised
loudly which would indicate their presence and attract would-be predators in the natural
environment. Even in captivity the mother never abandoned her young for long periods
during the first few weeks, and ıf she was away from the nestbox and heard the young
vocalısing she returned immediately, which effectively silenced them.

The scruff-hold method of transporting offspring ıs widespread amongst mongooses
and results in the young curling up into the “Tragstarre’ posture (ZANnNIER 1965). The effect
of a scruff-hold was two-fold: fırstly, it promoted a curling response which prevented the
young from bumping over the ground, given the short forelimb length of the adult
mongoose; secondly, it appeared to render the young helpless and inhibited struggling,
which was essential for efficient transportation. Rasa (1985) showed that disturbed dwarf
mongooses moved their young to a new and safer nest. It ıs likely that Atzlax would act
sımilarly, as ıllustrated by the mother transporting her young about the enclosure
whenever disturbed.

Details of vocalizations are provided in BAKER (1988). The attention call was exclusıvely
a juvenile sound and showed structural affınıty with the ‘humph’ call of adults. The main
difference appeared to be ın the marked frequency modulation of the attention call (BAKER
1988). The last use of the attention call coincided with increased locomotory capabilıties in
hand-raised mongooses and probably signalled the ability of the young to remain near the
mother by their own efforts. As thıs also coincided wıth weanıng it ıs likely that the young
begin to accompany the mother on short foraging trıps at this age. Field data are required
to substantiate this ın naturally raised mongooses.

Weaning coıncided closely with the eruption of the canınes on day 29 and premolars on
day 33 (BAKER and MEESTER 1986). Continuation of suckling beyond the age of nutritional
dependency on the mother may have helped to ensure that the bond formed between
mother and young remained intact until the young were fully capable of survival on their
own.

It was clear that young marsh mongooses had to learn how to deal with terrestrial prey,
both through maternal guidance and experience. However, as soon as it was established
that small moving objects were potential prey, mongooses were able to adapt their killing
behaviour accordingly. Food envy appeared to play a role in encouraging the young to eat
solids, and a maternal feeding growl stimulated attempts to retrieve prey from maternal
possession. ‘Hip-slamming’ has been described by Rasa (1973a) in dwarf mongooses. In
Atılax ıt developed around day 34, soon after the start of solid food intake, and appeared to
contribute to the complex of behaviour patterns associated with food envy.

The fact that there is no significant difference in the onset of prey killing between
naturally raised mongooses and hand-raised ones is not surprising as prey killing ıs an
ability which develops with maturation of skills, such as speed of movement as well as
ability to deliver a killing bite. In mongooses prey killing is most often a result of a bite
directed at the crown of the head, such that the canıne teeth inflict a fatal wound (BAKER
1989; Rasa 1973a). Only when mongooses have reached a certain level of development will
the killing bite be successfully administered. For this reason, perhaps, the attempt by
naturally raised mongooses to kill prey at 102 days was unsuccessful. In the case of the crab
killby a hand-raised anımal (K) at 129 days, the method of killing is different from that of

340 Carolyn M. Baker

rodent capture. Marsh mongooses usually dispatch this prey by throwing it onto the
ground (BAKER 1989).

In capturing aquatic prey the necessary techniques of feeling’ and searching for
submerged food appeared to be ones which required no learning in both naturally and
hand-raised mongooses. From an early age the mongooses manipulated objects between
the forefeet on the ground, almost as if unconsciously. The heightened sensory capacity of
the feet and the associated elaboration of the neocortex ın the brain (Ranınsky 1975) may
account for the immediate competence of forefoot activity.

In general results show little difference ın the rate of development of behaviour patterns
in naturally-raised and hand-reared mongooses. However, pattern of development was
different where maternal guidance was involved, such as in the development of prey killing
patterns.

Detailed work on the postnatal behavioural development of herpestines is scarce. Table
3 summarises available information and shows close similarities in feeding patterns,
locomotory development, grooming patterns and alarm responses amongst the sıx genera.

Table 3. Postnatal behaviour development in herpestines
Ages given ın days

Character Mungos H. ichneum. Suricata Helogale Galerella Atılax

High-sit 60 23-33
Wean 32-64 30-63
Alarm 12
Fleaing

Egg break (hen)

Rodent kill 78
Play-biting

Anal drag

Cheek mark

42-53

Run well
Defaecate alone
Scratch

Lick well

21-40
22

D2
30

absent
?grizzle

Purring alone present present present present

Sources: Mungos -— RooD (1975), VILJOEN (1980); Herpestes ichneumon — RENSCH and DÜckER
(1959), DÜckER (1965), BEN-Yaacov and Yom-Tov (1983); Suricata -— DÜCKER (1962, 1965),
Ewer (1963); Felogale - Dücker (1965), Rasa (1973a, b, 1977, 1985), Roop (1983); Galerella -
JacoBsEn (1982); Atılax — BAKER (1987), present study.

Resemblance ın the rate of postnatal physical development (BAKER and MEESTER 1986) is
probably the underlying cause of this similarity, as development of certain behaviour
patterns is clearly contingent upon development of locomotor abilities and visual ability,
for example. The development of the alarm response is the clearest example of this, as
vision is the faculty which releases thıs behaviour pattern. In Atılax eye-opening occurs
around day 11 (BAKER and MEESTER 1986) and the alarm response develops on the same
day. Eye-opening in Mungos begins on day 8 with alarm reactions developing on day 12
(VILJOEN 1980), while in Suricata eyes open around day 12 and the alarm response is
shown on the same day (EwER 1963).

The development of the ‘high-sit’ (EwER 1963) or ‘Männchenmachen’ (Dücker 1962)
showed some variation in maturation with social species developing the pattern earlier
(Tab. 3). It seems likely that in the natural environment it would be more adaptıve for the
sociable species, such as Mungos and Suricata, which are also diurnal and which rely on

Behavioural development in the Marsh mongoose 341

visual perception to detect predators, and probably also to maintain contact with con-
specifics, to develop the ‘high-sit’ as early as possible in order that they are able to elevate
themselves and extend their visual field. On the other hand, the solitary genera such as
Atılax and Herpestes ichnenmon tend to occur in more densely vegetated habitats, where
visual predator detection is less important due to availability of continuous cover. In the
case of Atılax this cover ıs extended by virtue of ıts nocturnal habit.

Manipulation and breakıng open of hen’s eggs varıes quite markedly, with dwarf
mongooses and marsh mongooses developing the ability earliest. Because all the herpesti-
nes appear to favour eggs little ecological significance can be attributed to the time at which
this pattern develops ın the different species, and it ıs more likely to be related to physical
ability. Rasa (1973a) notes that young Helogale are particularly voracious and for such a
small anımal to manipulate objects clearly requires considerable motivation and dexterity.
In relation to head-body length, limb length ın Galerella ıs shorter even than that of
Helogale and this may account for the much delayed development in this genus.

In all herpestines the rapıd development of locomotory abilities is clearly adaptive, in
that it allows young to accompany their parents on foraging trips as soon as weaning
commences, thus reducing parental responsibility as far as provisioning the young are
concerned.

Development of scent-marking behaviour shows some variation. The socıiable species
(Mungos and Helogale) exhibit earlier development of both anal and cheek-marking, than
the solitary Atılax, although slight overlap ın anal marking development occurs between
Atılax and Helogale. In order to promote integration into a sociable group it would be
expected that early development of scent-marking methods would occur. As the anal mark
is the “identity mark’ of the individual (Rasa 1973b; GoRMAN 1976; HEFETZ et al. 1984), ıt
is not surprising that ıt develops early in sociable mongooses, where ıdentification of all
group members ıs desirable. In Felogale, however, ıt develops after cheek marking, which
might be related to the handstand position which ıs adopted during anal scent deposition.
It seems that this would be a more difficult task to perform than the sımple anal drag
produced by Mungos and Atılax, and so develops when locomotion and balance are co-
ordinated. In Atılax the cohesiveness of the rearing group is not well developed, and so the
early development of anal marking is essential to reinforce the short-lived rearıng bond.

Purring has been recorded for most herpestines (Tab. 3). PETERS (1984) considers that
vocalızations wıth a uniform structural pattern consisting of a rhythmical series of short,
low-intensity sounds constitute close range friendly communication (including purring).
In Atılax the only sound that falls into this category is the “grizzle” (BAKER 1988).

Despite the marked differences ın rearıng systems between solitary and socıable
herpestines, the similarıties in the development of postnatal behaviour patterns illustrates
the overall cohesiveness of the group and provides few clues concerning phylogeny.

Zusammenfassung

Beobachtungen über die postnatale Verhaltensentwicklung von Sumpfmangusten (Atılax paludınosus)

Die mütterliche Pflege bei Sumpfmangusten wird beschrieben. Sie besteht aus Säugen, Reizen zum
Harnen, Schutz und Lehren aller Geschicklichkeiten. Der Beginn von neun verschiedenen Verhaltens-
kategorien wird kontrolliert und beschrieben. Diese schlossen Lautgebung, Bewegungen, Putzen,
Schreck, Geruchsmarkierung, Spiel und sexuelles sowie agonistisches Verhalten ein. Im Vergleich mit
der nachgeburtlichen Verhaltensentwicklung anderer Vertreter der Herpestinen, zeigten Sumpfman-
gusten gewisse Ähnlichkeiten.

Acknowledgements

Sincere thanks are due to Prof. J. MEESTER who supervised this project and made helpful suggestions
to improve the manuscript. Dr K. Wırran and Mr D. BasckIn and two unknown referees made
valuable comments regarding the manuscript contents. Prof. G. MacLean translated the abstract into

342 Carolyn M. Baker

German, and Ms E. RıcHarpson and Mr G. Hayes cared for the mongooses in my absences.
Financial assistance from the South African Council for Scientific and Industrial Research, the
University of Natal and the University of Durban-Westville is gratefully acknowledged.

References

BAKER, C. M. (1987): Biology and behaviour of the water mongoose (Atılax paludinosus). PhD.
Thesis, Univ. Natal, Durban.

— (1988): Vocalizations of captive water mongooses, Atilax paludinosus. Z. Säugetierkunde 53,
83-91.

— (1989): Feeding habits of the water mongoose (Atilax paludinosus). Z. Säugetierkunde 54, 31-39.

BAKER, C. M.; MEESTER, J. (1986): Postnatal physical development of the water mongoose (Atilax
paludinosus). Z. Säugetierkunde 51, 236-243.

BEn-Yaacov, R.; Yom-Tov, Y. (1983): On the biology of the Egyptian mongoose, Herpestes
ichneumon, ın Israel. Z. Säugetierkunde 48, 3445.

Dücker, G. (1962): Brutpflegeverhalten und Ontogenese des Verhaltens bei Surikaten (Suricata
suricatta Schreb., Vıverridae). Behaviour 14, 305-340.

— (1965): Das Verhalten der Schleichkatzen (Viverridae). In: Handb. Zool. VIII, 10. Teil. Ed. by
J--G. HELMcCKE, H. v. LENGERKEN, D. STARCcK. Berlin: de Gruyter, 1-48.

EWER, R. F. (1963): The behaviour of the meerkat, Suricata suricatta (Schreber). Z. Tierpsychol. 20,
570-607.

FRESE, R. (1980): Notes on breeding the marsh mongoose Atzlax paludinosus at Berlin Zoo. Int. Zoo.
Yearbk. 21, 147-151.

GORMAN, M.L. (1976): A mechanısm for individual recognition by odour in Herpestes auropunctatus
(Carnivora: Viverridae). Anım. Behav. 24, 141-146.

HEFETZ, A.; BEn-Yaacov, R., Yom-Tov, Y. (1984): Sex specificity in the anal gland secretion of the
Egyptian mongoose (Herpestes ichneumon). J. Zool. Lond. 203, 205-209.

JacogBsen, N. H. G. (1982): Observations on the behaviour of slender mongooses, Herpestes
sanguineus, in captivity. Säugetierkdl. Mitt. 307, 168-183.

PETERS, G. (1984): On the structure of friendly close range vocalizations in terrestrial carnıvores
(Mammalia: Carnıvora: Fissipedia). Z. Säugetierkunde 49, 157-182.

Rapınsky, L. (1975): Viverrid neuroanatomy: Phylogenetic and behavioral implications. J. Mammal-
ogy 56, 130-150.

Rasa, O. A. E. (1973a): Prey capture, feeding techniques and their ontogeny ın the African dwarf
mongoose, Helogale undulata rufula. Z. Tierpsychol. 32, 449-488.

— (1973b): Marking behaviour and its social significance in the African dwarf mongoose, Helogale
undulata rufula. Z. Tierpsychol. 32, 293-318.

— (1977): The ethology and sociology of the dwarf mongoose (Helogale undulata rufula). Z.
Tierpsychol. 43, 337406.

— (1985): Mongoose watch: A family observed. London: John Murray.

— (1989): Helping in dwarf mongooses societies: An alternative reproductive strategy. In: The
socıobiology of sexual and reproductive strategies. Ed. by ©. A. E. Rasa, E. VoLAND, and C.
VoceL. Beckenham: Croom Helm.

ReEnscH, B.; DÜckER, G. (1959): Die Spiele von Mungo und Ichneumon. Behaviour 14-15, 185-213.

Roop, J. P. (1974): Banded mongoose males guard young. Nature 248, 176.

— (1975): Population dynamics and food habits of the banded mongoose. E. Afr. Wildl. J. 13,
89-111.

— (1983): The social system of the dwarf mongoose. Spec. Publ. Amer. Soc. Mammal. 7, 454-488.

Vırjorn, $. (1980): Early postnatal development, parental care and interaction in the banded
mongoose Mungos mungo. S. Afr. J. Zool. 15, 119-120.

ZANNIER, F. (1965): Verhaltensuntersuchungen an der Zwergmanguste, Helogale undulata rufula, im
Zoologischen Garten Frankfurt a.M. Z. Tierpsychol. 22, 672-695.

Author’s address: CaroLyn M. BakER, Zoology Department, University of Durban-Westville, PbX
54001, Durban, 4000, R.S.A.

Z. Säugetierkunde 57 (1992) 343-350
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Interpreting social behaviour of Wood bison using tail postures
By P. E. KomeErs, KATHRIN ROTH and RUTH ZIMMERLI

Department of Biology, University of Saskatchewan, Saskatoon, Saskatchewan, Canada

Receipt of Ms. 28. 10. 1991
Acceptance of Ms. 15. 4. 1992

Abstract

Free ranging wood bison were observed to investigate the use of tail postures during social
interactions. Our observations support the following conclusions: 1. Different tail postures were
exhibited in different social contexts. Tail wagging was associated with grazing, while holding the tail
horiızontally or up were associated with aggression, sexual behaviour, and danger. 2. When bulls and
cows were found together in groups, mostly cows raised their tails when disturbed by predators,
while bulls raised their taıl in sexual contexts. 3. In aggressive interactions between bulls, tail up was
associated with dominance, taıl wagging with submissiıon. 4. The taıl up posture was exhibited in more
intensive situations than the horizontal taıl posture, suggesting that the tail up posture was a graded
form of the tail horizontal posture. 5. Individuals involved in play fights did not raise their tails, while
at least one of two contestants raised the taıl at the end of (but not during) escalated fıghts. We
conclude that the recording of tail postures of bison can serve as an objective tool in the interpretation
of bison social behaviour. The role of the tail posture as a possible sıgnal in bison communication is
discussed.

Introduction

Understanding social behaviour of anımals requires the knowledge of the behavioural
repertoire employed by anımals in social interactions. For this reason a detailed account of
body postures has been given, for example, for wolves (Canıs lupus) and domestic cats
(Felis catus) (SCHENKEL 1947; LEYHAUSEN 1956). Tail postures in these species could be
related to either dominance status, or state of emotions (level of fear or aggression).
HAUSFATER (1977) presented a quantitative analysıs of taıl postures in baboons (Papio
cynocephalus), in which he showed that tail posture correlated with age but not rank. Some
studies on ungulates describe tail postures ın addition to descriptions of body postures
(JARMAN 1979; BARRETTE 1977; Caro 1986).

Our observations of free-ranging wood bison (Bison bison athabascae) support the
concern put forward by McHuchH (1958) that bison behaviour patterns are often subtle
and, therefore, difficult to determine objectively. Tail postures of bison have been often
referred to ın reports on bison socıal behaviour (McHucH 1958; FULLER 1960; EGERTON
1962; HERRIG and HAucen 1969; LoTT 1974; MAHAN 1978), suggesting that taıl postures
of bison might be indicative of either dominance status, level of aggression, or fear. In
bison, strong development of hair on the head and neck region, and the large hump
obscure objective descriptions of body postures such as the position of ears, stretching of
the neck, and archıng or stretching of the back. The taıl, however, is a conspicuous body
part and can be easıly observed ın relation to social behaviour.

In the above mentioned studies bison were observed to raise their tails to varıous
degrees during aggressive, sexual, and alert behaviours, while they wagged their tails
during grazing. However, no quantification or rigorous examinations of relationships were
presented. Understanding the use of the tail in bison could be helpful in the interpretation
of bison social behaviour. This paper describes the position of the taıl of wood bison as a
character feature in different socıal contexts.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5706-0343 $ 02.50/0

344 P. E. Komers, Kathrin Roth and Ruth Zimmerli

Materials and methods

The study was conducted on a free-ranging wood bison population in the Mackenzie Bison Sanctuary
(MBS), Northwest Territories, Canada. There are no human settlements in the MBS, only one road
leads through the area, and no fences restrict the movements of bison. During the time of this study,
the population size was estimated at 2500 wood bison. The area used by the bison was approximately
10 000 km? (GatEs and LARTER 1990). The study was carried out from July 16 to August 16, 1990.
The study area was Falaise Lake which was considered to be the core of the range of bison in the MBS
(GATEsS and LARTER 1990). Falaise Lake extends over approximately 60 km“. It is a shallow lake
consisting largely of open sedge (Carex spp.) meadows and willow (Salıx spp.) savannah. The lake is
surrounded by boreal forest.

Bison groups are highly fluid and associations among individuals are considered near random
(Lorr and MıntA 1983; VUREN 1983). Observations on individuals marked with radıo transmitters
suggest that individuals range widely, using most of the area in and around the MBS. It is our
impression that a major part of the individuals in the population spent some time on the study area
during the data collection for the present study, and that the events sampled largely represent different
individuals.

For behavioral observations, the mınımum number of bison observed was three. When we spotted
bison groups at a distance (usually > 150 m), we left the all terrain vehicles behind and approached the
anımals by foot. By hiding in the vegetation, we made an effort not to be detected by the anımals.
Bison which detected humans generally left the area immediately. Therefore, we believe that the
behavioral data collected during this study was not affected by the presence of observers.

Binoculars and telescopes were used to observe the anımals. Each observational session lasted one
to three hours. We left the site after this time interval, in order to search for anew group of bıson. This
method was chosen in an attempt to maximize the number of different individuals observed.
Approximately 80 h of observation were conducted by each of the authors and one additional
observer. In addition to recording behaviour in the field, a video camera with a 12 x lens was used to
record bison behaviour on VHS video tape.

Categories of behaviour

Seven categories of behaviour were noted: walk towards another individual; walk away from another
individual; walk with another individual (includes parallel and one behind another); standing (anımal
standing with its head up); grazing (anımal standing or walking with mouth in grass); lyıng; and
flehmen (HERRIG and HAUGEN 1969; LoTT 1974).

Tail postures

Four categories of tail posture were recorded (Fig.): tail wagging (tail hanging down and whipped to
either side at least every ten seconds; McHuc#H [1958] termed thıs posture “taıl switching”); taıl down
(tail hanging down with no lateral movement); tail horizontal (proximal half of tail held horizontally;
distal half of tail my or may not hang down); tail up (tail raised higher than 45° from horizontal).
These tail postures were recorded when they were displayed for at least ten seconds. Transitory
postures lasted less than ten seconds and were thus not recorded (for example, when lifting the taıl
from tail down to tail up, the taıl was held for a brief moment at the horizontal position).

Context situations

Five context situations were recognized.

l. Grazing: The animal stood or walked with its head in the grass. Data on tail postures in the
grazing context were collected from video tape. Each grazing anımal was recorded on a data sheet
once, when it and its tail posture could be first identified. Tape sequences were discarded, when there
was a chance that individuals would be recorded a second time.

2. Alert: The anımal stood with its head up and ears directed towards the source of danger. Bison
groups disturbed by humans, were recorded on video tape. Each bison was recorded on a data sheet
once, at the instant when it and its tail posture could be first identified. Because the different scenes of
each group likely included the same individuals, the average frequency of bison adopting a given tail
posture was calculated over the number of scenes. The averages from different groups were used as
independent data points for statistical analysıs.

3. Sexual context: A bull sniffed the genitals of acow. Tail posture and category of behaviour were
recorded for each of two interacting animals at the beginning and at the end of an interaction. An
interaction started when one animal approached another to within two body lengths. This distance

Tail use of Wood bison 345

N

@) ) >
ZIR

D

Schematic representation of tail postures of wood bison. A: taıl down; B and C: two forms of tail
horizontal at the lower (B) and upper (C) margın of our definition (see text); D: tail up. Tail wagging
was similar to taıl down, except with lateral movements

was an arbitrary measure. The end was marked when one anımal moved away from the other or when
at least one anımal changed its behaviour. Although some events were recorded ın the same groups of
bison, we assume that different individuals contributed to our observations. This assumption is based
on the large number of individuals in groups, and the frequent changes of individuals between groups
(Komers, unpubl. data). Tail postures of bison during sexual contexts were also recorded on video
tape. For each interaction in which the bull showed tail up, his tail posture was also noted, by
rewinding the tape, when he was more than two body lengths from the cow.

4. Aggression: An aggressive interaction was defined as one bull approaching another to within
two body lengths and, subsequently, one of the two bulls turning away using at least two steps. The
individual that turned away was considered the loser. This definition included subtle forms of
interactions as well as escalated fights. Data were collected and analyzed in the same way as under
“sexual context”, except that instead of acow, a bull was approached by another bull.

5. Locking horns: Two anımals of any sex and age class standing head to head with horns touching
when the interaction was fırst recorded. If an aggressive interaction resulted in a fight and, therefore,
the two anımals locked horns, the locking horn behaviour was considered part of an aggressive
interaction and consequently not recorded under 5. Category 5 was established because some
interactions were only noticed at the time when two anımals locked horns.

When video tape recordings were used for data collection, the same criteria for behaviour and tail
postures were applied, as for observations in the field. The tape was not played back in slow motion to
make behaviours or taıl postures more obvious.

Results
Tail postures in different contexts

On average, 97.3% #+ 7.0% (SD) of grazing animals were tail wagging. Of the 115
anımals sampled, two held their tail horizontally, and four showed taıl down. No anımal
was grazing with its taıl up.

346 P. E. Komers, Kathrin Roth and Ruth Zimmerli

Table 1. Tail postures of wood bison displayed in different contexts at the start and at the end of an
interaction

The numbers represent all anımals involved, including both interacting partners

Behavioural context
Aggression Locking horns Sexual

Tail Posture

Horizontal
Down
Waggıing
End
Up
Horizontal
Down
Waggıng

Tail posture varıed in different context sıtuations (Tab. 1: start of interactions,

x = 40.4, df = 6, p<0.001; end of interactions: x? = 24.8, df = 6, p< 0.001). Both at the
start and at the end of interactions, taıl wagging was most often displayed in the locking
horns context, while tail up was used more often in aggressive and sexual contexts (Tab. 1).
During alert behaviour, the average frequencies of the four tail postures observed were
sıgnificantly different (up: 3.7; horizontal: 1.6; down: 3.2; wagging: 0.3; averaged over
three groups with three video sequences each), indicating that tail up was observed most,
and taıl wagging least frequently (Kruskal-

Table 2. Tail postures of wood bison bulls and Wallis test with x°-approximation,

cows during sexual context x = 8.08, df = 3, p=0.044).
The numbers represent all anımals involved, in- In sexual contexts, bulls that sniffed the
cluding both interacting partners genitals of cows exhibited tail up most fre-
quently, while females exhibited taıl down

Tail posture most oiten (Tab, 22 Eısheusssezacr
Boizoniel Dawn. Werzns p<0.001). Note that females exhibited tail
down more often than tail wagging. Con-
ceivably, tail wagging would interfere with
the investigative behaviour of bulls.

Also in the sexual context, taıl up was
mostly associated wıth walk towards, while taıl down and horizontal were associated wıth
standing and grazing at the start of interactions (Tab. 3, Fisher exact, p<0.001). At the
end of interactions taıil up was mostly associated with flehmen, while tail down and
wagging mostly with standing and grazing (Tab. 3, Fisher exact, p<0.001). Because sex
probably influenced tail posture and behaviour, a two-way analysıs of the contingency
table would have been appropriate. However, small cell frequencies did not allow for such
an analysıs.

Tail posture as indicator of dominance

Only 6 of the 16 pairs of aggressively interacting bulls contained at least one of the
contestants with a wagging tail at the start of the interaction, compared to 13 of 16 paırs at
the end (x? = 6.3, df = 1, n = 32, p= 0.012). This suggests that one of the two bulls changed
his tail posture to wagging during the interaction.

Independently of the above results, we recorded the winners, losers and the taıl
postures in 23 interactions for which the tail could be observed only at the end. Winners
had their tails either up (21) or down (2), while losers had their taıl either down (14) or

Tail use of Wood bison 347

Table 3. Tail postures of wood bison at the start and at the end of sexual interactions

The numbers in parentheses represent tail postures for males only. The difference between the sample
sizes at the start and end was because some tails were out of sight at the end of the interaction

Tail posture Behavioural category

Start
Walk towards Stand
Up (19) 0
Horizontal (2) 3.5.0)
Down 0) (0)

Waggıing 525.(0)
End

Graze
Up )
Horizontal )
Down 5240)
Waggıng IE)

waggıng (8) (Fisher exact, p<0.001). Tail horizontal was not observed. This suggests that
dominant bulls exhibit taıl up, while submissive bulls exhibit tail wagging.

Tail as an indicator of intensity

We assumed that the distance between an actor and an interacting partner ıs equivalent to
the intensity of a possible stimulus on the actor (Mannıng 1979; Alcock 1989). If true, and
if tail up reflects a stronger reaction than taıl horizontal, then one would expect that
animals further away from their interacting partners would exhibit taıl horizontal more
often than taıl up. Alternatively, bulls that are aggressive could remain with taıl up for
extended periods of time, irrespective of the proximity of interacting partners.

Bulls were recorded with their tails up within two body lengths of a cow (sexual
context) in nıne video sequences. When they were further than two body lengths, either
before or after approaching and sniffing, they showed tail horizontal ın eight and taıl up ın
one instances (bınomıal two-tailed test, p=0.02).

Bulls were recorded with their tails up within two body lengths of a bull (aggressive
context) in nıne video sequences. When they were further than two body lengths, either
before or after approaching, they showed tail horizontal in eight, and tail up in one
instances (binomial two-tailed test, p= 0.02).

We conclude that the taıl up posture was exhibited in more intensive situations than the
tail horizontal posture. This response suggests that tail up was a graded form of taıl
horizontal.

Play fights and escalated fights

Nine fights among mature bulls were recorded on video tape. In all cases, bulls wagged
their tail during the fight. In seven of the nine cases, one of the contestants exhibited tail up
at the end of the fight. Thus, the tail was raised significantly more often at the end than
during a fight (Fisher’s exact, df=1, p=0.002). This observation suggests that in order to
distinguish play fights (termed “play battles” by McHuc#H 1958) from escalated fights, the
position of the tail should be noted at the end of an interaction, and not while the anımals
lock horns.

This conclusion is further supported by results presented ın Table 1. Both individuals
exhibiting taıl up under the locking horns context were mature bulls interacting with other
mature bulls. The other individuals recorded in this context included three pairs of

348 P. E. Komers, Kathrin Roth and Ruth Zimmerli

subadult bulls, three pairs of yearlings, and one pair of calves. Presumably, immature
bison fight for training their motor skills as opposed to competing for resources ROTHS-
TEIN and GrIswoLD 1991). Indeed, in only one of the cases involving immature bison,
interacting partners walked away from each other. The others either remained standing
together or walked away together. In both cases in which one of the bulls raised his tail, the
two contestants walked away from each other.

Discussion

When bison in our study did not interact in a way that could be detected by the observers,
then they were mostly waggıng their tails. This suggests that tail wagging was a neutral tail
posture, thus it was exhibited when no social stimulus was present (HAUSFATER 1977).
However, tail wagging ıs presumably used by herbivores to repel biting insects. The
impact of biting insects on the behaviour of wood bison can be substantial (MErTon et al.
1989). We did not observe wood bison during insect free seasons. It is conceivable, that
bison do not wag taıl during the winter. If true, we suspect that they keep their tails down
as a neutral position.

Tail horizontal and up was associated with aggression, sexual behaviour, and danger.
Thus, the same taıl posture was associated with different behaviours ın different contexts.
This could potantially make the interpretation of tail postures difficult. We point out,
however, that when recording tail postures of bison, it ıs important to know the
behavioural context and the sex of the anımal. We feel that this requirement is easily met by
an observer, because the behaviour for each anımal under observation and that of the
surrounding anımals is usually known for a period of a least a few seconds.

The above consideration ıs further illustrated by tail postures not examined in our
study. For example, cows can exhibit tail horizontal or tail up after copulation. The taıl
posture of cows ın such a situation may last for one to several hours (McHucH 1958;
HERRIG and HAuGEn 1969; BERGER 1989). Tail up ıs also exhibited during defecation
(HERRIG and HAUGEN 1969). The contexts of such taıl postures are unmistakable.

We agree wıth McHuch#H (1958) and ROTHSTEIN and GRISWOLD (1991) that discriminat-
ing between playful and agonistic interactions in the wild ıs often difficult wıthout relying
on subjective interpretation. Our results suggest that bison did not raise their taıl ın a
playful context, while they dıd so at the end of aggressive interactions. Moreover, the
intensity of an interaction seemed to be indicated by the height to which the tail was raised.

Tail up in the alert context seemed to be associated with irritation (McHucH 1958).
While we presented data on bison reacting to human disturbance, we also observed that
bison reacted similarly to the disturbance by wolves.

Results presented in this study support the concept that the tail in bison may be
employed in visual communication. We do not claım, however, that the evidence is
conclusive. A rigorous investigation of behavioural relationships among bison receiving a
signal and bison sending a signal is required. Our results suggest that tail postures of bison
can serve as an objective tool in the interpretation of bison social behaviour. In fact, ın
many studies describing social behaviour of anımals and the corresponding body postures,
the tail was part of the description (SCHENKEL 1947; LEYHAUSEN 1956; WALTHER 1958;
Jarman 1979; BARRETTE 1977; CARoO 1986). Conceivably, the tail could be used in species
other than bison as an easily observable, objective tool to describe and interpret behaviour.

Acknowledgements

We thank F. MEssıEr, G. BARTOLOTTI, L. MARINELLI, E. J. Komers, and B. R. NEAL for constructive
comments on an earlier draft of this paper. CH. Bürkı and E. J. Komers assısted with data collection.

Taıl use of Wood bison 349

The research was supported by: the National Science and Engineering Research Council of Canada
through a scholarship to P. KomERs and an operational grant to F. MEssıEr; the Government of the
Northwest Territories, Canada; the endangered species recovery fund cosponsored by the Depart-
ment of the Environment, Canada, the World Wildlife Fund Canada, and the National Sportsman
Shows; the Northern Scientific Training Program; the Science Institute of the Northwest Territories
and the Northern Heritage Society.

Zusammenfassung

Das Interpretieren sozialen Verhaltens von Waldbisons anhand von Schwanzhaltungen

Freilebende Waldbisons wurden beobachtet, um die Schwanzhaltungen während sozialer Interaktio-
nen zu studieren. Unsere Beobachtungen lassen auf die nachstehenden Folgerungen schließen: 1.
Unterschiedliche Schwanzhaltungen wurden in unterschiedlichen sozialen Zusammenhängen gezeigt.
Schwanzwedeln hing mit Grasen zusammen, während ein waagrecht angehobener und ein aufrechter
Schwanz sowohl mit aggressivem und sexuellem Verhalten, als auch mit Gefahr in Zusammenhang
gebracht werden konnten. 2. Wenn Kühe und Bullen sich gemeinsam in einer Gruppe aufhielten,
zeigten Kühe einen aufrechten Schwanz in Gefahrensituationen und Bullen während sexuellen
Verhaltens. 3. Während aggressiver Interaktionen zwischen Bullen hingen ein aufrechter Schwanz mit
dominantem Verhalten und Schwanzwedeln mit subdominantem Verhalten zusammen. 4. Ein auf-
rechter Schwanz wurde in extremeren Situationen gezeigt als ein waagrecht angehobener Schwanz.
Also war ein waagrecht angehobener Schwanz eine gemäßigte Form von einem aufrechten Schwanz.
5. In Spielkämpfen zeigten Bisons keinen aufrechten Schwanz, während bei ernsthaften Kämpfen
zumindest einer der Kämpfenden am Ende des Kampfes einen aufrechten Schwanz zeigte. Das
Beobachten von Schwanzhaltungen kann als ein objektives Mittel zur Interpretation des Sozialverhal-
tens von Bisons dienen. Die mögliche Rolle von Schwanzhaltungen in der Kommunikation von
Bisons wird diskutiert.

References

ALcock, J. (1989): Anımal behavior. Sunderland, Massachusetts: Sinauer.

BARRETTE, C. (1977): The social behaviour of captive muntjacs Muntiacus reevesi (Ogilby, 1839). Z.
Tierpsychol. 43, 188-213.

BERGER, J. (1989). Female reproductive potential and its apparent evaluation by male mammals. ].
Mammalogy 70, 347-358.

Caro, T. M. (1986): The function of stotting in Thompson’s gazelles: some tests of the predictions.
Anım. Behav. 34, 663-684.

EGERTON, P. J. M. (1962): The cow calf relationship and rutting behavior in the American bison. M.
Sc. Thesis, Univ. Alberta, Edmonton.

FULLER, W. A. (1960): Behaviour and social organization of the wild bison of the Wood Buffalo
National Park, Canada. Arctic 13, 2-19.

GATES, C. C.; LARTER, N. C. (1990): Growth and dispersal of an erupting large herbivore population
in northern Canada: the Mackenzie wood bison (Bison bison athabascae). Arctic 43, 231-238.
HAUSFATER, G. (1977): Tail carriage in baboons (Papio cynocephalus): relationship to dominance rank

and age. Folia Primatol. 27, 41-59.

HERRIG, D. M.; Hausen, A. ©. (1969): Bull bison behaviour traits. Iowa Acad. Scı. 76, 245-262.

JaRMAn, M. V. (1979): Impala social behaviour, territory, hierarchy, mating, and the use of space.
Advances in Ethology, Suppl. 21, pp. 1-93.

LEYHAUSEn, P. (1956): Verhaltensstudien an Katzen. Z. Tierpsychol., Beiheft 2, pp. 1-200.

LoTT, D. F. (1974): Sexual and aggressive behaviour of adult male American bison (Bison bison). In:
Behaviour in ungulates and ıts relation to management. Ed. by V. Geist and F. WALTHER.
Morges, Switzerland: IUCN. Pp. 382-394.

LoTT, D. F.; Mınta, $. C. (1983): Random individual association and social group instability ın
American bison (Bison bison). Z. Tierpsychol. 61, 153-172.

Manan, B. R. (1978): Aspects of American bison (Bison bison) social behavior at Niobara National
Wildlife Refuge, Valentine, Nebraska, with special reference to calves. M. Sc. Thesis, Univ.
Nebraska, Lincoln.

MAnnIng, A. (1979): An introduction to anımal behaviour. London: Edward Arnold.

McHuch, T. (1958): Social behaviour of the American buffalo (Bison bison bison). Zoologica 43,
140.

MELTon, D. A.; LARTER, N. C.; Gates, C. C.; VırGL, J. (1989): The influence of the rut and
environmental factors on the behaviour of wood bison. Acta Theriol. 34, 179-193.

ROTHSTEIN, A.; GRISWOLD, J. G. (1991): Age and sex preferences for social partners by juvenile bison
bulls, Bison bison. Anım. Behav. 41, 227-238.

SCHENKEL, R. (1947): Expression studies of wolves. Behaviour 1, 81-129.

350 P. E. Komers, Kathrin Roth and Ruth Zimmerli

VUREN, D. van (1983): Group dynamics and summer home range of bison in southern Utah. ].
Mammalogy 64, 329-332.

WALTHER, F. (1958): Zum Kampf- und Paarungsverhalten einiger Antilopen. z. Tierpsychol. 15,
340-381.

Authors’ addresses: PETR E. KoMERS, Department of Biology, University of Saskatchewan, Saska-
toon, Saskatchewan, S7N OWO, Canada; KATHRIN ROTH and RUTH ZIMMERLI,
University of Berne, Ethologische Station Haslı, Wohlenstr. 50a, CH-3032
Hinterkappelen, Switzerland

Z. Säugetierkunde 57 (1992) 351-363
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Social environment of Isard kids, Rupicapra pyrenaica p.,
during their ontogeny

By C. RıicHARD-Hansen and R. CAMPAN

Institut de Recherche sur les Grands Mammiferes, Toulouse, France

Receipt of Ms. 2.12.1991
Acceptance of Ms. 29.6.1992

Abstract

Investigated the monthly social environment of cohorts of young isards, Rupicapra pyrenaica p.
during one and a half years, in an attempt to understand some aspects of their socialization process.
We postulate that the sociality of adults ıs greatly influenced by their ontogeny. The composition, in
age-sex classes, of 2,001 groups observed in open mountainous environment is described. During their
childhood, young isards go through high socıiality periods, during which they are in contact with
many and various conspecifics. During other periods, they are in closer association with females only.
Both association patterns may play a role in the socialization process. Contact with males is less
frequent and occurs for the first time during the rutting period. The most drastic changes in the socıal
environment of the young occur with the arrıval of the new generation of kids. The high sociality
period of spring is a rather sensitive period during which social associations are very diversified, and
social networks may be reshaped. The role of ontogenetic experience in formation of social
associations is discussed.

Introduction

The social structure of wild ungulates has been the subject of many studies. Comparisons
of data concerning varıous populations of a given species under different ecological
conditions have often indicated intraspecific varıations ın social systems (LoTT 1983). This
suggests that a species do not have a fixed specific social organization or structure, but that
both vary greatly under different environmental conditions (HırTH 1977; SCHAAL 1982;
LoTT 1983; ALapos 1985; MAaugLanc et al. 1987). According to LOTT, this would make
developmental questions more salient. BERGER (1979b) noted from reviews describing
adult spacing patterns that only few authors considered the process itself, ı.e., the
ontogeny of social behaviour. He stated that, in Bighorn sheep Ovıis canadensis, socıal
behaviour and subsequent spatial associations of lambs were influenced by the sıze of
groups within which they were reared (BERGER 1979a, b).

An individual exhibits a social predisposition depending on its sex, age and socıal
experience during its ontogeny, wıthin the limits of specific characteristics (Mason 1978).
This social tendency develops in a social and physical context, in constant dialectic
interaction with it. Each new generation modifies all existing relations ın a group, and
receives the influence of the whole group as feedback (Bon and Campan 1989). An
individual goes through an “ontogenetic trajectory” (Mason 1978; WıLEy 1981; Bon and
CamPpaAn 1989), shaped both through internal and external constraints.

This study ıs based on the assumption that the social context is the framework in which
behaviour develops and thus that shapes it into that of the full adult. The sociality of the
isard is thus dealt with through a developmental ‚approach. The results are presented ın
terms of kids’ social environment, which is amore “anımal centered” approach than a mere
description of the social structure in different group types or sizes. Moreover, the
information presented may provide the basıs for future comparative investigations ın
isards.

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5706-0351 $ 02.50/0

952 C. Richard-Hansen and R. Campan

Materials and methods

Observations were made ın the National Wildlife Reservation of Orlu, in the Pyrenees Mountains,
France. In this area, the ısard, Rupicapra pyrenaica pyrenaica, a species close to the chamois Rupicapra
rupicapra, but now considered as distinct (NASCETTI et al. 1985; Masını and Lovarı 1988) has been
protected since 1943. The population reached a high density of about 30 anımals/100 ha based on
annual counts made by the National Game Agency, responsible for the management of the
reservation. Most of the observations were made on about half of the protected area, which covers
4,265 ha. The altitude ranged from 1,400 m in this valley, up to 2,765 m for the highest summit.
Vegetation consisted mainly of meadows in the valleys, beech forest with Fagus sylvatica up to
2,000 m, some mountain pine forest, Pinus uncinata, and alpine pasture above.

Data were collected from May 1989 to December 1990. A “group”, at any given time, was
distinguished from a neighbouring one when the distance between them was greater than the average
inter-individual distance within the group (CLuUTToNn-Brock et al. 1982). Under field conditions, this
generally corresponded to intergroup distances of 50 m or more (BERDUCOU and Bousses 1985;
RıcHARD and MEnAUT 1989; RıcHARD and P£rım 1990). All visible groups observed on wide
panoramas from fixed observation points were recorded throughout the day. Hence, the data only
concern observations ın open habiıtats ın which visibility was sufficient. Groups were described by
their location on an aerıal photograph and by the number and nature of their components. 15,179
anımals in 2,001 groups of known composition were recorded (9.2 % males, 43.3 % females, 47.5 %
young). In this study we generally referred to “mixed groups” as associations containing males,
females and young, and to “matriarchial groups” as ones without males.

This work describes the monthly social environments of cohorts of young born in the same year.
The field work was conducted over a period of 1.5 years, so the young born in 1988 were observed at
the age of 1 to 2.5 years, those born in 1989 from birth up to 1.5 years, and the 1990-generation from
birth up to 7 months. Ages were estimated in months as all births were relatively synchronous.

Since the study was centered on the ontogeny of associations of young animals, no strict
classification was used to separate them artificially into pre-determined classes. The customary
classification of anımals as kids, yearlings and subadults did not suit this study, because it created
artificial gaps in calculating proportions of various classes at the very sensitive period of parturition.
Such artifacts would hide the behavioural events occurring during the same time.

To describe the social environment from the “young’s point of view”, the young were named with
reference to a focal cohort Y. Thus, Y+1 refers to the previous generation (young 1 year older than the
focal ones), Y+2 refers to anımals 2 years older, Y-1 to the succeeding generation, (1 year younger)
and Y-2 to anımals two-years younger.

For the sake of clarıty, we use “kid” to refer broadly to less than one-year-old young, “yearling”
for one- to two-year-old young, and the general term “young” for anımals less than 2.5 years old.
“Elders” refers to non-adult anımals older than the individual in question.

As it ıs very difficult to determine the ages of adult isards (because of the poorly defined annual
horn growth and the large inter-individual variations) individuals of 2.5 years of age or more were
simply separated into sex classes: adult female (F) and adult male (M).

The results are presented as percentages of anımals of each age class involved in various types of
associations. This accurately represents the real distribution of anımals in different groups, and thus
their social experience, better than the commonly used system enumerating the proportions of groups
encountered, which does not take into account group sıze (BARRETTE 1991). The sizes of different
associations are described here by the “Typical Group Size”, calculated using Jarman’s (1974)
formula:

where G; is the group size of each of the ı groups considered. Typical Group Size is also a more
animal-centered estimation, representing the group size experienced by the majority of anımals, in
other words by the “average individual”. This value is especially suitable for species that form many
small groups and few large ones (Hırıman 1987), or for species in which groups are very fluid
(BARRETTE 1991). Actually, both these conditions were present in our population.

Since our data concern individuals distributed in various group types, the samples are distributed
nonuniformly, and are not independent (when several kids are in the same group, they are not
independently distributed). Statistical analysis was not attempted in our study for the same reason as
that stated by Festa-BıancHET (1986) and since sample sizes were sufficient to make the figures for
variations of proportion reliable.

Social environment of Isard kids during their ontogeny 353

Results
Social associations of young up to 1.5 years of age

Monthly variations of the young/female ratio is presented in Figure 1, showing that the
period of parturition was very short. The first kids were observed on the 20th of May, 1989
and almost all of them were born by the beginning of June. The ratio kids/females seemed
to be rather stable during the fırst year.

® 1990 cohort (Y-1)
OD 1989 cohort (Y)

m 1988 cohort (Y+1 )
© 1987 cohort (Y+2 )

Young/Females ratio
0.8

0.4

0.0
May Jul Sep Nov Jan Mar May Jul Oct Dec

1989 1990

Fig. 1. Young/female ratio for 4 temporary cohorts of young, during 1.5 annual cycles

During theır fırst 7-8 months of life, kids were mostly observed associated with females
only, or with females and elders (Fig. 2a). Exclusive association of kids with females
decreased during summer, and increased slightly again at the beginning of winter (Fig. 2a,
c). Two categories of elders were distinguished for 1990 (Fig. 2c), indicating that kids were
in contact earlier wıth one-year-old anımals (June), rather than with the two-year-olds.
From May to December, only about 10 % of the kids were not in groups containing peers.
These occurrences corresponded to isolated mother-kid dyads, or, to a lesser extent, to
mother-kid-yearling trıos.

Females were always present in the kids’ social environment. Young kids (up to 9
months old) were never observed without the presence of at least one female (Fig. 2b). The
presence of kids in mixed groups, with at least one male, increased steadily during the
summer and the autumn. This was particularly obvious during the second study-year (Fig.
2c). In November (Fig. 2b), at the peak of the rutting period, the frequency of observa-
tions of kids in mixed groups reached its maximum (44 %).

In the winter (January-February) eight-to-nine-month-old kids were involved mainly
in complex associations: 48% wıth older young (Y+1) and females, 32 % within mixed
groups (Fig. 2) and the remaining 20 % were with females only.

The following March, when they were ten months old, more than half of the young
were again associated with females only. This increase may be related to the peak of the
young/female ratio ın March (Fig. 1). Spring was also marked by a second rise of
frequentation of mixed groups in April and by the emergence of associations with other
young and/or males without any female. It reached ıts maximum in May (Fig. 2b).

354 C. Richard-Hansen and R. Campan

HM wihr
E& withF+elders

with F + younger kids
[9 with F + younger kids+ elders

DE

1989 1990

Birth period

EEE

60 Oct.
% r? Dec.
20 AYV
ZAFAY;
AG,

10 11

-_
S
-_
[eo e)
[7
\O

?

Estimated age in
months

withM + FF (+ elders) with M (+ elders)
EI without adults U] withM +F + younger kids (+ elders)

KIDS born in 1990

BE wihrF
3 with F+elders: Y+1
El with F+elders: Y+l and Y+2

GE) with M+F (+ elders)

Fig. 2. Patterns of association of young between birth (in 1989) and 1.5 years of age. a: associations

without males; b: association with at least one male or without adults; c: young born in 1990

The most noticeable irregularıty in these smooth seasonal variations occurred in May,
when the mothers left their offspring and isolated themselves to give birth. At that time,
the young/female ratio dropped abruptly (Fig. 1). This reflects the sudden break off the
exclusive bond between young and mother. During this period, the young presented the
largest diversity ın their assocıiative tendencies: 14 % with peers and males, 27 % alone with
females, 26 % in matriarchial groups and 12 % in mixed groups (Figs. 2,
to note that, as observed during the first 8 months, about 10% of the kids were not in

contact with peers in groups.

3). It ıs of interest

Social environment of Isard kids during their ontogeny 333

In June 1990, while almost all females had given bırth, all the yearlings massively joined
females with their newborn kids (Fig. 2a), and also some elders as we already observed ın
the previous May (1989). Note that before and after birth, these two kinds of groups
(young wıth F, Y+1, Y+2 as well as young with F, Y-1, Y+1) were both composed of
females and three generations of young. However, for the focal kids, social environment
was quite distinct since, in the first case, they stayed only with elders, whereas ın the
second case, they were with elders and younger, and had lost the primacy of the bond with
the mother.

The young/female ratio increased agaın in July 1990 (or even later ın 1989), but some
yearlings probably became dispersed, since this ratio never regained the previous level
(Fig. 1). The association of one-year-old young with females and new-born kids (Y-1) was
predominant during Summer 1990; only a few stayed apart from the females, and were
associated with siblings and males. Although we could not always confirm their sex, we
feel the majority of the latter group were young males.

Social associations of young between 1.5 and 2.5 years of age

Figure 3 shows the generation of young born in 1988. One-year-olds (in Summer 1989,
Fig. 3a) were more often associated with elders (Y+1) in matriarchial units (52% in

E withF + elders EC] with F+ young Y-1 + elders
HM wihrF with F+ young Y-1

with F + youngers Y-1 and Y-2

1989 1990

Birth period

AV
1 =49p gu
% HMaygz P G 4 7 J: 7 2 a
ml 1% d G 7 DAVAYG mn
|: Au Do:
u #121212[0| DV Z
AV AUG er
| IZIZIAZZAZIAZZRSIS AZ Z
12013, 14 15 16 17. 18,19 20, 21022 23.25 23 26 27 09 29 30 31 ee
0 2 GG Erz BEN [55 Wu [:
20
40 5
%
60
80

EI without adults with M (+ elders or young Y-1)

withM+F(+eldrs)B [DJ withM +F+young Y-1 (+ elders)

DO) withM +F + young Y-2 (+ young Y-1)

Fig. 3. Patterns of association of young (born in 1988) between 1 and 2.5 years of age. a: association
without males; b: association with at least one male or without adults

356 C. Richard-Hansen and R. Campan

September 1989) than the one-year-old young observed in the following summer (29 % in
August 1990, Fig. 2a).

In November 1989, at the peak of the rutting season, 53% of the yearlings were
observed in mixed herds, while 36% were in matriarchial ones. They were in reversed
proportions compared to the months before and after. In 1990, yearlings born in 1989 were
observed ın mixed herds from October to December (Fig. 2b).

In the winter, most of the 20-month-old young were still involved in matriarchial or
mixed units until the next breeding season, while the 25-month olds once more tended to
associate with peers or wıth males (Fig. 3). Later, they were observed mainly in matriar-
chial groups, and again joined mixed associations that were formed ın November.

Associative tendencies of adult females

As grouping with females is very important in the social environment of the kids, it ıs of
interest to note that association of females with males occurred mainly between October
and April (Fig. 4). These mixed associations, with several generations of young, corre-
sponded, most of the time, to large gatherings in favourable grazing areas. These were the
largest type of association and reached a maximum in Aprıl and in November 1990 (Table
1). During the summer, the sexes were separated, (with a brief exception ın July 1989), and
most of the females were observed in matriarchial groups. About 15 % became isolated or
formed small all-female units in the breeding period (May).

FEMALES ASSOCIATED WITH:

100 Young —
Curves In +younge-
alone
\
2 N Sans femalesE2

40

Percent of females

20

0 SS - SI [
May Jul. Sep. Nov. Jan Mar. May Jul. Oct. Dec. Month
m
1989 1990

Fig. 4. Patterns of association of adult females during 1.5 annual cycles

The frequency of female associations with kids only decreased from parturition and
during the rearing period, but reached a new peak in March. During the summer, females
with newborn kids progressively frequented groups of increasing social complexity.

Typical Group Size of female-kid groups reached its maximum just after parturition
(Tab. 1): about 15 in May 1989, and 27-33 in May-June 1990. It then sharply decreased
during the summer (about 4 in August or September).

Matriarchial associations (containing at least 2 generations of young: FY), were largest

Table 1. Typical Group Size (TGS) and mean group size (mgs) of the various associations

Social environment of Isard kids during their ontogeny 357

in June 1989 (TGS = 40), and
in May-June 1990 (TGS = 30;
Tab. 1). During Summer
1989, although the most of
the kids, yearlings and fe-
males were in this type of
herd, these groups were scat-
tered ın small unıts.

Dec.

Oct.

Nov
groups including male(s)

Aug. Sept.

Associative tendencies of
adult males

July

As males were part of the so-
cial environment of kids and
young at least at some periods
of the year, it is of interest to
look at the assocıative tenden-
cıies of the males themselves.
During the year, on average,
about 33 % of the adult males
grouped together and up to
87% ıf we consider that the
male-young associations ob-
served in May concern mainly
young males. The relative
proportion of these all-male
associations reached its
minimum ın winter (16% ın
December 1989 and in
November 1990). Around
10-30% of the males were ob-
served alone, others in mixed
associations with females and
young, mostly during Winter
1989 and Autumn 19%.

The sıze of male-male as-
sociations reached its highest
peak ın Aprıl-May, as did
male-young and young as-
sociations. However, thıs
type of group was not more
frequent at this period, only
the number of anımals per
group was higher (up to 22
adult males).

Year 1990
male groups; MY

May June

Apr.

Feb. Mar.

Jan
groups including male(s), female(s) and young; MM

Year 1989

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and young; YY

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358 C. Richard-Hansen and R. Campan
Discussion

Following the social environment of the kids of Rupicapra pyrenaica, one can project the
presence of a pattern similar to that proposed by Bon and CAampan (1989) for moufflons,
and trace a “standard ontogenetic social trajectory” of an “average individual”. Each step
of such a trajectory as well as the variations of the social environment along the yearly life
cycle, may be influenced by either biological or ecological factors.

Isolation for parturition ıs a well known phenomenon, described in most ungulate
species, wild or domestic (LENT 1974). It allows the establishment of an exclusive bond
between mother and newborn, each learning to recognize the other individual (LENT 1974;
LICKLITER and HERON 1984; POINDRON et al. 1984). Mother-kid association is generally
considered to be the basıs of ungulate sociality, and often as the only stable entity
(Bouissou and Hövers 1976; GONZALEZ and BERDUCOU 1985; Bon et al. 1986). In
“follower” species, kıds stay close to the mother during their first weeks of life, and
accordingly are found together within the same groups (ErsMmArk 1971; LEnT 1974). Social
environments of kids initially seem to depend mainly on those of their mothers.

After parturition, in our population of isard, mothers gather together in large flocks (up
to 40 females) in open areas, each one followed by her kid. The kid/female ratio ıs usually 1
in such groups. FERRARI et al. (1988) related these matriarchial groupings in the Appenine
chamois Rupicapra pyrenaica ornata to the particular diet of females during lactation and
early weanıng of kids. On the other hand, Hırıman (1987) thought that, in the common
eland Tragelaphus oryx aggregations of females with young might be due to the active
gathering of the calves, which were physically attracted to one another. In this case, the
females follow their offspring into those gatherings. In our study, although kids seem to
follow primarily their mothers, they also have a great attraction for peers, which might
play a role in the formation of the post- -breeding nursery groups. These associations were
actually the first occasion of high social interactions in the kids’ experience, and the kids
often strayed away from their mothers and had many contacts with peers and engaged in
long sequences of play involving most of them (RıcHArnp-Hansen 1992b). Additional
yearlıngs joined these associations, staying more or less peripheral, and providing new
social partners for the kids and a progressive enrichment of the social context. These large
flocks seemed to include, for a short time, most of the females, who usually and
independently frequented partly overlapping home ranges, as demonstrated by following
some marked anımals (RiICHARD-HAansEnN, unpubl. data). However, differences may exist
in the social environment of the kıds. In the Ossau population (another area of the
Pyrenees) BERDUCOU and Bousses (1985) observed 1/5 of ısard kids ın mixed herds as
early as June.

In our observations, the large nursery flock did not last more than 1-2 weeks (end of
May-beginning of June) after which most of the anımals moved up to summer ranges. We
suspect that they moved to the higher altıtudes to find more rocky areas, to avoid heat,
direct sunshine or insect harassment, as well as pressure from domestic anımals that range
on alpıne meadows.

In the summer home ranges, the groups were smaller during mid-day and in many
instances were reduced to mother-kid or mother-kid-yearling units, the anımals spending
these hot hours lying down in narrow shaded shelters, behind rocks (P£pın et al. 1991).
Larger herds of isards occurred in the morning and in the evening, when the small units,
hardly observable during the day, gathered to graze on prairies (P£rpın et al. 1991). Males
were seen to join these flocks for short periods, especially in the highly attractıve zones,
where salt-licks were laid out for domestic sheep and cows (Hansen et al. 1992; INGOLD
and MARBACHER 1991). Similar observations of smaller group sizes of moufflons in the
summer were made by Bon and Campan (1989). These authors proposed that the small
group sizes were formed in response to high temperatures and impoverishment of the

Social environment of Isard kids during their ontogeny 959

meadows. It is of interest to note, however, that other studies on the chamois (ELSNER-
ScHAcK 1985; KRÄMER 1969) or Appenine chamois (Lovarı and CosEnTino 1986) have
shown the opposite to be true, maximum group size being attained in summer.

Isards came back to their previous home range during September, which seemed to be a
transitory period. Latter on, during the rutting period, many kids were included in large
flocks gathered on prairies. Males, actively looking for mates, were then running from one
group to the other and temporarily becoming part of them. Once more, we may note
differences between distinct areas: while 80 % of the females belonged to mixed assocıa-
tions in Ossau in November (BERDUCOU and Bousses 1985), less than 50% did in Orlu.
This difference can be related to the higher proportion of mixed groups in the Ossau
population. Thus, in our study as in the Carlıt population (a further area of the Pyrenees,
GONZALEZ and BERDUCOU 1985), kıds were ın sustained contact with males for the first
time in their lives in November, ı.e. during the rutting season. Bon and CamPan (1989)
also noted that 7-8 months-old moufflon lambs Ovis ammon musimon joined mixed
groups, following their mothers, ın the rutting season. During winter, the anımals were
usually found at higher altitudes (about 2,000 m) where clıffs, high slopes and windy
ridges reduce the thickness of snow. Thus it appears that the causes of this move, like that
in summer, are mainly environmental factors. Actually, when there was no snow, as
occurred during the Winter of 1989-1990, most anımals continued to frequent the
pastures.

In March, as they approached one year of age, the young went through a period of
reinforcement of exclusive association with females, as shown by the increase in the
percentage of this type of association, and of the young/female ratio. We already suggested
in a previous study (RıicHArD and P£rın 1990) that kids could go through regressive
periods in their development, during which they stayed closer to females and spatially
more central within the groups, as observed for 1-2 month-old kids. This may have
important implications in the social system by its possible causal value explaining the
formation of matriarchial assocıations of females and daughters as suggested by HORWITCH
(1977) for the ıbex. This hypothesis still has to be confirmed by estimation of mother-kid
distances and kıd’s behaviour. LovarI (pers. comm.) also suggested that Appenine
chamois in Abruzzo Rupicapra pyrenaica ornata may form matriarchial units in which
daughters stay with their mothers. Furthermore, one marked mother-daughter dyad ın our
study area remained closely associated for over two years (RICHARD-HANSsEN 1992a), until
they were broken up by accidental death.

April was another period of high socıality with formation of very large herds on the
lower prairies, where the grass grows first. These aggregations, certainly due to feeding
Opportunities, were also the occasıon of intense social contact between yearlıngs, gathering
into subgroups of peers, leading to the groups of young observed in April and May. Some
males were also present in these gatherings, integrated or in separate male groups, and
some yearlıngs were observed to follow them very closely and appeared to be integrated
into the groups, as shown by emergence of “MY” associations. In the Ammergauer
Mountains, Bavarıa (ELSNER-SCHACK 1985), seasonal factors had inverse consequences: in
this area, smallest group sizes were observed in spring and autumn, due to scattered food
sources.

During the parturition period, in May, we observed many associations of young, as
more and more females ısolated themselves. Most authors state that these juvenile
associations exist during parturition or during summer, in varıous ungulate species: ısard
(GONZALEZ and BERDUCOU 1984; BERDUCOU and Bousses 1985), Spanish ıbex (ALADOoSs
1985), white-tailed deer (HırTH 1977), Siberian ıbex (HORWITcH et al. 1977), mouftlon
(GONZALEZ and BERDUCOU 1985; Bon and CamPpan 1989), reindeer (EpsMARK 1971), and
red deer (CLUTTON-Brock et al. 1982). The wide varıety of social environments of young
described in this study at this transitory period of parturition reflects the instability of their

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Social environment of Isard kids during their ontogeny 361

status, as well as their great plasticity of grouping behaviour. Most of them rejoined
nurseries of females with newborn kids during the summer. In June, half the yearlıng
isards were observed ın female-young groups ın Ossau (BERDUCOU and Bousses 1985),
whilst 4/5 were observed in Orlu at the same time. This difference, as noted before for
kids, can be related to the higher proportion of mixed groups in the Ossau population. It ıs
possible that some of the yearlings may disperse, or follow adult males, as the young/
female ratio did not recover the pre-parturition levels. CLUTTON-Brock et al. (1982) also
reported, in red deer, a marked decline of mother-calf association during the new calving
period, followed by an increase during the summer, which never reached the same level as
that observed previously.

Young isard females are sexually mature and may already participate in reproduction in
the second autumn of their life, as proved by a marked 2-year-old female observed nursing
a kid in July. Table 2 shows a general view of the whole standard social trajectory with the
various factors that might shape ıt.

On the one hand, social environment and, consequently, the social ontogenetic
trajectory of an individual isard is, all along its path, submitted to external constraints. In
our work as in many other studies, weather and snow-cover conditions were shown to
have a great influence on the distribution of food and on the anımal’s pattern of habitat use
(PETocz 1972; HırTH 1977; LaGory 1986; Bon et al. 1990). In thıs work as ın others, the
presence of very large prairies, for instance, proved to be responsible for large gatherings
(CLUTTON-BrROcK et al. 1982; ScHAAL 1982; MAaugLanc et al. 1987). But all the external
constraints that can occur are different, for a given species, amongst the varıous living
areas, and even within the same area, between varıous home ranges. Furthermore, these
environmental conditions are not sımilar from one year to another. Thus, the socıal
environment of an individual isard appears to be fluid, and its own social experience is
distinct from that of its conspecifics.

On the other hand, ıt ıs clear that biological events play a major role in shapıng the
individual social trajectories through various social environments. They are: a. experience
before birth, through maternal stress for instance (LOTT 1983), b. early mother imprinting
(Lent 1974; Bouissou and AnDRIEU 1978; BERGER 1979a; LICKLITER and HERoN 1984;
POINDRON et al. 1984), c. mating (MıurA 1983), d. breeding (Bon et al. 1990), e. rearing
young (FERRARI et al. 1988; Hırman 1987). The social context also shapes the trajectory
through the relative proportion, density and social trajectories of the conspecifics (BERGER
1979b; CLUTTON-BRocK et al. 1982; Arapos 1985). These factors act together to bring
about a diversity of social environments that each individual will experience, that makes its
actual social trajectory unique. The social structures are the complex pictures observed and
they result from the network of interacting individuals, themselves ınfluenced by the
interacting factors mentioned. Social structures become constructed in the same way as the
individuals during their ontogeny. Studying the interactions between individuals should
contribute to a fuller understanding of the establishment of such a network, and the self-
organisation mechanisms of anımal associations (RICHARD-HAnsEN 1992b).

On another hand, only long-term studies on marked animals, like the one in progress in
the Orlu population, will allow the general rules of the mechanisms underlying the self-
construction of a social trajectory to be established.

Acknowledgements

We gratefully acknowledge the “Office National de la Chasse” for the technical assitance and financial
support, D. P£rın, G. GONZALEZ and ]J. F. GERARD for useful comments on an early draft of thıs
paper, D. ALTMann for the German translation, Pr NagıL Yousser for his useful suggestions and P.
WINTERTON for the revision of the english version.

362 C. Richard-Hansen and R. Campan

Zusammenfassung

Soziale Umwelt junger Gemsen (Rupicapra pyrenaica p.) aus den Pyrenäen während der Ontogenese

Die soziale Umwelt junger Gemsen (Rupicapra pyrenaica p.) aus den Pyrenäen wurde einige Monate
lang untersucht, um die Entwicklung partieller sozialer Prozesse zu verfolgen. Wir nehmen an, daß
das Sozialverhalten der Adulten zum großen Teil durch die Ontogenese bestimmt wird. Von 2001
Gruppen in offenen Bergregionen werden Alters- und Geschlechterverteilung beschrieben.

Während der Kindheit durchlaufen Gemsen beim Kontakt mit Artgenossen allgemein und
innerhalb von Weibchengruppen ım besonderen soziale Perioden. Beide Muster der Verbände können
eine Rolle im Sozialisierungsprozeß spielen. Kitz-Bock-Kontakte erfolgen erstmals in der Brunstzeit
und sind seltener. Die drastischsten Veränderungen in der sozialen Umwelt erfolgen in der nächsten
Geburtsperiode. Im Frühjahr findet eine besonders sensible Sozialisierungsperiode statt, in der soziale
Vereinigungen sehr wechselhaft sind und neue soziale Netzwerke entstehen. Die Rolle der Erfahrung
der Ontogenese bei der Bildung sozialer Verbände wird diskutiert.

References

Arapos, C.L. (1985): Group size and composition of the Spanish ibex (Capra pyrenaica Schinz) in
the sierra of Cazorla and Segura. In: The Biology and Management of Mountain Ungulates. Ed.
by S. Lovarı. London: Croom Helm. Pp. 134-147.

BARRETTE, C. (1991): The size of Axis deer fluid groups in Wilpattu national park, Sri Lanka.
Mammalıa 55 (2), 207-220.

BERDUCOU, C.; Bousses, P. (1985): Social grouping patterns of a dense population of chamois in the
Western Pyrenees National Park, France. In: The Biology and Management of Mountain
Ungulates. Ed. by S. Lovarı. London: Croom Helm. Pp. 166-175.

BERGER, ]. (1979a): Social ontogeny and behavioural diversity: consequences for Bighorn sheep Ovıs
canadensis inhabiting desert and mountain environments. J. Zool. Lond. 188, 251-266.

BERGER, J. (1979b): Weaning, social environment and the ontogeny of spatial association in Bighorn
sheep. Biol. Behav. 4, 363-372.

Bon, R.; CamPan, R. (1989): Social tendencies of the Corsican mouflon Ovis ammon musimon in the
Caroux-expinouse massif (South of France). Beh. Proc. 19, 57-78.

Bon, R.; CAMPan, R.; DARDAILLON, M.; DEMEAUTIS, G.; GONZALEZ, G.; TEILLAUD, P. (1986):
Comparative study of the social structures in three french wild ungulates. Wiss. Z. Humboldt-
Univ. Berlin, Math.-Nat. 35, 254-258.

Bon, R.; GONZALEZ, G.; Im, $.; BADra, J. (1990): Seasonal grouping in female moufflons in relation to
food availability. Ethology 86, 224-236.

Bousssou, M. F.; AnDrıeu, $. (1978): Etablissement des relations preferentielles chez les bovins
domestiques. Behaviour 64, 148-157.

Bousssou, M. F.; Hövers, J. (1976): Effet d’un contact precoce sur quelques aspects du comporte-
ment social des bovins domestiques. Biol. Behav. 1, 17-36.

CLUTTON-BROcK, T. H.; Guingss, E. E.; ALgon, $. D. (1982): Red deer: the behavior and ecology of
two sexes. Chicago: University of Chicago Press.

ELSNER-SCHACK, I. von (1985): Seasonal changes in the size of chamois groups in the Ammergauer
mountains, Bavarıa. In: The Biology and Management of mountain Ungulates. Ed. by S. Lovarı.
London: Croom Helm. Pp. 148-153.

EPsMARK, Y. (1971): Mother-young relationship and ontogeny of behavior in reindeer (Rangıfer
tarandus L.). Z. Tierpsychol. 29, 42-81.

FERRARI, C.; Rossı, G.; CAvanı, C. (1988): Summer food habits and quality of female kid and
subadult Apennine chamois Rupicapra pyrenaica ornata (Neumann, 1889). Z. Säugetierkunde 53,
170-177.

FEstA-BIANcHET, M. (1986): Site fidelity and seasonal range use by bighorn rams. Can. J. Zool. 64,
2126-2132.

GONZALEZ, G.; BERDUCOU, C. (1985): Les groupes socıaux d’isards et de mouflons au massif du carlıt
(Pyrenees orıentales). Gibier Faune Sauvage 4, 85-102.

Hansen, E.; RICHARD, C.; MENAUT, P. (1992): Mise au point d’une methode de captures multiples
d’Isards par enclos-piege. Symposium sur les captures et marquage d’ongules sauvages. Meze,
France, (in press).

Hırıman, J. H. (1987): Group size and association patterns of the common eland (Tragelaphus oryx).
J. Zool., Lond. 213, 641-663.

HırrH, D. H. (1977): Social behavior of white-tailed deer in relation to habitat. Wild. Monogr. 53,
4-54.

HorwItcH, R. H.; Dyke, R. von; CoGswELL, S. J. H.; Mırıs, G. (1977): Regressive growth periods
as a mechanism for herd formation in Siberian ibex (Capra ibex). Zool Garten N. F., Jena 47(1),
59-68.

Social environment of Isard kids during their ontogeny 363

InGoLD, P.; MARBACHER, H. (1991): Dominance relationships and competition for resources among
chamois Rupicapra rupicapra rupicapra ın female social groups. Z. Säugetierkunde 56, 88-93.
Jarman, P. J. (1974): The social organisation of antelopes ın relation to their ecology. Behaviour 48,

215-267.

KrÄMER, A. (1969): Soziale Organisation und Sozialverhalten einer Gemspopulation (Rupicapra
rupicapra L.) der Alpen. Z. Tierpsychol. 26, 889-964.

Lacory, K. E. (1986): Habitat, groupsize and the behaviour of white tailed deer. Behaviour 98,
168-175.

Lent, P. C. (1974): Mother-infant relationships in Ungulates. In: The behavior of ungulates and its
relation to management: Ed. by V. Geist and F. WALTHER. Morges: IUCN. Pp. 15-55.

LICKLITER, R. E.; Heron, J. R. (1984): Recognition of mother by newborn goats. Appl. Anım. Beh.
Sc12,187- 192.

LoTT, D. F. (1983): Intraspecific variation in the social systems of wild vertebrates. Behaviour 88,
266-325.

Lovarı, S.; COSENTINO, R. (1986): Seasonal habitat selection and group sıze of the Abruzzo chamois
(Rupicapra pyrenaica ornata). Boll. Zool. 53, 73-78.

Masını, F.; Lovarı, S. (1988): Systematics, phylogenetic relationships and dispersal of the chamois
(Rupicapra spp.). Quaternary Res. 30, 339-349.

Mason, W. A. (1978): Ontogeny of social systems. In: Recent advances ın primatology. Ed. by D. ].
CHiIvErs and J. HERBERT. London: Academic Press. Vol 1: Behavior. 5-14.

MaußBLanc, M. L.; BiDEAU, E.; VIncENT J. P. (1987): Flexibilite de l’organısation sociale du chevreuil
en fonction des caracteristiques de l’environnement. Rev. Ecol. (Terre Vie) 42, 109-133.

Miura, S$. (1983): Grouping behaviour of male Sıka deer ın Nara Park, Japan. J. Mamm. Soc. Japan 9,
279-284.

NASCETTI, G.; LOVARI, S.; LANFRANCHI, P.; BERDUCOU, C.; MATTIUcCI, $.; Rossı, L.; BuLLinı, L.
(1985): Revision of Rupicapra genus. III. Electrophoretic studies demonstrating species distinc-
tion of Chamois population of the Alps from those of the Apennines and Pyrenees. In: The
biology and management of mountain ungulates. Ed. by S. Lovarı. London, Croom Helm. Pp.
567.

P£rın, D.; ABBeEc, C.; RıcHArD, C. (1991): Diurnal activity patterns within female herds of Isard
around parturition time. Can. J. Zool. 69, 776-782.

PETocZz, R. G. (1972): The effect of snow cover on the social behavior of bighorn rams and mountain
goats. Can. J. Zool. 51, 987-993.

PoINDRoNn, P.; LE NEINDRE, P.; Levy, F.; KEVERNE, E. B. (1984): Les mecanısmes physiologiques de
l’acceptation du nouveau ne chez la brebis. Biol. Behav. 9, 65-88.

RICHARD, C.; MENAUT, P. (1989): Seasonal changes ın group sıze and association patterns in a dense
population of Isard (Rupıcapra pyrenaica). World Conf. Mountain Ungulates, Camerino, Italy.

RICHARD, C.; P£rın, D. (1990): Seasonal varıation in intragroup-spacing behavior of foraging isards
(Rupicapra pyrenaica). J. Mammalogy 71, 145-150.

RıiCHARD-HAnsEn, C. (1992a): Associations between indıvidually marked ısards (Rupicapra
pyrenaica): seasonal and inter annual varıations. In: Ongules/Ungulates 91. Ed. by F. Spitz, G.
JANEAU, G. GONZALEZ and $. AULAGNIER, SFEPM-IRGM, Paris, Toulouse. (France).

RıcHARD-HAnsen, C. (1992b): Socıalisation et modalıtes d’organısation sociale chez l’Isard
(Rupicapra pyrenaica p.) dans le cadre des theories systemique et d’auto-organisation. Implications
evolutives. Ph. D. Thesis. Univ. P. Sabatier, Toulouse, France.

Rounps, R. C. (1980): Aggregation behavior of Wapıti (Cervus elaphus) ın Riding Mountain National
Park, Manitoba. Canadıan Field-naturalist 94, 148-153.

SCHAAL, A. (1982): Influence de l’environnement sur les composantes du groupe social chez le daim
Cervus (Dama) dama L. Rev. Ecol. (Terre Vie) 36, 161-174.

WıLeEy, R. H. (1981): Social structure and individual ontogenies: problems of description, mechanism,
and evolution. In: Perspective in Ethology. Ed. by P. P. G. Bartzson and P. H. KLoPpFEr.
Landau: Plenum Publishing Corp.

Authors’ addresses: C. RICHARD-Hansen, Institut de Recherche sur les Grands Mammiferes, Institut
National de la Recherche Agronomique, BP 27, F-31326 Castanet Tolosan,
Cedex, France, and R. Campan, Department of Biology, College of Science,
Utah State University, Logan, Ut 84322-5500, USA

Z. Säugetierkunde 57 (1992) 364-372
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Capture-recapture study of a population of the Mediterranean
Pine vole (Microtus duodecimcostatus) in Southern France

By G. GuEpon, E. Parapıs, and H. CRosET

Laboratoire d’Eco-ethologie, Institut des Sciences de !’Evolution, Universite de Montpellier II,
Montpellier, France

Receipt of Ms. 28. 11. 1991
Acceptance of Ms. 3. 3. 1992

Abstract

Investigated the population dynamics of a Microtus duodecimcostatus population by capture-recapture
in Southern France during two years. The study was carried out in an apple orchard every three
months on a 1 ha area. Numbers varıed between 100 and 400 (minimum in summer). Reproduction
occurred over the year and was lowest in winter. Renewal of the population occurred mainly in
autumn. The population contained erratic individuals which did not take part in the reproduction.
Resident individuals had a longer life-span and home ranges always located at the same place. Mean
adult body weight varied only among females in relation to the reproductive rate. The observed
demography of M. duodecimcostatus could be explained by biological traits (litter size, longevity) and
by features of the habitat (high and constant level of resources, low level of disturbance), suggesting
that social behaviours are an important regulating factor of numbers.

Introduction

The Mediterranean pine vole (Microtus duodecimcostatus de Selys-Longchamps) has a
narrow geographic range: Portugal, Spain and Southern France (NIETHAMMER 1982). Its
population dynamics in natural habitats is unknown. The Mediterranean pine vole lives
also ın cultivated areas. Vineyards are very ancıent in the Mediterranean Region (several
centuries), and the Mediterranean pine vole ıs abundant in such a habitat though it causes
no particular damage. But the culture of perennial plants (e.g. orchards) wıth summer
irrigation transtormed the Mediterranean pine vole’s habitat in such a way that this rodent
species has become a pest to agriculture for a few years (GuEpon 1987, 1988). This
indicates the potentialities of Microtus duodecimcostatus to colonize successfully particular
habitats.

A research program conducted by several institutes (Association de Coordination
Technique Agricole, Institut de la Recherche Agronomique, Service de la Protection des
Vegetaux) was started in 1986. The aim of this program is to study reproductive biology
and population ecology of the Mediterranean pine vole and to develop an integrated
struggle system (a risk foresight method and biological, chemical, physical, mechanical,
and agrıcultural struggle methods based on a good knowledge of the species). We here
present demographic data from a study focused on local population dynamics of Microtus
duodecimcostatus in cultivated areas.

Material and methods

A capture-recapture study was started in 1989 in Southern France, in an arcea located 30 km east of
Montpellier (43°39’ N, 4° 11’ E). The region is an agroecosystem with intensive cultures distributed in
many patches separated by thick boundaries made with shrubs, cypress or poplar. During two years
we trapped a population in a 20-year-old apple orchard (Golden Delicious/E.M.9; pollinization is

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5706-0364 $ 02.50/0

Capture-recapture study of Microtus duodecimcostatus 365

made by branches of other varıeties). The main agricultural practices are: cutting and crunching of the
branches in winter, regular weeding, chemical treatment by pulverization all along the cultural cycle,
chemical manuring. The influence of the Mediterranean climate is partially masked because of summer
watering. The main disturbance which occurred during the study was a plough partially breaking up
the soil in winter 1989. No chemical treatment against the Mediterranean pine vole was carried out
during our study. Presence of this vole ıs revealed, as this species digs up soil from the ground when it
is burrowing.

The trapping procedure for subterranean rodents was developed by Pascaı (1984; PascAL and
MEyLAN 1986) for the fossorial form of the water vole (Arvicola terrestris scherman). This procedure
was adapted for snap-trappıng (GuEDon and PascaAr 1992) and for live-trapping of the Mediterranean
pine vole (present study). We used Longworth traps (baited with apple) the efficiency of which has
previously been demonstrated (GuEDon et al. 1990). Traps were distributed on a 1 ha area, along sıx
parallel 5 m x 100 m strips divided into 25 m? squares (Fig. 1). Two trap-stations (when possible) were

100 m
>

trapping-strips hi m

trap

wen
Fig. 1. Arrangement of the traps in the study area. In each square two, one, or no trap-station(s) were

arranged in relation to the number of presence signs of Mediterranean pine vole on the ground. Each
trap-station contained one, two or three traps

arranged in each square, each trap-station contained one, two or three traps orientated in the axis of
the tunnel previously dug out. Each trap was open during 42 hours, and was checked 7 times. The
caught animals were weighed (to the nearest g), marked by toe-clipping and ear-cutting, reproductive
conditions (males: testes scrotal or abdominal, females: pregnant, lactating, and vulva open or closed)
and coat color were noted before being released. It was also noted whether the trap was covered up
with soil by the vole (named “trap-stuffing” by Kress and BoonsTRrA 1984), which ıs a typical
behaviour of this species when its tunnels are opened. Two age-classes were distinguished according to
weight, adult: > 17 g, and juvenile: < 17 g. Strips were trapped two by two, so a trapping-session
lasted 9 days. Trapping-sessions were carried out every 3 months.

Results
Demography

We caught 1,534 anımals 4,656 times in 18,818 trap-checks. The observed numbers (Fig. 2)
varıed according to the seasons, with a decrease during summer droughts. Proportion of
juveniles in the population was always low (Fig. 2). Sex ratio of the caught anımals never
differed from 1:1 (x’-tests), for adults as well as juveniles (Fig. 3, the greater fluctuations
observed among the juveniles are caused by their smaller numbers compared with the
adults).

Among the 429 individuals caught in February 1989, five were recaught in February
1991 (3 males and 2 females of which one was pregnant).

366 G. Guedon, E. Paradis, and H. Croset

=
Q
-

D jweniles

IN
N
N

sapusAanl pue sınpe Jo %

Feb89 May89 Aug89 Nov89 Feb90 May90 Aug90 Nov9% Feb 91

Fig. 2. Total number of caught voles (curve) and percentage of the two age-classes (histogram) during
two years

3,0
+ adults
25 -D- juveniles
— whole population

sexratio

Fıg. 3. Sex ratio of the juveni-
les (voles less than 18 g), the
adults (voles heavier than
17 g), and all the voles caught
(juveniles and adults)

Feb 89 May89 Aug89 Nov89 Feb90 May9% Aug90 Nov90 Feb 91

Reproductive activity occurred over the year but showed seasonal varıations. We
exceptionally observed male individuals with scrotal testes, indicating that this position of
testes ıs not a reliable sign for sexual activity in male M. duodecimcostatus. The proportion
of females sexually active was at maximum in May, August and November, but seemed to
show inter-annual varıations (Fig. 4). This is corroborated by the proportion of juveniles

100

WH marked females
[[] unmarked females

80

i%k%

60

% of females with external
signs of reproductive activity

Feb 89 May 89 Aug89 Nov 89 Feb 90 May90 Aug90 Nov 90 Feb 91

Fig. 4. The adult females caught during each trapping-session are divided into two categories: marked
and unmarked (numbers of each category caught are indicated). The proportion of individuals with
external signs of sexual activity for each category are plotted and compared (x”-tests, *0.01 < p
< 0.05; **0.001 < p < 0.01; ***p < 0.001)

Table 1. Mean body weight of the caught voles in each trapping-session

(mean + standard deviation)

session

Capture-recapture study of Microtus duodecimcostatus 367

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females

adults
juveniles

in the population: maximum in August 1989 and in November
the following year (Fig. 3). Captures of pregnant females which
were lactating confirmed the existence of post-partum feconda-
tion as was observed ın the laboratory (GuEnon et al. 1991a).
The distinction between marked adult females (present for at
least 3 months) and unmarked ones shows the following pat-
tern: the proportion of females with external signs of reproduc-
tive activity was always higher among the former than among
the latter (Fig. 4). This difference is not always statistically
significant (x°-tests).

The variations in mean body weight of the caught voles did
not show seasonalıty (Tab. 1). Mean adult body weight was
slightly higher for females in contrast to males (range:
21.5-24.2, and 20.7-22.1, respectively), due to the presence of
pregnant females. Standard deviation of adult body weight was
slightly larger for females than for males (range: 1.6-3.0, and
1.4-2.2, respectively); this is probably due to the heterogeneity
of pregnancy among the females (Fig. 4).

The proportion of unmarked anımals (immigrants, animals
born during the three previous months, or residents not previ-
ously caught: Fig. 5) varıed with the seasons: it was at
minimum in August and at maximum in November, indicating
that renewal of the population occurred mainly in autumn.

Individual movements recorded during the study

Despite the low distance between two trapping-strips (20 m),
the recapture rates from one strip to another were very low
(0.4-16 %) indicating that, either movements of the Mediterra-
nean pine vole were very restricted during the time of a
trapping-session, or a decrease in the trappability of the voles
occurred after a first capture. Analysıs of movements between
two trapping- sessions corroborates the former explanation: the
majorıty of anımals was recaught at the same place as they were
caught three months before. Such sedentary anımals were
observed during several consecutive sessions: among 48 anı-
mals caught in four consecutive sessions, 38 (79%) were
always located at the same place. Home range locations seem
constant over time, however, we cannot speculate on variations
of home range sızes.

The proportion of anımals caught twice or several times
during the 7 checks (within trappıng-session recapture rate)
varıed with the seasons (Fig. 6), suggesting a decrease in
trappability during summer. This proportion was always
higher for marked than unmarked animals (except August
1989).

Parameters related to the trapping procedure

Trapping-intensity varıed slıghtily with the seasons: at
minimum in August, and at maximum in November (Fig. 7).
These variations were related to the lesser number of presence
signs on the ground. Proportions of captures and of trap-

368 G. Guedon, E. Paradis, and H. Croset

100 IE marked
[I] unmarked
80
& N
40

Feb 89 May89 Aug89 Nov 89 Feb 90 May 90 Aug%W Nov% Feb 91

Fig. 5. Proportions of marked and unmarked voles caught in each trapping-session

100
unmarked

A en gg marked
82

2o

det

go

Ss

od

35

So

SE

Ki

28

8

SE

Feb 89 May89 Aug89 Nov89 Feb90 May90 Aug90 Nov90 Feb91

Fig. 6. Comparison of the proportion of voles caught at least twice during the 7 checks (within
trappıng-session recapture rate) between marked and unmarked voles

—— nbchecks -3 nb trap-stuffings/nb checks
-Tr nb captures/nb checks
2600 100
2400 E
>» 2200
E h ;
2 1800 (7
2
1600
1400 0

Feb89 May89) Aug89 Nov89 Feb90 May90 Aug% Nov90 Feb91

Fig. 7. Trapping-intensity (expressed as number of trap-checks: left axis) and trapping-results (number
of captures and number of trap-stuffings reported to the number of checks: right axis) in each
trapping-session

Capture-recapture study of Microtus duodecimcostatus 369

stuffings (reported on trapping- intensity) varied greatly with the seasons (Fig. 7). The
proportion of captures was at minimum in August (= 10 %) and varıed between 20 % and
45 % for the other sessions, the results of February 1989 (45 %) were not obtained again in
1990 and 1991. The proportion of trap-stuffings varıed inversely wıth the proportion of
captures.

Other species

Five other species were caught in our traps: Crocidura russula, Apodemus sylvaticus, Mus
musculus, Rattus norvegicus, and Mustela nivalıs. Numbers of captures for these species
are indicated in Table 2. Herbivorous and granivorous small mammals were scarce in the
underground habiıtat suggesting that competitive interactions with M. duodecimcostatus are

Table 2. Numbers of captures for other species in the Longworth traps disposed in the under-
ground habitat of M. duodecimcostatus

species Feb 89 May 89 Aug 89 Nov 89 Feb 90 May 90 Aug 90 Nov 90 Feb 91

Crocidura russula
Apodemus sylvaticus
Mus musculus
Rattus norvegicus
Mustela nivalıs

not important in our study area. Only one weasel (Mustela nivalıs) was caught, indicating
that predation by this species may not influence the population dynamics of the
Mediterranean pine vole in our study area. A domestic cat (Felis catus) was observed in the
orchard while hunting; however, raptor birds (Strix aluco, Buteo buteo, Falco tinnunculns)
were regularly observed and were probably the main predators of the voles.

Discussion

Nearctic and Palearctic pine vole species are generally all included in the “Pıtymys group”
which ıs considered as a genus (Honackt et al. 1982; CorBET and Hırr 1991) or as a
subgenus included in the genus Microtus (NIETHAMMER and Krapp 1982; Nowak and
PArADISO 1983). CHALINE et al. (1988) argued that the subgenus Pitymys ıs polyphyletic
and proposed to divide it into the two subgenera; Pıtymys (nearctic species) and Terricola
(palearctic species). If CHALINE et al. (1988) are right, it would implicate a converging
evolution of some characters (particularly life-history traits as will be shown below)
between Pitymys and Terricola.

In our population of M. duodecimcostatus we observed a decreased trappability during
summer. The same phenomenon was observed in M. pinetorum (Lınpquist et al. 1981;
CORNBOWER and KıRrKLAND 1983) and several Microtus species (KREBS and BOONSTRA
1984). Added to the fact that the proportion of trap-stuffings increased in summer, this
leads us to invoke a more subterranean behaviour of the Mediterranean pine vole ın order
to avoid the hot and dry atmosphere. This changing behaviour may explain the decrease ın
captured voles during summer, however we cannot exclude a mortality peak during this
season.

The age-classes chosen in our study were ad hoc: anımals less than 18 g weighed more
than 17 g three months later. A snap-trapping study demonstrated that some females less
than 18 g could already be pregnant (Gu£Don unpubl. data). Body growth may be slower
in nature than in captivity (GuEDon et al. 1991b). However, the proportions of juveniles

370 G. Guedon, E. Paradis, and H. Croset

were always low. This can be explained by a low trappability of this age-class: voles were
not caught before they weigh at least 8 g. Mc Gu1rE and Novak (1984) and SALVIONI
(1988) observed that behavioural development was slow in juveniles of other pine vole
species (M. pinetorum and M. subterraneus, respectively). Several studies showed that the
proportion of juveniles was always low in populations of M. pinetorum (Sımpson et al.
1979; Linpquist et al. 1981; CORNBOWER and KırKLAND 1983). Fecundity in pine vole
species is low compared with other Microtus species or other microtine genera (LEFEVRE
1966; PELIKAn 1973; SCHADLER and BUTTERSTEIN 1979; SaLvIonI 1986; GUEDoN et al.
1991a, see InnEs 1978 or KELLER 1985 for reviews), and may influence the age-structure of
the population.

A long life-span was observed in other pine vole species (LE LouARN 1974; CoRN-
BOWER and KIRKLAND 1983; SAaLVIONI 1986), and seems to be a trait of these microtine
species. Some studies suggested that populations of M. pinetorum present a high turn-over
(MiLLER and GETZ 1969; STAPLEsS and TERMAN 1977; Sımpson et al. 1979). Such a pattern
is also present in our study; however, preliminar statistical analysis revealed that this was
an artıfact: most of the unmarked individuals were erratics and were not subsequently
recaught (Paranıs 1990).

The fact that reproduction occurs over the year in M. duodecimcostatus was also
observed ın Spain (CLARAMUNT 1976; Paromo et al. 1989), and in populations of
M. pinetorum living ı in orchards (Simpson et al. 1979; CORNBOWER and KIıRKLAND 1983),
though this species lives ın a cooler clımate. Reproduction in our population was at
minimum during winter. This result ıs not in agreement wıth PALoMmo et al.’s study ( 1989)
who showed that reproduction decreased dramatically during summer. This result is
supported by a small number of caught anımals (210 individuals during 2 years and only 4
females in summer), however, and a monthly snap-trapping study in Southern France
(more than 7,000 individuals caught during 5 years) showed that reproduction decreased in
June and July but increased in August (GuEpon and PascaAr unpubl. data). Discrepancy in
the results of the two approaches (snap-trapping and lıve-trapping) can be explained by the
fact that pregnancy cannot be detected in alive voles before about 10 days, but it can be
determined at a state of about 6 days in dead samples (KELLER 1985). COHEN-SHLAGMAN et
al. (1984) observed a decreased reproductive activiy in summer in Microtus guenther,
another Mediterranean microtine species. The seasonal varıations of reproduction
observed in our population could be explained by high summer survival of resident
individuals due to high level of resources in underground habitat of apple orchards. This
hypothesis could be tested by studying seasonal varıations of reproduction in uncultivated
habıtats.

In the studied habitat, food ıs abundant and uniformly distributed, therefore reproduc-
tion is probably conditioned by available space (possibility to construct a burrow). In a
population with sustained high densities, space ıs probably a limiting factor for access to
reproduction (at least for females). This assumption is strengthened by the fact that
reproductive females are resident (present for at least three months). Social behaviours
were evidenced to mediate access to reproduction in many species of mammals (HEN-
DRICHS 1983; DunBar 1985; ARMITAGE 1987). Such a phenomenon may play a role in the
local population dynamics of M. duodecimcostatus.

Acknowledgements

We thank JEAan-MARcC DUPLANTIER, PIERRE DELATTRE, MICHEL PascaAL for their comments on an
early draft of the manuscript, Nick CourT for correcting English, SERGE LEGENDRE for the German
translation of the abstract, and FRANCOIS CATZEFLIS for encouraging us. We are indebted towards Mr.
GIAMMATEI for allowing us to work on his property. We also thank various people tor their assıstance
in the field. This work was financially supported by the FNCA, and a CIFRE grant.

Capture-recapture study of Microtus duodecimcostatus 371

Zusammenfassung

Markierungsfangstudien an einer Population der Mittelmeer-Kleinwühlmaus
(Microtus duodecimcostatus) in Südfrankreich

Eine Population der Mittelmeer-Kleinwühlmaus (Microtus duodecimcostatus) wurde in Südfrankreich
über einen Zeitraum von 2 Jahren durch Fang, Markieren und Wiederfang untersucht. In Abständen
von 3 Monaten wurden Fänge ın einem Apfelgarten auf einer Fläche von 1 ha durchgeführt. Pro
Fangtermin wurden 100 bis 400 Individuen gefangen, am wenigsten im Sommer. Die Reproduktion
fand das ganze Jahr über statt, war aber im Winter am geringsten. Eine Erneuerung der Population
fand insbesondere im Herbst statt. Einzelne Individuen nahmen nicht an der Fortpflanzung teil.
Seßhafte Individuen hatten eine längere Lebensdauer und ihr Aktionsraum blieb sehr konstant. Das
Durchschnittsgewicht varıierte nur bei Weibchen in Abhängigkeit von der Reproduktionsrate. Die
beobachtete Demographie von M. duodecimcostatus kann durch biologische (Wurfgröße, Lebens-
dauer) und ökologische Merkmale (hohes und regelmäßiges Nahrungsangebot, geringes Störungs-
niveau) erklärt werden und weist darauf hin, daß das Sozialverhalten eın wichtiger Regulationsfaktor
für die Populationsgröße sein könnte.

References

ARMITAGE, K. B. (1987): Social dynamics of mammals: reproductive success, kinship and individual
fitness. Trends Ecol. Evol. 2, 279-284.

CHALINE, J.; BRUNET-LECOMTE, P.; GRAF, J.-D. (1988): Validation de Terricola Fatio, 1867 pour les
Campagnols souterrains (Arvicolidae, Rodentia) pal&arctiques actuels et fossiles. C. R. Acad. Scı.,
Parıs, Ser. III 306, 475478.

CLARAMUNT, P. T. (1976): Sobre la actividad sexual de Pıtymys duodecimcostatus de Selys-Long-
champs, 1839, en Cataluna. P. Dept. Zool. 1, 47-54.

COHEN-SHLAGMAN, L.; YoM-Iov, Y.; HELLwIng, $. (1984): The biology of the Levant vole,
Microtus guentheri in Israel. I. Population dynamics ın the field. Z. Säugetierkunde 49, 135-147.

COoRBET, G. B.; Hırr, J. E. (1991): A world lıst of mammalian species (3" Ed.). Nat. Hist. Mus.
Publ., Oxford Univ. Press.

CORNBOWER, T. R.; KIRKLAND, G. L., Jr. (1983): Comparisons of pine vole (Pitymys pinetorum)
populations from orchards and natural habitats in southcentral Pennsylvanıa. Proc. Pa. Acad. Scı.
37, 147-154.

Dunsar, R. I. M. (1985): Population consequences of social structure. In: Behavioral ecology:
ecological consequences of adaptive behaviour. Ed. by R. M. Sısry and R. H. SmitH. Oxford:
Blackwell Scient. Publ. Pp. 507-519.

Guepon, G. (1987): Influences de diverses speculations et pratiques culturales sur certains parame£tres
de la cinetique de populations de campagnols A douze cötes, Pitymys duodecimcostatus (de Selys-
Longchamps, 1839) dans le Montpellierais (France). D.E.A. report, Univ. Montpellier II.

GuEpon, G. (1988): Cinetique de population de Pıtymys duodecimcostatus dans le Montpellierais
(France). Bull. OEPP 18, 453—461.

GUEDoN, G.; BELAIR, M.; Pascar, M. (1990): Comparaison de l’efficaciıte de cing pieges non
vulnerants A l’egard de la capture du Campagnol provengal (Pitymys duodecimcostatus de Selys-
Longchamps, 1839). Mammalıa 54, 137-145.

GUEDON, G.; PascAaL, M. (1992): Elements de valıdation d’une methode d’Echantillonnage lıneaire
standardisee adaptee au Campagnol provengal (Pıtymys duodecimcostatus de Selys-Longchamps,
1839). Rev. Ecol. (Terre Vie) 47, 85-102.

GuEDon, G.; PascArL, M.; Mazoumn, F. (1991a): Le campagnol provengal en captıvıre (Pıtymys
duodecimcostatus de Selys-Longchamps, 1839) (Rongeurs, Microtides) I. La reproduction. Mam-
malıa 55, 97-106.

Guepon, G.; PascarL, M.; Mazoui, F. (1991b): Le campagnol provencal en captıvıte (Pıtymys
duodecimcostatus de Selys-Longchamps, 1839) (Rongeurs, Microtides) II. La croissance, Mam-
malıa 55, 397-406.

HENDRICHs, H. (1983): On the evolution of social structure in mammals. In: Advances in the study of
mammalian behavior. Ed. by J. F. EısengEers and D. G. Kıeıman. Spec. Publ. Amer. Soc.
Mammal. 7, 738-750.

Honackı, J. H.; Kınman, K. E.; Korper, J. W. (1982): Mammal species of the world: a taxonomic
and geographic reference. Lawrence, Kansas: Allen Press.

Innes, D. G. L. (1978): A re-examination of litter size in some North American microtines. Can. ].
Zool. 56, 1488-1496.

KELLER, B. L. (1985): Reproductive patterns. In: Biology of New World Microtus. Ed. by R.H.
Tamarın. Spec. Publ. Amer. Soc. Mammal 8, 725-778.

Kress, C. ]J.; BOONSTRA, R. (1984): Trappability estimates for mark-recapture data. Can. J. Zool. 62,
2440-2444.

372 G. Guedon, E. Paradis, and H. Croset

LEFEVRE, C. (1966): Etude de la croissance en Elevage de Pitymys duodecimcostatus de Selys-
Longchamps originaires du Gard. Mammalıa 30, 56-63.

LeLovarn, H. (1974): Etude par marquage et receptures du campagnol des champs et du campagnol
de Fatio en montagne. Mammalıa 38, 54-63.

Linpauist, $. B.; TıprTon, A. R.; YARROW, G. K.; HAsBRouck, J. J. (1981): Analysıs of seasonal
dynamics of pine vole populations in two Virginia orchards. In: Proceedings of the fifth eastern
pıne and meadow vole symposium. Ed. by R. E. Byers. Gettysburg, PA. Pp. 79-83.

MCeGuise, B.; Novak, M. (1984): A comparison of maternal behaviour in the meadow vole (Microtus
pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Anim. Behav. 32,
1132-1141.

MiLLer, D. H.; GETZ, L. L. (1969): Life-history notes on Microtus pinetorum in central Connecticut.
J. Mammalogy 50, 777-784.

NIETHAMMER, ]J. (1982): Microtus duodecimcostatus (de Selys-Longchamps, 1839) — Mittelmeer-
Kleinwühlmaus. In: Handbuch der Säugetiere Europas, Bd. 2/I, Nagetiere II. Ed. by J. NIETHAM-
MER and F. Krapp. Wiesbaden: Akad. Verlagsges. Pp. 463-475.

NIETHAMMER, J.; Krapp, F. (eds) (1982): Handbuch der Säugetiere Europas, Bd. 2/I, Nagetiere II.
Wiesbaden: Akad. Verlagsges.

Nowar, R. M.; Parapıso, J. L. (1983): Walkers’ Mammals of the world (4'® Ed.). Baltimore,
London: John Hopkins Univ. Press.

Paromo,L. J.; VARGAS, J. M.; ANTÜNEZ, A. (1989): Reproduction de Microtus (Pitymys) duodecım-
costatus (de Selys-Longchamps, 1839) (Mammalıa, Rodentia) dans le sud de !’Espagne. Vie et
Milieu 39, 153-158.

Parapıs, E. (1990): Demographie d’une population de campagnol provengal (Pitymys duodecimcos-
tatus): hypotheses sur les mecanısmes de regulation en milieu anthropise. D.E.A. report, Univ.
Montpellier II.

PascAr, M. (1984): Methode d’echantillonnage d’un rongeur souterrain, la forme fouisseuse du
campagnol terrestre (Arvicola terrestris scherman). Recherche des limites d’utilisation de la
methode. Acta (CEcologica/(Ecol. Applıc. 5, 303-317.

PascAr, M.; MEyYLAn, A. (1986): L’Echantillonnage lineaire des populations de la forme fouisseuse du
campagnol terrestre (Arvicola terrestris scherman [Shaw]). Description des techniques. La Defense
des Vegetaux 237, 3-12.

PELiKän, J. (1973): Notes on the reproduction of Pitymys subterraneus (de Sel. Long.). Zoologicke
Listy 22, 285-296.

SALVIONI, M. (1986): Domaines vitaux, relations sociales et rythmes d’activite de trois especes de
Pitymys (Mammalıa, Rodentia). Ph. D. diss., Univ. Lausanne.

SALVIoNI, M. (1988): Rythmes d’activite de trois especes de Pitymys: Pitymys multiplex, P. savıı,
P. subterraneus (Mammalıa, Rodentia). Mammalıa 52, 483496.

SCHADLER, M. H.; BUTTERSTEIN, G. M. (1979): Reproduction in the pine vole, Microtus pinetorum.
J. Mammalogy 60, 841-844.

Sımpson, D. A.; AntHonY, R. G.; Kerry, G. M.; STORM, G. L. (1979): Dynamics of a pine vole
population in a Pennsylvanıa orchard. In: Proceedings of the third eastern pine and meadow vole
symposium. Ed. by R. E. Byers. New Paltz, N. Y. Pp. 47-51.

STAPLES, P. P.; TERMANn, C.R. (1977): An experimental study of movement in natural populations of
Mus musculus, Microtus pennsylvanıcus, and Microtus pinetorum. Res. Popul. Ecol. 18, 267-283.

Authors’ addresses: G. GUEDoN, Delegation regionale ACTA, Maison de l’Agriculture de Vendee,
Boulevard Reaumur, F-85013 La Roche-sur-Yon cedex, France; E. PARADIs and
H. CroseET, Laboratoire d’Eco-ethologie, Institut des Sciences de l’Evolution,
Case Courrier 64, Universit€ de Montpellier II (U.S.T.L.), Place Eugene Batail-
lon, F-34095 Montpellier cedex 5, France

Z. Säugetierkunde 57 (1992) 373-379
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

Evaluation of hare abundance allowed by their use of attraction
points

By A. Lazo, C. DE LE COURT, and R. C. SORIGUER

Estacion Biologica de Donana, Sevilla, Spain

Receipt of Ms. 6. 4. 1992
Acceptance of Ms. 5. 7. 1992

Abstract

Studied the space use by hares (Lepus granatensis) which was affected by wooden stakes placed in an
open grassland at Donana Biological Reserve (SW Spain). Densities of hare pellets on plots centered
on the stakes were higher than on plots not centered on them. The use of stakes by hares seems to be
related either to an anti-predator behaviour or to a social behaviour of ground marking. Neither the
time nor spatial varıation ın hare abundance was related to food supply or to the herbaceous layer
characteristics. Rather, the seasonal abundance of hares in the study area depended on the floodıng
patterns of adjacent plant communities. The use of stakes as an improved version of the pellet-count
method is proposed. This modified method considerably reduces the sampling effort necessary to
carry out realistic estimations of spatial and seasonal varıations in the relative abundance of hares in
open fields.

Introduction

The ecology and behaviour of hares of the South Iberian Peninsula (Zepus granatensis
Rosenhauer) is practically unknown. Their taxonomiıc status and geographic distribution
were described by Paracıos and MEIJIDE (1979) and Paracıos (1983), but these aspects
have recently been questioned (SCHNEIDER and LEIPOLDT 1983; BONHOMME et al. 1986;
CorBET 1986; Paracıos 1989). These anımals live in habitats characterized by a high
abundance and diversity of predators (SORIGUER and ROGERS 1979) that can strongly
influence their activity pattern and space use.

Among other reasons for the lack of information about this species is the high time-and-
monetary cost of the tradıtional methods for studying lagomorph abundance and its
temporal and spatial varıation: capture-recapture, road-sıde surveys and pellet counts
(TayLor and Wırrıams 1956; BURNHAM et al. 1980). These methods do not seem to be
very suitable for low density populations because of the high sampling effort necessary to
obtain realistic estimations.

An alleged behaviour of hares due to the presence of attraction points in an open
grassland is described ın this study. It allows the application of a new method to estimate
spatial and temporal varıations of their abundance in open fields at low population
densities. Through its application the first information about the seasonal pattern of hare
distribution at Donana Biological Reserve (SW Spain) ıs given, as well as ıts relation to
environmental varıables.

Material and methods

Study area

The Donana Biological Reserve (37°N, 6°W; SW Spain) ıs an area wıth Mediterranean climatic
characteristics and a strong seasonality in the temperature and rainfall regimes. Two biotopes can be
distinguished mainly within its 67 km’: the salt marsh, and the scrubland on sandy soil (ROGERs and
Myers 1980). The salt marsh is flooded during the winter and spring months (November to May), and
remains dry the remainder of the year. Its plant cover is mainly sedges (Scirpus maritimus and

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5706-0373 $ 02.50/0

374 A. Lazo, C. de le Court, and R. C. Soriguer

Eleocharis palustris), whereas the scrubland shows a high basal cover by browse species (mainly
Halimium spp., Stanracanthus genistoides, and Erica spp.). An ecotone zone located between the
scrubland and the salt marsh ıs occupied by communities of herbaceous plants with a floristic
composition determined both by the depth of the water level and the soil salinity (ALLıEr and BREssET
1978).

The work was carried out within a plant community of the ecotone zone. The study area is located
on sandy-clay soil, between the salt marsh and a Juncus maritimus community. The ground is
characterized by a complete lack of relief, and is usually flooded during the winter dependent on
rainfall. The plant cover ıs very homogeneous and only small-sıze forbs and grasses are present. Some
representative species are Plantago coronopus, Aeluropus httoralis, Hordeum marinum, Polypogon
maritimus and Frankenia laevis. Plant nomenclature follows VALDE£s et al. (1987).

Pellet counts

In October 1989, 20 pairs of 1 m? plots were fixed in the study area. Each plot in a pair was 10 m away
from the other one. Paired plots were numbered in sequence and placed every 20 m along a straight
line perpendicular to the line delimited by the two plots ın a pair (Fig. 1). A wooden stake, 16 cm“ in
square-section with its top 30 cm above the ground level was driven at the centre of the right plot of
each pair (marked plot). The minimum distance between each stake and the nearest rush bed (JD) was
measured with an accuracy of Im.

er
Au ——

RUSH
OM

a —-

Zr ie

Da a ae BB, elerene
ee @ @ el [le [el [el [el

Ol 127132 147R sr ler

Fig. 1. Location of marked plots (squares filled with a point) and un-marked plots (white squares) in
the study area. For clarıty, plots appear larger than would be expected according to scale. Black points
at the rush community edge do not represent its actual limits but the minimum distance from each
stake to the nearest rush bed

From November 1989 to the beginning of March 1990 the study area remained flooded. Monthly
pellet counts on the marked plots were carried out from March to September and in November. The
number of pellets on each plot (PN) was counted and a mean density of pellets (MDP) was calculated
for each month. In the June sampling all the pellets from the odd-numbered plots marked with stakes
were removed. Thereafter until the end of July an intensive sampling was carried out (18 counts), the
numbers of pellets appearing since the last count being recorded. The average time (+ s.e.) elapsed
between two consecutive counts was 3.59 + 1.05 days. After each count the pellets were removed
only from the odd-numbered plots. Additional pellet counts were carried out on the un-labelled plots
in April, June, September and November.

Vegetation sampling

Estimates of the dry biomass availability (DB), the water content of vegetation (HC), the maximum
height of green grass (MH), the basal cover of the herbaceous vegetation (SC), the forb contribution to
the total cover (FC), and the contribution of dead grasses to the total basal cover of grasses (GC) were
obtained monthly. The aerial biomass of the herbaceous layer was estimated on five 0.2 m? plots, fixed
regularly along the straight line delimited by the stakes. 'The pasture samples were weighed with an
accuracy of 0.1 g and drıied in a hot-air oven at 50 °C until constant weight. The maximum height of

Evaluation of hare abundance allowed by their use of attraction points 9,75

green grass was measured on each labelled plot with an accuracy of 1 cm. Cover estimates were carried
out visually on each plot using an ordinal scale (WALKER 1976).

Some data were analysed using non-paramerric statıstical tests (SIEGEL 1956). A significance level
of 0.05 was fıxed for all analyses.

Results
Use of stakes

The differences between the mean density of pellets on both marked and unmarked plots
were obvious during the entire study period (Tab. 1). Visual inspections of the un-labelled
plots did not show different pasture characteristics with regard to the labelled plots, as
expected by the short distance between them. Thus, the high number of pellets on the
marked plots suggests that the stakes operated as attraction centres for hares.

Table 1. Mean pellet densities + s.e. for the marked and the non-marked plots

Pellets were removed from the odd-numbered plots marked with stakes after the counts in June. Thus,
only the even-numbered plot counts (n = 10) were used for estimating mean pellet density at the
marked plots in September

Marked Un-Marked

Apr 4.80 = 1.17
Jun 92789 =1=4.110
Sep 659541932
Nov 24489)=513,33

n = number of 1- m? quadrats

Time variatıon

The use of the stakes by hares during the study period shows a pronounced seasonal
pattern (Fig. 2). In March the sampling was carried out when the area had recently emerged
from the winter flood and no pellets were detected on the plots. The maximum pellet
densities around the stakes were observed in May, June and July. During the more
intensive sampling of the marked plots carrıed out in the second half of this period, an
appearance rate of 0.15 pellets m”? day ' was recorded. From July to September an

number of pellets m”?

35
30
25

mar apr may jun jul aug sep oct nov

Fıg. 2. Changes in the mean density of pellets (x + s.e.) corresponding to the even-numbered plots of
the transect line (n = 10). The arrows show: (a) the end of the flooding period at the study area, (b) the
end of the flooding period in the marshland and (c) the beginning of autumn rains

376 A. Lazo, C. de le Court, and R. C. Soriguer

important reduction in MDP was observed. In August and September the presence of hares
at the study area was verified through the counting of new pellets appearing on the odd-
numbered plots marked with stakes. Data for November showed a new increase in the
mean density of pellets.

Lag-correlogram between the monthly values of MDP and the mean value of each
vegetation variable (DB, HC, MH, SC, FC and GC), both estimated at the marked plots,
showed no significant Spearman cross-correlation coefficient (P > 0.05 for all correla-
tions).

Spatial variation

Spearman correlation coefficients (r,) between PN and the vegetation varıables estimated
on each labelled plot (MH, SC, FC and GC) were calculated for each month. Due to the
number of coefficients (28), by chance alone it could be expected that one would be
significant under the no relationship hypothesis, and ın fact, only one correlation between
pasture characteristics and the number of pellets is significant (Tab. 2). However, a relation
between the number of pellets and the distance from the stake to the nearest rush bed (]JD)
was indicated: the correlation coefficients are significant and positive for May, June and
July and negative for November (Tab. 2).

Table 2. Spearman correlation coefficients between the pellet number and the vegetation variables
estimated on each plot of the marked transect line

GC JD

Apr . 0.338 0.102
May i -0.363 099
Jun 5 i 0.032 0.648”
Jul 6 2 0.540 0.748*
Aug h £ -0.075 0.480
Sep 3 .686” ; -0.076 0.295
Nov ; Ä 5 0.215 -0.620**

n = number of I- m? quadrats; MH = maximum height of green grass; SC = basal cover of the
herbaceous vegetation; FC = forb contribution to the total cover; GC = contribution of dead
grasses to the total basal cover of grasses; JD = minimum distance between the stake and the rush
bed 22 P=20.052- 3 P2=0X01

The r, between the number of new pellets appearing in the odd-labelled plots during the
period of continuous sampling and JD showed a related probability very near the
significance level (r, = 0.642, P = 0.054, n = 10). No significant difference was detected
between sampling distributions of the number of new pellets appearing ın odd and even-
numbered plots marked with stakes (Ka = 0.3, P = 0.99, n, = n> = 10, two-tailed test).

Discussion

VALVERDE (1960) and Kurner (1986) have pointed out that the salt marsh is the biotope of
Donana with the highest intensity of use by hares ın summer and autumn. From
November 1989 to June 1990 the salt marsh was flooded. During this period hares would
have been forced to occupy the ecotonal areas between the marshland and the scrubland, as
VALVERDE (1960) and Rau et al. (1992) suggest. As new areas emerged because of the
decrease in the water level, the animals probably moved progressively into the salt marsh.
This hypothesis would explain the absence of pellets in March, the slow increase detected
subsequently in the mean density of pellets and their progressive decrease from June to

Evaluation of hare abundance allowed by their use of attraction points ST,

September. Early rains in October, usually responsible for the salt marsh floodıng, could
again cause the migration of hares towards the highest fields of the ecotone with the
scrubland. This could be responsible for the increase in the mean pellet density recorded in
November relative to the previous sampling in September. The observed seasonal pattern
in hare abundance thus seems to be the result of a “concentration-dilution process“ of hare
numbers in the study area due to drastic reductions and increases of the available land
surface.

The extent of the differences observed between the pellet counts ın the marked and non-
marked plots shows that stakes have operated as centres of attraction for hares. The
accumulations of pellets around the stakes could reflect a ground-marking behaviour as
well as an anti-predatory adaptatıon.

A social behaviour of ground marking through pellet grouping has been described for
several lagomorph species. This behaviour is often manitested at points characterized either
by their ground elevation or by the existence of easily identifiable landscape elements
(Be 1985). In the study area the stakes break the uniformity of a very homogeneous
landscape and appear to be suitable points for the manifestation of such behaviour by
hares. Pellet accumulations have been observed in brown hare (Lepus enuropeaus Pallas)
ranges, but seem to be more related to the high levels of use of small areas than to the
formation of latrınes (BELL 1985).

On the other hand, the relevance for lagomorphs of vegetation cover as shelter against
predation ın Mediterranean environments has been pointed out by Jaksıc and SORIGUER
(1981). In the study area diurnal and nocturnal predators of hares (e.g. Spanish imperial
eagle Aguila adalbertı, Iberian Iynx Lynx pardellus and fox Vulpes vulpes) occur at very
high densities (KuFnEr 1986). Therefore, in the absence of marked relief, high vegetation
or relevant rocks, sufficiently large wooden stakes could provide hare shelter from
predation. Perhaps the stakes break the hare figure, making it more difficult for predators
to detect their prey and also could provide protective elements against direct attacks.

Both hypotheses can explain the significant and positive correlation observed for May,
June and July between pellet numbers per plot and distance from the stake to the rush bed;
they also explain the absence of a relationship between pellet numbers and the descriptive
varıables of the herbaceous layer at each labelled plot. Thus, stakes far away from the rush
bed would be more attractive as reference elements for ground marking by pellet
accumulations. On the other hand, during resting periods hares would use the stakes
distant from the rush bed, situated in areas more exposed to predation, at higher
frequency. The low use of the area before April and after the draining of the salt marsh can
explain the absence of a relation between the pellet number and the distance to the rush bed
for the sampling ın April, August, and September. The ground level at the rush beds is
elevated over the soil level at the plot locations. Thus, the November results could be
interpreted in the sense of hares having to use the safe rush beds, and theretore the stakes
adjacent to them, with regard to the flooding risk of the area after the first intense raın.

Hares do not show a conspicuous behaviour and commonly are solitary anımals,
although temporary grouping in feeding areas have been described for brown hare
(MoNAGHAN and METCALFE 1985) and during the oestrus period for mountain hare Lepus
timidus (HEwson and Hınce 1990). For that reason, estimations of their relative abund-
ance with standard methodology are not usually feasible in areas occupied by low-density
populations. Based on road-side surveys, time-and-spatial varıations in hare abundance are
very difficult to quantify because of the large number of visual contacts necessary to carry
out the estimations (BURNHAM et al. 1980). Similarly, a large sample size is necessary,
either in the number or sıze of plots, to obtain suitable data for estimating variations in
abundance by the pellet count method (Tayror and WırLıams 1956). The results above
suggest that the use of stakes could be a way to improve the pellet count technique
reducing the sampling efforts for obtaining adequate sample sızes. This method has not

378 A. Lazo, C. de le Court, and R. C. Soriguer

been tested at any other sites except at Donana. However, this behaviour of hares is well
known by Spanish hunters, who look for hares around land-marks and poles in open
country. Also, personal observations by one of the authors, previous to the design of this
study, at two other locations (Guadalquivir marshland and Cazorla Mountains, Southern
Spain), suggest that this improved version of the pellet-count method could be widely used
in open areas wıthout high plant cover or relief. In such conditions a differential use of
stakes would be expected to be due to variations in hare abundance.

Acknowledgements

E. Garcfa MARQUEZ supplied field work assistance. Dr. R. TROUT improved a preliminary version of
the manuscript and made interesting suggestions. We are in debt to CrAauDIA KELLER for her
colaboration.

Zusammenfassung

Ermittlung der Abundanz von Hasen durch Nutzung von Anziehungspunkten

Die Raumnutzung des Iberischen Hasen Lepus granatensis in einem offenen Wiesengelände des
Biologischen Reservates Donana wurde experimentell durch eingebrachte Holzpfähle beeinflußt. Die
Häufigkeit von Kotpillen war auf den Flächen größer, die mıt Holzpfählen bestückt waren. Das
Aufsuchen der Pfähle durch die Hasen steht wahrscheinlich im Zusammenhang mit Feindvermei-
dungs- oder Markierungsverhalten. Weder die zeitliche noch die räumliche Variation der Hasendichte
ließ sich mit dem Futterangebot oder dem Kräuterspektrum korellieren. Dagegen scheinen Über-
schwemmungen die saisonale Dichte zu beeinflussen. Der Einsatz von Holzpfählen wird als Verbesse-
rung der bisherigen Zählmethode vorgeschlagen. Er verringert deutlich den Aufwand, der nötig ist,
um an zuverlässige Schätzungen der zeitlichen und räumlichen Schwankungen der relativen Dichte
von Hasen im offenen Gelände zu gelangen.

References

ALLIER, C.; BRESssET, V. (1978): Etude phytosociologique de la marısma et sa bordure (Reserve
Biologique de Donana-Espagne). Carte phytosociologique. In: Donana: Prospecciön e Inventario
de Ecosıstemas. Madrid: Monografias del Ministerio de Agrıcultura, ICONA. Vol. 18, 59-109.

Ber, D. J. (1985): Th rabbits and hares: order Lagomorpha. In: Social odours in mammals. Ed. by R.
E. Brown and D. W. McDonaıp. Oxford: Clarendon Press, Pp. 507-530.

BONHOMME, F.; FERNÄNDEZ, J.; PALACIOS, F.; CATALAN, J.; MACHORDON, A. (1986): Caracterisation
biochimique du complexe d’especes du genre Zepus en Espagne. Mammalıa 50, 495-506.

BURNHAMm, K. P.; AnDERsoN, D. R.; LAAkE, ]J. L. (1980): Estimation of density from line transect
sampling of biological populations. Wildl. Monog. 72, 1-202.

CoRBET, G. B. (1986): Relationships and origins of the European lagomorphs. Mammal Rev. 16,
105-110.

Hewson, R.; Hınge, M. D. (1990): Characteristics of the home range of mountain hares ZLepus
timidus. J. Appl. Ecol. 27, 651-666.

Jaxsıc, F. M.; SORIGUER, R. C. (1981): Predation upon the European rabbit (Oryctolagus cuniculus) ın
Mediterranean habitats of Chile and Spain: a comparative analysis. J. Anım. Ecol. 50, 269-281.

Kurner, M. B. (1986): Tamano, Actividad, Densidad Relativa y Preferencia de Habitat de los
Pequenos y Medianos Mamiferos de Donana como Factores Condicionantes de su Tasa de
Predaciön. Ph. D. Thesis, Univ. Autönoma de Madrid.

MONAGHAn, P.; METCALFE, N. B. (1985): Group foraging in wild brown hares: effects of resource
distribution and socıal status. Anım. Behav, 33, 993-999.

Paracıos, F. (1983): On the taxonomic status of the genus Lepus in Spain. Acta Zool. Fennica 174,

2730.
— (1989): Biometric and morphologic features of the species of the genus Lepus in Spain. Mammalıa
53, 227-264.

Paracıos, F.; MEIJIDE, M. (1979): Distribuciön Geogräfica y Habitat de las Liebres de la Peninsula
Iberica. Naturalia Hispanıca 19, 1-40.

Rau, J. R.; Kurner, M. B.; BELTRANn, J. F.; Derıses, M. (1992): Habitat segregation and temporal
overlap between rabbits and hares in Coto Donana, $.W. Spain. Säugetierkdl. Mitt. (in press).
Rocks, P. M.; Myers, K. (1980): Animal distribution, landscape classification and wildlife manage-

ment, Coto Donana, Spain. J. Appl. Ecol. 17, 545-565.
SCHNEIDER, E.; LEIPOLDT, M. (1983): D.N.A. relationship within the genus Lepus ın SW Europe.
Acta Zool. Fennica. 174, 31-33.

Evaluation of hare abundance allowed by their use of attraction points 372

SIEGEL, $. (1956): Non Parametric Statistics for the Behavioral Sciences. New York: McGraw Hill.

SORIGUER, R. C.; RoGERs, P. M. (1979): The European Wild Rabbit in Mediterranean Spain. In:
Proc. World Lagomorph Conf. Ed. by K. Myers and C. D. MacInnes. Guelph, Ontario: Univ.
Guelph. Pp. 600-613.

TayLor, R. H.; WırLıams, R. M. (1956): The use of pellet counts for estimating the density of
populations of the wild rabbit, Oryctolagus cuniculus (L.). N. Z. J. Sci. Tech. Sect. B, 38,
236-256.

VaLn£s, B.; TALAVERA, $.; FERNÄNDEZ-GALIANO, F. (Eds.) (1987): Flora Vascular de Andalucia
Occidental. Barcelona: KETRES Editora.

VALVERDE, J. A. (1960): Vertebrados de la Marisma del Guadalquivir. Almeria: Archivos del Instituto
de Aclimatacıön. Vol. IX.

WALKER, B. H. (1976): An approach to the monitoring of changes in the composition and utilization
of woodland and savanna vegetation. S. Afr. J. Wildl. Res. 6, 1-32.

Authors’ address: ALFONSO LAZO, CLAUDINE DE LE COURT, and RAMÖN C. SORIGUER, Estaciön
Biolögica de Donana, Consejo Superior de Investigaciones Cientificas, Apdo.
1056, E-41080 Sevilla, Spain

Z. Säugetierkunde 57 (1992) 380-381
© 1992 Verlag Paul Parey, Hamburg und Berlin
ISSN 0044-3468

WISSENSCHAFTLICHE KURZMITTEILUNG

Unusual record of the Spotted hyena (Crocuta crocuta)
in Rio Muni, Equatorial Guinea (Central Africa)

By J. Juste and J. CAsTROVIEJO

Estacion Biologica de Donana, Consejo Superior de Investigaciones Cientificas, Sevilla, Spain

Receipt of Ms. 13.3. 1992
Acceptance of Ms. 23.6. 1992

The spotted hyena (Crocuta crocnta Erxleben, 1777) has a subSaharan distribution,
spreading out over the savannah of Guinea and Sudan, showing preference for flat, open
grassland areas, and avoiding the closed forest areas of the Congo basın (Kruuk 1972;
RoseEvEAR 1974; KınacDon 1977).

On the night of September 27 to 28, 1991, a strange specimen, even for local people,
was killed by an automobile near Ndumu village (Nsork) on the south-eastern side of Rio
Muni, Equatorial Guinea (1°27’N, 11°10’E). The anımal, spotted and dog-like, was
photographed before being dissected. The photographs and some recovered skeletal
remains (tympanic bulla, left mandible together with its dentition, upper premolars,
phalanxes and cervical vertebrae), were compared with the available material deposited in
the collection of the Estacıön Biolögica de Donana, (Sevilla), which allowed us to identify
the specimen as a spotted hyena (Crocuta crocuta) beyond any doubt. It has not been
possible to determine its sex from the photographs because sexual dimorphism is very
slight ın this species and genitalia of both sexes appear very similar externally.

According to the third lower premolar wear, the specimen was a young adult, being
included ınto Kruur’s age class III (between 3 and 6 years old) (Kruuk 1972). This agrees
with the spot pattern of the skin, clearly defined all over the body. By counting the
incremental lines in cementum of the decalcified and stained medium incisor, an age of
seven years could be established for the individual, in accordance with the first estimation
based on teeth wear, according to VAN JAARSVELD et al. (1987).

The importance of this record lies ın the fact that the spotted hyena killed ın Equatorial
Guinea was in a closed wet lowland forest, ın the middle of the Congo basın forest block.
The existence of a stable population of spotted hyena in Equatorial Guinea can be rejected
because of the long distance from ıts known distribution area and because ıt would have
been detected by us over a period of more than 5 years, living in thıs small country (26,000
km’).

It seems more plausible that the record is related to an individual dispersal movement
away from a distant population. Regarding the mobility of the spotted hyena, important
displacements have been reported by Kruuk (1972) in Serengeti Park (Tanzania), related to
the seasonal migrations of the large or medium-sized ungulates which they prey upon. In
the Kalaharı desert (Botswana), the spotted hyena wanders as far as 80 km a day (ELOFF
1964). Occasionally, the spotted hyena occurs in gallery forests not far from grass-
woodlands, following tracks or roads. This could be the explanation of a possible record ın
Ibadan, Nigeria, on the western limit of the equatorial forest block (ROSEVEAR 1974). In
these western populations, it ıs not unusual to see lone individuals (HAarroıLD 1987), a

U.S. Copyright Clearance Center Code Statement: 0044-3468/92/5706-0380 $ 02.50/0

Unusual record of the Spotted hyena in Rio Muni, Equatorial Guinea 381

behavior possibly related to the diet and the distribution of food supply (Kruuk 1972;
Mırıs 1990).

The nearest appropriate savannah vegetation where the spotted hyena killed in Equato-
rial Guinea may have originated ıs located either in Cameroon or Gabon.

In fact, the nearest stable populations of Crocuta crocuta occur in Cameroon in Benoue
and Boubandjıdda Reserves (RONNEFELD 1969), but the species has not been seen south of
8°N. In Gabon, MALBRANT and MACLATCHY (1949) stated the farthest extension of the
species to the north was N’Dende (4°S), at the southern boundary with the Republic of
Congo. SMITHERS (1983) also reported its occurrence in the southern corner of the
country, but apparently the spotted hyena has been exterminated from the savannah
around Franceville. From either of these two possible points of origin, thıs spotted hyena
specimen would have been faced with almost insurmountable hydrographic barriers
(Sanaga, Ntem, Uoro, Ivindo, Ogooue£ rivers) on its way to Equatorıal Guinea, more than
700 km distant in a straight line.

The present record of a spotted hyena ın Equatorial Guinea, although exceptional, may
not be the first. The existence of a specific name (Ocam-niat) in the Fang vernacular
language, its presence in several popular tales and the different descriptions recorded
among villagers by BasıLıo (1962) as well as by ourselves, support this idea; its presence
has also been mentioned by hunters in several localities in the Gabon forest. These
displacements could be seen as evidence for deforestation or forest degradation on the
edges of the Congo forest.

Acknowledgements

Wethank Mr. UrcoLA and R. DELGADOo for their assistance in field work, C. IBANEZ, M. DeLiBEs, C.
KELLER, J. NEGRO and H. CAsweELL for their helpful comments to the first draft of this manuscript. S.
ZaAPATA kindly made teeth preparations and counted the incremental dental lines. STEPHEN GARTLAN,
WWF Representative for Cameroon, ALLARD BLom, WWF Advisor, and some specialists gave us
invaluable information. The work has partially been supported by the Spanish Instituto de Coopera-
cıön para el Desarrollo.

References

BasıLıo, A. (1962): La vida anımal en la Guinea espanola. Madrid: I.E.A. (CSIC).

ELOFF, F. C. (1964): On the predatory habits of lions and hyaenas. Koedoe 7, 105-112.

Harroıp, D. C. (1987): The mammals of Nigeria. Oxford: Clarendon Press.

Kıncoon, J. (1977): East African mammals. An atlas of evolution in Africa. Vol. IIIA. London:
Academic Press.

Krutvk, H. (1972): The spotted hyena. A study of predation and socıal behavior. Chicago: University
of Chicago Press.

MALBRANT, R.; MACLATCHY, A. (1947): Affınites australes de la faune du Congo frangaise et du
Gabon. Mammalia 11, 129-138.

Mirzs, M. G.L. (1990): Kalaharı hyenas. A comparative behavioral ecology of two species. London:
Unwin Hyman Ltd.

RONNEFELD, V. U. (1969): Verbreitung und Lebensweise afrıkanischer Feloidea (Felidae und
Hyaenıdae). Säugetierkundl. Mitt. 17, 285-350.

ROSEVEAR, D.R. (1974): The carnıvores of West Afrıca. London: British Museum (NH).

SMITHERS, R. H. (1983): The mammals of the Southern African subregion. Pretoria: University of
Pretoria Press.

VAN JAARSVELD, A. $.; HENSCHEL, J. R.; SKINNER, ]J. D. (1987): Improved age estimation in spotted
hyenas (Crocuta crocuta). J. Zool. Lond. 213, 758-762.

Authors’ address: Dr. JAVIER JuUsSTE and Dr. JAVIER CAsTROVIEJO, Estacıön Biolögica de Donana,
Aptdo. 1056, E-41080 Sevilla, Spain

BEKANNTMACHUNGEN

Ausschreibung des FrıTz-FRAnk-Preises
Förderpreis der Deutschen Gesellschaft für Säugetierkunde

Die Deutsche Gesellschaft für Säugetierkunde schreibt diesen Förderpreis in Höhe von
DM 3000,- als Anerkennung für hervorragende wissenschaftliche Leistungen junger
Forscher/innen aus.

Voraussetzung ist eine im Druck vorliegende Arbeit oder eine hervorragende Disserta-
tion aus den Gebieten Phylogenie und Systematik, Verbreitung, Ethologie, Ökologie und
Populationsbiologie der Säugetiere. Die Arbeit muß in den drei vorausgehenden Kalender-
jahren erschienen oder als Dissertation begutachtet worden sein. Die Bewerber/innen
dürfen beim Erscheinen der Arbeit bzw. beı ihrer Promotion nicht älter als 33 Jahre sein.

Bewerbungen der Vorschläge erbitten wir an die Geschäftsstelle der Gesellschaft, Prof.
Dr. H. ERKERT, Zoologisches Institut der Universität, Auf der Morgenstelle 28, D-7400
Tübingen, unter Beifügung von 5 Sonderdrucken bzw. Kopien der Dissertation bis zum
3391993:

Der Jury gehören Wissenschaftler verschiedener Universitäten oder Museen und Mit-
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Der Preis wird bei der Eröffnung der Jahresversammlung der Gesellschaft ın Tübingen
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Protokoll über die Mitgliederversammlung der Deutschen Gesellschaft
für Säugetierkunde e.V. am 21. September 1992 im Vortragssaal
in der Landesbibliothek Karlsruhe

Der 1. Vorsitzende, Herr SCHMIDT, eröffnet die Versammlung um 16.30 Uhr.

1. Die Tagesordnung wird angenommen.

2. Herr SCHMIDT verliest den Bericht über das abgelaufene Geschäftsjahr 1991. Im
Berichtsjahr erschien der 56. Band der „Zeitschrift für Säugetierkunde“ ın 6 Heften
mit 384 Seiten. Zusätzlich wurde allen Mitgliedern das Sonderheft mit den Kurzfas-
sungen der Vorträge und Posterbeiträge der Tagung in Hamburg zugesandt.

Auf Einladung von Herrn SCHLIEMAnN fand dıe 65. Hauptversammlung der Gesell-
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Die leichte Zunahme der Gesamtzahl der Mitglieder beruht auf Eintritten von
Interessenten aus den neuen Bundesländern.
Durch den Tod verlor die Gesellschaft folgende Mitglieder:

Dr. K. Birkmann, Karlsruhe,

Prof. Dr. J. KRATOCHVIL, Brno,

Prof. Dr. W. SCHULTZ, Preetz,

Prof. Dr. W. VoGeEL, München.

3. Herr ScHmiDT erläutert den durch Frau Kühnrich vorgelegten ausführlichen Jahres-
abschluß.

4. Die Kassenprüfer BOHLKEN und SCHLIEMANN haben keinen Anlaß zu Beanstandungen
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Bekanntmachungen 383

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studentische Mitglieder und DM 10,- für Ehepartner von Vollmitgliedern zu belassen.
Der Vorschlag, den Beitrag auf DM 45,- für Studenten aus den neuen Bundesländern
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verbilligten Zeitschriftenbezug für diesen Kreis studentischer Mitglieder noch ein
weiteres Jahr aufrechterhalten wird.

8. Die Mitglieder nehmen die Einladung von Herrn MAIER an, die 67. Hauptversamm-
lung vom 26.-30. September 1993 in Tübingen abzuhalten. Als Schwerpunktthemen
werden „Offene Probleme der Phylogenie und Systematik der Großgruppen“,
„Geruchssinn und olfaktorische Kommunikation bei Säugern“ und „Biologie der
Primaten“ gewählt. Die Einladung von Frau SPITZENBERGER, 1994 ın Wien zu tagen,
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weitere konkrete Vorschläge für eine Modernisierung bzw. Aktualisierung der Sat-
zung der DGS unter Einbeziehung von Vorschlägen der Reformkommission (TOP 11)
erarbeiten und formulieren soll.

11. Herr HUTTERER trägt die Vorschläge der Reformkommission vor, die anschließend
von der Versammlung ausführlich diskutiert werden. Die Mitglieder werden aufgefor-
dert, dem Vorstand bis zur nächsten Hauptversammlung Anregungen zu diesem
Thema zukommen zu lassen. Die Mitglieder werden gebeten, sich ın die Listen der zu
gründenden Arbeitsgemeinschaften einzutragen. Bei fünf Enthaltungen billigen die
Mitglieder den Beschluß des Vorstandes, DM 20000,- auf ein Festgeldkonto zu
übertragen und die Zinsen zu Förderzwecken zu verwenden.

12. a. Herr ScHmI1DT würdigt nachdrücklich die Arbeit von Herrn NIETHAMMER, dessen

Gesundheitszustand unverändert geblieben ist.

b. Er gibt die Einsetzung einer Tierschutz-Kommission unter dem Vorsitz von Frau
FEDDERSEN-PETERSEN bekannt und bittet die Mitglieder, sich mit Fragen, Vorschlä-
gen und Anregungen zu dieser Thematik direkt an sie zu wenden.

c. Herr HUTTERER erklärt sich bereit, einen Fragebogen zu erarbeiten, der als
Grundlage für eine Dokumentation über die Zentren der Säugetierforschung ın
Deutschland dienen soll.

d. In der Zeitschrift für Säugetierkunde sollen pro Heft zwei Seiten für „Mitteilungen
der Gesellschaft“ zur Verfügung stehen. Frau FEDDERSEN-PETERSEN sammelt Bei-
träge der Mitglieder und redigiert diese Mitteilungen.

Die Sitzung endet um 19.30 Uhr.

Prof. Dr. U. ScHMIDT Prof. Dr. H. ERKERT Dr. H. FRÄDRICH

1. Vorsitzender Geschäftsführer Schriftführer

BUCHBESEREGEIINKIEN

Gaıpa, K.; PROKOT, $.: Microchiroptera. Wien: Falter Verlag 1992. 144 pp., 48 Abb. 22
Farbtafeln. ISBN 3-85439-088-2 !

Das Büchlein enthält neun individuelle Beiträge über Fledermäuse in den Bereichen Zoologie,
Ethnologie und Kunstgeschichte, Bildende Kunst, Literatur und Sinologie. Die Absicht der Heraus-
geber war es, die Spuren, die diese außergewöhnlichen Tiere in den verschiedenen Kulturkreisen
hinterließen, in kurzen Übersichten darzustellen. Besonders eindrucksvoll gelang dies auch in dem
Abschnitt „Sinologie der Fledermaus“, vertreten doch gerade in diesem Kulturbereich die Fleder-
mäuse in vielfältiger Form das Glück der Menschen. In weiteren Beiträgen wurden die Probleme der
Echoortung, ihrer Evolution und schließlich die Besonderheiten des Fledermausfluges dargestellt. Die
22 verschiedenfarbigen, zum Teil kaum erkennbaren Sonagramme von Ortungslauten, lassen sich in
der vorliegenden Form eigentlich nur unter der Rubrik „Bildende Kunst“ einordnen.

E. KuLzer, Tübingen

SEIFERT, $. (Hrsg.): Verhandlungsbericht 5. Internationales Symposium zur Erhaltung
des Przewalskipferdes. Leipzig: Zoologischer Garten Leipzig, Pfaffendorfer Straße 29,
O-7010 Leipzig 1990. 343 S., zahlr. Abb. und Tab.

Wie man es bei Verhandlungsberichten häufig findet, ist auch in diesem Symposiumsband die Qualität
der Beiträge sehr variabel. Das Spektrum reicht von mehr anekdotischen Beiträgen bis zu inhaltsrei-
chen Darstellungen. Vier Hauptabschnitte (Komplexe) untergliedern den Band: I. Zucht und globaler
Masterplan, II. Wiederauswilderung, Ill. Veterinärmedizinische, genetische und allgemeine Themen,
IV. Anhang. 45 Einzelbeiträge werden entweder in deutscher, russischer oder englischer Sprache
geboten. Insbesondere im Abschnitt über Wiederauswilderung finden sich die Informationen, welche
in der ehemaligen Sowjetunion gewonnen wurden, nicht nur ım russischen Original, sondern auch in
einer deutschen Übersetzung. 1

Der erste Abschnitt beginnt mit der Übersetzung (IRMGARD SCHENK) eines historischen Doku-
ments aus dem Jahre 1881, der Beschreibung des Przewalskipferdes durch I. S. PoLJakov. Anschlie-
ßend bietet G. KrIScHE eine historische Bilddokumentation (56 Abb.) zur Entwicklung der Zucht
von Przewalskipferden. Für die Zucht der Art in Halle, welche durch die Lieferung eines Paares im
Jahre 1901 begann, liefert L. Baumann eine mit 25 Abb. illustrierte Darstellung.

Von der im natürlichen Lebensraum höchstwahrscheinlich ausgestorbenen Art steht wieder eine
Gefangenschaftspopulation von über 900 Tieren zu Verfügung. Diese schafft die Voraussetzung „für
die Rückführung des Przewalskipferdes in seine angestammte Heimat“ (S. SEIFERT). Insbesondere im
Abschnitt Wiederauswilderung wird der Leser mit Problemen, welche sich bei diesem Vorhaben
ergeben, konfrontiert. So wird geschildert, daß die Tiere in „Semireservaten“ von der menschlichen
Fürsorge relativ unabhängig werden sollen (WALTRAUT ZIMMERMANN). Dort erhalten Junghengste die
Möglichkeit, in Junggesellengruppen heranzuwachsen, in spielerischen Kämpfen ihre Kraft zu erpro-
ben um dann, 4- bis 5jährig, erfahren genug zu sein, sich in einem Harem durchsetzen zu können. Die
Auswilderung muß unter streng kontrollierten Bedingungen erfolgen, wie W. E. FLinT et al. in einem
Beitrag darlegen. Es sind immer nur kleine Gruppen auszuwildern; schon in den Semireservaten
sollten soziale Haremsgruppen gebildet worden sein, und zur genauen Überprüfung der Tiere muß
gewährleistet sein, daß die Tiere vor der Freisetzung individuell markiert wurden. Es ıst für die
Kontrolle der Pferde vor und nach der Wiederauswilderung notwendig, daß bewährte und aufeinan-
der abgestimmte tiermedizinische und genetische Verfahren angewandt werden. Diesen methodischen
Gesichtspunkten sind die Kapitel im dritten Abschnitt des Bandes gewidmet, in dem auch von L.
SCHLAWE das Problem der Nomenklatur domestizierter Arten in einem detailreichen Beitrag disku-
tiert wird. Mehr technische und organisatorische Probleme werden im Anhang behandelt.

Leider sind bei der redaktionellen Endkorrektur zahlreiche Druckfehler übersehen worden.

Der Herausgeber bezeichnet es in der Einleitung des Bandes als „Sternstunde.... dabei zu sein
und mitzuwirken, wenn eine Großtierart vor dem Aussterben bewahrt und der Natur zurückgegeben
wird“. Es ist zu hoffen, daß sich der in dieser Außerung mitschwingende Optimismus bei der
praktischen Arbeit bestätigt! P. LAnGER, Gießen

Subscription information for USA, Canada and Mexiko obtainable from Paul Parey Scientific
Publishers, PO Box 1815, New York, NY 10156-0610, USA. Phone (212) 679-0782, Telefax (212)
2159 3498.

Erscheinungsweise und Bezugspreis 1992: 6 Hefte bilden einen Band. Jahresabonnement Inland: 358,-
DM zuzüglich 13,80 DM Versandkosten, Gesamtpreis 371,80 DM einschließlich 7% Mehrwert-
steuer. Jahresabonnement Ausland: 358,- DM zuzüglich 18,- DM Versandkosten. Das Abonne-
ment wird zum Jahresanfang berechnet und zur Zahlung fällig. Es verlängert sich stillschweigend,
wenn nicht spätestens am 15. November eine Abbestellung im Verlag vorliegt. Die Zeitschrift
kann bei jeder Buchhandlung oder bei der Verlagsbuchhandlung Paul Parey, Spitalerstraße 12,
W-2000 Hamburg 1, Bundesrepublik Deutschland, bestellt werden. Die Mitglieder der „Deut-
schen Gesellschaft für Säugetierkunde“ erhalten die Zeitschrift unberechnet im Rahmen des

Mitgliedsbeitrages.
Z. Säugetierkunde 57 (1992) 6, 321-384

Mit einer Beilage des Verlages Paul Parey und mit dem Bandinhaltsverzeichnis

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