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ZEITSCHRIFT FÜR SAÄUGETIERKUNDE

INTERNATIONAL JOURNAL OF MAMMALIAN BIOLOGY

Organ der Deutschen Gesellschaft für Säugetierkunde

Volume 356, 1991 ISSN 0044-3468

Herausgeber / Editors

P. J. H. van Bree, Amsterdam — W. Fiedler, Wien — H. Frick, München — W. Herre, Kiel - 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. —- F. Strauß, Bern - E. Thenius, Wien — P. Vogel, Lausanne

Schriftleitung/Editorial Office D. Kruska, Kiel — P. Langer, Gießen

Mit 141 Abbildungen

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Verlag Paul Parey Hamburg und Berlin

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Wissenschaftliche Originalarbeiten

ALCANTARA, M.; TELLERfA, J. L.: Habitat selection of the Wood mouse (Apodemus sylvaticus) in cereal steppes of Central Spain. - Habitatwahl von Waldmäusen (Apodemus sylvaticus) ın Gesneidesteppen Zentralspaniens er... 00 u haeel en ne en ee le Le N

AscaRAY, C. M.; PERRIN, M. R.; McLacHtan, A.; Eıs, S. F.: Population ecology of the Hairy- footed gerbil, Gerbillurus paeba, in a coastal dunefield of South Africa. — Populationsökolo- gie des Rauhfußgerbills Gerbillurus paeba in einem Dünenfeld an der Küste von Südafrika . .

BRANDL, R.; BEZZEL, E.; REICHHOLF, ]J.; VÖLKL, W.: Population dynamics of the Red squirrel in Bavaria. - Populationsdynamik des Eichhörnchens in Bayern ........ 2.2.20...

BRITTON-DAVIDIAN, JANICE; VAHDATI, MEHRNOUCH; BENMEHDI, FATIMA; GROS, PAULE; NANCE, VALERIE; CROSET, H.; GUERASSIMOV, S.; TRIANTAPHYLLIDIS, C.: Genetic differ- entiation in four species of Apodemus from Southern Europe: A. sylvaticus, A. flavicollis, A. agrarins and A. mystacinus (Muridae, Rodentia). — Genetische Differenzierung bei vier Apodemus-Arten in Südeuropa: A. sylvaticus, A. flavicollis, A. agrarius und A. mystacinus (Mluneidlae; None) In FE TEN RE SR SL EN ER E RORRE EN

BRÜNNER, H.; NEET, C. R.: A parapatric scenery: The distribution and ecology of Sorex araneus and $. coronatus (Insectivora, Soricidae) in southwestern Germany. — Die parapatrische Szenerie: Die Verbreitung und Okologie von Sorex araneus und Sorex coronatus (Insecti- oraWSorierdae in Südwestdeutschland 2 2.0. 0 zen een le Felle

BRUORTON, M. R.; PERRIN, M. R.: Comparative gut morphometrics of Vervet (Cercopithecus aethiops) and Samango (C. mitis erythrarchus) monkeys. — Vergleichend-morphometrische Untersuchungen am Verdauungskanal von Grünaffen (Cercopithecus aethiops) und Diadem- alten (CET ET RENNER EEE EL AN OR a EEE

COMPARATORE, VIVIANA M.; MACEIRA, N. O.; BuscH, CrısTına: Habitat relations in Cteno- mys talarum (Caviomorpha, Octodontidae) in a natural grassland. — Habitat-Beziehungen von Ctenomys talarum (Caviomorpha, Octodontidae) auf natürlichem Grasland .......

Errıson, G. T. H.; SKINNER, J. D.: Thermoregulation and torpor ın African woodland dormice, Graphiurus murinus, following cold acclimation. — Thermoregulation und Torpor bei afrıkanischen Baumschläfern, Graphiurus murinus, nach Kältebelastung............

Espınosa, MARIA BEATRIZ; REIG, ©. A.: Cytogenetics and karyosystematics of South American oryzomyine rodents (Cricetidae, Sigmodontinae). Part III. - Zytogenetik und Karyosyste- matık von südamerikanischen Reisratten (Cricetidae, Sıgmodontinae) .... 2.2.2222...

FLADERER, F. A.: Der erste Fund von Macaca (Cercopithecidae, Primates) im Jungpleistozän von Mitteleuropa. — The first find of Macaca (Cercopithecidae, Primates) in the Late Hleistocenesol Central Europe Ge FE nee Nena eigape

GRANJON, L.; VAssaRT, M.; GRETH, A.; CRIBIU, E.-P.: Genetic study of Sand gazelles (Gazella subgutturosa marica) from Saudi Arabia. Chromosomal and isozymic data. — Genetische Untersuchungen an Sandgazellen (Gazella subgutturosa marıca) aus Saudi-Arabien. Chro- mosomalesundlelektrophoresische, Daten p e e nn

HERZIG-STRASCHIL, BARBARA; HERZIG, A.; WINKLER, H.: A morphometric analysis of the skulls of Xerus mauris and Xerus princeps (Rodentia; Sciuridae). -— Morphometrische Analyse der Schädel von Xerus inauris und Xerus princeps (Rodentia, Sciuridae)........

InGoLD, P.; MARBACHER, H.: Dominance relationships and competition for resources among chamois Rupicapra rupicapra rupicapra ın female social groups. -— Dominanzbeziehungen und Konkurrenz um Resourcen in Gruppen von weiblichen Gemsen (Rupicapra rupicapra VODRGDNE) No ee ee en oa N A Eee REG

JacoBsen, N. H. G.; NEwBERY, R. E.; DE WET, M. ].; VILJoEn, P. C.; PIETERSEn, E.: A contribution of the ecology of the Steppe pangolin Manis temminckü in the Transvaal. — Ein Beitrag zur Okologie des Steppenschuppentieres Manistemminckü in Transvaal .......

KeLT, D. A.; Parma, R. E.; GALLARDO, M. H.; Cook, J. A.: Chromosomal multiformity in Eligmodontia (Muridae, Sigmodontinae), and verification of the status of E. morgani. - Chromosomale Vielfalt bei Eligmodontia (Muridae, Sigmodontinae) und Bestätigung des STIUSVOML AN IONgaN En ne nee

Korz, V.: Social relations and individual coping reactions in a captive group of Central American Agoutis (Dasyprocta punctata). — Soziale Beziehungen und individuelle Bewälti- gungsreaktionen in einer Gehegegruppe mittelamerikanischer Agutis (Dasyprocta punctata) .

Kvam, T.: Reproduction in the European lynx, Lynx Iynx. — Fortpflanzung beim europäischen Lues, messen ora 06 men ol oc A ee

MADE, J. VAN DER: Sexual bimodality in some recent pig populations and application of the findings to the study of fossils. - Geschlechtsbimodalität bei einigen rezenten Schweinepo- pulationen und Anwendung der Befunde für das Studium an Fossilien... ...........

Near, B. R.: Seasonal changes in reproduction and diet of the Bushveld gerbil, Tatera leucogaster (Muridae: Rodentia), in Zimbabwe. — Saisonale Schwankungen in der Fortpflan- zung und in der Nahrungszusammensetzung beim Bushveld Gerbil Tatera lencogaster (Wusiel aeaRodentia)unyZmbabwer nennen

25

1912

41

306

272

169

177,

88

94

D92

207

146

Pessöa, LEıLa; Dos Reıs, $. F.: Cranial infraspecifie differentiation in Proechimys iheringi Thomas (Rodentia: Echimyidae). — Intraspezifische Schädelvariabilität bei Proechimys ihe- m eoihomasi(Rodentıa-Echimyıdae)

PEssÖA, LEıLA MARIA; Dos Reıs, $. F.: The contribution of cranıal indeterminate growth to non-geographic variation in adult Proechimys albispinus (Is. Geoffroy) (Rodentia: Echimyi- dae). -— Der Anteil des unbegrenzten Schädelwachstums an der Variabilität von Schädeln gleicher Herkunft bei adulten Proechimys albispinus (Is. Geoffroy) (Rodentia: Echimyidae) .

POGLAYEN-NEUWALL, 1.: Notes on reproduction of captive Bassariscus sumicrasti (Procyoni- dae). — Bemerkungen zur Fortpflanzung von Bassarıscus sumichrasti (Procyonidae) in Gelangenschalt 2... ca We. ee

POGLAYEN-NEUWALL, 1.; SHIVELY, J. N.: Testicular cycles of the Ringtail, Bassariscus astutus (Carnivora: Procyonidae). — Testicularzyklen des Katzenfretts, Bassariscus astutus (Carni- vora® Proeyonidae)”. nun a. en Pe A N u

PRINSLOO, PAULETTE; ROBINSON, T. J.: Comparative cytogenetics of the Hyracoidea: chromo- somes of two Hyrax species from South Africa. - Vergleichende Cytogenetik der Hyraco- idea: Chromosomen von zwei Schlierer Arten aus>Südalrıka

REır, URSULA; KLinGeL, H.: Hiding behaviour in wild Gerenuk (Zitocranius walleri) fawns. — Abliegeverhalten bert@erenuk- Kützent(Wtocranıny wall) a

ROPER, T. J.; TAIT, A. I; CHRISTIAN, $. F.; FEE, D.: Excavation of three badger (Meles meles L.) setts_ Die Strukturidreier BauerdesDachses(Melesıneles) re

SANTOS, T.; TELLERTA, J. L.: An experiment to test the consumption of arboreal food by Wood mouse Apodemus sylaticns. — Eın Experiment zur Ermittlung der Nahrungsaufnahme der Waldmaus Apodemusisylvanıens) au Baumenn a

Snıpes, R. L.; KRIETE, A.: Quantitative investigation of the area and volume in different compartments of the intestine of 18 mammalıan species. - Quantitative Untersuchung an Gesamtoberfläche und Volumen verschiedener Darmabschnitte von 18 Säugetierarten ..... .

SOMSOOR, S$.; STEINER, H. M.: Zur Größe des Aktionsraumes von Microtus arvalis (Pallas, 1779). — Home-range s1zelo 1 Mierotnstanoahs Wallasyle770)

SOMSOOKR, $.; STEINER, H. M.: Fangmethoden und Geschlechterverhältnis in Stichproben von Feldmauspopulationen, Microtus arvalıs (Pallas, 1779). — Sex ratio of Microtus arvalıs (Ballas, 1779) samplesieaushtiniehtferenugy,pesto ker ps

STORCH, G.; HABERSETZER, J.: Rückverlagerte Choanen und akzessorische Bulla tympanica bei rezenten Vermilingua und Eurotamandua aus dem Eozän von Messel (Mammalia: Xenar- thra). — Posteriorly displaced internal nares and supplementary auditory bulla in extant Vermilingua and Eurotamandua from the Eocene of Messel (Mammalıa: X enarthra) ee

SUCHENTRUNK, F.; WILLING, R.; HARTL, G. B.: On eye lens weights and other age criteria of the Brown hare (Lepus europaeus Pallas, 1778). — Über Augenlinsengewichte und andere Altersmerkmale beim Feldhasen (Lepus europaeus Pallas, 1778) ................

TAYLoR, P. ]J.; CAMPBELL, G. K.; MEESTER, J. A. J.; van Dyk, DEBORAH: A study of allozyme evolution in African mongooses (Viverridae: Herpestinae). - Untersuchungen zur Evolution afrıkanischer Mangusten (Viverridae: Herpestinae) aufgrund von Allozymen .........

VAN WAEREBEEKR, K.; CANTO, ].; GONZALEZ, ].; OPORTO, J.; BRITO, J. L.: Southern Right wahle dolphins, Zissodelphis peronii, off the Pacific coast of South America. - Das Vorkommen des südlichen Glattdelphins Zissodelphis peronui vor der Pazifik-Küste von Südamerika... ...

VrruLLo, A. D.; Cook, J. A.: The role of sperm morphology in the evolution of Tuco-Tucos, Ctenomys (Rodentia, Ctenomyidae): confirmation of results from Bolivian species. — Die Rolle von Spermienmorphologie in der Evolution der Kammratten, Ctenomys (Rodentia,

Otenomyidae) . „3. «2 aber dt an ve a N e VOLLETH, MARIANNE; TIDEMANN, C. R.: The origin of the Australian Vespertilioninae bats, as indicated by chromosomal studies. -— Die phylogenetische Herkunft der australischen

Vespertilionnaemachreytogenetischen Ersebn1Sse ng WIRTZ, P.; OLDEKOP, G.: Time budgets of Waterbuck (Kobus ellipsiprymnus) of different age, sex and social status. — Zeitbudgets bei Wasserböcken (Kobus elhpsiprymnus) von unter- schredlichem Alter @eschlechtund So zul statu se sr En

Wissenschaftliche Kurzmitteilungen

ANDERA, M.: First records of Microtus (Pitymys) felteni ın Albanien. — Erste Nachweise von Mhcrotusi (atyıny)S)Keltenun Ab anıene ANDREASSEN, H.-P.; BONDRUP-NIELSEN, $.: A comparison of the effects of a moss diet and a varıed diet on the growth of juvenile Wood lemmings, Myopus schisticolor (Lilljeb.). — Ein Vergleich über die Effekte von Moos- und Mischnahrung auf das Wachstum von jungen Waldlemmingen,Mpopusischistzeolon lLilljeb>) rer re re ee

34

219

195

722

3a

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129

19

225

200

a)

27

365

135

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339

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48

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378

ANsSORGE, H.: Diphyodont dentition of first premolar in the Red fox Vulpes vulpes (Linng, 1758). - Diphyodonte Dentition des ersten Prämolaren beim Rotfuchs Vulpes vulpes (Linng,

TEE) ee nn a ee 188 ROOKMAAKRER, L. C.: The scientific name of the bontebok. — Der wissenschaftliche Name für dien Buncbock » 5 sinken Sa a 2 a ER 190

BARRETTE, CYRILLE: Fully formed first lower premolars ın a White-tailed deer (Odocoilens virginianus Zimmermann, 1780). — Vollständig ausgebildete erste untere Prämolaren bei einem Weißwedelhirsch (Odocozleus virginianus Zimmermann, 1780)... .. 2.22.22... 121

BAvER, K.: Ein Fund des pliozän/pleistozänen Marderhundes Nyctereutes megamastoides (Pomel, 1843) in Österreich. - A first find of the pliocene to villafranchian raccoon dog INgerenentesmesamastoidesBomel, 1843)... 0... 2... onen nn.ne 245

Espınosa, MARIA BEATRIZ; VITULLO, A. D.; MErAnNI, Marıa $.: Chromosomes of the Argentine Andean mouse, Akodon andınus (Cricetidae: Sigmodontinae). - Chromosomen

der argentinischen Andenmaus Akodon andinus (Cricetidae: Sigmodontinae) ......... 124 Fıstanı, A.: First record of a fossil Cervus elaphus L., 1758, from Albania. - Erster Nachweis Emessossilenk@erunstelaphusıe, 1758 aus Albanien rn... 248

HEINRICH, D.: Some remarks on sıze differences of northwest German game populations from Neolithic to modern times. — Einige Bemerkungen über Größenunterschiede bei nordwest- deurschenWuldpopulauionenseitdemiNeolithikum . 2 In... .noeooneecen.n,. 59

JAEcK, KATHrın: Anomalies of the upper incisors in the genus Microtus (Cricetidae, Rodentia).

— Anomalien der oberen Schneidezähne innerhalb der Gattung Microtus (Cricetidae, Ro- demme) ara 0 0 ee er NER 2 BROT a EEE 254

PALOMARES, F.: Use of an active badger sett by Egyptian mongooses, Herpestes ichneumon, in

Southwest Spain. — Benutzung eines bewohnten Dachsbaus durch Ichneumone, Herpestes

hm emo IOISUd est. Spanien in en ee 119 QUMSIYEH, M. B.: Karyotype of the East European hedgehog, Erinaceus concolor, from Jordan. — Der Karyotyp beim osteuropäischen Igel, Erinaceus concolor, aus Jordanien ........ 375

ROTHE, H.; KoENnIG, A.: Sex ratio in newborn Common marmosets (Calhthrix jacchus): no indication for a functional germ cell chimerism. — Geschlechterverhältnis bei neugeborenen Weißbüschelaffen (Callıthrıx jacchus): keine Anzeichen von funktionalem Keimzellenchi-

MITSNUS #6 ee ee EN er DE ANGE 318 SAAVEDRA, BARBARA; SIMONETTI, J. A.: Archaeological evidence of Pudu pudu (Cervidae) in central Chile. - Archäologischer Beleg von Pudu pudu (Cervidae) in Zentralchile ..... ... 252 Bekanntmachungen SCHEN 5 u 0 2 0.8 a Be ee ee A EN 64, 126, 381 Buchbesprechungen

SCHLECHTE a N a le Re 1271922565383

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 in dieser Zeitschrift veröffentlichten Beiträge sind urheberrechtlich geschützt. Die dadurch begründeten Rechte, insbesondere die der Übersetzung, des Nachdrucks, des Vortrags, der Entnahme von Abbildungen und Tabellen, der Funk- und Fernsehsendung, der Mikroverfilmung oder der Vervielfältigung auf anderen Wegen, bleiben, auch bei nur auszugsweiser Verwertung, vorbehalten. Das Vervielfältigen dieser Zeitschrift ist auch ım Einzelfall grundsätzlich verboten. Die Herstellung einer Kopie eines einzelnen Beitrages oder von Teilen eines Beitrages ist auch im Einzelfall nur in den Grenzen der gesetzlichen Bestimmungen des Urheberrechtsgesetzes der Bundesrepublik Deutschland vom 9. September 1965 ın der Fassung vom 24. Juni 1985 zulässig. Sie ist grundsätzlich vergütungs- pflichtig. Zuwiderhandlungen unterliegen den Strafbestimmungen des Urheberrechtsgesetzes. Ge- setzlich zulässige Vervielfältigungen sind mit einem Vermerk über die Quelle und den Vervielfältiger zu kennzeichnen.

© 1991 Paul Parey. Verlag: Paul Parey, Hamburg und Berlin. Anschriften: Spitalerstraße 12,

W-2000 Hamburg 1; Seelbuschring 9-17, W-1000 Berlin 42, Bundesrepublik Deutschland. Printed in Germany by Westholsteinische Verlagsdruckerei Boyens & Co., Heide/Holstein

ISSN 0044-3468 56 (1-6) 1-384 (1991)

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01.56 (1), 1-64, Februar 1991 ISSN 0044-3468 C21274F

ZEITSCHRIFT FÜR SAUGETIERKUNDE

INTERNATIONAL JOURNAL OF MAMMALIAN BIOLOGY

Irgan der Deutschen Gesellschaft für Säugetierkunde

ur

3rünner, H.; Neet, C. R.: A parapatric scenery: The distribution and ecology of Sorex araneus and S. coronatus (Insectivora, Soricidae) in southwestern Germany. — Die parapatrische Szenerie: Die Verbreitung und Okologie

von Sorex araneus and Sorex coronatus (Insectivora, Soricidae) in Südwestdeutschland 1 3randl, R.; Bezzel, E.; Reichholf, J.; Völkl, W.: Population dynamics of the Red squirrel in Bavaria. — Populations- dynamik des Eichhörnchens in Bayern 10

jantos, T.; Telleria, J. L.: An experiment to test the consumption of arboreal food by Wood mouse Apodemus sylvaticus. - Ein Experiment zur Ermittlung der Nahrungsaufnahme der Waldmaus (Apodemus sylvaticus) auf

Bäumen 19 3ritton-Davidian, Janice; Vahdati, Mehrnouch; Benmehdi, Fatima; Gros, Paule; Nance, Valerie; Croset, H.;

Guerassimov, S.; Triantaphyllidis, C.: Genetic differentiation in four species of Apodemus from Southern Europe:

A. sylvaticus, A. flavicollis, A. agrarius and A. mystacinus (Muridae, Rodentia). —- Genetische Differenzierung bei

vier Apodemus-Arten in Südeuropa: A. sylvaticus, A. flavicollis, A. agrariuss und A. mystacinus (Muridae,

Rodentia) 25 >essöa, Leila, M.; Dos Reis, S. F.: Cranial infraspecific differentiation in Proechimys iheringi Thomas (Rodentia:

Echimyidae). — Intraspezifische Schädelvariabilität bei Proechimys iheringi Thomas (Rodentia: Echimyidae) 34

zlison, G. T. H.; Skinner, J. D.: Thermoregulation and torpor in African woodland dormice, Graphiurus murinus, following cold acclimation. - Thermoregulation und Torpor bei afrikanischen Baumschläfern, Graphiurus muri- nus, nach Kältebelastung

Wirtz, P.; Oldekop, G.: Time budgets of Waterbuck (Kobus ellipsiprymnus) of different age, sex and social status. — Zeitbudgets bei Wasserböcken (Kobus ellipsiprymnus) von unterschiedlichem Alter, Geschlecht und Sozialstatus 48

Wissenschaftliche Kurzmitteilungen

Heinrich, D.: Some remarks on size differences of northwest German game populations from Neolithic to modern times. — Einige Bemerkungen über Größenunterschiede bei nordwestdeutschen Wildpopulationen seit dem Neolithikum 59

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A parapatric scenery: the distribution and ecology of Sorex araneus and S. coronatus (Insectivora, Soricidae) in southwestern Germany

By H. BrÜnNER and C. R. NEET

Institut für Biologie I (Zoologie), Universität Freiburg, FRG, and Institut de Zoologie et d’Ecologie Animale, Universite de Lausanne, Switzerland

Receipt of Ms. 7. 6. 1990 Acceptance of Ms. 31. 7. 1990

Abstract

Studied the distribution of Sorex araneus and S. coronatus in southwestern Germany along a transect from the Upper Rhine Valley to the highest elevation, the Feldberg, in the Black Forest. 'The species were determined by polyacrylamide gel electrophoresis of total blood proteins. In the study area, the two species occurred in parapatry and showed an alternating altitude distributional pattern.

S. araneus was found in the bottom of the Upper Rhine Valley and in the heights of the Feldberg, while S. coronatus was present in the lower and intermediate altitude levels of the Black Forest. In the Zastler Valley, S. coronatus advances 400 m farther uphill than in the St. Wilhelmer Valley where the climate is relatively cold and inclement. Two contact zones were found, situated at different altitudes according to the valley. In the study area, the species appeared to be altitudinal vicariads.

The ecology and distributional history of S. araneus and $. coronatus are discussed in comparison with available data on their respective areas of distribution. It is argued that $. aranens occupies regions with rather continental climatic characters either on dry or wet soils. On the other hand, S$. coronatus prefers Atlantic climates and balanced soil humidity. The competitive interaction between S. coronatus and S. araneus and its biogeographical consequences are discussed.

Introduction

During the last 40 years, it gradually became obvious that in central and western Europe, the taxon Sorex araneus included a second, cryptic species: Sorex coronatus (e.g. HAUSSER et al. 1985; NEET 1989a; Hausser 1990; HaAusser et al. 1990). The two species are actually defined by their karyotypes (MEyLan and Hausser 1978) and have been shown to be clearcut species that do not hybridize (NEET and HAusser 1989).

Since the first records of $. coronatus in Germany (OLERT 1973; SCHWAMMBERGER 1976), some information has been published on its distribution in the Rhineland and Westphalia by HAnDweErk (1987). However, only very few data are available for southern Germany (BRÜNNER and HoFFRICHTER 1987; Braun and Kıschnick 1987; KnocH 1989).

In this paper we present new information on the distribution and ecology of S. araneus and $. coronatus in southwestern Germany (Freiburg region) and discuss their parapatric distribution in Europe, making special reference to the comparison of the distribution of the two species in southwestern Germany and western Switzerland.

- Material and methods

Shrews have been trapped in the dense, herbaceous vegetation found along small rivers or in similar vegetation along woodland paths. The trapping sites lie on a transect from the Kaiserstuhl in the Upper Rhine Valley to the Feldberg in the Black Forest. 100 live traps (Sherman, Tallahassee, USA) baited with a mixture of sardines in oil and rolled oats were exposed during 23 trapping dates in 19 trapping sites. A total amount of 87 shrews was captured and determined biochemically.

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2 H. Brünner and C. R. Neet

For electrophoretic determination, a blood sample of about 2 ul was taken from the tail. Blood samples were diluted ın a buffer solution, analysed according to a standard technique (HAussEr and ZUBER 1983) and ıdentified by the characteristic albumin patterns (NEET and Hausser 1989). As the electrophoretic technique has been tested in Switzerland only, karyological analyses were undertaken with some of the specimens of S. araneus and S. coronatus ın order to ascertain the reliability of the electrophoretic method in southwestern Germany (see NEET 1989a, for a discussion of the limitations of the applicability of the technique).

Karyotypes were prepared in the laboratory from air dried mitotic chromosomes taken from bone marrow cells. The preparations were either Giemsa stained in a4 % solution (BAKER et al. 1982) or G- banded (SEABRIGHT 1971). All the S. araneus specimens analysed from southwestern Germany belonged to the “Vaud” karyotype with 22-24 (NF = 40) meta- and acrocentric autosomes, i.e. the same karyotype as the one used to test the biochemical determination techniques (NEET 1989a; NEET and Hausser 1989). The individuals of $S. coronatus all had 20 metacentric autosomes (NF = 44).

Results

In the study area, $. araneus and S. coronatus appear to be parapatrically distributed, ı.e. ın conjunct contact, without wıde zones of sympatry (Fig. 1). The corresponding lıst of trapping sites includes the altitudes at which the two species were caught (Table 1).

Only one species, $. araneus, was found in the Upper Rhine Valley near Freiburg (Mooswald) and on the Kaiserstuhl. On the lower slopes of the Black Forest (near Ehrenkirchen) and of the Zartener Becken (near Freiburg), $. coronatus was the only species to be captured. In the Feldberg region, $. coronatus was the only species found up to 730 m in the Zastler Valley, and up to 700 m in the Bruggatal and in the St. Wilhelmer Valley. The upper limit of distribution of $. coronatus is at about 1050 m ın the Zastler Valley and 700 m in the St. Wilhelmer Valley. S. araneus ıs found between 900 m and 1450 m in the Zastler Valley and between 790 m and up to the top at the Feldberg (1496 m) in the St. Wilhelmer Valley.

As one would expect according to thıs altitudinal segregation pattern where S. araneus ıs found in the lowlands and higher mountain altitudes, while $. coronatus ınhabits middle range altıtudes, two contact zones were found. In these zones, as in other contact zones studied ın Switzerland (NEET and Hausser 1990), the two species may coexist. The first contact zone is sıtuated in the middle of the Zastler Valley, at 900 m, and the second one on the Schönberg, a foothill of the Black forest, at 400 m.

Discussion Distribution of S. araneus and S. coronatus in southwestern Europe

The results presented here strongly suggest a parapatric Aislinion a che ma species ın southwestern Germany. This ıs consistent with the general pattern described ın central and western Europe by Hausser et al. (1985). The alternating altitude distribution found here also corresponds to the one found in western Switzerland (Hausser 1978) and confirms current views on the ecology of the two species.

As a matter of fact, $. coronatus inhabits wide areas of northwestern Spain and most parts of France. In these countries, $. araneus is restricted to higher altıtudes (Pyrenees, Massıf central, Alpes), and the parapatric distribution ıs clearcut (HAusser et al. 1985).

Moving towards the east and the north of Europe, the parapatrıcal distribution turns out to be progressively realized on a meso-distributional level and becomes more and more diffieult to visualize on a large scale. In Switzerland, S. coronatus is mainly present in the lowlands, the lower parts of the Jura and the Alps. In some places this species may, however, extend up to 1400 m of altitude. $. aranens ıs the dominant species above 800 m, but also occurs at low altitudes ın wet habitats such as the borders of the Lake ot Neuchätel. Although a simple histogram of their altıtudinal distributions suggests a wide

The distribution and ecology of Sorex araneus and 5. coronatus 3

zone of sympatry, all detailed distributional studies have confirmed strict parapatry with contact zones never exceeding a few hundred meters (HAusser 1978; HAUSSER and Bourquin 1988; NEET 1989a; NEET and Hausser 1990). In Belgium, S. coronatus is the most common species in the western parts of the country. $. aranens appears in the eastern lowlands and the medium altıtudes ın the south of the country (Mys et al. 1985). In Holland, $. araneus occurs alone in the depressions in the north but the two species are believed to co-occur in the remainder of the country (LocH 1977). There ıs, however, some evidence that $. araneus is mainly distributed in areas below sea level, while $. coronatus occurs ın areas above this level (Hausser pers. comm.). In northeastern Germany the two species co-occur over a large area: Niederrheinische Tiefebene, Mittel- rhein, westfälische Bucht, Rheinisches Schiefergebirge (HUTTERER and VIERHAUS 1984; HANDWERK 1987).

One can sum up at this point by stating that $. coronatus ıs found ın areas with a balanced Atlantic climate, while $. araneus occurs in colder or wetter habitats, and that the parapatric distribution ıs decreasingly distinct as one proceeds towards the north of

Europe.

Distributional ecology of S. araneus and S. coronatus in southwestern Germany

In southern Germany three climatic zones have been differentiated (LIEHL and Sıck 1984): 1. the warm, dry and continental Upper Rhine Valley; 2. the humid lower-altitude foothills of the Black Forest (up to 600 m), with an Atlantic climate; and 3. the heights of the Black Forest (up to 1500 m) with a typically subalpıne climate and abundant rainfall. These zones closely correspond to the altitudinal distribution zones of the two species S$. araneus and S. coronatus. The fırst species ıs found in the Upper Rhine Valley and above 790 m in the Black Forest, while the second ıs mainly found at low altitudes of the Black Forest. Interestingly, a correspondance between altıtudınal zones of vegetation and the distribution of the two species has also been demonstrated in western Switzerland (NEET 1989a).

The glacier-formed St. Wilhelmer Valley ıs wide with high nocturnal eradiation. It opens with a gradual slope into the Bruggatal almost right angles at a very narrow point (Fig. 1). Thus, the cold air is often congested providing a rough clımate. Moreover, the valley is on a lee position with rather low rainfall. In contrast, the Zastler Valley ıs narrow and steep sloping with several steps. It describes a slıght bow and opens widely into the Bruggatal (Fig. 1). Thus, the cold aır from the Feldberg heights can discharge quickly without any obstacle. As it ıs in a windward position, higher rainfall is noted (SCHWABE- KRATOCHWIL and BOGENRIEDER, pers. comm.). In the St. Wilhelmer Valley, S. coronatus was trapped up to an altıtude of 700 m, in contrast to the clımatıcally favoured Zastler Valley, where ıt can be found up to 1050 m.

An interesting parallelism with this observation has been reported for a contact zone of the Sorex species in a valley of the Valaısan Alps between Val d’Illiez and Champery (MEyLAn 1964; Orr 1968). There, $. coronatus occurred on the southeastern slopes of the valley about 1 km farther uphill than on the other sıde of the river at the bottom of the northwestern slopes. It can be supposed that the banks along the southeastern slopes are also climatıcally favoured, thus enabling S. coronatus to reach higher into the Valley. Other sımilar examples have been found for the distribution of the two species in Switzerland (Hausser and BourQuin 1988).

Another distributional pattern, similar to the one found in our study area, can be expected to be found for the two Sorex species in northern Baden, where S. araneus was trapped ın the Hardt Forest near Karlsruhe (BRÜNNER unpub.) and in several locations in the south of Rastatt (NIETHAMMER pers. comm.). $. coronatus was found in a beech forest at 300 m on the western slopes of the Black Forest. In this area, 26 individuals of S.

4 H. Brünner and C. R. Neet

0 1 2km

Fig. 1. Trapping sites and distribution of $S. araneus (black circles) and $. coronatus (white circles) in the study area. The contact zone is given by a black and white circle. A: Freiburg region, in southwestern Germany, B: Feldberg region in the Black Forest. Locality numbers correspond to

Table 1

coronatus and 3 of S. araneus were captured (Braun and KıscHnIck 1987). The shrews might have been taken from a contact zone but, at present, no additional data are available for this region.

Whereas the distribution of the Sorex species ın the Black Forest corresponds to the situation throughout Europe described above, the occurrence of S. araneus in the Upper Rhine Valley, where it has already been found ın Alsace by Hausser (1978), and the sımultaneous absence of $. coronatus reveal a possible significance of drought and heat factors of the continental climate for the distributional ecology of the two species. An additional indication comes from the Catalan parts of the Pyrenees where the climate ıs dry, warm and Mediterranean-like and where $. araneus descends to low altitudes, while S.

The distribution and ecology of Sorex araneus and $. coronatus 5

coronatus ıs only found at 800-1500 m, although it is wıdespread ın the Atlantic climate of northwestern Spain (LOPEZ-FUSTER et al. 1985).

Ecological comparison of the two species

In contrast to $. coronatus having a relatively limited distribution in western Europe, S$. araneus has a large distributional range from the Pyrenees to Lake Baikal in Sıberia with its distributional centre in the continental east. As a species, S. aranens reveals greater ecological valency (Hausser and BourQUIn 1988). This point is supported by some aspects of the evolutionary biogeography of the two shrew species. The British mainland, for example, with typical Atlantic climate, is only inhabited by $. araneus since $. coronatus did not arrıve before its separation from the continent after the last glaciations. This species also did not succeed ın passing the Alps to northern Italy. In these two regions S. araneus occupies all suitable habitats in the plains and in the mountain areas. As shown by Hausser and Bourquin (1988), in Switzerland S. araneus would be able to exist ın most biotopes of the country. Its absence ın the lowlands can more convincingly be explained by competition pressure going out from $. coronatus than by autoecological constraints (NEET and HAusser 1990). It should, however, be pointed out that $. araneus is not a simple species, but consists of several chromosomal types (e.g. SEARLE 1984; Hausser et al. 1985; HAusseEr et al. 1986; REUMER and MEyLAN 1986). To what extent are these races differentiated from an ecological point of view is not yet known and, obviously, this point may be of crucıal importance in explaining the apparently wide ecological valency of S. araneus.

The principle stating that ecologically ıdentical species cannot coexist (GAUSE 1934) is now widely accepted (BEGon et al. 1986). As a consequence of the general similarıty of S. araneus and S. coronatus, competition is an important factor ın the lack of overlap of their distributional ranges (HAusser 1978; NEET and Hausser 1990). An ecological field analysıs ın Switzerland revealed that in two contact zones, the two species coexisted over a

Table 1. List of trapping sites in southwestern Germany, classified by their altitudes

Altitude Species n (ind.) Locality

( m a.s.l.) S. araneus/ S. coronatus

1/0 1/0 0/1 2/0 3/3 2/0 0/1

1450 1230 1050 900 900 790 730 700 600 540 420 400 390 360 350 300 270

Feldberg, near top

Feldberg, Zastler Hut

Upper Zastler Valley

Upper St. Wilhelmer Valley Middle Zastler Valley

Upper St. Wilhelmer Valley Lower Zastler Valley

0/7 Middle St. Wilhelmer Valley

0/1 Lower Zastler Valley

0/5 Bruggatal, near Oberried

0/2 Zartener Becken, near Oberried 1/1 Schönberg, near Ebringen

0/1 Zartener Becken, near Kirchzarten 0/2 Zartener Becken, near Freiburg 0/1 Schönberg, near Ebringen

0/3 Border of Black Forest, near Ehrenkirchen 3/0 Kaiserstuhl, Liliental

230 4/0 Mooswald, northwest of Freiburg 21115 42/0 Mooswald, southwest of Freiburg

Black circles = $S. araneus, white circles = $. coronatus, black and white circle = contact zone. Locality numbers correspond to Fig. 1

DOoONONVURUDND-

® ® ®) © Ö © ©) ®) ©) ©) © Ö ©) ©) © ©) ® ® ®

6 H. Brünner and C. R. Neet

limited zone of overlap by selecting different microhabitats, those of $. araneus having a thicker litter layer and higher soil humidity (NEET and Hausser 1990). It was also shown that $. araneus and S. coronatus occupy the same trophic niche in their zones of contact (NEET 1989a) and that equal intensities of ıntra- and interspecific competition for food as a limiting factor lead to interspecific territoriality (NEET 1989b). In other words, the two species do differ in terms of their ecoclimatic adaptations but are still too similar to coexist. This example thus illustrates the usefulness of the principle of limiting similarıty proposed by Mac ARTHUR and Levins (1967).

If the high ecological similarity of $. araneus and S. coronatus does not allow sympatrical distribution, and although the contact zones we observe today seem to be relatively stabilized, one may suppose that, on an evolutionary time scale, one species will dominate the other and, with climatic changes, will replace it over an appreciable geographical space. This is how the distributional ecology of S. araneus and S. coronatus has been interpreted, since the actual distribution of the two species bears several indications that S. coronatus has forced $. araneus up to the north and east of Europe since the last glaciations. Moreover, the limited adaptations of both species to regionally or locally different climates in connection with mutual exclusion are considered to be characteristics of an early stage of ecological differentiation (HAUSSER 1984; HAussERr et al. 1985).

The results presented here confirm the parapatric interpretation (e.g. HAussEr et al. 1985; Hausser and BoURQUIN 1988) especially since there is a clear similarity between the situation in southwestern Germany and that in western Switzerland (Table 2). In central and northern Germany, the situation is less clear and the distribution is more mosaic-like. In that area, the distribution of the two species is sometimes considered as sympatrical (HUTTERER pers. comm.). HANDWERK (1987) reported ratios of $. araneus: S. coronatus of 1:1t0 1:3 for the plains of the Niederrhein and the Cologne-Bonn region, and 2:1 ratios

Table 2. Comparison of the distributional ecology of S. araneus and S. coronatus in southwestern Germany and western Switzerland

Data for western Switzerland are taken from NEET 1989a

Southwestern Germany Western Switzerland

Altıtude range S. araneus 215-1450 m 380-1950 m S. coronatus 300-1050 m 490-1340 m

Type of distribution parapatric parapatric

Relative habitat preferences S. araneus cold (continental) wet and cold S. coronatus warm (Atlantic) dry and warm balanced humidity

Breadth of contact zones 200-2000 m? 100-1000 m®

Ecological relationship

in the contact zones Habitat selection in response to interspecific competition Interspecific territorıality

“The breadth of the contact zones was estimated as follows: in the Zastler Valley, the breadth was estimated to be equivalent to the length of the trapping area, ı. e. 200 m; in the St. Wilhelmer Valley the maximal breadth was estimated to be 01 2000 m, which corresponds to the distance between capture points 6 and 8 (Fig. 1). - ° Nerr (1989) indicates breadths around 100 m. However, ın patchy areas (woodlands alternating with grasslands) it is difficult to estimate a precise value (see NEET and HAusser 1990). However, maximal values around 1000 m have been estimated.

The distribution and ecology of Sorex araneus and S. coronatus 7

for the adjacent regions of medium altıtude. NEET and Hausser (1990) consider that the work of Hanpwerk (1987) lacks sufficient detail to ascertain whether the two species are sympatrically or parapatrically distributed in that area. A detailed ecological study might reveal local differentiation, which may be very subtle, as in the Swiss contact zones. Nevertheless, an alternative hypotheses exists and is due to the simple fact that resource availability influences interspecific competition. In the contact zones studied by NEET and Hausser (1990), there is evidence that food was a limiting factor (NEET 1989a) and that competitive pressure induced interspecific territoriality (NEET 1989b). If there are no limiting ressources, the situation may change. An example is given in the work by LLEwELLYN and JENKINS (1987) on the cricetids Peromyscus maniculatus and P. trueı, where it was shown that there are seasonal changes in overlap of microhabitat niche, and that these changes may be explained by the degree of resource scarcity. In one of the contact zones studied in Switzerland, it was shown that the competitive pressure between S. araneus and S. coronatus ıs present throughout the year (NEET and Hausser 1990). However, the situation may be different in central and northern Germany. A seasonal variation in competitive pressures is a realistic hypothesis and may result in varıations of the degree of overlap between the two species and limited sympatry.

Acknowledgements

One of us (H. B.) gratefully received important impulse for this work from Prof. G. ÖscHE, University of Freiburg. We both thank Prof. P. VoGEL and Prof. J. HAaussEr from the University of Lausanne for their support, interest and help in this research. The electrophoretic determinations were started in the Institute of Zoology and Animal Ecology of the University of Lausanne and later performed in the laboratory of Prof. H. GUTZEIT, University of Freiburg, with friendly support of V. Grau. Traps were placed at disposal by M. Brau, Staatliches Museum für Naturkunde, Karlsruhe. The work was supported by Prof. FRIEDRICH KIEFER-FonDs, Badischer Landesverein für Natur- kunde und Naturschutz e.V. Many thanks are due to H. Brack for her invaluable help in the field.

Zusammenfassung

Eine parapatrische Szenerie: Die Verbreitung und Ökologie von Sorex araneus und Sorex coronatus (Insectivora, Soricidae) in Südwestdeutschland

Die Verbreitung von Sorex aranenus und Sorex coronatus ın Südwestdeutschland wurde in einem Transekt vom Oberrheingraben zum Feldberg ım Schwarzwald untersucht. Die Artbestimmung geschah mittels einer Polyacrylamıid-Gelelektrophorese des Gesamtbluteiweißes. Im Untersuchungs- raum waren die beiden Arten parapatrisch verbreitet, und dies in Form einer alternierenden Höhen- verbreitung. $. araneus wurde im Oberrheintal und am oberen Feldberg angetroffen, $. coronatus in den unteren und mittleren Schwarzwaldlagen. Im klimatisch begünstigten Zastler Tal reicht die Verbreitung von S. coronatus 400 Höhenmeter weiter talaufwärts als im kälteren und rauheren St. Wilhelmer Tal. Zwei Kontaktzonen, eine obere und eine untere, wurden ausfindig gemacht. Im Untersuchungsgebiet können die beiden Arten als höhenvikariierende Arten bezeichnet werden. Die Ökologie und Verbreitungsgeschichte von $. araneus und S. coronatus wird anhand der bisher bekannt gewordenen Daten über ihre Lebensräume diskutiert. $. araneus besiedelt Gebiete mit eher kontinen- talem Charakter sowie Lebensräume mit nassen und trockenen Böden. Dagegen bevorzugt S. coronatus atlantisches Klima und ausgeglichene Bodenfeuchtigkeit.

References

BAKER, R. J.; Haıpuk, M. W.; RoBBıns, L. W.; CADENA, A.; Koop, B. F. (1982): Chromosomal studies of South American bats and their systematic implications. Special publ. Pymatuning Lab. Ecol. 6, 303-327.

BEcon, M.; HARPER, J. L.; TownsenD, C. R. (1986): Ecology. Individuals, Populations and Communities. Oxford: Blackwell.

BRAUN, M.; Kischnick, P. (1987): Spitzmäuse und ihre Nahrung in einem Buchenwald. Carolinea 45, 159-160,

8 H. Brünner and C. R. Neet

BRÜNNER, H.; HOFFRICHTER, ©. (1987): Neue Fundorte der Alpenspitzmaus (Sorex alpinus Schinz, 1837) im Südschwarzwald. Mitt. bad. Landesver. Naturkunde u. Naturschutz N.F. 14, 403-408.

Gause, G. F. (1934): The struggle for existence. Baltimore: Wıiliams and Wilkins Co.: (1934). New York: Hafner Publ. (Repr. 1964). 3

HANDWERK, J. (1987): Neue Daten zur Morphologie, Verbreitung und Okologie der Spitzmäuse Sorex araneus und $. coronatus ım Rheinland. Bonn. zool. Beitr. 38, 273-297.

Hausser, J. (1978): Repartition en Suisse et en France de Sorex araneus L., 1758 et de Sorex coronatus Millet, 1828 (Mammalia, Insectivora). Mammalıa 42, 329-341.

— (1984): Genetic drift and selection: Their respective weights in the morphological and genetic differentiation of four species of shrews in Southern Europe (Insectivora, Soricidae). Z. zool. Syst. Evolut.-forsch. 22, 302-320.

— (1990): Sorex coronatus Millet, 1828. In: Handbuch der Säugetiere Europas. Ed. by J. NIETHAM- MER and F. Krapp. Wiesbaden: Aula-Verlag.

Hausser, J.; Bouraumn, J.-D. (1988): Repartition de douze especes de mammiferes en Suisse. Atlas des Mammiferes de Suisse. Societe suisse pour l’Etude de la faune sauvage, Lausanne.

HaAussER, J.; CATZEFLIS, F.; MEyLAN, A.; VOGEL, P. (1985): Speciation in the Sorex araneus complex (Mammalia: Insectivora). Acta Zool. Fennica 170, 125-130.

HaussER, J.; DANNELID, E.; CATZEFLIS, F. (1986): Distribution of two karyotypic races of Sorex araneus (Insectivora, Soricidae) in Switzerland and the post-glacıial recolonization of the Valais: First results. Z. zool. Syst. Evolut.-forsch. 24, 307-314.

HaAUuSSER, J.; HUTTERER, R.; VOGEL, P. (1990): Sorex araneus L. 1758. In: Handbuch der Säugetiere Europas. Ed. by J. NIETHAMMER and F. Krapp. Wiesbaden: Aula-Verlag.

HaussER, J.; ZUBER, N. (1983): Determination specifique d’individus vıvants des deux especes jumelles Sorex araneus et $. coronatus, par deux techniques biochimiques (Insectivora, Soricidae). Rev. suisse Zool. 90, 857-862.

HUTTERER, R.; VIERHAUS, H. (1984): Waldspitzmaus, Schabrackenspitzmaus. In: Die Säugetiere Westfalens. Ed. by R. SCHRÖPFER; R. FELDMANN and H. VIERHAUS. Münster: Abh. Westf. Mus. Naturkunde 4, 54-60.

Knoch, D. (1989): Säugetiere im Belchengebiet. In: Der Belchen im Schwarzwald. Die Natur- und Landschaftsschutzgebiete Baden-Württembergs 13. Landesanstalt für Umweltschutz, Baden- Württemberg, 1159-1165.

LiEHL, E.; Sick, W. D. (1984): Der Schwarzwald - Beiträge zur Landeskunde. 3 ed. Ver. Allemann. Inst. Freiburg ı. Br. 47. Bühl, Baden: Konkordıa.

LLEWELLyYN, J. B.; JEnKIns, $. H. (1987): Patterns of niche shift in mice: Seasonal changes in microhabitat breadth and overlap. Am. Nat. 129, 365-381.

LocH, R. (1977). A biometrical study of karyotypes A and B of Sorex araneus Linnaeus, 1758, in the Netherlands (Mammalıa, Insectivora). Lutra 19, 21-36.

LOPEZ-FUSTER, M. J.; GOSALBEZ, ]J.; Sans-CoMA, V. (1985): Presencia y distribucion de Sorex coronatus Millet, 1828 (Insectivora, Mammalıa) en el NE iberico. P. Dept. Zool. Barcelona 11, 93-97.

Mac ARTHUR, R. H.; Levins, R. (1967): The limiting sımilarity, convergence and divergence of coexisting species. Am. Nat. 101, 377-385.

MeEyLan, A. (1964): Le polymorphisme chromosomique de Sorex araneus L. (Mammalia, Insectiv- ora). Rev. suisse Zool. 71, 903-983.

MEyLAn, A.; HaussEr, J. (1978): Le type chromosomique A des Sorex du groupe araneus: Sorex coronatus Millet, 1828 (Mammalıa, Insectivora). Mammalıa 42, 115-122.

Mys, B.; VAN DER STRAETEN, E.; VERHEYEN, W. (1985): The biometrical and morphological ıdentification and the distribution of Sorex araneus L., 1758 and $. coronatus Millet, 1828 in Belgium (Insectivora, Soricıdae). Lutra 28, 55-70.

NEET, C. R. (1989a): Ecologie comparee et biog&ographie Eevolutive de deux especes parapatriques: Sorex araneus et S. coronatus (Mammalıa, Insectivora, Soricidae). Ph. D. thesis, University of Lausanne.

— (1989b): Evaluation de la territorialite interspecifique entre Sorex araneus et $S. coronatus dans une zone de syntopie (Insectivora, Soricidae). Mammalıa 53, 329-335.

NEET, C. R.; Hausser, J. (1989): Chromosomal rearrangements, speciation and reproductive isolation: the example of two karyotypic species of the genus Sorex. J. evol. Biol. 2, 373-378.

— — (1990): Habitat selection in zones of parapatric contact between the common shrew Sorex araneus and Millet’s shrew S. coronatus. J. Anım. Ecol. 59, 235-250.

OLERT, J. (1973): 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.

OTT, J. (1968): Nachweis natürlicher reproduktiver Isolation zwischen Sorex gemellus sp. n. und Sorex araneus Linnaeus, 1758 ın der Schweiz (Mammalıa, Insectivora). Rev. suisse Zool. 75, 53-75.

The distribution and ecology of Sorex araneus and S. coronatus 9

REUMER, J. W. F.; MEyLan, A. (1986): New developments in vertebrate cytotaxonomy IX: Chromo- some numbers in the order Insectivora (Mammalia). Genetica 70, 119-151.

SCHWAMMBERGER, K. H. (1976): Nachweis der Schabrackenspitzmaus (Sorex gemellus Ott, 1968) in Westfalen. Natur u. Heimat 36, 66-69.

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

SEARLE, J. B. (1984): Three new karyotypic races of the common shrew Sorex araneus (Mammalıa: Insectivora) and a phylogeny. Syst. Zool. 33, 184-194.

Authors’ addresses: HARALD BRÜNNER, Institut für Biologie I (Zoologie), Albertstraße 21a, Albert- Ludwigs-Universität, W-7800 Freiburg/Br., FRG, and Dr CorneLis R. NEET, Conservation de la faune, Chemin du Marquisat 1, CH-1025 St. Sulpice, Switzer- land

Z. Säugetierkunde 56 (1991) 10-18 © 1991 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-3468

Population dynamics of the Red squirrel in Bavaria By R. BranDı, E. BEZZEL, J. REICHHOLF and W. VÖöLkL

Lehrstuhl für Tierökologie I, Universität Bayreuth, FRG, Institut für Vogelkunde, Garmisch-Partenkirchen, FRG and Zoologische Staatssammlung München, FRG

Receipt of Ms. 23. 5. 1990 Acceptance of Ms. 30. 7. 1990

Abstract

Describes the population dynamics of the red squirrel (Sciurus vulgaris) in Bavaria since the early 1970s. A decline ın the population of squirrels was found between 1970 and 1980, while recently an increase was recorded. The decline can be attributed to reproductive waves caused by mast years of coniferous trees. The recent increase can be explained by general forest decline, since damage to trees desynchronizes seed production and squirrels are provided with a constant food resource over a number of years.

Weather conditions were found to be unimportant for the population dynamics of squirrels. For the beech marten (Martes foina), however, a negative correlation could be demonstrated between number of squirrels and this predator at one study site.

Introduction

Compared to birds the available data on long-term fluctuations of medium-sized mammals are very rare. This is due to the difficulties to trap and count these animals within a reasonable period of time. Even for diurnal species like the red squirrel (Sciurus vulgaris) only a limited amount of information ıs available. Long-term series are badly needed to document the full range of patterns in the population dynamics of mammals. In game biology there ıs a long tradition to use hunting bags or other indirect measures to document fluctuations in game animals (for a recent example see PoTTs et al. 1984). We followed this line of investigations and present indirect density indices to describe the dynamics of the red squirrel in Bavaria. We concentrate on the following questions:

1. Are there any long-term trends in the population of squirrels in Bavaria? In two reports we suggested that there was a decline in numbers of squirrels since the early 1970s (BrAanDL 1983; REICHHOLF 1983).

2. Is the dynamics of the squirrel populations similar in different regions of Bavaria?

3. The main food of the red squirrel is the seeds of coniferous trees (WILTAFSKY 1978). Many studies have shown that the populations of squirrels follow seed production (Formosov 1933; PULLIAINEN 1984; REICHHOLF 1974). Is this pattern also evident within our sets of data?

4. The red squirrel is the prey of several predators such as the pine and beech marten (Martes martes, M. foina; STUBBE 1988). Do these species have some influence on the populations of the red squirrel?

Material and methods

In the following we name each data set by its geographical location (see Fig. 1):

1. Pressath: This data set consists of specimens delivered to a taxidermist between September and March from 1965/66 onwards to 1982/83 with a gap between 1967/68 and 1972/73 (550 individuals; Branpı 1983). The working period of the taxidermist was not constant over the years. We used the

U.S. Copyright Clearance Center Code Statement: 0044-3468/91/5601-0010 $ 02.50/0

Population dynamics of the Red squirrel in Bavarıa 11

U] Bad Berneck

Pressath

8 Nürnberg

München

Garmisch - Partenkirchen Fig. 1. Geographical location of the investigated areas in Bavaria

number of mammals and birds to standardize red squirrel data and calculated percentages of red squirrels delivered to the taxidermist.

Around Pressath the dominating types of vegetation are spruce forests (Picea abies) and at poorer sites pine forests (Pinus sylvestris). Altitudes range from about 400 to 600 m NN.

2. Bad Berneck: Similar to Pressath these data are specimens delivered to a taxidermist between 1970 and 1988 (922 individuals). This taxidermist worked over the entire year. We standardized the data because the overall working effort appeared to vary from year to year. The number of delivered birds was used as an independent measure of the working effort. Numbers of red squirrels are expressed in individuals delivered per 100 birds.

Bad Berneck is situated within the Fichtelgebirge. Spruce forests are the dominating type of vegetation, and the altitudes range from 500 to 1000 m. At higher altitudes winters may be quite severe.

For this area we have also data about weather, seed production of the spruce and dynamics of one potential predator.

a. Monthly information of rainfall and temperature was available for Bayreuth, only 10 km from

Bad Berneck. b. The forest authorities estimate the seed production in four categories: “Vollmast” = very high

12 R. Brandl, E. Bezzel, J. Reichholf and W. Völkl

seed production, “Halbmast” = good seed production, “Sprengmast” = low seed production and no seed production. We ranked each year on this scale from O0 to 3 and allowed for intermediate values according to information of the forest authorities (available years 1971 to 1988).

c. The number of martens delivered to the taxidermist (pine and beech marten) may be used as an indicator of the predator density. The pine marten is rather uncommon in the area around Bad Berneck, so we concentrate on the beech marten. Data were standardized similar to those for squirrel numbers.

3. Inn: These data are from squirrel sightings made during standard excursions between 1971 and 1982 (153 records; REICHHOLF 1983).

4. B12: Road kills are often good indicators of the population dynamics of medium-sized mammals. The B 12 data sets are the sums of road kills during a year along the federal highway B 12 between Munich and Bad Füssing (89 individuals; REICHHOLF 1983; 1976-1988). The killed martens were also counted along the same route.

5. Garmisch-Partenkirchen: Data are from squirrel sightings along three transects (1979 to 1988; 195 records), situated at the lower mountain forests about 800 to 900 m NN and were sampled twice each month. The dominating tree species is the spruce, but deciduous species of trees are also present. Winters may be severe with snow cover between November to April.

Results Phenology

The seasonal distribution of data (Inn, B 12, Garmisch-Partenkirchen) is plotted in Fig. 2. The phenological patterns are sımilar for Inn and Garmisch-Partenkirchen (r = 0.55; P< 0.05; one-tailed). No road kills were found during January and December ın contrast to the data based on squirrel sightings. All three plots showed a mınımum during July.

10

JR TMTAT MINEN TEAT SSTZOZENZED

Fig. 2. Seasonal distribution of road kills (B12) and sighting records (Inn, Garm. = Garmisch- Partenkirchen) of the red squirrel, given as the sum of sightings or road kills recorded within each month

Population dynamics of the Red squirrel in Bavarıa 13

40 Garm. 30 Inn N 20 10 B12

1964 1196825197.21197.6 21980771984 11988 Fig. 3. Population fluctuations of the red squirrel in 60 different areas of Bavarıa. For the areas Inn, B 12 and Garmisch-Partenkirchen (Garm.) the sum of all sightings or road kills within each year ıs given. The data from Bad Berneck and Pressath are relative % indices calculated as percentages of squirrels deli- vered per all anımals (Pressath) or squirrels delivered per 100 birds (Bad Berneck; see Material and methods)

Bad Berneck

Pressath

0 1964 1968 1972 1976 1980 1984 1988 YEAR

Population dynamics

In Fig. 3 all data sets are plotted across the years studied. The data from northern Bavaria (Bad Berneck and Pressath) show a clear decline in the squirrel populations. This decline ıs also apparent within the Inn data, but with an obvious peak in 1974. Since 1980 there seems to be a slight increase of squirrel populations, evident ın all data sets covering this period. Furthermore, the plots show a rough concordance in minor peaks (e.g. 1975, 1978, 1983, 1985). Table 1 presents the correlation coefficients between sampling areas: all correlation coefficients are positive and six from ten are significant.

Table 1. Matrix of pairwise correlation coefficients (upper half of the matrix) between the squirrel density indices of Fig. 3 Each coefficient measures the sımilarity in the population dynamics of squirrels between a particular pair of geographical locations, considering only the years with data for both areas. The lower half of the matrix gives the significance levels of the correlation coefficients (one-tailed)

1 Inn

215112

3 Garmisch-P. 4 Bad Berneck 5 Pressath

Squirrels and predators

We concentrated on the data from Bad Berneck, because this is the longest time series. In Fig. 4A we removed the negative trend apparent in Fig. 3 by linear regression. Runs with several transformations produced identical results. Firstly, some very prominent peaks are evident by the resıduals, and secondly, there is a depression in squirrel densities between 1976 and 1980. This depression within the squirrel data seems to correlate with a maxımum in the population index of the beech marten (Fig. 4B). A stepwise multiple regression was

14 R. Brandl, E. Bezzel, J. Reichholf and W. Völkl

performed with the squirrel data as dependent variable and years and predator density index as independent variables. The sequence of varıables entering the regression was 1. year and 2. predator with a significant negative regression coefficient (see also Table 2). Fig. 5A plots the residuals from a simple regression of squirrels to years (data in Fig. 4A) against the marten index (Fig. 4B): the negative correlation between squirrels and the beech marten is evident.

20

10

-10

0 1968 1972 1976 1980 1984 1988

40 B 30 20 10 1968 1972 1976 1980 1984 1988 Fig. 4. A: Residuals of the red squirrel density after 15 C removing the negative trend over the years investi- gated. B: Dynamics of the beech marten in the same > area, given as number of martens delivered per 100 birds (see Material and methods). C: Residuals of the ” red squirrel density after removing the trend over the 2 years examined and the influence of the marten (all N] a . 1968 1972 1976 1980 1984 1988 data from Bad Berneck, Fichtelgebirge)

YEAR

Residuals Bad Berneck

Fig. 5. A: Scatter plot of the red squirrel (after removing the negative trend over the years ex- amined) and the populations of the beech marten (see Fıg. 4 A, B; area: Bad Berneck). B: Scatter

10 plot of road kills of squirrels and beech marten Martes foina along the highway B 12

Population dynamics of the Red squirrel in Bavaria 15

Table 2. Stepwise multiple regression with red squirrel index from Bad Berneck as dependent variable and year, marten population and mast index of the spruce in the previous year as independent variables

A: sequence of varıables entering the regression Step Variable

1 year 2 marten 3 mast ındex

B: regression equation after step 3 Variable Slope Stand.slope

Year -1.532 Marten -0.533 Mast index al

Constant 3065

! note that P is two-tailed in Table 2; in the text we used a one-tailed probability.

In Fig. 5B a scattergram was also plotted for the road kills of red squirrel and beech marten along the B12. Contrary to the area around Bad Berneck we found no negative correlation between predator and prey (r = 0.37; P > 0.2; two-tailed).

Squirrels, food and weather

For the data set from Bad Berneck information on seed yield of spruce was available (Fig. 6B). The residuals from the multiple regression after step two ın Table 2 are also shown. Seed index and residuals are significantly correlated with a time lag of one year (r = 0.48; p = 0.04; one-tailed; note that degrees of freedom have to account for the number of varıables used to calculate the residuals). Table 2 shows the stepwise multiple regression of squirrel population index and the independent varıables 1) year, 2) marten population and 3) mast index (one year time lag). The mast index entered the regression during the last step.

The influence of monthly rainfall and temperature patterns on the residual (Fig. 4C) for time lags for up to two years were also tested. From 60 calculated correlation coefficients

20 A

Residuals ©

-20 1IES TITTEN ITZEFANISEOTENIEATE 11988 6)

Fıg. 6. A: Dynamics of the red squirrel after remov-

ing the influence of years and beech marten. B:

Fluctuations in seed production of the spruce (area ö : (0)

Bad Berneck, Fichtelgebirge) 1968 1972 1976 1980 1984 1988

Seed Production

16 R. Brandl, E. Bezzel, ]J. Reichholf and W. Völkl

only two were significant at the 5 % level, a result expected by chance alone. Therefore, it seems rather safe to conclude that weather conditions are unimportant for the dynamics of red squirrels.

Discussion

The seasonal distribution of the observational data and the road kills of red squirrels are quite different. During winter the red squirrel shows a reduced overall activity (ZWAHLEN 1975; Tonkın 1983). The reduced number of road kills are in accord with this fact. But why are so many sightings recorded during winter? The squirrel is a diurnal species with a long bimodal activity during summer, and a short unımodal pattern in winter (TONnkINn 1983). In winter the peak activity is during late morning. This activity pattern may correlate with the activity of observers. Squirrels search for food during winter in the vicinity of the dreys without making longer excursions to save energy (PULLIAINEN 1973). That is why during transect counts squirrels are easily detected by an observer. A reduced foraging range may decrease the probability of beeing killed on the road.

Fig. 3 suggests a decline in the squirrel population in nearly all regions of Bavaria. Is this decline a natural phenomenon within the population dynamics of the squirrel, or is this decline the result of the environmental damage caused by man?

From studies in boreal regions it is well known that squirrels increase their numbers after years of a high seed yield (Formosov 1933; PULLIAINEN 1984). At first glance, the correlation between seed production and squirrel numbers seems to be weak in Bavaria (Table 2), but we believe that this impression is incorrect. For example MÖckEL (1987) described a clear increase ın the red squirrel after a mast year ın the West-Erzgebirge and a decline to the original density within 5 years. The availability of food after a mast year seems to improve the condition of females and thereby the probability of reproduction (WAUTERS and DHONnDT 1989; GURNELL 1983) also under normal ambient conditions ın Central Europe. The increased probability of reproduction, an increased litter size as well as better survival of young produces a population explosion in squirrels. The maximum age of red squirrels is more than 10 years, and about 1 % of individuals may reach 5 years of age or older (WILTAFskY 1978). Therefore, the explosion needs around 5 years to fade, as long as adult survival is nearly independent of seed production by trees.

1971 was one of the most important mast years of spruce within the examined time span (REICHHOLF 1974). As most of our data sets start in 1971 or later we are unable to document the increase in squirrel numbers: our data only show the fadıng of the “population wave”. Furthermore, the minor mast years also produced smaller waves, and they all superposed. This scenario provides an explanation of the decline in the red squirrel since the early 1970s (Fig. 3). The negative regression coefficient of the varıable year in Table 2 describes in part the lasting effects of a very prominent “population wave”. The weak effect of our mast index in Table 2 is an artefact, because some of the mast-induced variation in squirrel numbers ıs covered by the variable year. We attribute the observed decline of the red squirrel to natural varıations of the seed production of coniferous trees. The good correlations between data sets (Table 1) may be a consequence of synchronized masts across Bavaria.

SCHRÖDER et al. (1982) describe a simulation model for the capercaillie (Tetrao urogallus) similar to our explanation of the squirrel dynamics. Random variations in reproduction may impose long-term cycles in a species, only because adults are long-lived and independent from the factors influencing reproduction. Bad weather conditions are the cause in the capercaillie, seed production in the red squirrel. We would like to stress that the data in Fig. 3 and the sımulations of SCHRÖDER et al. (1982) should act as examples for investigators studying the dynamics of long-lived species. A time series of 20 years may be

Population dynamics of the Red squirrel in Bavaria 17

too short for a complete analysis, because historical events outside the analysed time span may have lasting and confusing effects.

The high level of the squirrel index at Pressath between 1965 and 1967 is inconsistent with the view that the dynamics of the squirrel is mainly influenced by seed production. Möcker’s (1987) data indicate a very low density during that period. Consequently, one may suggest that the population density of the red squirrel dropped below the level of the late 1960s after an intermediate increase induced by spruce mast ın 1971. Note that we have no data for the period around 1971 for Pressath (question mark ın Fig. 3).

Perhaps some people would invoke forest decline as a factor, which may negatively influence forst anımals. Damage ot forests ıs frequent ın northern Bavarıa (SCHULZE 1989). Forest decline has been prominent since the late 1970s, but the squirrel populations have increased since 1980 (see Fig. 3; Garmisch-Partenkirchen and B 12). Furthermore, forest decline may have a positive effect on species depending on seeds. The synchronized production of seeds is reduced by the damage to trees. Every year some trees produce seeds and the food supply may be more constant compared to periods with synchronized, but unpredictable seed production. Around Garmisch-Partenkirchen nests of the crossbill (Loxia curvirostra) were found nearly each year in the late 1980s, whereas in the 1970s broods were only observed during mast years (BEZZEL unpubl.).

In the Fichtelgebirge the beech marten is negatively correlated to squirrel density (Fig. 5A). This suggests that within certain circumstances predators have some influence on prey species (note that the B 12 data did not show such a correlation!). Squirrels are only an alternative prey of the beech marten and the densitiy of the marten is regulated by different factors: the population dynamics of the squirrel has no effect on marten populations. PULLIAINEN (1984) found no increase in the pine marten after an increase in squirrels. In turn, an increase in predator populations may, increase predation pressure on alternative prey species. This situation is sımilar to the “alternative prey hypothesis” of ANGELSTAM et al. (1984), which explains why certain anımal species show synchronized fluctuations in Fennoscandıa. Voles are known to fluctuate wıth a cycle of about 3 to 4 years and the dynamics of the predators (like the red fox Vulpes vulpes) are coupled to this prey. When the main prey declines the predators turn to alternative prey species inducing a cylce on these prey species. Our explanation implies no fluctuations in the main prey of the beech marten; we only hypothesize that an increased predator density should have an inhibiting impact on the alternative prey. This ıs sımilar to JANZEN’s (1976) explanation of the low reptile biomass in Africa. JANZENn believes that many predators are able to maintain high population sizes because of the large herbivore biomass. The carnivores impose predation pressure on minor prey species and lower the reptile biomass (JanzEn 1976; but see KREULEN 1979).

Acknowledgements

We thank F. van DEN HEUVEL, who provided the squirrel data from Bad Berneck. We are also grateful to the forest authorities of Bayreuth (spruce mast) and the Wetteramt Nürnberg (weather) who made their data available to us.

Zusammenfassung

Populationsdynamik des Eichhörnchens in Bayern

Für fünf Gebiete Bayerns werden die Populationsschwankungen des Eichhörnchens (Sciurus vulgaris) dargestellt. Zwischen 1970 und 1980 war eine Abnahme der Eichhörnchen zu beobachten, seit 1980 hingegen kam es wieder zu einer leichten Zunahme. Die Abnahme ist wohl keine Folge menschlicher Eingriffe, sondern kann auf Reproduktionswellen zurückgeführt werden, die durch die Mastjahre der Fichte bedingt sind. Die Zunahme seit 1980 wird als Folge des Waldsterbens diskutiert, da die Schädigung der Nadelbäume zu einer Desynchronisation der Zapfenproduktion geführt hat. Damit stand den Eichhörnchen eine konstante Nahrungsquelle zur Verfügung.

Wetterfaktoren scheinen die Dynamik der Eichhörnchenpopulation nicht zu beeinflussen. Dage- gen finden wir eine negative Korrelation zwischen Steinmarder (Martes foina) und Eichhörnchen.

18 R. Brandl, E. Bezzel, J. Reichholf and W. Völkl

References

ANGELSTAM, P.; LINDSTRÖM, E.; WIDEn, P. (1984): Role of predation in short-term fluctuations of some birds and mammals in Fennoscandia. Oecologia 62, 199-208.

Branpı, R. (1983): Populationstrend des Eichhörnchens Sciurus vulgaris L. in der Oberpfalz. Säugetierkundl. Mitt. 31, 76-78.

ForMmosov, A. N. (1933): The crop of cedar nuts, invasions into Europa of the Siberian nutcracker (Nucifraga caryocatactes macrorhynchus Brehm) and fluctuations in numbers of the squirrel (Sciurus vulgaris L.). J. Anım. Ecol. 2, 70-81.

GURNELL, J. (1983): Squirrel numbers and the abundance of tree seeds. Mammal Rev. 13, 133-148.

Möckeı, R. (1987): Bemerkenswerter Massenwechsel des Eichhörnchens (Sciurus vulgarıs) im West- Erzgebirge. Säugetierkdl. Inf. 11, 489-493.

Janzen, D. A. (1976): The dependence of reptile biomass by large herbivores. Am. Nat. 110, 371-400.

KrEULEN, D. A. (1979): Factors affecting reptile biomass in African grasslands. Am. Nat. 114, 157-165.

Ports, G. R.; TAPPER, $. C.; Hupson, P. J. (1984): Population fluctuations in red grouse: analysis of bag records and a simulation model. J. Anım. Ecol. 53, 21-36.

PuLLiamen, E. (1973): Winter ecology of the red squirrel (Sciurus vulgaris L.) in northeastern Lapland. Ann. Zool. Fennicı. 10, 487494.

PuLLıaınen, E. (1984): The predation system seed-squirrel-marten under subarctic conditions. Z. Säugetierkunde 49, 121-126.

REICHHOLF, J. (1974): Die Auswirkungen der Fichtensamen-Rekordernte von 1971 auf die Populationen von Buntspecht und Eichhörnchen am Unteren Inn. Natur und Landschaft 49, 77-78.

REICHHOLF, J. (1983): Bestandsentwicklung und Farbphasen des Eichhörnchens Sciurus vulgaris L. in Südbayern. Säugetierkundl. Mitt. 31, 73-75. .

SCHRÖDER, W.; SCHRÖDER, ]J.; SCHERZINGER, W. (1982). Über die Rolle der Witterung in der Populationsdynamik des Auerhuhns (Tetrao urogallus). J. Orn. 123, 287-296.

SCHULZE, E.-D. (1989): Air pollution and forest decline in a spruce (Picea abies) forest. Science 244, 776-783.

STUBBE, H. (1988): Das Buch der Hege. Bd. 1: Haarwild. Berlin; VEB Deutscher Landwirtschafts- verlag.

Tonkın, J. M. (1983): Activity patterns of the red squirrel (Sciurus vulgaris). Mammal Rev. 13, 99-111.

WAUTERS, L.; DHONDT, A. (1989): Body weight, longevity and reproductive success in red squirrels (Scinrus vulgaris). J. Anım. Ecol. 58, 637-651.

WILTAFskY, H. (1978): Sciurus vulgaris Linnaeus, 1758 — Eichhörnchen. In: Handbuch der Säugetiere Europas. Ed. by J. NIETHAMMER and F. Krapp. Wiesbaden: Akademische Verlagsgesellschatt. Bd. 1, 86-105.

ZWAHLEN, R. (1975): Die lokomotorische Aktivität des Eichhörnchens (Sciurus vulgaris). Oecologia 22, 79-98.

Authors’ addresses: Dr. RoLAnD BrAnDL and Dr. WOLFGANG VÖLKL, Lehrstuhl für Tierökologie I, Universität Bayreuth, Postfach 101251, W-8580 Bayreuth, FRG; Dr. EINHARD BEZZEL, Institut für Vogelkunde, Gsteigstr. 43, W-8100 Garmisch-Partenkir- chen, FRG; Prof. Dr. JosEr REICHHOLF, Zoologische Staatssammlung, Münch- hausenstr. 21, W-8000 München 60, FRG

Z. Säugetierkunde 56 (1991) 19-24 © 1991 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-3468

An experiment to test the consumption of arboreal food by Wood mouse Apodemus sylvaticus

By T. Santos and J. L. TELLERfA

Departamento de Biologia Anımal (Zoologia), Universidad Complutense, Madrid, Espania

Receipt of Ms. 24. 4. 1990 Acceptance of Ms. 31. 7. 1990

Abstract

Analysed factors affecting the arboreal feeding activity of wintering wood mice in a set of woodlots ın central Spain. Stations were baited with acorns on branches, trunk and ground of 429 trees to test the arboreal behaviour of mice. Acorn intake on branches was positively and significantly related to accessibility of food but not to mice abundance. The best predictor of food consumption on branches was, however, the ground-trunk acorn intake, suggesting that this varıable was a good index of the scarceness of food. We conclude that morphological constraints in the arboreal ability of the species were evident.

Introduction

Wood mice (Apodemus sylvaticus) are recognized as expert climbers (HoLisovA 1969; LE Louarn and SAINT-GIRONS 1977; GURNELL 1985), but there ıs a lack of information about the factors determining this behaviour (MONTGOMERY and GurnELL 1985). The use of arboreal substrata may be subject to conflicting factors, such as predation risks, resource availability, and others (e.g. Kıng 1985; BRown 1989; SIMONETTI 1989). The trade-oft between rısks and benefits ın a particular microhabitat may change, however, as a result of increased pressures on other microhabitats nearby. For example, high population densities may force some individuals to use less preferred resources (FRETWELL 1972; GURNELL 1985). Thus, decreased availability of food, frequently related to peak densities (FLOWER- DEw 1985; Hansson 1985), may stimulate the exploratory behaviour of rodents (STICKLE 1979; MONTGOMERY and GURNELL 1985; PENNYCUIK and REISNER 1989). Morphological constraints and travel expenditures seem to be the another relevant factor influencing the selection of feeding microhabitats (WıEns 1973; GURNELL 1985; BROwNn 1989; SIMONETTI 1989).

In this work, we explore the incidence of mice abundance and food accessibility on the arboreal feeding activity of wintering wood mice (Apodemus sylvaticus) in Holm oak woodlots of central Spain. The winter is a period wıth heavy food constraints for many temperate endotherms (NEwToN 1981; MERRIT 1984), so mice arboreality could be stimulated in this season.

Study area

The study area is located in Burgos province, central Spain. Average altitude is 850 m and phytoclima- tie conditions are inland mediterranean, with long and cold winters (Rıvas-MArTinEz 1981). The area has a deforested agricultural landscape, with extensive cereal cropping and sheep grazing as main usages. Some tracts of the original forests remain, with a dominant vegetation formed by Holm oaks (Quercus rotundifolia) and shrubs of the genera Cistus, Genista, Thymus and Lavandula. These woodlots support wintering populations of wood mouse, but mice are scarce during winter in the surrounding fields (TELLERTA et al. 1990; see also ALCAnTARA 1986). Previous trapping work showed that rodent species other than wood mice are scarce or absent in these forests; Common voles (Microtus arvalıs) settle some grassy sectors and Garden dormice (Ehomys quercinus) hibernate throughout the winter. Seventeen isolated woodlots, ranging from 0,1 to 280 ha (Table), were studied in order to evaluate the use of arboreal preys by mice.

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20 T. Santos and J. L. Telleria

The 1988 autumn crop of acorn, preceding the study winter, was very scarce; at the start of December only 0.8 % (n = 131) of the Holm oaks beared fruits and 3.2 % (n = 158) had shed acorns to the surrounding ground. By the 20th of January a high degree of depletion was evident, since tree and ground acorns were lacking in most woodlorts.

Material and methods

Food accessibility

Holm oak half-acorns were pierced with wire and tied round branches with different diameters and at different distances from the tree basıs to test the relationship between the arboreal feeding efficiency of mice and food accessibility. The wood mouse is an omnivore, and includes fruits in its diet (OBRTEL and Houısova 1983; Hansson 1985), so that we could assume that Holm oak acorns should be profitable baits. Acorns were arranged during one dark night in each woodlot, and placed and controlled in the same order, so all acorns were exposed the same time. Two experiments were carried out in 1989, from 12 to 16 January and from 2 to 5 February. One half-acorn per tree were tied on 429 trees distributed among the 17 Holm oak forests. Numbers of acorns ranged from 6 to 49 in each experiment (Table), according to a logarıthmic function of forest area. Branch diameter was estimated visually for 380 acorns; distance from ground was estimated for each acorn as the shortest path from the base of the tree. Branches ranged from 0.3 to 10 cm in diameter, with the majority between 0.5 and 3cm (87.9 %). Distances ranged from 0.5 to 12m, those between 2 and 4m accounting for 78.5 %. Half-acorns were also placed on the trunk, 1.5 m above ground and on the base of the trunk, in the same trees, to assess the global food searching incidence by mice in each forest.

As wintering mice mainly use underground burrows (DUFOUR 1978; MONTGOMERY and GURNELL 1985), accessibility of arboreal food should be negatively related to ground distance, and positively to branch diameter for morphological reasons. Since separate analysis of these two varıables can produce confounding results, a ditficulty index (ID) was estimated for each acorn as the product of distance by the inverse of diameter; ID ranged from 0.2 to 26.7, with values between 0.2 and 6 summing 92.1 %. We calculated mean values of distance, diameter and ID for each forest. Percentages of acorns preyed upon by mice were used as estimates of feeding incidence in the three positions sampled. Acorn use on ground was significantly associated with acorn use on trunks (r = 0.824, p < 0.001, 15 d.f.), therefore both positions were analysed together. Acorn intakes in January and February were positively correlated (r = 0,78, p < 0.001, 15 d.f.; see TELLERTA et al. 1990), so both samples were pooled. Preyed acorns were easily recognizable by teeth marks and fecal rests. The acorns preyed by birds or lost were not considered in the analyses.

Mice abundance

At the beginning of March 1989, 213 stations were provided with two snap-traps during two consecutive nights (SMITH et al. 1975); number of traps ranged from 12 to 196, according to woodlot area. Abundance indexes were obtained as the number of individuals captured by trap in each forest (Table; see TELLERfA et al. 1990, for more details on the trapping design). Wood mouse was the only species caught.

Statistical analyses were made according to SokaL and RoHLF (1981) and Zar (1984). Mice abundance and acorn intake rates were arcsin transformed, and distance, dıameter and ID values logtransformed.

Results

Branch acorns were exclusively preyed upon in locations placed between 0.5 and 3.5 m from the base of the tree; 71 acorns arranged between 3.6 and 12 m remained untouched, most of these placed in the canopy edge. Acorns were consumed from branches of all diameters, although twigs of less than 1 cm supported the lowest predation (see Figure). Relationship between acorn predation rate and accessibility was first explored classıfying the acorns in 9 classes according to distance, diameter and ID. The results show that the proportion of preyed acorns decreased significantly with the increase of distance and ID, but a diameter response was not obvious (Figure). ID was the only variable among these three used in the following analyses, since it may be considered a synthetic index representative of acorn accessibility.

An experiment to test the consumption of arboreal food by Wood mouse 2]

Table. Area, mice abundance (No. individuals/trap x 100), number of acorns placed and controlled (N) and acorn intake rates (percentage of acorns preyed) in each forest

woodlot mice intake

area abundance ground branches

According to relationships between the feeding incıdence on branches and the indepen- dent varıables estimated in each forest, ID accounted for more varıatıon (r = -0.569, p < 0.05; R? = 32.4 %) than mice abundance (r = 0.183, n.s.; R? = 3.3 %), but this was less than that accountable for acorn intake on ground and trunks (r = 0.711, p < 0.01; R’ = 50.6 %). Ihese results were supported by partial correlation analyses of feeding incıdence on branches with 1) mice abundance and ID: partial r values were 0.287 (n.s.) for abundance and -0.599 (p < 0.02) for ID; 2) with mice abundance and ground-trunk acorn intake: r = -0.299 (n.s.) and r = 0.731 (p < 0.01), respectively; and 3) with ground-trunk acorn ıntake and ID: r = 0.649 (p < 0.01) and r = -0.457 (n.s.), respectively.

ACORN INTAKE ON BRANCHES

30 Ps:-0.905** 30 f3:-0.933%**

26 17 18 _90 09 225 33545 6 61 09 1 15 2 253 4 5 541 distance diameter ID

Relationships of acorn intake on branches (in percentages) to distance (m), diameter (cm) and acorn accessibility (ID). r, is the Spearman’s rank correlation coefficient; **: p < 0.01

22 T. Santos and ]J. L. Telleria Discussion

Mice consumed acorns placed in branches regardless of diameter and up to a distance 3.5 m from the tree base, but not further away. Thus, our results agreed with the arboreality of the species, although a limit in its arboreal exploration was apparent in our study. This could be directly due to constraints in movement ability of mice in trees, but other factors may operate simultaneously (CArAco 1980).

In crowded conditions, some island populations of rodents increase their resource partitioning, with younger individuals obliged to live in suboptimal patches (GrLiwıcz 1984; see also Lomnick1 1988). Therefore, we should expect a rıse of food demands with the increase in mice density in the woodlots studied, and hence a searching increase towards the least accessible acorns. Since this expected relationship did not occur, it is plausible that even the higher densities obtained were very low and mice did not need to explore the most inaccessible acorns; actually, mice abundance accounted for a relatively low variance of the acorns consumed on ground and trunks (R? = 26.2 %). On the other hand, if resource levels differed among woodlots, the total acorn intake would be a better estimator of trophic stress than mice abundance. In fact, some small woodlots with “low” abundances of mice gave the highest intakes (Table). This view is consistent with our results, suggesting that under conditions of limited food supply mice could search for supplementary food above ground. Also, an increase of searching actıvity in the adjacent fields, including dispersal behaviour, could be an alternative response. Exploratory and dispersal ability, agricultural field use and habitat tolerance in the Wood mouse (JONGE and DiEnskeE 1979; JENSEN 1982; GEUSE et al. 1985; GurNnELL 1985; WOLTON and FLOWERDEW 1985), suggest that this response would be more profitable than an exploratory increment towards presumably little accessible substrata, such as branches, but at present experimen- tal evidence is lackıing.

In conclusion, the findings of our experiment, namely, the clear limit observed in the ability of the Wood mouse to obtain arboreal food, and the association of acorn use on branches with ID, suggest morphological constraints of this species in the searching of tree food, and would indicate a negative yield in the handling of distant arboreal preys. At the same time, this study suggests that mice are capable of overcoming local situations of food scarcity on the ground by using alternative arboreal resources.

In another context, the decreasing gradient observed in the feeding incidence of mice from ground to trunk-branches, implies potential consequences for forest avian species feeding mainly on the ground and trunks (e.g. pariforms; see ULFSTRAND 1977). The high densities of mice registered in island conditions in this and other works (e.g. GLıwIcz 1984; GEUSE et al. 1985), point out a probable competition between birds and rodents whose main biological effects are unknown at present, although composition and densities of avıian species could be affected. As JanzEn (1986) recently expressed, other topics than customary (area, distance to continent, habitat diversity, etc.) are involved ın island biology; the ones related to high densities of generalist anımals, such as wood mice (FLOWERDEW 1977; LE LOUARAN and SAINT-GIRONS 1977), represent an ımportant threat for stenoecious or scarce organısms.

Acknowledgements

We thank MAnUEL ALCANTARA for field assistance and TomAs SANTOS Rıncön for useful advice. JosE A. Diaz made helpful comments on a previous draft of the manuscript. This paper is a contribution to the project “Biology and distribution of Iberian forest vertebrates”, funded by the Spanish C.1.C.Y.T. (project PB-86-0006-C02).

An experiment to test the consumption of arboreal food by Wood mouse 28

Zusammenfassung

Ein Experiment zur Ermittlung der Nahrungsaufnahme der Waldmaus (Apodemus sylvaticus) auf Bäumen

Untersucht wurden mehrere Faktoren, die die Aktivitäten von Waldmäusen bei der Nahrungssuche auf Bäumen beeinflussen. Dazu wurden in mehreren Waldparzellen in Zentralspanien während des Winters Eicheln am Boden, an Stämmen und auf Zweigen von 429 Bäumen angeboten. Der Konsum von Eicheln auf Zweigen war positiv und signifikant korreliert mit der Erreichbarkeit der Nahrung, aber nicht mit der Häufigkeit der Waldmäuse. Die Ficheln wurden vornehmlich von Boden und Stämmen aufgenommen, aber auch von Zweigen unterschiedlicher Stärke, allerdings nur bis zu 3,5 m Höhe. Dieses weist auf Grenzen der Art hin, den arboricolen Lebensraum zu nutzen.

References

ALCANTARA, M. (1986): Preferencias de häbitat del Ratön de Campo (Apodemus sylvaticus L.) en medios agricolas. Memoria Lic. Universidad Complutense, Madrid.

Brown, J. S. (1989): Desert rodent community structure: a test of four mechanisms of coexistence. Ecol. Monogr. 59, 1-20. f

CArRAco, T. (1980): On optimal selection in a multiattribute stochastic environment. Evol. Theor. 5, 127-133.

Durous, B. (1978): Effect of external and internal factors upon burrowing and nest-building activities of the wood mouse (Apodemus sylvaticus L.) ın terrarıum conditions. Behav. Processes 3, 57-76.

FLOWERDEW, J.R. (1977): Wood mouse Apodemus sylvaticus. In: The Handbook of British Mammals. Ed. by G. B. CorgET and H. N. SOUTHERN. Oxford: Blackwell, pp. 206-217.

— (1985): The population dynamics of wood mice and yellow-necked mice. Symp. zool. Soc. Lond. 55, 315-338.

FRETWELL, S. (1972): Populations in a seasonal environment. Princeton: Princeton Univ. Press. GEUSE, P.; BaucHat, V.; LE BOULENGE, E. (1985): Distribution and population dynamics of bank voles and wood mice in a patchy woodland ın central Belgium. Acta Zool. Fennica 173, 65-68.

Giwicz, J. (1984): Rodents on islands: living in a crowd. Acta Zool. Fennica 172, 95-98.

GURNELL, J. (1985): Woodland rodent communities. Symp. zool. Soc. Lond. 55, 377411.

Hansson, L. (1985): The food of bank voles, wood mice and yellow-necked mice. Symp. zool. Soc. Lond. 55, 141-168.

Horısova, V. (1969): Vertical movements of some small mammals in a forest. Zool. Listy 18, 121-141.

JANZEn, D. H. (1986): The eternal external threat. In: Conservation Biology. The Science of Scarcity and Diversity. Ed. by M. E. Souz£. Sunderland: Sinauer, pp. 286-303.

JENsEn, T. S. (1982): Seed production and outbreaks of noncyclic rodents populations in deciduous forests. Oecologia, Berlin, 54, 184-192.

JONGE, G. DE; DIENSKE, H. (1979): Habitat and interspecific displacement of small mammals in The Netherlands. Netherlands J. Zool. 29, 177-214.

Kıng, C. M. (1985): Interactions between woodlands rodents and their predators. Symp. zool. Soc. Lond. 55, 219-247.

LE Lovarn, H.; SAINT-GIRoNSs, M.-C. (1977): Les Rongeurs de France. Parıs: I.N.R.A.

LomnIckt, A. (1988): Population ecology of individuals. Princeton, N. J.: Princeton Univ. Press.

MERRIT, J. F. (ed.) (1984): Winter ecology of small mammals. Pittsburgh: Spec. Publ. Carn. Mus. Nat. Hist. 10.

MONTGOMERY, W.1.; GURNELL, J. (1985): The behaviour of Apodemus. Symp. zool. Soc. Lond. 55, 89-115.

NEwTon, 1. (1981): The role of food in limiting bird numbers. In: The integrated study of bird populations. Ed. by H. Kromp and J. W. WOLDENDORP. Amsterdam: North Holland Publ. Comp, pp. 11-30.

OBRTEL, R.; HoLisova, V. (1983): Winter and spring diets of three coexisting Apodemus spp. Folia Zoologica 32, 291-302.

PEnNnycuIk, P. R.; REISNER, A. H. (1989): Food restriction: mechanisms limiting numbers and home site utilization in populations of house mice, Mus musculus. Oikos 55, 159-164.

Rıvas-MARTINEZ, $. (1981): Les &tages bioclımatiques de la vegetation de la Peninsule Iberique. Anales Inst. Bot. Madrid 37, 251-268.

SIMONETTI, J. A. (1989): Microhabitat use by small mammals in central Chile. Oikos 56, 309-318.

SMITH, M. H.; GARDNER, R. H.; GENTRY, J.; Kaurman, D. W.; O’FARRELL, M. H. (1975): Density estimators of small mammal populations. In: Small mammals: Their productivity and population dynamics. Ed. by F. B. GoLı£v, K. Perrusewicz and L. Ryszkowskı. Cambridge: Cambridge Univ. Press, pp. 25-53.

24 T. Santos and ]J. L. Telleria

SoKAL, R. R.; ROHLF, F. J. (1981): Biometry. 2nd ed. San Francisco: W. H. Freeman.

STICKLE, L. F. (1979): Population ecology of house mice in unstable habitats. J. Anım. Ecol. 48, 871-887.

TELLERSA, J. L.; SANTOS, T.; ALCANTARA, M. (1990): Abundance and food-searching intensity of wood mice (Apodemus sylvaticus) in fragmented forests. J. Mammalogy (in press).

ULFSTRAND, $. (1977): Foraging niche dynamics and overlap in a guild of passerine birds in a south Swedish coniferous woodland. Oecologia, Berlin, 27, 23-45.

WiıEns, J. A. (1973): Pattern and process in grassland bird communities. Ecol. Monogr. 43, 237-270.

WOLToN, R.; FLOWERDEW, J. R. (1985): Spatial distribution and movements of wood mice, yellow- necked mice and bank voles. Symp. zool. Soc. Lond. 55, 249-275.

ZAR, J. H. (1984): Biostatistical Analysıs. 2nd. ed. London: Prentice-Hall.

Authors’ address: TomAs Santos and Jos£ Luıs TELLERfA, Departamento de Biologia Animal (Zoologia), Facultad de Biologia, Universidad Complutense, E-28040 Madrid, Espana

Z. Säugetierkunde 56 (1991) 25-33 © 1991 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-3468

Genetic differentiation in four species of Apodemus from Southern Europe: A. sylIvaticus, A. flavicollis, A. agrarius and A. mystacinus (Muridae, Rodentia)

By JAnIcE BRITTON-DAVIDIAN, MEHRNOUCH VAHDATI, FATIMA BENMEHDI, PAULE GROS, VALERIE NAnc£, H. CROSET, $. GUERASSIMOV and C. TRIANTAPHYLLIDIS

Laboratoire de Genetique, Institut des Sciences de !’Evolution, USTL, Montpellier, France

Receipt of Ms. 15. 5. 1990 Acceptance of Ms. 10. 8. 1990

Abstract

Genic varıability was estimated for four Apodemus species from Southern Europe by electrophoresis at 20 loci. Genic divergence data agree well with the subgeneric classification, A. agrarıns (subgenus Apodemus) being very distant from the three other species (subgenus Sylvaemus), as was previously shown by GEMMERkE (1980) using 11 locı. However, the large dıvergence between these two groups suggests that their taxonomic relationships should be revised. The morphological overlap between A. sylvaticus and A. flavicollis is confirmed throughout Southern Europe which stresses the use of biochemical methods for unambiguous identification of specimens. The karyological analysis of samples of A. sylvaticus, A. flavicollis and A. agrarins revealed chromosomal varıation in only one individual (A. flavicollis wıth 2 n = 49 ın Bulgarıa).

Introduction

The genus Apodemus ıs one of the most widespread noncommensal rodent groups ın the Paleartic. In the Western part of their range, the use of biochemical genetics has proven extremely useful in unambiguously discriminating morphologically similar species. This has been the case for A. sylvaticus and A. flavicollis, ın particular, which although easily distinguishable in Central and Northern Europe, show a morphological overlap in the more southern areas. That this overlap is due to clinal variation in sıze and pelage color following opposite trends in both species and not to hybridization, has been shown by a number of authors (NIETHAMMER and Krarp 1978; GEMMEKE 1980; BENMEHDI et al. 1980; NascETTI and Fırıppuccı 1984). This discrete morphological varıation seems to be a general trait within the subgenus Sylvaemus (A. mystacinus excepted), although genic differentiation as measured by electrophoretic methods is quite extensive. Recent studies of more eastern populations suggest that this subgenus will most likely reveal a complex of species (NIETHAMMER 1969; DARVICHE et al. 1979; GEMMERE and NIETHAMMER 1982).

Karyotypie varıability ıs also well documented within the subgenera Sylvaemus and Apodemus. All species carry 48 chromosomes but differ in the NF number showing that chromosomal evolution has proceeded mainly by pericentric inversions (KrAaL 1970; SOLDATOVIC et al. 1975; for a review see ZımA and Krau 1984).

The evolutionary relationship between Apodemus species was previously investigated at 11 locı by GEMmMERE (1980). The genetic differentiation between Apodemus species belonging to the two subgenera Sylvaemus (A. sylvaticus, A. flavicollis, A. mystacinus) and Apodemus (A. agrarins) is here extended to populations from Greece, Bulgaria and Spain for which morphological, chromosomal and allozymic data at 20 loci are presented.

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26 Janıce Britton-Davidıan et al.

Material and methods

Specimens belonging to four species of the genus Apodemus (A. sylvaticus, A. flavicollis, A. mystacinus and A. agrarins) were live-trapped in localities (see Figure 1 for names) from five southern European countries. Nine populations were analyzed for genic varıability: France (1), Italy (2), Greece (3, 4, 5, 6), Spain (7) and Bulgarıa (8). Starch gel electrophoresis techniques are described in PASTEUR et al. (1987). A total of 20 locı were analysed: alcohol dehydrogenase (Adh), alpha-glycerophosphate dehydrogenase (alpha-Gpd), albumin (Alb), amylase (Amy-1), glutamate oxaloacetate transaminase (Got-1), glucose phosphate isomerase (Gpi), hemoglobin (Hbb), ısocitrate dehydrogenase (/dh-1 and Idh-2), lactate dehydrogenase (Ldh-1 and Ldh-2, respectively coding for the A and B subunits; see EnGEL et al. 1973), the regulator gene for Zdh-2 ın red cells (Ldr), NAD-dependent malate dehydrogenase (Mdh-1 and Mdh-2), NADP-dependent malate dehydrogenase (Mod-1), nucleoside phosphorylase (Np), phosphoglucose dehydrogenase (Pgd), phosphoglucomutase (Pgm), sorbitol dehydrogenase (Sdh) and superoxide dismutase (Sod). Allelic designations were determined by comparison to the mobility of the most frequent allele in A. sylvatıcus which was arbitrarily assıgned the value 100. The HBB pattern in Apodemus consists in two spots, the slower one showing no variation, so the genetic varıability scored refers only to variation ın mobility of the faster migrating spot. Genetic varıabılity measures, genetic distances (NEI 1978) and the UPGMA phenogram were computed and performed using the BIOSYS-1 program of SWOFFORD and SELANDER (1981).

. sylvaticus

. flavicollis . agrarius . mystacinus

Fig. 1. Distribution of sampled localities and technique of analysıs: empty symbols = allozymes; dark symbols = morphology; dotted symbols = chromosomes. Localities: France (1. St Cyr-les-Colons, 9. Gardiole, 10. Avene, 21. Mauguio, 22. Iseron, 25. Cuxac, 26. Banyuls); Italy (2. Ticino region near Pavia); Greece (3. Gallikos, 4. Strimonikon, 5. Doiranı, 6. Prosotsanı hills, 16. Aggitis river, 17. Prosotsani river, 18. University farm Thessaloniki, 19. Avas); Spain (7. Calonge, 11. Granada); Bulgaria (8. Plovdiv, 12. Karnobat, 13. Vranıa, 14. General Toshevo, 23. Orizare); Germany (20. Lübeck) and Austria (24. Burgenland)

Morphological data were collected on specimens from France (1, 9, 10), Italy (2), Spain (7, 11), Bulgaria (8, 12, 13, 14), Greece (3, 15, 16, 17, 18, 19) and Germany (20).

The chromosomal study was performed on field mice from difterent localıties: A. sylvatıcus from France (9:1 male, 21:1 male, 22:1 female, 26:1 male), Spain (11:1 female), Bulgaria (13:1 female, 23:1 female) and Austria (24:1 female); A. flavicollis from France (25:1 female) and Bulgaria (14:1 male, 13:1 male); A. agrarius from Greece (4:1 male, 1 female). The karyotypes were established using the classical air-drying technique. No results were available for A. mystacınus.

In both the morphological and chromosomal study, all mice, except for A. agrarins and A. mystacinus which were unambiguously identified in the field, were ascribed to A. sylvatıcus or A. flavicollis on the basis of their LDH-2 alleles. The specimens are deposited as pickled carcasses at the Institut des Sciences de l’Evolution.

Genetic dıfferentiation in four species of Apodemus from Southern Europe 27

Table 1. Allele frequencies at the 19 variable loci

Species / Locality

28 Janıce Britton-Davidıan et al. Table 1 (continued)

Species / Locality

1.00 0.00

1 0.00 1.00 0.00

AS=A. sylvaticus; AF = A. flavicollis; AA = A. agrarıns; AM = A. mystacinus. FR = France; IT = Italy; GR = Greece; SP = Spain; BU = Bulgaria.

Results Genetic variability and differentiation

Genetic varıability parameters (Table 2) were computed from the allelic frequencies (Table 1). Only one locus (/dh-2) was found monomorphic for the same allele in the four Apodemus species. Twelve locı (Alb, Amy-I, Got-1, c+l.c, Hbb, Idh-1, Lah-1, Ldh-2, Mdh-1, Pgd, Sdh and Sod) discriminated at least two of the four species, whereas two locı were species diagnostic: Mod-! and Np.

All varıiability parameters were highest for A. sylvatıcus (mean H = 0.08, mean Po.o5 = 21% and mean A = 1.3) than for the other three species which ranged between 10 %-15 % for the rate of polymorphism and 4-6 % for mean heterozygosity. However, where sample sizes are small, this measure of variability may not be representative of the species as a whole.

Genetic differentiation in four species of Apodemus from Southern Europe 2)

Genetic distances (Table 3) calculated Table 2. Genetic variability measures according to NEI (1978) were used to gen- erate aUUPGMA phenogram (Fig. 2). The Locality

latter agrees well with expectations ın that

A. sylvaticus and A. flavicollis cluster to- A. sylvaticus gether, and both of these wıth A. mysta- a cinus. A. agrarius, on the other hand is set en 6) well apart from the first three species, Spain (7) yielding a mean genetic distance of 1.28. Mean Intraspecific genetic distances were com- A. flavicollis puted for A. sylvaticus and A. agrarius only France (1) and yielded respectively a mean of 0.045 A. agrarins and 0.067 which falls within the value gen- Greece (5) erally recorded for subspecific genetic Bulgaria (8) differentiation. Mean

A. mystacınus Greece (6) 2 lei Morphological discrimination

mean number of alleles; P =

Morphological data are presented ın Table polymorphic locı (5 % level); H

mean

4 and Figure 3. Whereas discrimination of heterozygosity (NEı 1978 except for A. mys- tacınus for which the sample size was too

A. agrarins and 4. ST IE small). Numbers in parenthesis refer to phological grounds is immediate, this ıs not Inealliice

the case between A. sylvatıcus and A. flavicollis which show a large overlap ın body lengths. Additionally, although the presence of a complete collar is species diagnos- tic, its absence is not since 35 % of the A. flavicollis we captured exhibited only a more or less large chest spot ın lieu of a collar.

France

A. sylvaticus Italy

Greece

Spain A. flavicollis

France A. mystacinus Greece

. agrarius Greece

Bulgaria

Nei's (1978) genic distance

1.4 1.2 1.0 0.8 0.6 0.4 0.2 009

Fıg. 2. UPGMA phenogram computed from genic distances

Chromosomal variability

The chromosomal analysis of specimens from each species corresponded to results from previous studies (Krar 1970; SOLDATOVIC et al. 1975; BEKASOva et al. 1980; ZımA 1984). The karyotypes of A. sylvaticus and A. flavicollis both carrıed 48 acrocentric chromosomes except for the A. flavicollis from Bulgarıa (14. General Toshevo) which had 49 chromosomes showing an additional small acrocentric chromosome. Such varıation is common in this species and has been attributed to the presence of supernumerary chromosomes (SOLDATOVIG et al. 1975; Zıma 1984; Zıma and Krar 1984). A. agrarıns (2n

30 Janice Britton-Davidian et al. Table 3. Genetic distance coefficients (NEı 1978)

Locality

. AS-FR -—--

AS-IT 0.016 = ——

AS-GR 0.065 0.067 ===

AS-SP 0.039 0.063 0.022

AF-FR 0.601 0.548 0.478 ; ===>

AA-GR 1.236 1.284 11415 x 1.446 -—--

AA-BU 15133 1.166 1.170 ; 16522 0.067 = . AM-GR 0.876 0.866 0.932 . 0.823 12592 LS

1

2R 38 Zi Io 6. 7 8

AS = A. sylvaticus; AF = A. flavicollis; AA = A. agrarius; AM = A. mystacinus. FR = France; IT = Italy; GR = Greece; SP = Spain; BU = Bulgarıa.

Table 4. Morphological data for samples of three Apodemus species

Numbers after countries refer to localities sampled

Chest spot Locality BL DE

(mm) (mm)

A. sylvaticus

Italy (2) 93(3) 7765) 0.84(0.07) Bulgaria (8. 12-14) 96(6) 81(4) 23(0) 0.86(0.05) Spain (7. 11) 93(5) 88(7) 22(1) 0.96(0.07) Greece (3. 15-18) 107(2) 91(2) 23(0) 0.85(0.02) France (1) 84(2) 792) 21(1) 0.93(0.02)

(9) 97(2) 84(3) 21(1) 0.87(0.03)

Mean 97(2) 84(1) 22(0) 0.88(0.01)

A. flavicollis Greece (16-17) Yo) ee 2 ee Bulgaria (8. 12-14) 98(7) 86(1) 22(2) 0.88(0.08) France (10) 94(5) 95(4) 23(1) 1.03(0.04) (1) 94(5) 99(5) 24(0) 1.06(0.03) Mean 95(3) 958) 23(0) 1.01(0.03)

A. agrarıns Greece (5) 11265) 78(2) 22(1) 0.69(0.02) Germany (20) 6 102(5) 70(12) 19(1) 0.69(0.17) Mean 108(4) 756) 21(1) 0.69(0.05) BL = body length; TL = tail length; HF = hind foot length; chest spot color: no, small (Sm) or large (L) spot; Col = complete collar. STandard errors in parenthesis.

= 48) showed four pairs of small metacentric chromosomes which increased the NF to 56. No other chromosomal variability was found within samples.

Discussion

Interspecific genetic differentiation at 20 loci is presented for four species of the genus Apodemus. Previous studies on these same species were made by GEMMERE (1980) but the electrophoretic survey included only 11 loci. More recent and extensive work was performed by Nascerri and Fırıppuccı (1984) on 27 loci but was restricted to the subgenus Sylvaemus. The overview of these three independent studies shows that the

Genetic differentiation in four species of Apodemus from Southern Europe 3

Li

120

110

100

den

90

Bas 25 (@)

oO 00 ©)

80

70

BL(mm)

70 80 90 100 110 120

Fig. 3. Body (BL) and tail length (TL) distribution. Empty circle = A. sylvaticus; dark circle = A. flavicollis. Envelopes show the morphological varıability of samples from Bulgaria and Greece for both species

overall specific discrimination (the number of diagnostic locı between two species) is sımilar and often more important with the set of locı and the electrophoretic buffers we used. This reasoning is based on the assumption that the differences in scoring results are probably more related to the techniques used than to varıability of the biological material. These differences in discriminating capacıty do not, however, alter the phylogenetic relationships as determined by the genetic distances.

Our results agree wıth previous work on this genus (GEMMERE 1980) ın that A. sylvaticus, A. flavicollis and A. mystacinus belonging to the same subgenus Sylvaemus cluster together whereas A. agrarius, which represents a different subgenus (Apodemus) ıs exterior to this group.

That morphological discrimination is difficult and even impossible between specimens of A. sylvaticus and A. flavicollis inhabiting Southern Europe has previously been shown for France (BENMEHDI et al. 1980), Italy (NascETTI and FıLıppuccı 1984) and Germany (EnGEL et al. 1973; GEMMERE 1980) and is here extended to Bulgarıa and Greece. Previous results are here again confirmed in that in all cases of morphological ambiguity, the biochemical analysis allowed to assıgn the specimens to either species and showed the absence of any introgression between them. It is therefore suggested that field specimens be identified by electrophoretic methods (on albumin for example, DEBROT and MERMOD 1977; GEMMERE 1981) or by using the morphological criteria put forth by FıLıppucct etal. (1984) which enabled to discriminate at least 95 % of Italian specimens and should be tested elsewhere.

This study shows that the separation of the four Apodemus species studied into two subgenera is supported by the biochemical distance data. Within the subgenus Sylvaemus, A. sylvaticus and A. flavicollis are remarkable in that they represent morphologically and chromosomally very similar species with relatively large genic distances.

The particular position of A. agrarius is worth commenting on, however. The very important genic distance between this species and those of the subgenus Sylvaemus is

92 Janice Britton-Davıdian et al.

probably an underestimate, being at the limit of the discriminating power of electrophore- tic methods. In fact, IsKANDAR and BONHOMME (1984) showed that sequential elec- trophoresis allowed to uncover 27 % more alleles between the two subgenera whereas no additional variation was revealed between the three species of the subgenus Sylvaemus. These data then suggest that A. agrarıns ıs probably even more distantly related to the Sylvaemus species group than what we indicate herein. Based on these data, we agree with BONHOMME et al. (1985) in suggesting that a taxonomıic revision of this group be made. It is probable that the two current subgenera will be elevated to a genus rank since Apodemus appeared not to be more closely related to Sy/vaemnus than to other murid (BONHOMME et al. 1985) or even arvicolid (data not based on sequential electrophoresis: GILL et al. 1987) genera. For this analysis, it would be imperative that biochemical data be collected for species belonging to the third subgenus (Alsomys) in order to correctly establish the evolutionary relationships within the Apodemus complex.

Acknowledgements

We wish to thank F. BONHOMME, J. CATALAN, ]J. CASSAING, F. CATZEFLIS, ]. GROBERT, D. ISKANDAR, U. Jünes, P. Orsınt, F. Portevin and L. THALER for their help in gathering and processing specimens and discussions. Field trips were financially supported by a NATO grant and Franco-Bulgarian cooperation agreements.

Zusammenfassung

Genetische Differenzierung bei vier Apodemus-Arten in Südeuropa: A. sylvaticus, A. flavicollis, A. agrarius und A. mystacinus (Muridae, Rodentia)

Die genetische Variabilität von vier südeuropäischen Apodemus-Arten wurde durch Elektrophorese von Proteinen geschätzt, die über 20 Genloci kodiert werden. Die nach Neı (1978) berechneten Abstandswerte entsprechen ungefähr den bisherigen Vorstellungen von der abgestuften Verwandt- schaft dieser Arten. So unterscheidet sich A. agrarins (Untergattung Apodemus) beträchtlich von den drei anderen, in der Untergattung Sylvaemus zusammengefaßten Arten. Apodemus sylvaticus und A. flavicollis überschneiden sich in ihren morphologischen Merkmalen in Südeuropa stark, lassen sich aber gelelektrophoretisch stets einwandfrei bestimmen. Alle vier Arten haben gewöhnlich 48 Chro- mosomen. Nur 1A. flavicollis von 27 aus Bulgarien hatte mit einem kleinen zusätzlichen akrozentri- schen Element insgesamt 49 Chromosomen.

Literature

BEKAsOva, T. S.; VORONTSov, N. N.; KOROBITSYNA, K. V.; KoRABLEV, V.P. (1980): B-chromosomes and comparative karyology of the mice of the genus Apodemus. Genetica 52/53, 3343.

BENMEHDI, F.; BRITTON-DAVIDIAN, J.; THALER, L. (1980): Premier apport de la genetique biochimi- que des populations ä la systematique des mulots de France continentale et de Corse. Biochem. Genet. Ecol. 8, 309-315.

BONHOMME, F.; ISKANDAR, D.; THALER, L.; PETTER, F. (1985): Electromorphs and phylogeny in muroid rodents. In: Evolutionary Relationships among Rodents. Ed. by W. P. LuckErTT and ].-L. HARTENBERGER. London: Plenum Publishing Corp. 671-683.

DARVICHE, D.; BENMEHDI, F.; BRITTON-DAVIDIAn, J.; THALER, L. (1979): Donnees preliminaires sur la systematique biochimique des Genres Mus et Apodemus en Iran. Mammalıa 43, 427-430.

DEBROT, $.; MERMOD, C. (1977): Chimiotaxonomie du genre Apodemus Kaup, 1829 (Rodentia, Muridae). Rev. Suisse Zool. 28, 521-526.

EnGEL, W.; VoGEL, W.; VoıcuLsscv, 1.; RopErs, H.-H.; ZEnzEs, M. T.; BENDER, K. (1973): Cytogenetic and biochemical differences between Apodemus sylvaticus and Apodemus flavicollis, possibly responsible for the failure to interbreed. Comp. Biochem. Physiol. 44B, 1165-1173.

Fırıppuccı, M. G.; CrISTALDI, M.; Tızı, L.; Contouı, L. (1984): Datı morfologici e morphomerrici in popolazioni dı Apodemus (Sylvaemus) dell’Italia centro-meridionale determinati elet- troforeticamente. Ric. Biol. Selv. 9, 85-125.

GEMMEKE, J. (1980): Proteinvariation und Taxonomie in der Gattung Apodemus (Mammalıa, Roden- tia). Z. Säugetierkunde 45, 348-365.

GEMMEKE, H. (1981): Albuminunterschiede bei Wald- und Gelbhalsmäusen (Apodemus sylvaticus und A. flavicolls, Mammalia, Rodentia) auch in getrockneten Muskeln und Bälgen elek- trophoretisch nachweisbar. Z. Säugetierkunde 46, 124-125.

Genetic differentiation in four species of Apodemus from Southern Europe 389

GEMMEKE, H.; NIETHAMMER, ]. (1981): Die Waldmäuse Apodemus sylvaticus und A. flavicollis vom Monte Gargano (Süditalien). Z. Säugetierkunde 46, 162-168.

GEMMEKE, H.; NIETHAMMER, J. (1982): Zur Charakterisierung der Waldmäuse (Apodemus) Nepals. Z. Säugetierkunde 47, 33-38.

GiLL, A.; PETRov, B.; Zıvkovid, $.; Rımsa, D. (1987): Biochemical comparisons in Yougoslavian rodents of the families Arvicolidae and Muridae. Z. Säugetierkunde 52, 247-256.

ISKANDAR, D.; BONHOMME, F. (1984): Variabilite electrophoretique totale a 11 locı structuraux chez les rongeurs murides (Muridae, Rodentia). Can. J. Genet. Cytol. 26, 622-627.

Krar, B. (1970): Chromosome studies in two subgenera of the genus Apodemus. Zool. Listy 19, 119-134.

NAscETTI, G.; FıLıppuccı, M. G. (1984): Genetic variability and divergence in Italian populations of Apodemus sylvaticus and Apodemus flavicollis (Rodentia, Muridae). Ric. Biol. Selv. 9, 75-83. Neı, M. (1978): Estimation of average heterozygosity and genetic distance from a small number of

individuals. Genetics 89, 583-590.

NIETHAMMER, J. (1969): Die Waldmaus, Apodemus sylvaticus (Linne, 1758) ın Afghanistan. Säugetierkdl. Mitt. 17, 121-128.

NIETHAMMER, J.; Krapp, F. (1978): Handbuch der Säugetiere Europas. Wiesbaden: Akademische Verlagsges. pp. 476.

PASTEUR, N.; PASTEUR, G.; BONHOMME, F.; CATALAN, J.; BRITTON-DAVIDIAN, J. (1987): Manuel d’electrophorese appliquee A la genetique des populations. Paris: Editions Techniques et Documentation. pp. 232.

SOLDATOVIGC, B.; SavIC, 1.; SETH, P.; REICHSTEIN, J.; TOLKSDORF, M. (1975): Comparative karyologi- cal study of the genus Apodemus (Kaup, 1829). Acta Veterinaria, Beograd, 25, 1-10.

SWOFFORD, D. L.; SELANDER, R. B. (1981): BIOSYS-1: aFORTRAN program for the comprehensive analysıs of electrophoretice data in population genetics and systematics. J. Hered. 72, 281-283. Zıma, J. (1984). Chromosomes of certain small mammals from Southern Bohemia and the Sumava

Mts (CSSR). Folia Zool. 33, 133-141.

ZımA, J.; Krar, B. (1984): Karyotypes of European Mammals II. Acta Nat. Acad. Sci. Bohemos-

lovacae, Brno 18, 34-35.

Authors’ addresses: JaANICE BRITTON-DAVIDIAN, MEHRNOUCH VAHDATI, FATIMA BENMEHDI and VALERIE NanceE Laboratoire de Genetique, Institut des Sciences de l’Evolution, USTL, Place E. Bataillon, F-34095 Montpellier Cedex 5, France; PAULE GRoS and HENRI CROSET, Laboratoire d’Eco-ethologie, Institut des Sciences de l’Evolution, USTL, Place E. Bataillon, F-34095 Montpelier Cedex 5, France; SVETOSLAV GUERASSIMOV, Zoology Institute, Bulgarıan Academy of Sciences, Bd Rouski 1, Sofia 1000, Bulgaria; CosTAs TRIANTAPHYLLIDIS, Arıstotelian Univer- sity of Thessaloniki, School of Sciences, Division of Genetics, Development and Molecular Biology, GR-54006 Thessaloniki, Greece

Z. Säugetierkunde 56 (1991) 34-40 © 1991 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-3468

Cranial infraspecific differentiation in Proechimys iheringi Thomas (Rodentia: Echimyidae)

By LeırLa M. PessöA and S$. F. Dos Reıs

Departamento de Zoologia, IBS, Universidade Federal do Rio de Janeiro and Departamento de Parasitologia, IB, Universidade Estadual de Campinas, Brazil

Receipt of Ms. 6. 3. 1990 Acceptance of Ms. 8. 6. 1990

Abstract

Proechimys iheringi Thomas ıs an echimyid rodent occurring in eastern Brazil from the states of Bahia to Säo Paulo. MOOJENn (1948) recognized sıx subspecies of P. iheringi primarily on the basis of clinal variation in the number of cheekteeth countertfolds. In this study we analyzed infraspecific differentia- tion in 13 morphometric cranıal characters ın three populations assıgnable to three subspecies of P. iheringi. Cranıal dımensions vary clinally increasing from north to south and morphomerric differ- entiation is correlated with geographic distance. The congruence between the clinal variation in cheekteeth counterfolds and cranıal traits indicates that the trinomial nomenclature should not be applied to P. iheringı.

Introduction

Proechimys iheringi Thomas is an echimyid rodent which occurs ın eastern Brazil, ranging from Bahıa to Säo Paulo (MooJEn 1948). In a detailed analysıs of infraspecific differentia- tion ın P. iheringi MOOJEN (1948) detected varıation in several skull traits including incisive foramen, tympanıc bulla, mesopterigoid fossa, palatine foramen, and vomerine sheath. In spite of the varıation in these characters, MOOJEn (1948) relied prımarily on the number of cheekteeth counterfolds, which varies clınally increasing from north to south, to recognize sıx subspecies ın P. zheringi, namely P. ı. denigratus from Bahia, P. :. gratiosus, P. 1. paratus, and P. i. panema from Espirito Santo, P. 1. bonafidei from Rio de Janeiro, and P. :. iheringi from Säo Paulo (Fig. 1). The subspecific structure in P. zheringı ıs thus based on a trait that varıes on a cline and whose differentiation ıs correlated wıth geographic distance (MoojJeEn 1948).

In this paper, we analyzed cranial varıation in three populations of P. iheringi assignable to the following subspecies: P. 1. denigratus, P. i. gratiosus, P. i. bonafıdei from the states of Bahia, Espirito Santo, and Rio de Janeiro, respectively. The primary objective of thıs study was to determine whether the pattern of differentiation in cranıal quantitative traits is congruent with the clınal varıation in cheekteeth counterfolds and to address the question of recognition of infraspecific units ın P. iheringı.

Material and methods

A total of 54 specimens of P. iheringi available in the mammal collection of the Museu Nacional (Rıo de Janeiro) was examined in this study. All specimens were classıfied to one of the 10 age categories defined by Parron and RoGers (1983) for P. brevicanda on the basıs of tooth eruption and occlusal surface wear criteria. This procedure was employed in order to control the ontogenetic source of variation, and 42 specimens from age classes 8-10 were selected for the analysıs of geographic varıation because they were adults by the criteria of Patron and RocGers (1983).

The specimens analyzed in this study represent samples collected at the following localities: Ilheus, state of Bahia (13° 01’ S, 40°01’ W; n = 16), Santa Tereza, state of Espirito Santo (19° 55’ S, 40°36’ W;

U.S. Copyright Clearance Center Code Statement: 0044-3468/91/5601-0034 $ 02.50/0

Cranial infraspecıfic variation in Proechimys iheringi Thomas 35

Fig. 1. Ranges for the subspecies of Proechimys iheringi Thomas according to MooJEn (1948). The stars denote localıty samples analyzed in this study

n = 18) and Teresöpolos, state of Rio de Janeiro (22° 26’ S, 42° 36’ W; n = 8). Sexes were pooled in the analysıs of geographic varıation to increase sample sizes.

Twelve cranıal measurements defined in Parron and RoGers (1983) in addition to one mandibular measurement were taken with electronic digital calipers accurate to 0.01 mm, as follows: palatal length A (PL), zygomatic breadth (ZB), nasal length (NL), interorbital constriction (IC), rostral breadth (RB), diastema length (DL), rostral depth (RD), skull length (SL), basal length (BL), rostral length (RL), maxillary breadth (MB), pospalatal length (PP), and mandibular length (ML) (Fig. 2).

Cranial character variation ın P. iberingi was analyzed by univariate and multivariate procedures (Sokar and ROHLF 1981; NEFF and Marcus 1980). Cranial characters were tested for significant differences among localities by univariate analysis of variance (AnovA). Significant characters were tested for maximally non-significant subsets of means employing Ryan-Einot-Gabriel-Welsch (REGWF) test on the main effect represented by the variable localıty.

36 Leila M. Pessöa and S. F. dos Reis

Fig. 2. Thirteen measurements taken on the skulls of Proechimys iheringi Thomas (see text for explanation of measurement abbreviations)

The pattern of variation in multivarıate character space was analyzed by principal components analysis (NEFF and Marcus 1980) and size-independent canonical discriminant analysis (STRAUSS 1985). The first pooled among-group principal component was used to study size variation among populations of P. iheringi. Scores derived from the fırst principal component were used as a measure of individual overall cranıal sıze and were tested by unıvariate anovA for heterogeneity among the populations.

Size-independent canonical discriminant analysis was employed to analyze patterns of discrimina- tion and ordination among the P. iheringi populations. This procedure removes the effect of size variation within groups by performing canonical discriminant analysıs on the residuals obtained from the regressions of each log-transformed character separately on the first pooled within-group principal component (STRAuss 1985). This procedure was employed because P. iheringi shows post-ontogenetic growth (indeterminate growth) that generates size variation within populations (PessöA 1989) that may confound the analysıs of geographic varıation (THORPE 1983). Scores derived from canonical discriminant analysis were plotted to assess the pattern of ordination and discrimination among the populations of P. iheringi. Canonical loadings were expressed as bivarıate correlations calculated between original character values and scores on the canonical variates (Strauss 1985).

Statistical analyses were performed using SAS-PC Version 6, the current microcomputer edition of the Statistical Analysıs System (SAS Institute, 1988).

Cranial infraspecıfic variation in Proechimys iheringi Thomas 97. Results

All cranial characters, except for palatal length and diastema length, increase in mean size from north to south, i.e. from the state of Bahia to the state of Rio de Janeiro (Table 1). Univariate analysis of variance indicates that all cranial traits differ significantly in the three populations of P. iheringi (Table 1). Nevertheless, the pattern of inter-locality differentia- tion in cranial traits is not uniform as indicated by the REGWF procedure (Table 1). Cranial

Table 1. Standard statistics for 13 cranial characters (in mm) in three populations (BA, ES, and RJ) of Proechimys iheringi Thomas

Character

Palatal length

Zygomatic breadth Nasal length Interorbital constriction Rostral breadth Diastema length Rostral depth

Skull length

Basal length

Rostral length Maxillary breadth

Mean (SD)

ES 15.82 (0.79)

BA 24.02 (1.21) BA 15.91 (0.98

) BA 11.06 (0.57) BA 7.03 (0.58) ES 10.16 (0.80) ) ) )

BA 9.36 (0.52 BA 46.27 (1.81

BA 34.74 (1.67

Mean (SD)

BA 16.30 (0.79) ES 25.32 (1.12) ES 17.47 (0.99) ES 11.53 (0.96) ES 7.36 (0.58) RJ 10.98 (0.63) ES 10.05 (0.83) ES 49.89 (2.31

ES 34.84 (1.55

BA 19.39 (0.99)

BA 8.17 (0.42)

ES 8.45 (0.88

Mean (SD)

RJ 16.80 (0.76)

RJ 26.08 (1.18) RJ 19.33 (1.27) RJ 12.47 (0.55) RJ 8.26 (0.43) BA 11.15 (0.78) RJ 10.87 (0.63) RJ 53.00 (2.66) RJ 37.22 (1.57)

RJ 23.28 (1.35) RJ 9.09 (0.51)

E

A)

9.58 28.41 9.50 12.97. 7.38 18:24 26.87 7.30

22.26 5.28

B

0.0201

0.0004 0.0001 0.0005 0.0001 0.0020 0.0001 0.0001 0.0022

0.0001 0.0096

) ) ES 21.43 (1.71) ) )

27.20 7.87

0.0001 0.0014

Pos-Palatal length Mandibular length

BA 2.72 (0.75) BA 23.87 (1.23)

ES 23.40 (0.94

( RJ 24.58 (1.26) ES 24.70 (1.38) (

RJ 26.20 (1.54)

Statistics given are mean, standard deviation, F-value of an analysıs of varıance and associated probability levels (P), and results of REGWF analysıs. Lines below population means connect nonsignificant subsets. BA = Bahia, ES = Espirito Santo, and RJ = Rio de Janeiro.

characters such as interorbital constriction, rostral breadth, basal length, maxillary breadth, and mandibular length are not significantly different ın the populations of Bahia and Espirito Santo, although individuals in both populations are significantly smaller than those ın the population from Rio de Janeiro. The three populations differ statistically in several cranıal traits including nasal length, rostral depth, skull length, rostral length, and pos-palatal length. Palatal length, zygomatic breadth, and diastema length have unique patterns of varıiation among the three populations (Table 1).

In order to analyze size varıation among populations of P. ıheringi in multivariate character space, the first pooled among-group principal component (PAGPc-1) was extracted from the covarıance matrix of log-transformed character values. PAGPc-1 can be interpreted as a general sıze factor since all vector coefficients are positive and have significant correlations with log-transformed character values (Strauss 1985) (Table 2). The scores from principal components analysis for the individuals in the three populations of P. iheringi can then be used as a measure of multivariate cranial size. Mean score values increase from north to south in the populations of Bahia (-0.0729), Espirito Santo (0.0056), and Rıo de Janeiro (0.1163) and these mean values were shown to be highly significant different by an univariate anovA (F = 16.48; P < 0.0001).

The pattern of ordination and discrimination of P. iheringi populations was assessed by

38

Table 2. Principal component and canonical variate loadings for 13 cranial morphometric

Leila M. Pessöa and S. F. dos Reis

characters in Proechimys iheringi Thomas

Character PAGPC-1

Palatal length Zygomatic breadth Nasal length Interorbital constriction Rostral breadth Diastema length Rostral depth Skull length

Basal length Rostral length Maxillary breadth Pos-Palatal length Mandibular length Percent of variance

0.160 0.212 0.380 0.134 0.339 0.178 0.357 0.285 94195 0.401 0.306 0.242 0.247

CV-1

0.845** -0.083ns -0.650**

-0.652**

—0.053ns

0.966”

—-0.253ns

-0.764** 0.590** -0.709**

O.211ns

-0.667**

0849

89.79

CV-2

0.06/ns 0.416” 0.238ns 0.205ns 0.341” 0.002ns —0.116ns —-0.078ns 0.201ns —0.132ns —0.050ns —0.045ns —0.153ns

10.21

explained 737

Canonical varıate loadıngs are expressed as vector correlations between log-transformed character values and canonical scores. PAGPC-1 is the pooled among-group first principal component. r is the Pearson product-moment correlation coefficient between cranial characters and the first principal component. * P<0.05; ** P<0.0001; n = non significant

SVi

Fıg. 3. Scatterplot of individual scores from a size-independent canonical discriminant analysis from three populations of Proechimys iheringi. Bahia (triangles), Espirito Santo (circles), and Rio de Janeiro (squares)

sıze-independent canonical discriminant analysıs. The first canonical varıate (CV-1) ex- plains 89.79 % of the total among-group varıation while CV-2 accounts for the remaining 10.21 %. The plot of canonical varıate scores shows that the three populations of P. iheringi occupy different positions in the reduced space of canonical varıates (Fig. 3). The population from Bahıa is discriminated from the populations from Espirito Santo and Rio de Janeiro along CV-1, whereas individual scores for the latter populations have non- overlapping distributions along CV-2. Figure 3 also indicates that the populations from Espirito Santo and Rıo de Janeiro, which are the geographically closest, are also mor- phometrically more sımilar. These populations are more differentiated morphomertrically from the population of Bahia which is geographically farther.

The vectors of correlations between canonical varıates and original log-transformed character values indicate that the population from Bahia differs from those of Espirito Santo and Rio de Janeiro ın most cranial measures of length (Table 2). Canonical variate 1 correlations indicate a contrast between palatal length, diastema length, basal length, and mandibular length with positive significant correlations and nasal length, interorbital

Cranial infraspecific varıation in Proechimys iheringi Thomas 39

constriction, skull length, rostral length, and pos-palatal length with negative significant correlations. On the other hand, the population from Espirito Santo differs from that of Rio de Janeiro in zygomatic breadth with a negative significant correlation and rostral breath with a positive significant correlation (Table 2).

Discussion

The univariate statistical analysis of cranıal character varıation did not produce a consistent pattern of inter-locality population differentiation in P. iheringi, although most characters vary in a cline increasing in size from north to south. The lack of consistency ın character trends observed for P. iheringi ın this study is acommon result, whenever morphomertric characters are analyzed univarıately (BAKER 1980; THORPE 1983; MAcEDO and MARES 1987).

The multivariate procedures employed produced a much clearer picture of the nature and extent of inter-locality ditferentiation in P. zheringi. Multivarıate cranıal size, esti- mated by mean score values derived from principal components analysis, increases from north to south confirming the clıne observed for most cranıal morphometric traits ın P. iheringi in the univariate analysıs. This clıne follows the same direction of the gradient in cheekteeth counterfolds observed by MoojJEn (1948). The pattern of ordination of P. iheringi populations in the space of canonıcal varıates further indicates a correlation between morphometric and geographic distance confirming MooJeEn’s (1948) observations based on qualitative arguments.

The analysıs of geographic differentiation in ?. iheringi reported in thıs paper ıs based upon population samples representing three subspecies among the sıx forms recognized by MoojJEn (1948). We believe nevertheless that our findings are representative of the overall pattern of varıatıon ın P. ıheringi since the three subspecies we analyzed are distributed over most of the range of thıs species (Fig. 1). Our results, in addition to MOOJEN’s (1948) findings, indicate that the varıation in P. iheringi ıs geographically structured in a clıne of increasing cranıal dimensions and number of cheekteeth counterfolds from northern to southern populations. The recognition of subspecies on the basıs of clinal varıation, as is the case for P. iheringi, has been criticızed primarily due to the continuous nature of the variation expressed ın a cline (BARROWCLOUGH 1982; THORPE 1987). The validity of the recognition of subspecific units in P. iheringi can be questioned since the application of trinomials has been considered suitable to describe character varıatıon that do not sımply form clines but rather diagnoses groups of populations indicating the existence of inde- pendent infraspecific units (BARROWCLOUGH 1982; THORPE 1987; SMITH and PATTON 1988; PATTon and SMITH 1989).

Our preliminary study indicates that, on the basis of the pattern of cranıal varıation, the use of the subspecific nomenclature is not justified for P. iheringi. Nevertheless, other character systems should be surveyed to assess the nature and structure of variation in order to understand the process of differentiation in this species and determine whether independent evolutionary units (sensu SMITH and PATToN 1988; PATTON and SMITH 1989) should be recognized for P. iheringı.

Acknowledgements

We thank Drs. A. S. Age and I. Sazıma for critically reading the manuscript and contributing to its improvement. Dr. U. Caramaschi kindly allowed the examination of museum specimens under his care. We are indebted to M. F. PEssöA for drawing the skulls and J. A. DE OLıveira for making the photographs. This study was supported by grants from CNPq (402265/87.4.20), FAPESP (88/2227- 4, 89/0772-1, and 89/3405-0), and FAP (503/89). Work by L.M.P. and S.F.R. was partially supported by graduate and research fellowships from CNPg, respectively.

40 Leila M. Pessöa and S. F. dos Reis

Zusammenfassung

Intraspezifische Schädelvariabilität bei Proechimys iheringi Thomas (Rodentia: Echimyidae)

Schädel von Igelratten (Proechimys iheringi) aus drei Populationen, die drei der sechs beschriebenen Unterarten dieser Art zuzuordnen sind, wurden in 13 Maßen verglichen. Danach nimmt die Schädelgröße von Norden nach Süden zu. Die allgemeinen morphometrischen Abstände zwischen den Populationen sind mit ihren geographischen Abständen korreliert. Da sich auch die Zahl der Schmelzfalten in gleicher Richtung klinal ändert, läßt sich eine Gliederung von Proechimys iheringi in Unterarten mit diesen Merkmalen nicht rechtfertigen.

Literature

SAS Institute Inc. (1988): SAS/STAT User’s Guide, Release 6.03 Ed. Cary, NC.

BAkKER, A. J. (1980) Morphomertric differentiation in New Zealand populations of the house-sparrow (Passer domesticus). Evolution 34, 638-653.

BARROWCLOUCH, G. F. (1982): Geographic varıation, predictiveness, and subspecies. Auk 99, 601-603.

Mac£no, H. R.; Mares, M. A. (1987): Geographic varıation in the South American cricetine rodent Bolomys lasiurus. J. Mammalogy 68, 578-594.

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

NErr, N. A.; Marcus, L. F. (1980): A survey of multivarıate methods for systematics. New York: privately published.

PATTon, J. L.; ROGERs, M. A. (1983): Systematic implications of non-geographic variation in the spiny rats genus Proechimys (Echimyidae). Z. Säugetierkunde 48, 363-370.

PaTTon, J. L.; SMITH, M. F. (1989): Population structure and the genetic and morphologic divergence among pocket gopher species (Genus Thomomys). In: Speciation and its Consequences. Ed. by D. OTTE and J. A. EnDLER. Sunderland: Sinauer Ass. 284-306.

Pessöa, L. M. (1989): Diferenciagäo cranıana infraespecifica em Proechimys iheringi Thomas e P. dimidiatus (Guenther) (Mammalia: Rodentia: Echimyidae). Unpub. MSc diss., Univ. Fed. do Rio de Janeiro.

SMITH, M. F.; Parron, J. L. (1988): Subspecies of pocket gophers: Causal basis for geographic differentiation in Thomomys bottae. Syst. Zool. 37, 163-178.

SokaL, R. R.; ROHLEF, F. ]J. (1981): Biometry. 2nd. ed. San Francisco: Freeman.

Strauss, R. E. (1985): Static allometry and varıation in body form in the South American catfısh genus Corydoras (Callichthyidae). Syst. Zool. 34, 381-396.

THORBE, R. S. (1983): A review of numerical methods for recognising and analysıng racıal differentia- tion. In: Numercial Taxonomy. Ed. by J. FELSENSTEIN. Berlin: Springer Verlag. 404423.

— (1987): Geographic varıation: A synthesis of cause, data, pattern and congruence in relation to subspecies, multivariate analyses and phylogeny. Bull. Zool . 54, 3-11.

Authors’ addresses: LeıLa M. PessöA, Departamento de Zoologia, CCS, Universidade Federal do Rio de Janeiro, BR-21941, Rio de Janeiro, R], Brazil; $S. F. Dos Reıs, Depar- tamento de Parasitologia, IB, Universidade Estadual de Campinas, €7P.26109 BR-13081, Campinas, SP, Brazil

Z. Säugetierkunde 56 (1991) 41-47 © 1991 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-3468

Thermoregulation and torpor in African woodland dormice, Graphiurus murinus, following cold acclimation

By G.T. H. Errison and J. D. SKINNER

Mammal Research Institute, University of Pretoria, Pretoria, South Africa

Receipt of Ms. 28. 11. 1989 Acceptance of Ms. 14. 9. 1990

Abstract

Studied thermoregulation of 3 adult woodland dormice (Graphiurus murinus) following acclimation to 15 °C and 10 °C. The dormice entered hibernation under these conditions characterised by a fall ın body temperature to within 1°C of ambient, and a prolonged reduction in oxygen consumption measured over 24 h at 10 °C and 5 °C. Non-shivering thermogenic capacity exceeded that required to re-attain homeothermy by 20 %, but would permit these dormice to maintain normothermia down to -5 °C. The cycle of body mass displayed by G. murinus in the present study is characteristic of hibernating temperate dormice, but was not observed in specimens collected throughout the year in southern Africa. It therefore appears that woodland dormice may not enter hibernation throughout their distribution during winter, but may exhibit facultative torpor under adverse climatic conditions.

Introduction

Afrıcan woodland dormice, Graphiurus murinus, are small, arboreal rodents found throughout large areas of tropıcal and subtropical Afrıca (SMITHERS 1983). Although EISENTRAUT (1962) could not elicit torpor in G. murinus from West Africa (Cameroon), SMITHERS (1983) suggested that this species shows sıgns of lethargy during cold weather ın South Africa. Following the discovery of a torpıd woodland dormouse during rodent trapping by the authors outside Pretoria ın March 1987, the following study was initiated to ıinvestigate thermoregulation and torpor in G. murinus under controlled laboratory conditions.

Material and methods

Three Afrıcan woodland dormice (2 adult females, 1 adult male) were collected at Vaalkop Dam Nature Reserve (25°23’ 27°28’E) during April 1989. Within one week of capture the dormice were transferred to a windowless climate chamber (Specht Scientific, Johannesburg) at Pretoria University (25°45'S 28°12’E) wherein photoperiod and temperature could be accurately controlled. Throughout the study the photoperiod within the chamber was maintained at 10 h light: 14 h dark (lights on at 07h00 and off at 17h00) which closely resembled the photoperiod prevailing at Vaalkop Dam during mid-winter. The dormice were initially acclımated for 50 days at an ambient temperature (T,) of 15 °C followed by a further 50 days at T, = 10°C. The dormice were housed separately in standard laboratory rat cages containing sawdust, shredded paper and a 500 ml plastic beaker which served as a nest box. Water, sunflower seeds, rat cubes and rabbit pellets (Epol, Vereniging) were provided ad libitum, a diet occasionally supplemented with pieces of fresh apple.

The body mass of each dormouse was recorded upon capture and subsequently at regular intervals throughout the study. In addition, rectal temperatures (T,) were measured between 07h00-13h00 on five occasions during acclimation to both T, = 15 °C and T, = 10 °C. T, was determined by inserting a chromel alumel thermocouple (K-Type: Fluke, Everett), attached to a digital thermometer, approxi- mately 2 cm into the rectum for a period not exceeding 15 sec. To avoid undue perturbation, body mass and rectal temperature were recorded at intervals of 3 days or more, and at all other times the dormice remained undisturbed within the climate chamber.

Following 50 days acclimation at 10°C the oxygen consumption (VO;) of the dormice was measured as an indication of metabolic rate (MR) using an open-circuit system (as described by Depocas and Harr 1957, and Hırr 1971). The dormice were placed in perspex metabolic chambers

U.S. Copyright Clearance Center Code Statement: 0044-3468/91/5601-0041 $ 02.50/0

42 G. T. H. Ellison and ]J. D. Skinner

through which a flow of dried air (Silica Gel: Holpro, Johannesburg) was passed at a rate of 600 ml x min”!. The chambers were immersed in a constant temperature water bath (Labotec, Isando), and a chromel alumel thermocouple within the chamber was used for monitoring chamber tempera- ture (T.). Following full equilibration VO, was recorded using an Ametek S-3A/I oxygen analyser (Applied Electrochemistry, Pittsburgh) linked to a multi-channel data logger (Grant Instruments, Chambridge). The oxygen analyser was calıbrated before and after measurement, and VO, was corrected to standard temperature and pressure, dry (STPD).

Average daily metabolic rate (ADMR) was measured over 48 h in large (13 I) metabolic chambers. The dormice were transfered to these chambers, together with their bedding and food, 20 h prior to the start of measurement, and were subsequently subjected to 24 h at T. = 10 °C followed by 24 hat T.=5°C. Aır leaving the chambers was connected to a three-way valve and time-switch (Air/Water 350 KPA: Ascoreg, Johannesburg), so that VO; from two dormice could be monitored simultane- ously every 30 min using a single oxygen analyser. At the end of measurement the mass and rectal temperature of each dormouse was recorded.

Resting metabolic rate (RMR) was measured following one hour’s exposure to T.=5 °C and 10 °C within smaller metabolic chambers (700 ml). VO, was monitored over 30 min after which rectal temperature and body mass were recorded.

Maximum oxygen consumption (VO,,,.x) following an injection of noradrenaline (NA) was used as an indication of non-shivering thermogenetic capacity (as described by HELDMAIER 1971). The dormice were anaesthetised with sodium pentobarbitone (70 mg/kg intraperitoneally. Sagatal: May- baker, Port Elizabeth) after which a chromel alumel thermocouple (J-Iype: Grant Instruments, Cambridge) was inserted deep into the rectum to measure T, and secured to the base of the tail with tape. Following a subcutaneous injection of 1.5 mg/kg NA (HELDMAIER 1971) the dormice were transfered to a small metabolic chamber (700 ml) at T. = 30°C and VO, and T}, were recorded simultaneously at one minute intervals for 60 min using the multichannel data logger. VOzmax and Tumax were taken as the highest values of VO, and T, recorded following NA injection.

All results are presented as mean + one standard deviation unless otherwise stated.

Results Body mass

Following acclımation, the mean body mass of dormice in the present study entered a cycle comprising a rapıd period of weight gain followed by a slower sequence of weight loss. From a mean capture mass of 29.1 # 4.3 gthe dormice weighed 43.2 # 4.3 g after 25 days in captivity, an increase of almost 50 %. Following a gradual decline the dormice returned to capture mass by Day 65, after which they retained a stable mean body mass for the remainder of the study.

Body temperature

All the measurements of T, taken during acclımation to T, = 15 °C and 10 °C were pooled and displayed in two histograms (Fig. 1). Under both T, regimes the dormice were predominantly torpid, with the majority of T}, measurements fallıng at, or slightly above T,. At these Typs the dormice were stiff and displayed the lack of responsivity and coordination characteristic of deep torpor. In addition, the level of hypothermia recorded was dependant upon T,, being lower ae 17, - 1O,@zthanrarıT, — SS CHE measurements fell within the normothermic range for mammals (33 °C-36 °C) which suggests that the dormice were usually in torpor between 07h00 and 13h00 when T}, was recorded.

Metabolism

At 10°C the mean RMR of the dormice was 3.74 + 0.14 mlO,xg'xh (T, = 34.7+0.4°C) and increased slightly at 5°C to 3.99+0.15 mlO,xg"'xh’' (T, = 34.1 #0.1 °C). In contrast, VO, measured over 24 h at these temperatures remained at low levels for prolonged periods, punctuated with brief increases in VO, lasting between 1 h and 6 h (Fig. 2). Excluding these incidents of increased metabolism, the mean ADMR

Thermoregulation and torpor in Graphiurus murinus 43

frequency

frequency

10 15 20 25 30 35 1,(00)

Fig. 1. Rectal temperatures recorded between 07h00 and 13h00 during acclimation to T, = 15°C and 10°C

12.19.@7(0.27.= 0.06 ml®©, Xen x<hr)) was only 7.3% RMR and at 5°€ (0.52 # 0.26 mlO,x g"'xh"') was 13.0 % RMR (Fig. 3). Despite the modest rise in ADMR following exposure to 5°C, the dormice exhibited a mean T, of 6.0 #0.3°C at the end of measurement.

The male dormouse died under anaesthesia during the measurement of NST, whilst the females displayed a mean VO, max of 5.75 # 0.67 mlO,x g"' x h"! following NA injection, accompanied by mean Tpmax Of 40.6 # 1.0 °C. When compared to ADMR and RMR in Fig. 3 VO,,.. was found to exceed the level of heat production required to maintain normothermia at either 10°C or 5°C. However, according to HELDMAIER’s (1971) allometric equation relating VO,., to body mass, the VO, „ax recorded in the present study ıs approximately 90 % of that predicted for mammals of similar body sıze following cold (5 °C) exposure (VO,max predicted: 6.37 mlO,xg"'xh’').

Discussion

The results of the present study clearly indicate that G. murinus from southern Africa is capable of spontaneous bouts of deep torpor when confronted with cold stress under sımulated winter photoperiod. Furthermore, these bouts of torpor exceeded 24h in duration, which suggests that G. murinus entered hibernation under these conditions. Hibernating dormice rarely arouse when challenged with declining temperatures and instead increase metabolic thermogenesis to maintain T, at non-lethal levels even as T, falls to O0 °C or below (WarHovD 1976; PAJunEn 1986). In the present study torpıd dormice displayed an increase in metabolism when T, fell from 10 °C to 5 °C, which indicates that torpor in G. murinus, in common with other dormice, ıs facultative and under strict thermoregulatory control. However, a consequence of this increase in metabolic rate is that an optimal T, exists for maximum energy savings during hibernation, as described for the garden dormouse, Eliomys quercinus (PAJunEN 1986). For G. murinus the optimal T, appears to fall between 10°C and 5°C which corresponds to the mean night-time temperature of around 5 °C prevailing during winter (June/July) at Vaalkop Dam (Pretoria Weather Bureau: Brits Met. Stn. 25°35’ S 27°49’ E 1939-1984).

44 G. T. H. Ellison and J. D. Skinner

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9 Time 12h00 18h00 00h00 06h00 12h00 18h00 00h00 06h00 12h00 (:[D)

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Fig. 2. Oxygen consumption (VO,) of 3 Graphiurus murinus measured over 24 h at 10°C and 5°C

Non-shivering thermogenesis is the dominant pathway for heat production in small mammals (BÖcKLER et al. 1988) although hibernators exhibit higher levels of NST than euthermic species of similar body sıze even in the absence of cold adaptation (JANsKY 1973). This enhanced capacity for NST amongst hibernators is believed to be associated with the heat required for arousal from hypothermia (ABBoTTs and Wang 1980). If we assume that the specific heat capacity of animal tissue is 3.4k]Jxg”' (CHArPELL and BARTHOLOMEW 1981) and that the calorific equivalent of oxygen is 20.1 JXmlO," (SCHMIDT-NIELSEN 1983) then rewarming a 31.9 g dormouse from T, = 6.1 °C to 34.4 °C (28.3 °C) in the present study would require 3.07 kJ or 152.74 mlO;. This compares with the total heat produced during NST of 5.75 mlO,xg"'xh! or 183.43 mlO,;xh, which exceeds that required for rewarming by 20 %. For this reason NST in G. murinus may be important not only for arousal from hypothermia, but also for the maintenance of homeothermy in the cold. In this context the lowest T, at which G. murinus can thermoregulate, using NST alone, can be calculated assuming that Newton’s law of cooling holds for this species as proposed by SCHOLANDER et al. (1950): (Thermal conductance below themoneutrality [C„] = VO>x[T,-T,]'). Based upon RMR and T}, measured at 5°C and 10°C, the mean Cr of dormicer in therpresent study, was 0145220078

Thermoregulation and torpor in Graphiurus murinus 45

7.0 150%

6.0

5.0

100%

40 100%

3.0

2.0

7.3%

VO,(mlo,.g°1:h"1)

ADMR RMR | 'ADMR RMR! | NA 102€ ea N

Fig. 3. The relationship between average daily metabolic rates (ADMR) during torpor and resting metabolic rate (RMR) during normothermia measured at 10°C and 5°C in 3 Graphiurus murinus. As an indication of non-shivering thermogenic ability, the metabolic response to noradrenaline injection (NA: VO) of 2 G. murinus ıs displayed to the rıght. Vertical lines indicate + one standard deviation of the mean

mlO,xg""xh"!x °C! with a mean normothermic T}), of 34.4 # 0.4 °C. Using NST to produce a VOymax of 5.75 mlO,x g!xh! these dormice could feasibly maintain a similar T; down to T,'s as low as -5 °C, which corresponds to the mean daily minimum temperature (-3 °C) recorded at Vaalkop Dam during winter (June/July: Pretoria Weather Bureau).

The body mass cycle displayed by G. murinus in the present study ıs sımilar to that reported for Glis glis and E. quercinus during winter and following cold acclımation (Mrosovsky 1986; PAJunEn 1986). These dormice undergo a distinct increase in body mass prior to hibernation, during which up to 25 % of body mass ıs subsequently lost (JALLAGEAS and AsSSENMACHER 1986). In order to assess whether or not G. murinus displays similar body mass cycles ın nature the mass of 77 specimens collected throughout the southern African subregion were grouped by month of capture and presented in the Table.

These specimens did not display a clear circannual cycle of body mass, which sugests that G. murinus does not naturally enter hibernation throughout southern Africa. Indeed,

Mean body mass of 77 G. murinus collected throughout the southern African subregion (From the archives of the Transvaal Museum, Pretoria)

Mar/Apr Sep/Oct

46 G. T. H. Ellıson and J. D. Skinner

the cycle of body mass observed in the present study may have been an artefact of laboratory conditions as both short photoperiod (Könıs 1960) and abundant food (ROTHwELL and Stock 1986) have been reported to elicit increased body mass and subsequent hibernation in other species of dormice. However, under similar conditions, EISENTRAUT (1962) could not elicit torpor or hibernation from G. murinus haedulus from tropical West Africa which suggests that different populations of this species differ in their ability to display torpor and/or hibernate. Similar geographic differences have been reported for forest dormice (Dryomys nitedula) which hibernate for 6 months in Eurasia yet remain active throughout the year in Israel (NEVO and Amır 1964). It therefore appears that G. murinus from southern Africa differ from tropical populations in their ability to enter deep torpor/hibernation, although, like garden dormice in Morocco, thıs ability is probably only expressed when local climatic conditions demand (MORENO and DeLiıBes 1964).

Acknowledgements

The authors would like to thank BassıE POTGIETER for providing excellent technical assistance throughout the study and Amy and Nick BEZUIDENHOUT for their generous hospitality at Vaalkop Dam. InGo BUCHERT, GUsSTAV PETERS, WOLFGANG RAMDOHR and BRIGITTE WENHOLD kindly helped with german translation and assisted in collating the final manuscript. Collection data was provided by the Mammal Department at the Transvaal Museum, and clımatic information was supplied by the Weather Bureau in Pretoria. G.T.H.E. was supported by grants from the Foundation for Research Development, Department of National Education, and University of Pretoria.

Zusammenfassung

Thermoregulation und Torpor bei afrıkanischen Baumschläfern, Graphiurus murinus, nach Kaltebelastung

Zahlreiche Arten der Gliridae aus den gemäßigten Klimazonen sind Winterschläfer. Über einen saisonbedingten Torpor bei Baumschläfern (Graphiurus murinus) aus den tropischen und subtropi- schen Gegenden Afrikas liegen nur Vermutungen vor. Drei erwachsene G. murinus wurden ım Herbst im südlichen Afrıka gefangen und ım Labor 50 Tage lang bei 15°C und 10°C sowie unter kurzer Lichtperiode gehalten. Sie gerieten dabei in Torpor. Die Körpertemperaturen sanken bis auf den Wert der Umgebungstemperatur. Die durchschnittliche Stotfwechselintensität fiel bei 10 °C und 5°C bis auf 73% bzw. 13,0% des Ruhewertes im normothermen Zustand. Die durch Noradrenalin induzierte zitterfreie Thermogenese übertraf die für das Erwachen aus dem Torpor benötigte Wärme. Die Bilche reagierten auf die Kältebelastung mit einer Gewichtszunahme und mit nachfolgendem Gewichtsver- lust. Tiere, die im Verlaufe des Jahres gefangen wurden, zeigten diesen Zyklus nicht. Vermutlich gibt es bei G. murinus nur unter sehr ungünstigten klimatischen Bedingungen Torpor.

References

ABBOTTS, B.; Wang, L. C. H. (1980): Seasonal thermogenic capacity in a hibernator, Spermophilus richardsonii. J. Comp. Physiol. B. 140, 235-240.

BÖCKLER, H.; STEINLECHNER, $.; HELDMAIER, G. (1982): Complete cold subsitution of noradrenaline induced thermogenesis in the Djungarıan hamster, Phodopus sungorus. Experientia 38, 261-262.

CHAPPELL, M. A.; BARTHOLOMEW, G. A. (1981): Activity and thermoregulation in the antelope ground squirrel Ammospermophilus leucurus in winter and summer. Physiol. Zool. 54, 215-223.

Derocas, F.; HART, J. S. (1957): Use of the Pauling oxygen analyser for measurements of oxygen consumption of anımals in open-circuit system and in short-lag, closed-circuit apparatus. J. Appl. Physiol. 10, 388-392.

EISENTRAUT, M. (1962): Wie verhalten sich verwandte Vertreter von heimischen Winterschläfern aus wärmeren Gebieten unter veränderten Temperaturbedingungen? Zool. Anz. 169, 429432.

HELDMAIER, G. (1971): Zitterfreie Wärmebildung und Körpergröße bei Säugetieren. Z. vergl. Physiol. 73, 222-248.

Hırı, R. W. (1972): Determination of oxygen consumption by use of the paramagnetic oxygen analyser. J. Appl. Physiol. 33, 261-263.

JALLAGEAS, M.; ASSENMACHER, 1. (1986): External factors controlloing hibernation and related endocrine cycles in the edible dormouse, Glis glis. In: Endocrine regulations as adaptıve

Thermoregulation and torpor in Graphiurus murinus 47

mechanisms to the environment. Ed. by I. AssEnMACHER and J. Boıssin. Paris: Editions du Centre National de la Recherche Scientifique. Pp. 363-369.

Janskv, L. (1973): Non-shivering thermogenesis and its thermoregulatory significance. Biol. Rev. 48, 85-132.

Könts, C. (1960): Einflüsse von Licht und Temperatur auf den Winterschlaf des Siebenschläters Glis g. glıs (Linnaeus 1766). Z. Morph. Okol. Tiere 48, 545-575.

MORENOo, S.; DELIBES, M. (1982): Notes on the garden dormouse (Eliomys; Rodentia, Gliridae) of northern Morocco. Säugetierkdl. Mitt. 30, 212-215.

Mrosovsky, N. (1986): Mirrors of the environment: the enigmatic dormouse and other hibernators. In: Endocrine regulations as adaptive mechanisms to the environment. Ed. by I. AssEnNMACHER and J. Boıssın. Paris: Editions du Centre National de la Recherche Scientifique. Pp. 331-341.

NeEvo, E.; Amir, E. (1964): Geographic variation in reproduction and hibernation patterns of the forest dormouse. J. Mammalogy 45, 69-87.

Pajunen, I. (1986): Ambient temperature dependance of physiological parameters during long-term hibernation in the garden dormouse, Ehomys quercinus. In: Endocrine regulations as adaptive mechanisms to the environment. Ed. by I. AssenMAcHER and J. Boıssın. Paris: Editions du Centre National de la Recherche Scientifique. Pp. 379-383.

ROTHWELL, N. J.; STOCK, M. J. (1986): Spontaneous and experimental varıiations in body weight, food intake and metabolic rate in captive dormice (Glis glis). Comp. Biochem. Physiol. 84A, 141-147.

SCHMIDT-NIELSEN, K. (1983): Anımal physiology: Adaptation and environment. 3rd ed. Cambridge: Cambridge University Press. Pp. 178.

SCHOLANDER, P. F.; WALTERS, V.; Hock, R.; Irving, L. (1950): Body insulation of some arctic and tropical mammals and birds. Biol. Bull. 99, 237-258.

SMITHERS, R. H. N. (1983): The mammals of the southern African subregion. Pretoria: Univ. Pretoria.

WALHOVD, H. (1976): Partial arousals from hibernation in a pair of common dormice, Muscardinus avellanarius, (Rodentia, Gliridae), in their natural hibernaculum. Oecologia (Berl.) 25, 321-330.

Authors’ address: G. T.H. ErLison, and J. D. SKınnEr, Mammal Research Institute, University of Pretoria, Pretoria 0002, Republic of South Afrıca

Z. Säugetierkunde 56 (1991) 48-58 © 1991 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-3468

Time budgets of Waterbuck (Kobus ellipsiprymnus) of different age, sex and social status

By P. WıRrTZ and G. OLDEKOP

Institut für Biologie I, Albert-Ludwigs-Universität, Freiburg, FRG, and Max-Planck-Institut für Verhaltensphysiologie, Seewiesen, FRG

Receipt of Ms. 26. 3. 1990 Acceptance of Ms. 10. 8. 1990

Abstract

Daytime budgets of waterbuck (Kobus elhpsiprymnus) of different age, sex, and social status were measured at Lake Nakuru National Park, Kenya.

Adult and subadult females spent more time feeding than adult and subadult males. Inside territories, females spent more time feeding than outside of territories. Time spent for agonistic behaviour was highest ın young males. Satellite males spent less time for sexual behaviour than territory holders, but more time than bachelor males. Territory holders and satellite males spent the same amounts of time feeding - much more than bachelor males. Because the amount of forage ingested by ruminants is positively correlated with forage quality, this indicates that bachelor males were relegated to nutritionally inferior areas. Time budgets of males and females, site preferences of females, and faecal crude protein content of animals feeding at different sites (TomLınson 1979) all suggest that territories are high quality feeding areas and that the social system of waterbuck is a resource defence polygyny.

Sex differences in time spent feeding at the same site probably reflect a fundamental difference in the behavioural programming of males and females: females of polygynous species are more likely to be “energy maximisers” than males. Recent evidence points to differences in levels of sexual hormones as a proximate cause of sex differences not only of sexual and agonistic behaviour but also of maintenance behaviour.

Introduction

Regardless of age, sex, or social status, all members of a species have the same amount of time available to spend every day. They can, of course, be expected to spend i it on different activities. In polygynous species, adult males will spend time to acquire females, whereas adult females will spend time to produce viable offspring (SCHOENER 1971; TRIVERS 1972;

CLUTTON-BROocK et al. 1982; HoFFMANn 1983; OwEN SMITH 1984). As the amount of time per day is a finite value, spending more time for one activity must mean spending less time for one or several other activities. This study shows how the age classes, sexes, and holders of different social status of a polygynous mammal differ in allotting time to their activities during the day.

Waterbuck (Kobus ellipsiprymnus) are antelopes similar in size to red deer; they occur throughout Africa south of the Sahara (Dorst and DAnDELOT 1970; HALTENORTH and Dirter 1977). The social structure of waterbuck living in Lake Nakuru National Park, Kenya, has been described previously (WırTz 1981, 1982). With an average of 30 waterbuck/km?, Lake Nakuru NP has by far the highest population density recorded for the species. Probably as a consequence of the high population density, only about 7 % of the adult males held a territory during the study period and half of the territory holders tolerated one or several additional adult males, “satellite males”, in the territory. Within the territory, satellite males were subdominant to the territory holder and participated in the defence of the territory. About 9% of the adult males acted as satellite males and the remaining 84% were bachelor males spending most of their time outside territories. Females moved in herds of changeable size and composition over home ranges encompas-

U.S. Copyright Clearance Center Code Statement: 0044-3468/91/5601-0048 9.025070

Time budgets of Waterbuck 49

sing several territories and non-territorial areas. Most territories were located along the lake shore and along rıvers. During the day most females were inside territories (WIRTZ 1982).

Material and methods

Study area and recording technique

The study area has been described previously (WırTrz 1982) in a paper that also gives the definitions of the age classes used: adult male, young male, juvenile male, adult female, subadult female, and calf.

Both study years (1978 and 1979) were exceptionally wet years compared to long-term means (KurıLek 1975); see figure 2 in Wırrz (1982) for the monthly rainfall values. Data on time budgets were collected throughout the course of the two study years.

Time budgets of the different age classes, sexes, and social classes (territory holder, satellite male, bachelor male) were measured between 7am to 7 pm. Groups of anımals were observed with binoculars (Leitz Trinovid 10x 40) from a Land-Rover or from tree hides. Observations were recorded on a tape recorder. The anımals were accustomed to cars and during observations would graze as close as 5 m from the Landrover; average observation distance is estimated to be about 50 m. Uninterrupted observations at the same site lasted from one to twelve hours, on average three hours.

Data were collected using the „scan sampling“ technique (RoıLinson et al. 1956; ALTMAN 1974; Marrın and BATEsoN 1986). The observer would scan the group at regular intervals and record the momentary activity of each anımal seen. The proportion of records of a behaviour pattern is an approximation of the proportion of time spent performing this behaviour pattern. Inter-scan interval was five minutes. Large groups sometimes took longer to scan and the inter-scan interval was then set at ten minutes.

All activities were classified into the eleven types described below (see WALTHER [1958] for a description of behaviour patterns such as Flehmen, and see Tomrınson [1980] for a description of the expressive behaviour of waterbuck in particular):

l. Browsing Feeding on dicotyledons, such as shrubs or Acacıa leaves 2. Grazing Feeding on grasses 3. Standing Standing on all four legs; part of the time in this position is spent ruminating 4. Lying head up Lying on the ground with head raised above the ground; part of the time in this position ıs spent rumınating 5. Lying head down Lying with the head resting on the ground 6. Walking Moving forward at slow to moderate speed 7. Running Trotting or gallopıng 8. Agonistic Female butting her head into the flank of another female; male confronting another male with head raised high and horns tipped forward; male approach- ing another male in submissive low stretch posture wıth horns tilted back- wards; males fighting with interlocked horns; male galloping after another male 9. Sexual Male sniffing female, rubbing a female with its head, performing Flehmen or Laufschlag, running after a female, attempting to mount or mounting a female, copulating 10. Grooming Scratching the own body with hoof or horn, licking own body (allogrooming was only observed in mothers grooming their calves; this was recorded as “others”) 11. Others Drinking, defaecating and any other behaviour not mentioned above; also

behaviour recorded as “unidentified” when an anımal was partially hidden by the vegetation (0.1% to 1.0 % of all records in the different age classes).

The observations are biased in at least the following ways. Only groups of more than five animals were used for activity records. Among other things, this means that the data for territory holders apply only to territory holders that have females with them and not to territory holders without females. Observations were made only on groups in open grassland, open shrub, and open forest but not on groups in dense shrub and dense forest where anımals were difficult to see. Less than 6% of the waterbuck were recorded in these two types of habitat during counts of habitat utilization (WIrTZ and Kaiser 1988). Nevertheless, a slightly higher proportion of “browsing” would probably have been recorded if these two types of habitat had not been ignored. Recording the activity of each animal at the moment it is seen through the binoculars meant that an animal walking a few steps whilst grazing was recorded as “walking” rather than “grazing”. Bouts of ruminating are frequently interrupted and anımals seen at such moments were then recorded as “standing” or “lying head up” instead of “standing ruminating” or “lying ruminating”. We therefore decided not to report values for the two

50 P. Wirtz and G. Oldekop

incomplete measures of ruminating activity and have included them in “standing” and “lying head up”, respectively.

The data presented here describe daytime activity of waterbuck at Lake Nakuru National Park. Waterbuck are also active at night. For technical reasons, only few quantitative observations on nighttime activity could be taken. During several clear nights, approximately 20 hours of observations were made and there was no indication that the major patterns might be different from those recorded during daytime.

Number of observations

A total of 957643 observations were taken between 7:00 h and 19:00 h (observations per hour: 5513, 8630, 8480, 8516, 8305, 7855, 6845, 9048, 9906, 8812, 11422, 2411). The numbers of observations for the different waterbuck classes are given in Tables 1-4. The data for territorial males are from 39 individuals, those for satellite males from 36 individuals. More than 100 different individuals contributed to the observations for adult females and for bachelor males.

Treatment of data and statistical procedure

Numbes of observations were unequally distributed through the course of the day. For instance, relatively more observations were taken during hours when the anımals spent most of their time grazing; a daily mean from unweighted data would then result in an overestimate of this activity. For each hour, the number of observations of each activity was expressed as the percentage of all observations during this particular hour; the daytime mean was then calculated from these percentages (cf Figure as an example).

When comparing two different waterbuck classes, their daytime means were reconverted into frequencies of observations on the basıs of the total numbers of observations. The proportions of an activity in the total time budget (e.g. number of observations “grazing” versus number of observations of all other activities) were then compared by chi-square test.

When there were fewer than 100 observations for one of the classes compared during one of the hours of the day, this hour was exluded from the comparison.

Daytıme budget of the “average waterbuck” was calculated by combining the data for all age classes in the proportions at which they were collected, i.e. by simply summing all observations per hour of all anımals, regardless of age, sex, and social status.

The shorter the inter-scan interval, the better the estimate of the true amount of time spent for various activities (HARKER et al. 1954). On the other hand, very short observations intervals can result in measuring the same phenomenon repeatedly and producing “dependent data”, ı.e. an inflated sample size unsuitable for statistical analysis. Scanning a group every five minutes may lead to dependent data for some activities wıth very long bout lengths. A statistical comparison would then lead to unrealistic levels of significance. To be on the safe sıde, we here call a difference “significant” only if p < 0.001 (chi-square value > 10.83, 1 degree of freedom).

Results The “average waterbuck”

The “average waterbuck” spent 37 % of its daytime feeding (35.9 % grazing plus 1.1 % browsing), 15.5 % standing, 37.8 % lying, 6.7 % walking and less than 3 % for all other activities (Fig.). The two social behaviour patterns “agonistic” and “sexual” took up only 0.3 % each of the daytime activity of the “average waterbuck”. Lying head down also was a comparatively rare behaviour, taking only a few minutes at a time, as ıs typical for large bovids (BALcH 1955).

The Figure shows the distribution of the major (most time consuming) activities throughout the day. There was amorning and an evening peak of the activities grazing and walking and a corresponding midday peak of lying. Solar radiation at Nakuru reaches a maximum at about 13-14 h (VArEscH1 1982, Fig. 3a), i.e. the time when the anımals spent the highest proportions lying head up (48 %) and lying head down (2.4 %).

The distribution pattern of the activities throughout the course of a day as shown in the Figure was essentially the same for all classes of waterbuck. In the following, we therefore compare only the daily means of animals of different age, sex, and socıal status.

Time budgets of Waterbuck 51

2.8% others

6.7% walking

1.5% Iying head down

Q,

3

36.3% Iying ead up

RN : RN RI

% of time &

15.5% standing «0 | »0- 20 35.9% grazing 10 0) 1.1 % browsing

TO SO 121312 1572168.172210019 time of day mean

Fig. 1. Distribution of activities of the “average waterbuck” through the course of a day and daily means of the different activities. See text for numbers of observations per hour

Sex differences Adult male - adult female

Adult males and adult females differed markedly in their time budgets (Table 1). Whereas adult males spent 26.8 percent of their time feeding, adult females spent 39.7 percent - almost 1.5 times as long as males (chi-square 877, p < 0.00001). In contrast, adult males spent more time |yıng than adult females (chi-square 464, p < 0.00001). Note that the majority of these adult males are bachelor males and that the time budget of adult males ın general ıs therefore largely determined by the time budget of bachelor males. A compari- son of the time budgets of bachelor males, terrıtory holders, and satellite males ıs given below.

Table 1. Comparison of time budgets (% of observations) of adult males, adult females, and subadult females (7-19 h)

Adult male Adult female Subadult female

Browsing Graszing Standing

Lying head up Lying head down

Walking Running Agonistie Sexual Grooming Others

n observations

32 P. Wirtz and G. Oldekop

Juvenile male - subadult female

For juvenile males, we have insufficient data for the time 18 to 19h. A direct comparison with subadult females is therefore impossible. After truncating the data for subadult females at 18 h, acomparison of juvenile males and subadult females (Table 2) also shows a

Table 2. Comparison of time budgets (% of observations) of subadult females, juvenile males, young males, and adult males (7-18 h)

Subadult female Juvenile male Young male Adult male

Browsing Grazing

Standing

Lying head up Lying head down

Walking Running Agonistic Sexual Grooming Others

n observations

large difference in the time spent feeding: whereas juvenile males spent 28.3 % of their time feeding, subadult females spent 37 % (chi-square 89.6, p < 0.00001). In contrast, juvenile males spent more time standing than did subadult females (chi-square 122, p < 0.00001).

Age differences Adult female - subadult female

Adult females and subadult females closely resembled each other in the times spent for the different activities (Table 1). There were no obvious age differences in their time budgets. Those activities restricted to sexually mature females (e.g. suckling a calf or licking a calf) were recorded in the category “others” and took up less than one percent of the adult females’ time.

Adult male - young male - juvenile male

Young males spent less time lyıng (38.5 %) than adult males (47.7 %) (Table 2, chi-square 262, p < 0.00001). Instead, they stood longer, groomed longer and spent more time in agonistic interactions (chi-square > 36, p < 0.00001 in each case). Feeding time of young males (26.9 %) was slightly higher than that of adult males (24.7 %) (chi-square 19.1, p < 0.0001).

Juvenile males spent even less time lyıng (32.3 %) and more time standing than young males (chi-square > 22, p < 0.00001 ın both cases). They also spent slightly more time feeding than young males, but this difference does not reach the significance level. Juvenile males spent approximately the same amount of time for agonistic behaviour as did adult males (chi-square 0.6), ı.e. much less than young males (chi-square 14.1, p < 0.0002).

Thus, with increasing age, males tended to spend less time standing and feeding and more time |ying; time spent for agonistic interactions was highest for young males.

Time budgets of Waterbuck 53

Social status Territory holder - Satellite male — Bachelor male

Table 3 compares the time budgets of territory holders, satellite males and bachelor males. As there were insufficient data for bachelor males from 7 to 8 h and from 18 to 19 h, the data for the other two classes were also reduced to the time span 8 to 18h.

Table 3. Comparison of time budgets (% of observations) of territory holders, satellite males, bachelor males, and adult females (8-18 h)

Territory holder Satellite Bachelor Adult female inside territory

Browsing 0.4 Grazing 2821 Standing 14.4 Lying head up 339 Lying head down

Walking Running Agonistic Sexual Grooming Others

n observations

Territory holders and satellite males spent the same amounts of time feeding (28.5 % and 28.6 %); in contrast, bachelor males spent much less of their time feeding (19.7 %; chi-square > 88, p < 0.00001 for both comparisons).

Bachelor males spent more than half (51.7 %) of their daytime hours lyıng head up or head down. Satellite males and territory holders spent much less time for this type of activity (38 % and 41.9 %; chi-square > 89, p < 0.00001 in both cases). Compared to territory holders, satellite males stood longer (chi-square 12.4, p < 0.0004) but spent less time lying; however, the latter difference does not reach the predetermined significance level (chi-square 7.7, p < 0.005).

Bachelor males spent more time grooming themselves than did satellite males (chıi- square 32, p < 0.00001), which in turn spent more time grooming themselves than did territory holders (chi-square 43.5, p < 0.00001).

Whereas territory holders spent 5.1 % of their time for sexual behaviour, bachelor males spent only a tenth of this time on sexual behaviour (chi-square 354.8, p < 0.00001). Satellite males spent less time on sexual behaviour than territory holders, but spent considerably more time on sexual behaviour than did bachelor males (chi-square 13.9, p < 0.0002 for comparison with territory holders, chi-square 130.1, p < 0.00001 for compari- son with bachelor males).

Territory holders with and without Satellite males

Table 4 compares the time budgets of territory holders when a satellite male was present and of terrıtory holders in the absence of a satellite male. Because of insufficient data for the time period of 18 to 19h in one of the classes, both data sets are truncated at 18 h. Territory holders without satellite males spent more time grazing, less time lying and more time for sexual activities but none of these differences reached the predetermined level of significance (6.95 > chi-square > 6.30, 0.02 > p > 0.005).

54 P. Wirtz and G. Oldekop

Table 4. Comparison of time budgets (% of observations) of territory holders with satellites and territory holders without satellites and of adult females inside territories and adult females outside territories

Territory holder Territory holder Adult female Adult female with satellite without satellite inside territory outside territory (7-18 h) (7-18 h) (8-12, 14-16, 17-18 h) (8-12, 14-16, 17-18 h)

Browsing Grazing Standing Lying head up Lying head down Walking Running Agonistic Sexual Grooming Others

n observations

Adult females inside territories and outside territories

During the day, most females were inside territories. Even though adult females were the largest class in the population (31 % of the waterbuck seen during monthly road strip counts were adult females, Wırrz and KAıser 1988), there were insufficient data for the time budgets of adult females outside territories for five of the twelve daytime hours. A comparison between adult females inside territories and adult females outside territories (Table 4) can therefore only be made for the following fragments of a day: 8-12, 14-16, and 17-18 h.

When inside territories, adult females spent much more time grazing (41.1 %) than when outside territories (27.6 %) chi-square = 112, p < 0.00001). Outside the territories, adult females spent more time browsing (chi-square = 13.8, p < 0.0002) and grooming themselves (chi-square 323, p < 0.00001) than inside territories.

Sex differences revisited : adult females - adult males, inside territories

The time budgets of adult females and of adult males were compared in a previous section. However, the two data sets differ not only in the sex of the animals but also in the location where they were taken: the majority of the data for adult males are of bachelor males (i.e. from outside territories), and the majority of the data for adult females are from females inside territories. To eliminate the bias caused by differences in site of observation, the time budget of adult females inside territories has to be compared with that of adult males inside territories. Table 3 shows the time budget of adult females (between 8 and 18 h) ın comparison with that of territory holders and satellites.

Inside territories, females still spent much more time feeding than dıd males (chi-square > 85 in both comparisons, p < 0.00001). The sex difference in time spent lyıng, however, is no longer significant when considering only anımals inside territories (chi-square 4.6 ın the comparison with territory holders, p < 0.05; chi-square 2.6 in the comparison with satellite males, p < 0.15). Adult females outside territories and inside territories differed conspicuously from adult males in spending almost no time on agonistic and sexual interactions (p < 0.00001 for all comparisons).

Time budgets of Waterbuck 93 Discussion

An understanding of the nutritional physiology of ruminants is essential for the interpreta- tion of their time budgets. The food intake of ruminants ıs limited by the time required to process the food in the rumen. They can ingest food only as fast as they can digest it. Better digestible forage moves faster through the digestive system and thus permits the anımal to take up more of it. Low digestibility of food cannot be compensated for by a greater food intake - on the contrary, food intake is reduced because the time required for processing is longer. Except for highly digestible food (Ammann et al. 1973), the amount of forage ingested and the time spent feeding are positively correlated with the quality of the forage (BLAXTER 1962; THORNTON and Mınson 1972; ARNOLD 1985). Waterbuck are “grass and roughage eaters” taking food of comparatively low digestibility requiring relatively long processing times (HoFMAnnN 1973).

The social structure of Lake Nakuru waterbuck

Inside territories, females spent more time feeding than outside territories. This indicates better quality of the forage conditions inside territories. Females are free to move between these areas and the observation that female density is higher inside than outside territories (WIRTZ 1982) suggests that territories are superior feeding sites. However, there could also be alternative and additional reasons for the female preference for territories (e.g. more frequent harassment by bachelor males outside territories). Adult males show sımilar site differences in feeding times: bachelor males spent less time feeding than territory holders and their satellite males. Waterbuck territories usually border on water and, to the human observer, the grass outside territories often appeared to be higher and dryer. Dry grass usually has a higher proportion of lignin and thus a lower digestibility (cf SIncLAIR 1975), which would cause longer processing times and lower rates of uptake.

Protein content ıs generally acknowledged as a major determinant of nutritive value of forage for ruminants (SINCLAIR 1975; FEsTA-BIANCHET 1988 and references therein). Faecal crude protein content is closely correlated with dietary protein and has been used to assess forage quality in studies of domestic cattle (BREDoN et al. 1963) and wild ungulates (see references in FESTA-BIANCHET 1988). In a Rhodesian population of waterbuck, the faeces of territory holders and of adult females had a higher crude protein content than the faeces of bachelor males (TomLınson 1979). This Rhodesian population of waterbuck had the same social structure as Nakuru waterbuck suggesting that TomLinson’s (1979) results would also apply to Nakuru waterbuck. Site-dependent differences ın faecal crude protein of males, site preference of females, site-dependent foraging times of females, and site- dependent foraging times of males all suggest that territories are high quality feeding areas. Bachelor males, being excluded from territories, are probably relegated to inferior feeding areas.

The spatial distribution of resources determines the distribution of receptive females, which in turn determines the distribution of males and hence the nature of the mating system (see EMLEn and OrınG 1977 for a general discussion and classification of social systems, and GEısT 1974 for the relationship of ecology and social evolution of ungulates in particular). Territory holders defend high quality feeding sites preferred by females and mate with the females coming to these areas. In the terminology of EmLEn and ORING (1977), the mating system of waterbuck is a “resource defence polygyny”. (Unfortunately, in their influential paper on the evolution of mating systems, EMLEN and Orıng [1977], erroneously refer to waterbuck as an example of “female defence polygyny”.)

In contrast to females (see below), the fitness of males of a polygynous species, such as waterbuck, is probably determined by non-foraging activities, in particular efforts to acquire females. Because comparatively little time is spent in aggressive encounters, the sex

56 P. Wirtz and G. Oldekop

difference in aggressive behaviour, likely to be very important in terms of energy and mortality risk, is only weakly expressed in the time budgets. Territory ownership did not cause a reduction in feeding time. On the contrary, territory owners spent more time feeding, on more nutritious food, than did bachelor males. The costs of territoriality are only weekly expressed in the time budgets by slightly higher percentages of walking and running. The differences ın energy budget and risk are probably more important.

Sex differences

Even when feeding at the same site and presumably on forage of the same nutritional value, females spent much more time on energy intake than males - a difference already apparent in subadult anımals. With increasing age of males (from juvenile male via young male to adult male), this sex difference in maintenance behaviour became more and more pro- nounced. SPINAGE (1968) observed the activity of three individually known adult female waterbuck and two individually known adult males (one of them a territory holder) in the Queen Elizabeth Park, Uganda, for continuous periods of up to three consecutive days. The absolute values of his data are not directly comparable with those of the present study, because an anımal walking a few steps from one grazing site to another was recorded as “walking“ at Nakuru but recorded as “grazing” by SPinAGE. Nevertheless, SPInAGE’s data sımilarly show sex-specific differences in maintenance behaviour: the three females spent more time feeding than the two males.

Female waterbuck are probably “energy maximisers” in the terminology of SCHOENER (1971), 1.e. their fitness is determined mainly by the amount of energy acquired. That females spend more time feeding than males is a general finding for all ungulates studied (cf review by BunnELL and GILLINGHAM 1985) and also for several other anımal species (e.g. Horrman 1983). This difference is probably a fundamental behavioural and physiological difference between the sexes, rather than an epiphenomenon of other factors such as differences in bite sıze. JEWELL (1986) showed that in a feral population of sheep at St. Kilda Island, Scotland, rams spent much less time grazing than ewes. Interestingly, castrated males spent almost as much time grazing (71 %) as females. The likely basıs for these differences lies in low testosterone levels of castrated males and the accompanying shift to a female type of maintenance behaviour. The proximate cause for the sex difference not only in aggressive and sexual behaviour but also in maintenance behaviour of ruminants could thus be a difference in levels of sexual hormones.

Acknowledgements

During most of the activity recordings, ANDREW BARTON worked with P. WIRTZ as a voluntary field assistant at Lake Nakuru National Park; he collected part of the data. The Government of the Republic of Kenya granted research permit OP 13/7C245/4. Prof. Dr. W. WICKLER and the Max- Planck-Gesellschaft financed the study. BARBARA KNAUER converted several hundred data sheets into computer files. Profs. V. GEisT and R. R. HOFMANN commented on an early draft of the manuscript. Many thanks to all of them.

Zusammenfassung

Zeitbudgets bei Wasserböcken (Kobus ellipsiprymnus) von unterschiedlichem Alter, Geschlecht und Sozialstatus

Im Nakuru Nationalpark, Kenia, wurde gemessen, wie sich Wasserböcke von unterschiedlichem Alter, Geschlecht und Sozialstatus die Tageszeit einteilten. Weibchen verbrachten mehr Zeit mit Fressen als Männchen und innerhalb von Territorien mehr als außerhalb. Bei jungen Männchen war der Anteil Zeit für kämpferische Interaktionen am höchsten. Satellitenmännchen verbrachten zwar weniger Zeit mit sexuellen Aktivitäten als Territoriumsbesitzer, aber mehr als Junggesellenmännchen. Territoriumsbesitzer und Satellitenmännchen wendeten gleich viel Zeit für Fressen auf — wesentlich mehr als Junggesellenmännchen. Da bei Widerkäuern Nahrungsqualität und Nahrungsaufnahme negativ korrelieren, deutet dies an, daß die Junggesellenmännchen in Gebiete schlechterer Furterquali-

Time budgets of Waterbuck >,

tät abgedrängt wurden. Sowohl die Zeitbudgets von Männchen und Weibchen, als auch die Ortsbe- vorzugung der fressenden Weibchen und der Proteingehalt von Kotproben (Tomrınson 1979) deuten an, daß Wasserbock-Territorien Orte hoher Futterqualität sind, und daf das Sozialsystem von Wasserböcken als Fortpflanzungsterritorialität bezeichnet werden kann.

Geschlechtsunterschiede im Zeitaufwand für Nahrungserwerb reflektieren wahrscheinlich funda- mentale Unterschiede im Verhaltensprogramm von Männchen und Weibchen: bei polygynen Arten sind Weibchen wahrscheinlicher “Energiemaximierer” als Männchen. Neuere Untersuchungen deuten an, daß unterschiedliche Niveaus von Sexualhormonen der proximale Grund nicht nur von Geschlechtsunterschieden im Sexualverhalten und im kämpferischen Verhalten sind, sondern auch der proximale Grund von Geschlechtsunterschieden im Ernährungsverhalten.

Literature

ALTMan, J. (1974): Observational study of behavior: Sampling methods. Behaviour 49, 227-267.

AMMAann, A. P.; Cowan, R. L.; MOTHERSHEAD, C. L.; BAUMGARDT, B. R. (1973): Dry matter and energy intake in relation to digestibility in white-tailed deer. J. Wildl. Manage. 37, 195-201.

ARNOLD, G. W. (1985): Regulation of forage intake. In: Bioenergetics of wild hervibores. Ed. by R.]. Hupson and R. G. WHITE, Boca Raton: CRC Press. pp. 81-101.

BAccH, C. C. (1955): Slerep ın ruminants. Nature 175, 940-941.

BLAXTER, K. L. (1962): The energy metabolism of ruminants. London: Hutchinson.

BREDoON, R. M.; HARKER, K. W.; MarRsHALL, B. (1963): The nutritive value of grasses grown ın Uganda when fed to Zebu cattle. J. Agr. Sci. 61, 101-104.

BunnELL, F. L.; GILLINGHAM, M. P. (1985): Foraging behaviour: the dynamics of dining out. In: Bioenergetics of wild herbivores. Ed. by R. J. Hupson and R. G. WHrtE. Boca Raton: CRC Press. pp. 53-79.

CLUTTON-BRocK, T. H.; Guingss, F. E.; ALson, $. D. (1982): Red Deer. Behavior and ecology of two sexes. Edinburgh: University Press.

Dossr, J.; DANDELOT, P. (1970): A field guide to the larger mammals of Africa. London: Collins.

EmLen, S. T.; Orınc, L. W. (1977): Ecology, sexual selection and the evolution of mating systems. Science 197, 215-223.

Festa-BIancHET, M. (1988): Seasonal range selection in bighorn sheep: conflicts between forage quality, forage quantity, and predator avoidance. Oecologıa 75, 580-586.

Geist, V. (1974): On the relationship of social evolution and ecology in ungulates. Amer. Zool. 14, 205-220.

HALTENORTH, T.; DILLER, H. (1977): Säugetiere Afrıkas und Madagaskars. München: BLV Ver- lagsges.

en K. W.; TavyLor, J. L.; RorLınson, D. H. L. (1954): Studies on the habits of zebu cattle. 1. Preliminary observations on grazing habits. J. Agr. Sci. 44, 193-198.

Horrman, $. G. (1983): Sex-related foraging behavior in sequentially hermaphroditic hogfishes (Bodianus spp.). Ecology 64, 798-808.

HOFMANN, R. R. (1973): The Ruminant Stomach. Nairobi: East African Literature Bureau.

JEwELL, P. (1986): Survival in a feral population of primitive sheep on St. Kilda, Outer Hebrides, Scotland. Nat. Geogr. Research 2, 402-406.

KUTILEK, M. J. (1975): Feeding strategies and foraging impact of non-migratory African antelope. Ph. D. thesis, Michigan State University.

MARTIN, P.; BATEson, P. (1986): Measuring behaviour. Cambridge: University Press.

OWEN-SMITH, N. (1984): Spatial and temporal components of the mating systems of kudu bulls and red deer stags. Anim. Behav. 32, 321-332.

Rorınson, D. H. I.; HARKER, K. W.; TAYLoR, ]. J.; LEECH, F. B. (1956): Studies on the habits of zebu cattle. IV. Errors associated with the recording technique. J. Agr. Sci. 47, 1-5.

SCHOENER, T. W. (1971): Theory of feeding strategies. Ann. Rev. Ecol. Syst. 11, 369-404.

SINCLAIR, A.R. E. (1975): The resource limitation of trophic levels in tropical grassland ecosystems. J. Anım. Ecol. 44, 497-520.

SPINAGE, C. A. (1968): A quantitative study of the daily activity of the Uganda Defassa Waterbuck. E. Afr. Wildl. J. 6, 89-93.

THOoRNTonN, R. F.; Mınson, D. J. (1972): The relationship between voluntary intake and mean apparent retention time ın the rumen. Aust. ]J. agric. Res. 23, 871-877.

Tomuinson, D. N. $S. (1979): The feeding behaviour of waterbuck in the Lake McIlwaine Game Enclosure. Rhod. Scı. News 13, 11-14.

— (1980): Aspects of the expressive behaviour of the waterbuck Kobus ellipsiprymnus ellipsiprymnus in a Rhodesian game park. $. Afr. J. Zool. 15, 138-145.

TRIVERS, R. L. (1972): Parental investment and sexual selection. In: Sexual selection and the descent of man. Ed. by B. Camper. Chicago: Aldine. pp. 136-179.

58 P. Wirtz and G. Oldekop

VARESCHI, E. (1982): The ecology of Lake Nakuru (Kenya). III. Abiotic factors and primary production. Oecologia 55, 81-101.

WALTHER, F. (1958): Zum Kampf- und Paarungsverhalten einiger Antilopen. Z. Tierpsychol. 15, 340-380.

WırTz, P. (1981): Territorial defence and territory take-over by satellite males in the waterbuck Kobus ellipsiprymnus (Bovidae). Behav. Ecol. Sociobiol. 8, 161-162.

— (1982): Territory holders, satellite males, and bachelor males in a high density population of waterbuck (Kobus ellipsiprymnus) and their associations with conspecifics. Z. Tierpsychol. 58, 277-300.

WırTz, P.; KAISER, P. (1988): Sex differences and seasonal variation in habitat choice in a high density population of Waterbuck (Kobus ellipsiprymnus). Z. Säugetierkunde 53, 162-169.

Authors’ address: Dr. PETER WIRTZ, Zoologisches Institut, Albertstr. 21a, W-7800 Freiburg, FRG

Z. Säugetierkunde 56 (1991) 59-63 © 1991 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-3468

ZISSENSICTENIETPLETIEFKUNRZINDIEEEEIEIN.G

Some remarks on size differences of northwest German game populations from Nebolithic to modern times

By D. HEINRICH

Institut für Haustierkunde, Universität Kiel, FRG

Receipt of Ms. 20.7. 1990 Acceptance of Ms. 20.9. 1990

Starting-point of this consideration is the bone material from medieval Schleswig, excava- tion Schild (Vocer 1983). For a certain period during the Middle Ages Schleswig, sıtuated in the northern part of Schleswig-Holstein (Fig. 1), was one of the most important trade centres in Europe, i.e., from the 11°" century after the decline of nearby Haithabu until the middle of the 13'® century when Lübeck, situated 100 km southeastwards and finally the capıtal of the Hanseatic League, succeeded in its place (HoFFMmann 1981).

At the excavation sıte nearly 112000 bones of mammals were found. Only 1350 of these bones, which ıs a small fraction of 1.2 %, were from wild mammals, the rest from domestic ones (HÜSTER 1990). This is typical for medieval sites (REICHSTEIN et al. 1980). According to the relative frequencies of the remains the most important game were the artiodactyl species red deer (n = 397), roe deer (n = 323) and wıld boar (n = 82), and further the brown hare (n = 312) and red fox (n = 97). Although the amount of bone material of

Denmark No

JO Schleswig RN

(} Haithabu

Scharstorf® Bischofswarder ®

Lübeck®

en

Hitzacker

Fig. 1. Schleswig-Holstein. Location of the medieval trade centres Haithabu, Schleswig, and Lübeck as well as some other medieval settlements

U.S. Copyright Clearance Center Code Statement: 0044-3468/91/5601-0059 $ 02.50/0

60 D. Heinrich

these species is hardly satistactory, ıt was the basıs for size analyses, and was compared with corresponding bones not only from other early historic and prehistoric sites, but also with recent skeletal material (collection of Institut für Haustierkunde, University of Kiel).

In roe deer and in wild boar no sıze differences are apparent between the Schleswig material and that of other medieval or neolithic sites. However, compared with recent skeletons from Schleswig-Holstein it is obvious that roe deer and wild boar today are significantly smaller than the individuals of these species identified for medieval Schleswig and for the other sites. In roe deer this is shown by the measurements ‘maximum length’ of radıus and metacarpus and ‘distal width’ of metacarpus (Fig. 2).

This tendency - evident differences in size between pre- or early historic findings and recent skeletal material - ıs also true for red deer (Fig. 3). In any case the recent material is relatively small-sızed and corresponding differences in body size can be deduced. But the comparison of the Schleswig material with other subfossil bones has shown that red deer of the early medieval strongholds Scharstorf and Bischofswarder, situated in eastern Hol- stein, partly must have been even larger. This is shown by the measurement ‘maximum length’ of calcaneus, whereas similar differences cannot be established in phalanx 1, the second skeletal element analysed.

RADIUS, maximum length (GL)

MIDDLE AGES Schleswig —— 10 RECENT Northern Germany + —— 35

150 158 166 174 182 190 mm

METACARPUS, maximum length (GL)

MIDDLE AGES Schleswig —— 16 RECENT Northern Germany + + — 38

140 148 156 164 172 180 mm

METACARPUS, distal width (Bd)

MIDDLE AGES Schleswig — 18

3 settlements —— 11 NEOLITHIC 2 settlements — En — 6 RECENT Northern Germany + + —— 38

17 19 21 23 25 mm kin — u — 11x -SE +SE

x

Fig.2. Roe deer, Capreolus capreolus. Comparison of size between finds from Schleswig, varıous northwest German sites (Middle Ages: Haithabu — REICHSTEIN 1990; Lübeck Königstraße — PauL 1980; Hitzacker - WALCHER 1978; Neolithic: Hüde I- HüBner et al. 1988; Rosenhof — Nogıs 1975) and recent material; + 24 22,11 8&d; ++25 292,13 dd

Size differences of game populations from Neolithic to modern times 61

PHALANX 1, maximum length of the peripheral half (GLpe)

MIDDLE AGES Schleswig — 19 Hitzacker — 46 Scharstorf — ln 37 Bischofswarder —— 29 NEOLITHIC 5 settlements ern og 15 RECENT Schleswig- Holstein + —— 88

48 52 56 60 64 68 mm

CALCANEUS, maximum length (GL)

MIDDLE AGES Schleswig — a — 14 Hitzacker ——— en — — 14 Scharstorf — — 19 Bischofswarder ze 18 NEOLITHIC 5 settlements —— arm 11 RECENT Schleswig- Holstein** ——l —— 21

——— nd nn nn ann Insben Iuper Er a en en [er FE Era] Tram ST ER ln RN TEE Er NN) TREE Fler TERRA EEN 104 110 116 122 128 134 mm

Fig.3. Red deer, Cervus elaphus. Comparison of size between finds from Schleswig, various northwest German sites (Hitzacker - WALCHER 1978; Scharstorf -— HEınRıcH 1985; Bischofswarder — REICHSTEIN et al. 1980; Neolithic: Hüde I- HÜBnER et al. 1988; Bistoft - JoHmansson 1979; Süssau — Nosıs 1971; Rosenhof - Nosıs 1975, Stinthorst - GEHL 1976) and recent material; +7 292,4 dd; ++6 2 2,4 8d,1 sex?

Corresponding analyses of brown hare and red fox dıd not yıeld such results. In the case of hare only very few measurements showed significant sıze differences, but always without a clear tendency. In the case of the fox sıze differences were found only in the mandibula, which is larger in recent specimens compared with those from Schleswig. In the analysıs of the large amount of material of red fox from Haithabu REIcHsTEIN (1990) obtained similar results.

The clear dissimilarities that could be shown especially in red deer, roe deer and wild boar, concern only size but apparently not shape. Shape differences between single bones would point to dissimilarıties of the stature of animals. But when correlating two measurements of phalanx 1 anterior of the red deer by regression methods these bones of all populations converged to one straight line, which describes the allometrical relationship of the two measurements taken (RöHrs 1959). Looking at roe deer, however, no correlations at all could be found. This points to a large varıability ın this species. Such methods could not be employed in the analysıs of wild boar, because the quality of the material was too poor.

This size reduction ın the artiodactyl species must be a modern phenomenon for one cannot see similar differences between the samples of the various early historic or prehistoric sites. This means that from neolithic to medieval times there were no changes

62 D. Heinrich

which could bring about diminution or enlargement. Thus, it can be noted that the degree ot climatıc influences in the course of this long period was too low to alter the size of the species in the sense of Bergmann’s rule (climate-size-rule). Corresponding results espe- cıially for red deer and roe deer have been repeatedly shown, for instance by BoEssNEcK (1956), REQUATE (1956), REICHSTEIN (1974), and KRATOCHViL (1988).

This phenomenon - no alterations in size over a long period followed by a sudden diminution in the recent past - can be explained by human influence on landscape and vegetation. Although man has modified the landscape by agrıcultural activities since centuries — e.g. especially the medieval clearıng of woodland for cultivation — the alterations caused by human activities are becoming more extensive and frequent especially in the last few decades. Here, one must not only see the modern cultivation, but also the development of settlements and the progress of traffic. Further, one must note that modern forestry is not suitable tor game. The same is true for modern hunting with its demand for trophies. Whereas these factors are essentially responsible for the diminution in red deer and probably also in wıld boar, the relatively small size of roe deer, however, presumably ıs only indirectly connected with them: According to KLEIN and STRANDGAARD (1972) in this species size ıs correlated with population density to a high degree, which in return is dependent on landscape and vegetation, cover, food value etc. The above-mentioned varıability of roe deer in shape must also be seen in this context (SÄGESSER 1966). All in all the transformation of the natural landscape to a cultural one with all of its implications can be considered the main cause for dıminution of these species, which are vegetarian or partly so (Sus scrofa) and which are more or less confined to the woods. It cannot be decided, whether this recent sıze reduction is a result of mutations or — until now — only expression of a modification caused by the bad conditions of life tor these species. However, it is obvious that a phylogenetic tendency of dıminution like that supposed by VON LEHMANN (1960) ın the case of roe deer after considering a far longer period cannot be the explanation for the present results, as the described size reduction ıs a modern event.

Hare and fox are not affected in this way. These species require quite different living conditions. Originally the hare is a mammal of the steppe. Thus, the development of the cultural landscape with fields and pastures instead of woodland improved its ecological basıs, although some other living conditions were worsened. Therefore ıt ıs understandable that one cannot observe a clear trend of diminution. But one should also bear in mind, for instance, that the recent population from Schleswig-Holstein is not a truly autochthonous one: In the beginning of this century hares from many areas, especially from southeast Europe, were released here (MoHR 1931). The fox ıs a carnıvore and for this reason ıs only indirectly dependent on vegetation or landscape like the other anımals. Moreover it has a good ecological adaptabilıry.

Acknowledgements

I am much indebted to Mr. CHR. FREITAG for checking the English manuscript. The studies were supported by the Deutsche Forschungsgemeinschaft.

References

BoESsSNECK, J. (1956): Zur Größe des mitteleuropäischen Rehes (Capreolus capreolus L.) ın alluvial- vorgeschichtlicher und früher historischer Zeit. Z. Säugetierkunde 21, 121-131.

GEHL, O. (1976): Die steinzeitliche Siedlung Stinthorst bei Waren/Müritz ım Spiegel des Säugetier- fundgutes. Bodendenkmalpflege in Mecklenburg, Jahrbuch 1975, 39-53.

HEINRICH, D. (1985): Scharstorf, eine slawische Burg in Ostholstein. Haustierhaltung und Jagd. Offa-Bücher 59. Neumünster: Wachholtz.

Horrmann, E. (1981): Schleswig und Lübeck im 12. und 13. Jahrhundert. Beitr. Schleswiger Stadtgeschichte 26, 26-38.

HÜBNER, K.-D.; SauR, R.; REICHSTEIN, H. (1988): Die Säugetierknochen der neolithischen Seeufer- siedlung Hüde I am Dümmer, Landkreis Diepholz, Niedersachsen. Göttinger Schr. z. Vor- u. Frühgeschichte 23, 35-142.

Size differences of game populations from Neolithic to modern times 63

Hüster, H. (1990): Untersuchungen an Skelettresten von Rindern, Schafen, Ziegen und Schweinen aus dem mittelalterlichen Schleswig (Ausgrabung Schild 1971-1975). Ausgrabungen in Schleswig. Berichte und Studien 8. Neumünster: Wachholtz.

JoHansson, F. (1979): Die Knochenfunde von Säugetieren und Vögeln von Bistoft LA 11. In: Socio- ekonomiska strukturer ı tidigt neolitikum och deras förutsättningar. Studier över Bistoft LA 11 - ett boplatsfynd frän Schleswig-Holstein. Hrsg. von L. Jomansson. 98-111. Göteborg.

Kreın, D. R.; STRANDGAARD, H. (1972): Factors affecting growth and body size of roe deer. J. Wildl. Manage. 36, 64-79.

KrarTochviL, Z. (1988): Körpergröße des Rehwildes (Capreolus capreolus L.) ın der Gegenwart und Vergangenheit (tschechisch mit deutscher Zusammenfassung). Folia Venatoria 18, 115-133.

LEHMANN, E. von (1960): Das Problem der Größenabnahme (Deminuations-Tendenz) beim Reh. Z. Jagdwiss. 6, 41-51.

Mon, E. (1931): Die Säugetiere Schleswig-Holsteins. Altona.

Nosıs, G. (1971): Die Tierreste der prähistorischen Siedlung Süssau Kr. Oldenburg (Schleswig- Holstein). Schr. Naturw. Ver. Schlesw.-Holst. 41, 89-99.

— (1975): Zur Fauna des ellerbekzeitlichen Wohnplatzes Rosenhof in Ostholstein I. Schr. Naturw. Ver. Schlesw.-Holst. 45, 5-30.

Paur, A. (1980): Untersuchungen an Tierknochen aus dem mnittelalterlichen Lübeck (Grabung Königstraße 59-63). Lübecker Schr. z. Archäologie u. Kulturgeschichte 2, 5-104.

REICHSTEIN, H. (1974): Ergebnisse und Probleme von Untersuchungen an Wildtieren aus Haithabu (Ausgrabung 1963-1964). Berichte über die Ausgrabungen in Haithabu 7, 103-144. Neumünster: Wachholtz.

— (1990): Die wildlebenden Säugetiere von Haithabu (Ausgrabungen 1966-1969 und 1979-1980). Berichte über die Ausgrabungen in Haithabu 29, Neumünster: Wachholtz (in press).

REICHSTEIN, H.; TAEGE, K.-C.; Vocer, H.-P. (1980): Untersuchungen an Tierknochen von der frühslawischen Wehranlage Bischofswarder am Großen Plöner See (Schleswig-Holstein). In: Bosau. Untersuchungen einer Siedlungskammer in Ostholstein 4. Hrsg. von H. Hınz. Offa- Bücher 42, 9-75. Neumünster: Wachholtz.

REQUATE, H. (1956): Die Jagdtiere in den Nahrungsresten einiger frühgeschichtlicher Siedlungen in Schleswig-Holstein. Schr. Naturw. Ver. Schlesw.-Holst. 28, 21-41.

Rönrs, M. (1959): Neue Ergebnisse und Probleme der Allometrieforschung. Z. wiss. Zool. 162, 1-95.

SÄGESSER, H. (1966): Über den Einfluß des Standortes auf das Gewicht des Rehwildes (Capreolus c. capreolus [Linne 1758]). Z. Jagdwiss. 12, 54-62.

VoceL, V. (1983): Archäologische Stadtkernforschung in Schleswig 1969-1982. Ausgrabungen in Schleswig. Berichte und Studien 1, 9-54. Neumünster: Wachholtz.

WALCHER, H. F. (1978): Die Tierknochenfunde aus den Burgen auf dem Weinberg in Hitzacker/Elbe und in Dannenberg (Mittelalter). II. Die Wiederkäuer. Diss. Univ. München.

Author’s address: Dr. Dirk Heinrich, Institut für Haustierkunde, Universität Kiel, Olshausen- str. 40, W-2300 Kiel, FRG

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Edgar Schallenberger

Charakterisierung von Sekretionsrhythmen der Gonadotropine und Ovarsteroide während des Brunstzyklus, der Gravidität und post partum beim Rind

(Advances in Veterinary Medicine - Fortschritte der Veterinärmedizin, No. 40)

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Ein aktuelles Arbeitsgebiet von Biotechnik und Medizin ist die willkürliche Steuerung und Manipulation von Fortpflanzungsfunktionen. Obwohl bei den landwirtschaftlichen Nutztieren häufig und oft durchaus erfolgreich Fortpflanzungssteuerung durchgeführt wird, sind die endokrinen Abläufe, in die eingegriffen wird, teilweise erst in Ansätzen bekannt. Deshalb wer- den in dieser Arbeit einige Zusammenhänge von Hormonsekretionsrhyth- men beim gesunden adulten Rind während Brunstzyklus, Gravidität und Post-Partum-Phase aufgezeigt, um einen Einblick in wesentliche Grund- prinzipien hierarchisch gegliederter neuroendokriner Regelsysteme zu geben. Viele der exemplarisch beim Rind aufgezeigten Zusammenhänge können zur vergleichenden Interpretation von Befunden bei anderen Spe- zies herangezogen werden. Die Daten sind für Veterinärmediziner, Tierpro- duzenten, Biologen und Endokrinologen gleichermaßen von Interesse.

Aus dem Inhalt:

Allgemeiner Überblick über die Steuerung der Reproduktion beim weiblichen Rind — Das Hypothalamus-Hypophysensystem — Endokrine Signalübertragung — Entwicklung von Versuchstechniken und Meßverfahren zur Erfassung diskonti- nuierlicher Hormonsekretion — Brunst- und Zyklusfeststellungen — Probenent- nahmen und -konservierung — Darstellung diskontinuierlicher Hormonsekretion — Radioimmunologische Hormonbestimmung — Eigene Ergebnisse — Sekretions- muster von Gonadotropinen und Ovarsteroiden während des physiologischen Brunstzyklus — Messungen der Gonadotropine in der V. jugularis bei 5 Minuten Probenintervall — Vergleichende Messungen in der V. cava caudalis und der V. jugularis während der Lutealphase - Vergleichende Messungen in der V. cava caudalis und der V. jugularis während der Vorbrunst- und Brunstphase — Hormon- sekretionsmuster während der Gravidität — Diskussion der eigenen Befunde — Hypophysen- und Gelbkörperfunktion p. p. — Regelkreis wichtiger Fortpflan- zungshormone -— Allgemeine Schlußfolgerung bezüglich der Relevanz der unter- suchten Hormone in Blutproben — Summary.

PAUL Berlin und Hamburg | P/REV

/ol. 56 (2), 65-128, April 1991 ISSN 0044-3468 C21274F

ZEITSCHRIFT FÜR SAUGETIERKUNDE

INTERNATIONAL JOURNAL OF MAMMALIAN BIOLOGY

Organ der Deutschen Gesellschaft für Säugetierkunde

Bruorton, M. R.; Perrin, M. R.: Comparative gut morphometrics of Vervet (Cercopithecus aethiops) and Samango _ (C. mitis erythrarchus) monkeys. — Vergleichend-morphometrische Untersuchungen am Verdauungskanal von

Grünaffen (Cercopithecus aethiops) und Diademaffen (C. mitis) 65 Poglayen-Neuwall, I.; Shively, J. N.: Testicular cycles of the Ringtail, Bassariscus astutus (Carnivora: Procyonidae). I Testicularzyklen des Katzenfretts, Bassariscus astutus (Carnivora: Procyonidae) 72 lade, J. van der: Sexual bimodality in some recent pig populations and application of the findings to the study of

_fossils. - Geschlechtsbimodalität bei einigen rezenten Schweinepopulationen und Anwendung der Befunde für das Studium an Fossilien 81

Ingold, P.; Marbacher, H.: Dominance relationships and competition for resources among chamois Rupicapra

u pra rupicapra in female social groups. — Dominanzbeziehungen und Konkurrenz um Ressourcen in

Gruppen von weiblichen Gemsen (Rupicapra rupicapra rupicapra) 88

Jacobsen, N. H. G.; Newbery, R. E.; de Wet, M. J.; Viljoen, P. C.; Pietersen, E.: A contribution of the ecology of the

Steppe pangolin Manis temminckii in the Transvaal. — Ein Beitrag zur Ökologie des Steppenschuppentieres

_ Manis temminckii in Transvaal 94

\eal, B. R.: Seasonal changes in reproduction and diet of the Bushveld gerbil, Tatera leucogaster (Muridae:

_Rodentia), in Zimbabwe. — Saisonale Schwankungen in der Fortpflanzung und in der Nahrungszusammenset-

"zung beim Bushveld Gerbil Tatera leucogaster (Muridae: Rodentia) in Zimbabwe 101

Jomparatore, Viviana M.; Maceira, N. O.; Busch, Cristina: Habitat relations in Cienomys talarum (Caviomorpha, "Octodontidae) in a natural grassland. — Habitat-Beziehungen von Ctenomys talarum (Caviomorpha, Octodonti-

‚dae) auf natürlichem Grasland 112

Nissenschaftliche Kurzmitteilungen

"alomares, F.: Use of an active badger sett by Egyptian mongooses, Herpestes ichneumon, in Southwest Spain. —

_ Benutzung eines bewohnten Dachsbaus durch Ichneumone, Herpestes ichneumon, in Südwest-Spanien 119

arrette, Cyrille: Fully formed first lower premolars in a White-tailed deer (Odocoileus virginianus Zimmermann,

- 1780). - Vollständig ausgebildete erste untere Prämolaren bei einem Weißwedelhirsch (Odocoileus virginianus Zimmermann, 1780) I pinosa, Maria Beatriz; Vitullo, A. D.; Merani, Maria S.: Chromosomes of the Argentine Andean mouse, Akodon andinus (Cricetidae: Sigmodontinae). - Chromosorgen. der argentinischen Andenmaus Akodon andinus (Criceti-

dae: Sigmodontinae) HSONIa 124 kanntmachung SM Se 126 Ichbesprechungen 127

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Z. Säugetierkunde 56 (1991) 65-71 © 1991 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-3468

Comparative gut morphometrics of Vervet (Cercopithecus aethiops) and Samango (C. mitis erythrarchus) monkeys

By M.R. Bruorton and M.R. PERRIN

Department of Zoology and Entomology, University of Natal, Pietermaritzburg, South Africa

Receipt of Ms. 2. 5. 1990 Acceptance of Ms. 18. 9. 1990

Abstract

A comparative morphometric examination of the gastrointestinal tracts of vervet (Cercopithecus aethiops and samango C. mitis erythrarchus monkeys revealed that samangos possess significantly larger volumes in the hindgut (caecum and colon). The surface area of the main absorptive region of the gastrointestinal tract (the small intestine) was also larger in samangos than in vervets. Samangos include larger amounts of fiıbrous leaf material in their diets than vervets, and the importance of the larger volumes are discussed with reference to the fermentative process required to digest and utilise this foliar component.

Introduction

The structure of the gastrointestinal tract (GIT) ıs faırly homogeneous among different orders of mammals (CHiveErs and Hrapık 1980), and development of different parts of the GIT generally retlect adaptations to different foods. Plant food with a high content of structural carbohydrates can be digested with the help of microbes in either the stomach or the hindgut, where the enzymes produced by the microbes degrade the food and render its chemical constitutents absorbable (LANGER 1988). Among the African primates are examples of both foregut (stomach) and hindgut (caecum and colon) fermenters. The folivorous colobines possess plurilocular, haustrated stomachs, while most of the frugivor- ous/omnivorous cercopithecines possess simple unilocular, glandular stomachs (LANGER 1988), a well-developed caecum and a large and haustrated colon.

The gross morphology and ultrastructure of the GIT of vervet monkeys (Cercopithecus aethiops) and samango monkeys (C. mitis) ıs similar (BRUORTON 1989). Samangos are frugivorous, but include a relatively high proportion of leaves in their diets (Rupran 1978; Corps 1987; Lawes 1990), while vervets are generally regarded as frugivorous/omnivor- ous and consume roughly equal proportions of fruit and anımal (mostly insect) material (Dunsar and Dunsar 1974; KavanacH 1978; Watson 1985). GIT morphology may show considerable varıation even between frugivorous primate species, depending on the amount of insects or leaves included in the primarily fruit diet (CHIvErs and HLanık 1980), and this may include expansion within the tract. This is usually associated with the fermentation process, since the larger the volume, the more fermentation can occur (CHIVERS and Hrapiık 1980).

A comparative examination was initiated to determine whether the volumes of varıous regions of the gastrointestinal tract (and surface area of small intestine) differ significantly between the two primate species. Volumes are indicators of physiological processes, such as microbial digestion, that are important in herbivore nutrition. This comparative examination might therefore assist in providing an explanation of the digestive strategies of the two species, and in determining how samangos digest the foliar components of their diet.

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66 M. R. Bruorton and M. R. Perrin

Materials and methods

Nine vervet monkeys (4 adult males, 5 adult females) and eight samangos (4 adult males, 4 adult females) were shot on the farm Braco in the Karkloof area of Natal and used in this examination. Animals were weighed in the field and body lengths were measured from tip of nose to tip of tail. Gastrointestinal tracts were removed immediately. These were examined in the laboratory 2-3 hours later, which allowed for complete relaxation of the musculature in the GIT wall. No specimens were fixed prior to measuring, as this can cause distortion of the tract wall.

Measurements of the stomach, small intestine, caecum and colon, completely cleared of all mesenteric tissue, were made in a water-filled 2 mx0.5 mx0.1 m basin. Measuring the length of the gut under water minimises stretching, and is especially important when measuring small intestinal length. Small and large intestines were treated as cylinders and volumes were calculated from mean measurements of length and circumference. Width varıes along the length of intestine, and at least 5 measurements of width (of intact tissue) were taken at regular points along the length. At a calculated mean width the tissue was opened and the circumference was measured. The surface area of the small intestine was also calculated from length and circumference measurements.

To calculate the volume of the caecum, an incision was made dorsally from the ıleocaecal junction to the apex of the caecum. The contents were then flushed out and the lateral walls of the caecum were flattened into an approximate cylindrical shape. The length measurement and average circumference could then be taken and the volume calculated as for the colume of a cylinder.

Accurate measurements of stomach volume were difficult to obtain, largely as a result of its irregular shape and size in different anımals. In most anımals the length of the intact stomach was measured. It was then opened up along the lesser curvature from the gastro-oesophageal opening to the pyloric sphincter, and the incision was extended dorsocranially along the greater curvature for approximately 3 cm (Fig.). The stomach could then be opened out (flattened), the circumference measured and the volume calculated as for the volume of a cylınder.

Two other methods used, a. estimation of stomach volume by filling it with water and b. calculation of stomach volume from the greater curvature measurement (CHIVERS and HrLADIK 1980), were found to be unacceptable and were discontinued. Previous comparative work on primate GIT morphometrics involved use of length and width measurements of intact organs (Jones 1970; MILTON 1981). Preliminary work in this study included this method, but these measurements were found to be unacceptable. Firstly, the varyıng thickness of gut musculature means that simple width measure- ments are mostly inaccurate (often by more than 1 cm). Secondly, the degree of stomach (or intestinal) fill, or the time elapsed since feeding, mean that stomachs of essentially similar size can provide very different measurements depending on when (time of day) they were collected. It is essential that measurements be taken only of dissected sections of the GIT with the contents removed. This negates the effects of varying muscle thickness (because measurements are taken on the mucosal surface of the gut), and is likely to provide more consistent results independent of whether the animal has recently fed or not.

Diagrammatic representation of a stomach, showing the incision made before stomach is opened out (flattened) and measured. P = pyloric sphincter, L = lesser curvature (gastro-oesophageal opening to pyloric sphincter), G = gastro-oesophageal opening, GC = greater curvature (gastro-oesophageal opening to pyloric sphincter)

Comparative gut morphometrics of Vervet and Samango monkeys 67

To compensate for the effect of the larger body size of samangos, volumes of regions of the GIT in each animal were divided by the metabolic live mass (mass°°”) of that animal. This provides a ratio that enables direct statistical comparison between species of the volumes of specific regions of the gut. Data were analysed using the Mann-Whitney two sample rank testing procedure (ZAr 1974).

Results

Table 1 compares the measurements