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Guide to the microscope analysis of Italianmammals hairs: Insectivora, Rodentia andLagomorphaAnna M. De Marinis a & Paolo Agnelli aa Sezione di Zoologia La Specola , Museo di Storia Naturale dell'Universit diFirenze , via Romana 17, 150125, Firenze, ItalyPublished online: 28 Jan 2009.

To cite this article: Anna M. De Marinis & Paolo Agnelli (1993) Guide to the microscope analysis of Italian mammalshairs: Insectivora, Rodentia and Lagomorpha, Bolletino di zoologia, 60:2, 225-232, DOI: 10.1080/11250009309355815

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Boll. Zool. 60: 225-232 (1993)

Guide to the microscope analysis ofItalian mammals hairs: Insectivora,Rodentia and Lagomorpha

ANNA M. DE MARINISPAOLO AGNELLIMuseo di Storia Naturale dell'Universit di Firenze,Sezione di Zoologia La Specola,via Romana 17, 1-50125 Firenze (Italy)

INTRODUCTION

The microscope analysis of hair can be a valuable aidboth in ecological research on the relationship betweenpredators and their prey, and in environment qualityresearch on the relationship between small mammalfauna and habitat variability.

Much research has been carried out in Europe on themicroscopic analysis of hair (Day, 1966; Dziurdzik, 1973,1978; Vogel & Kpchen, 1978; Keller, 1978, 1980, 1981,1983; Faliu et al., 1980; Debrot et al, 1982; Teerink,1991) but not on such mammal species as Erinaceus con-color, Suncus etruscus, Marmota marmota, Dryomysnitedula and Hystrix cristata. Some of these studiesrequire special techniques and equipment such as ascanning electron microscope and microtome which, inturn, require skilled labour, thus slowing down theanalyses.

The present paper proposes an identification key forItalian insectivores, rodents and lagomorphs. It alsoillustrates a new method of cross-sectioning hair, thus ad-ding a parameter which can be essential in correctly iden-tifying taxon in routine investigations. As a whole thetechniques used in this study can be easily, quickly andeconomically applied without compromising the resultsof the research.

MATERIALS AND METHODS

ABSTRACT

A key is proposed for identifying the hairs of Italian Insectvora,Rodentia and Lagomorpha to the genera and species level usingmicroscope analysis. The criteria used are: general morphology,scale cuticular pattern, cortex structure, medulla type, and shape incross-section. A new method of cross-sectioning hair is illustrated.

KEY WORDS: Hair identification - Insectvora - Rodentia -Lagomorpha.

ACKNOWLEDGEMENTS

The authors wish to thank Dr. R. Brizzi and Dr. C. Calloni (Depart-ment of Animal Biology and Genetics) and Nautilus ltd. of Florencefor their expert technical assistance. The authors are also grateful toDr. M. Poggesi (Florence Natural History Museum, Zoological Sec-tion), Prof. B. Lanza and Prof. M. Vannini (Department of AnimalBiology and Genetics) for their careful critical review of themanuscript. Thanks are also due to L. Lapini (Friuli Natural HistoryMuseum) who kindly supplied specimens of Erinaceus concolor andDryomys nitedula, and to Sarah Whitman (Florence Natural HistoryMuseum, Zoological Section) who corrected the English text.

(Received IS June 1992 - Accepted 15 September 1992)

Hair samples were taken from dry skins or specimens in alcohol inthe mammal collection of the Florence Natural History Museum,Zoological Section, except for those of Erinaceus concolor andDryomys nitedula which came from the Friuli Natural HistoryMuseum. The species examined are listed in Appendix.

The hair sample was drawn from the ventral region in Erinaceuseuropaeus, E. concolor and Hystrix cristata, from the latero-dorsalregion in the remaining species. The spines of the two Italian speciesof Erinaceidae were also examined.

Land mammals are covered with two distinct types of hair: long,pigmented guard hairs (overhairs) and short, less pigmented andmore numerous fine hairs (underhairs). In both guard and fine hairsmay be distinguished a proximal and a distal region. The proximalregion is usually constricted in the fine hairs but not in the guardhairs, and includes the hair root. Only the distal region has thediscriminant characteristics useful to identification. It generallycontains a thickened portion called shield, more pronounced inthe guard hairs, which was used to separate the taxonomiccategories.

Both guard and fine hairs, excluding Chiroptera (Tupinier, 1973),consist of three layers of keratin: cutcula (outermost layer), cortexand medulla (innermost layer).

The features used in this identification key are the following: ex-ternal morphology, cuticular scale pattern, structure of cortex, typesof medulla, and shape in cross-section.

External morphology

The following characteristics were recorded using a hand lens:hair profile (straight, zig-zag, or curved) presence or absence ofshield; presence or absence of constrictions; greater or lesser hairstiffness.

Hair length was measured in millimeters using a calibrated ocularmicrometer.

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Cuticular scale pattern

The cutcula pattern was determined from a cast of the hair sur-face. The cast is easily made as follows (Twigg, 1975): after rinsingthe hairs in ether for a few minutes to remove the natural oils, lay thehairs in a thin film of transparent nail polish on a microscope slide;when the nail polish has dried, peel away the hairs and observe thescale cast under the microscope (from lOOx to 400x).

The complicated nomenclature of the various types of cuticularscale patterns (Chehbar & Martn, 1989; Teerink, 1991) is not usedhere. Some of these patterns are not easily distinguishable from eachother and the chance for confusion is great. In our opinion, exceptfor a few species, such features have little diagnostic value.

Cortex

After rinsing the hairs in ether for a few minutes, the structure ofcortex examined under the microscope was transparent. The cortexallows the identification of shrews guard hairs.

Medulla

The procedure for examining the medulla types, partially accor-ding to Keller (1978), is: after rinsing the hairs in ether for a fewminutes, bleach the hairs by dipping them in a solution of hydrogenperoxide (70%) and ammonia (30%); after rinsing the hairs in waterto remove such solution, lay the hairs on a slide, mount them in anappropriate reagent and observe the medulla types under themicroscope (from lOOx to 400x).

The hydrogen peroxide-ammonia solution bleached the hair in allspecies studied. The degree of bleaching is easily modified bychanging the length of time in the solution. The types of medulla ob-served on the distal part are:- unicellular regular (es. Suncits etruscus, Fig. 9);- unicellular irregular (es. Eliomys quercinus, Fig. 26);- unicellular interrupted (es. Glis glis. Fig. 23);- unicellular vacuolated (es. Erinaceus europaeus, Fig. 2);- multicellular net-shaped (es. Clethrionomys glareolus, Fig. 14);- multicellular column-shaped (es. Lepus europaeus, Fig. 29);- multicellular globe-shaped (es. Hystri.x cristata, Fig. 28).

Cross-section

The hair cross-section can often be of greater diagnostic value thanthe cuticular scale pattern and medulla type.

The method used here allowed cross-sectioning the shieldwithout wasting time on cross-sections of the proximal part, thus op-timizing the data collection and reducing the analysis time in com-parison of traditional techniques (Mathiak, 1938; Day, 1966;Dziurdzik, 1973; Brunner & Coman, 1974; Keller, 1980).

Hair cross-sectioning is done as follows: cut two strips ofPolyurethane (about 60 x 30 x 10 mm) and spread a thin film of vinylglue over one of the surfaces; lay the hairs on this film with theirshields parallel to each other and place the other strip on top; whenthe glue has hardened, cut the polyurethane strips at the level of theshield with a scalpel blade.

The cross-sections examined were classified in the followingcategories, only partially according to Debrot et al. (1982):1. Convex profile- round (es. Arvcola terrestris, Fig. 16);- oval (es. Marmota marmota, Fig. 13).2. Concave profile- one side (es. Microtus arvalis, Fig. 18);- two sides like a dumb-bell (es. Lepus europaeus, Fig. 30);- three sides (es. Apodemus sylvaticus, Fig. 20);- four sides (es. Clethrionomys glareolus, Fig. 15).3. Angular profile- H shaped (es. Sorex araneus, Fig. 4);- square (es. Crocidura leucodon, Fig. 5);- key hole shaped (es. Crocidura leucodon, Fig. 6).

Appendix contains 21 cards summarizing the main features iden-tifying insectivores, rodents and lagomorphs.

RESULTS AND DISCUSSION

Hair profile of Insectvora is distinctly zig-zag withconstriction on each curve. The cuticular scales protudeon one side of the hair proximally to the constriction andon the opposite side distally to that constriction (Fig. 3),except at the constriction immediately preceding theshield, according to a scheme called crossing-over byDay (1966). Insectivore fur can be recognized examiningboth guard hairs and fine hairs. The latter far outnumberguard hairs which are therefore difficult to detect.

Rodentia and Lagomorpha guard hairs do not presentany constrictions and are straight except Glis glis andMuscardinus avellanarais showing slightly curvedguard hairs.

Rodentia fine hairs (with constrictions but with nocrossing-over, except in Sciuridae, Hystricidae and Glisglis which have hairs without constrictions) andLagomorpha fine hairs (with no constrictions) signal onlythe presence/absence of these orders. Such hair samplescannot be processed through the key and do not allowidentification as to family, genus or species. On the con-trary, Rodentia and Lagomorpha guard hairs are the onlyrepresentatives of their respective families, genera andspecies and only such hairs are identified in this keys.

Knowledge of the geographic range of the species inquestion tends to facilitate identification.

InsectvoraThe shrew and mole hairs included in this key have

two or more constrictions with crossing-over. The shrewguard hairs show a distinct spatulate shape with the distalsegment almost twice as long as the adjacent; the finehairs have a distal segment as long as the adjacent orsmaller. Crocidura (Card 3), Sorex and Neomys (Card 2)can be recognized only examining the cortex structure ofguard hairs (Vogel & Kpchen, 1978). Suncus etruscuswas identified to species level (Card 4) due to its smallsize (length < 2 mm). The mole guard and fine hairs havea distal segment as long as the adjacent or longer. Themedulla type of guard and fine hairs allows identifyingthe genus Talpa (Card 5).

The guard hairs of Erinaceidae, which in Italy isrepresented by Erinaceus europaeus and Erinaceus con-color (the latter occurring in Friuli Venezia Giulia only),have no constrictions, are stiff and not spatulated. Suchfeatures are completely atypical for insectivores. Acharacteristic medulla type (Fig. 2) with a row of bigroundish cells enclosed by a thick cortex wall, facilitatedidentification to the genus Erinaceus. We attempted toidentify the two species by examining the spines butthese show the same cuticular scale pattern, medulla typeand cross section (Card 1).

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HAIRS OF INSECTVORA, RODENTIA AND LAGOMORPHA 227

2 ;

. 5

8

Figs 1-10 - 1 - Erinaceus europaeus. Spine cross-section. x83. 2 - Erinaceus europaeus. Hair medulla. x4l6. 3 - Neomysfodiens. Crossing-overof cuticular scales (arrows). x4l6. 4 - Sorex araneus. Cross-section. x4l6. 5-6 - Crocidura leucodon. Cross-section. x4l6. 7 - Sorex araneus.Cortex. xl664. 8 - Crocidura leucodon. Cortex. xl664. 9 - Suncus etruscus. Medulla. x4l6. 10 - Talpa europaea. Medulla. x4l6.

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13

14 15

17

18

22 20

Figs 11-22 - 11 - Sciurus vulgaris. Cuticular pattern. x4l6. 12 - Marmota marmota. Cuticular pattern. x4l6. 13 - Marmota marmota. Cross-section. x4l6. 14 - Clethrionomys glareolus. Medulla. x4l6. 15 - Clethrionomys glareolus. Cross-section. x4l6. 16 - Arvcola terrestris. Cross-section. x4l6. 17 - Pitymys savii. Cuticular pattern. x4l6. 18 - Microtus arvalis. Cross-section. x4l6. 19 - Mycromys minutus. Cuticular pat-tern. x4l6. 20 - Apodemus sylvaticus. Cross-section. x4l6. 21 - Rattus rattus. Cuticular pattern. x4l6. 22 - Mus musculus. Cuticular pattern.x4l6.

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HAIRS OF INSECTVORA, RODENTIA AND LAGOMORPHA 229

25

26

27

^

j_y :.ii/ r.i / / / j ~ \ ,

29 30

Figs 23-30 - 23 - Glis glis. Medulla. x4l6. 24 - Muscardinus avellanarius. Cuticular pattern. x4l6. 25 - Muscardinus avellanarius. Medulla.x4l6. 26 - Eliomys quercinus. Medulla. x4l6. 27 - Dryomys nitedula. Cuticular pattern. x4l6. 28 - Hystrix cristata. Medulla. x4l6. 29 - Lepuseuropaeus. Medulla. x4l6. 30 - Lepus europaeus. Cross-section. x4l6.

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RodentiaRodents can be divided into two groups: those with

unicellular medulla and those with multicellular medulla.Among rodents only Gliridae have unicellular medulla.Glis glis and Eliomys quercinus are easily recognized bytheir different medulla (Figs 23-26). Muscardinusavellanarius and Dryomys nitedula have identicalmedulla types (Fig. 25) and their identification is possibleby examining the arrangement of the cuticular scales.The cutcula has a chevron pattern in Muscardinusavellanarius (Fig. 24) and an irregular wave pattern inDryomys nitedula (Fig. 27).

Sciuridae and Arvicolidae show a multicellular net-shaped medulla. The longest hairs (> 15 mm) are found inSciuridae, Arvcola terrestris and Rattus sp. Thecuticular scale pattern on the proximal part of the shieldprovides data for the classification of Sciuridae (Figs11-12). Rats and ground vole are easily recognizedmeasuring hair width.

The shortest hairs (< 12 mm) are found in theremaining rodents. Murinae (Apodemus sp.) and Ar-vicolinae {Microtus sp. and Pitymys sp.) can berecognized to the genus level by examining the cross-section silhouette (Figs 18-20) and cuticular scale pattern(Fig. 17). The identification may proceed to species forthe genera represented in Italy by a single species:Clethrionomys glareolus (Card 8) of Arvicolinae andMicromys minutus (Card 12) and Mus musculus (Card15) of Murinae.

The family Hystricidae is represented in Italy only byHystrix cristata. The unique medullary configuration(multicellular globe-shaped) together with external mor-phology allow to classify such species (Fig. 28). Spinesare not included in the key.

LagotnorphaThe medulla type of lagomorph guard hairs is unique.

The medullary cells are in longitudinal columns with anextremely characteristic pattern (Fig. 29). Lagomorphsare therefore the easiest order to recognize but the guardhairs of the genus Lepus and Oryctolagus cuniculus can-not be reliably distinguished, due to their close similarity(Day, 1966). Reynolds & Aebischer (1991) and Teerink(1991) proposed cross-section and cuticular scale patternas discriminant character. These features are not easilydistinguishable. Identification below the family level istherefore tentative.

KEY TO THE HAIRS OF THE ORDERS:INSECTVORA, RODENTIA AND LAGOMORPHA

la. Hairs with constrictio'ns 2lb. Hairs without constrictions 32a. Hairs with crossing-over of the cuticular scales at

each constrictions (Fig. 3) except the one im-mediately preceding the shield 4

2b. Hairs without crossing-over of the cuticular scalesat each constrictions Fine hairs

of Rodentia (excluding Sciuridae, Hystricidaeand Glis glis). Look for guard hairs (see text).

3a. Hairs bent Fine hairsof Lagomorpha, Hystricidae, Sciuridae andGlis glis. Look for guard hairs (see text).

3b. Hairs not bent 54a. Unicellular regular medulla on the shield (Fig. 9). 64b. Unicellular irregular medulla on the shield

Talpa sp. (Fig. 10)5a. Unicellular medulla on the shield (Fig. 25) 75b. Multicellular medulla on the shield (Fig. 14) 86a. Length > 4 mm 96b. Length < 2 mm Suncus etruscus7a. Unicellular not vacuolated medulla on the shield

(Fig. 25) 107b. Unicellular vacuolated medulla on the shield

.. Erinaceus europaeus as well E. concolor (Fig. 2)8a. Multicellular net-shaped medulla on the shield

(Fig. 14) 118b. Multicellular column-shaped medulla on the shield

Leporidae (Fig. 29)8c. Multicellular globe-shaped medulla on the shield ..

Hystrix cristata (Fig. 28)9a. Cortex of the shield with longitudinal lines sloping

inwards Sorex sp. as well Neomys sp. (Fig. 7)9b. Cortex of the shield without longitudinal lines

(Fig. 8) 1210a. Unicellular regular medulla on the shield

(Fig. 25) 1310b. Unicellular irregular medulla on the shield

Eliomys quercinus (Fig. 26)lia. Length s= 15 mm 14lib. Length

HAIRS OF INSECTVORA, R O D E N T I A AND LAGOMORPHA 231

APPENDIX - Synopsis of Insectvora, Rodentia and Lagomorpha hairs.

Card 1 - Erinaceus europaeus, K concolorSPINES:- Length 17 - 22 mm- "Variolated" cuticular pattern- Multicellular column-shaped medulla outwards and unicellular

vacuolated medulla inwards- Round cross-section with a characteristic pattern (Fig. 1)

HAIRS:- Stiffhairs without shield- Length 20 - 30 mm- Unicellular vacuolated medulla on the shield (Fig. 2)- Round cross-section of the shield

Card 2 - Sorex sp., Neomys sp.- From 4 to 6 constrictions- Crossing-over of cuticular scales (Fig. 3)- Length 4 -10 mm- Unicellular regular medulla on the shield- Cortex of the shield with longitudinal lines sloping inwards (Fig. 7)- "H" shaped cross-section of the shield (Fig. 4)

Card 3 - Crocidura sp.- From 3 to 5 constrictions- Crossing-over of cuticular scales (Fig. 3)-Length 4 - 10 mm- Unicellular regular medulla on the shield- Cortex of the shield without longitudinal lines (Fig. 8)- Square or "key hole" shaped cross-section of the shield (Fig.5-6)

Card 4 - Suncas etrnscus- From 2 to 3 constrictions- Crossing-over of cuticular scales (Fig. 3)- Length < 2 mm- Unicellular regular medulla on the shield (Fig. 9)- "Key hole" shaped cross-section of the shield

Card 5 - Talpa sp.- From 7 to 9 constrictions- Crossing-over of cuticular scales (Fig. 3)-Length 10- 13 mm- Unicellular irregular medulla on the shield (Fig. 10)- Round or oval cross-section of the shield

Card 6 - Sciurus vulgaris-Length 15-20 mm- Streaky chevron cuticular mosaic on the proximal part of the hair (Fig.

11)- Multicellular net-shaped medulla on the shield- Oval or one concave side in shield cross-section

Card 7 - Marmota marmota- Length > 25 mm- Irregular wave cuticular pattern on the proximal part of the hair (Fig. 12)- Multicellular net-shaped medulla on the shield- Oval or one concave side in shield cross-section (Fig. 13)

Card 8 - Clethrionomys glareolus- Length 8-10 mm- Multicellular net-shaped medulla on the shield (Fig. 12)- Four concave sides in shield cross-section (Fig. 13)

Card 9 - Arvcola terrestris-Length 15 - 16mm- Shield width 60 - 70 urn- Diamond petal pattern of cuticular scales on the proximal part of the hair- Multicellular net-shaped medulla on the shield- Round or oval cross-section of the shield (Fig. 16)

Note: the nomenclature is according to Corbet & Hill (1991).

Card 10 - Pitymys sp.- Length 6 - 7 mm- Cuticular scale margins "M" shaped on the concave side of the shield

(Fig. 17)- Multicellular net-shaped medulla on the shield- One concave side in shield cross-section

Card 11 - Microtus sp.- Length 10 -12 mm- Cuticular scale margins "M" shaped on the concave side of the shield- Multicellular net-shaped medulla on the shield- One concave side in shield cross-section (Fig. 18)

Card 12 - Mycromys minutas- Length < 10 mm- Irregular wave cuticular pattern under the shield (Fig. 19)- Multicellular net-shaped medulla on the shield- Round or one concave side in shield cross-section

Card 13 - Apodemos sp.-Length 10- 12 mm- Multicellular net-shaped medulla on the shield- Three concave sides in shield cross-section (Fig. 20)

Card 14 -Rattussp.-Length 15-25mm- Shield width 80 - 1 OOum- Diamond petal cuticular pattern on the proximal part of the hair (Fig. 21 )- Multicellular net-shaped medulla on the shield- Round, oval or one concave side in shield cross-section

Card 15 - Mus msculos-Length 9 - 12mm- Cuticular scale margins "U" shaped on the concave side of the shield (Fig.

22)- Multicellular net-shaped medulla on the shield- One concave side in shield cross-section

C?irA 16-Glisglis-Length 15-20mm- Unicellular interrupted medulla on the shield (Fig. 23)- Oval cross-section of the shield

Card 17 - Muscardinus avellanarius- Length 8-12 mm- Chevron cuticular pattern under the shield (Fig. 24)- Unicellular regular medulla on the shield (Fig. 25)- Round cross-section of the shield

Card 18 - Eliomys quercinus-Length 10- 15 mm- Unicellular irregular medulla on the shield (Fig. 26)- Oval cross-section of the shield

Card 19 - Dryomys nitedula- Length 10 - 15 mm- Irregular wave cuticular pattern under the shield (Fig. 27)- Unicellular regular medulla on the shield- Round or oval cross-section of the shield

Card 20 - Hystrix cristata- Stiffhairs without shield- Length > 50 mm- Multicellular globe-shaped medulla (Fig. 28)

Card 21 - Oryctolagus cuniculus, Lepus sp.- Length 25 - 35 mm- Multicellular column-shaped medulla on the shield (Fig. 29)- One or two concave sides (like a dumb bell) in shield cross section (Fig.

30)

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shield Muscardinus avellanaras (Fig. 24)16b. Irregular wave pattern of cuticular scales

under the shield Dryomys nitedula (Fig. 27)17a. 60-70 urn shield width Arvcola terrestris17b. 80-100 um shield width Rattus sp.18a. Cuticular scale margins M shaped on the

concave side of the shield (Fig. 17) 1918b. Cuticular scale margins U shaped on the concave

side of the shield Mus musculus (Fig. 22)18c. Irregular wave pattern of cuticular scales under the

shield Micromys minutus (Fig. 19)19a. Length 6-7 mm Pitymys sp.19b. Length 10-12 mm Microtus sp.

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