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HARVARD UNIVERSITY 
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Library of the 


Museum of 


Comparative Zoology 


BIOLOGY OF 
NEW WORLD MICROTUS 


SPECIAL PUBLICATIONS 


This series, published by the American Society of Mammalogists, 
has been established for papers of monographic scope concerned 
with some aspect of the biology of mammals. 

Correspondence concerning manuscripts to be submitted for pub- 
lication in the series should be addressed to the Editor for Special 
Publications, Hugh H. Genoways (address below). 

Copies of Special Publications of the Society may be ordered from 
the Secretary-Treasurer, Gordon L. Kirkland, Jr., Vertebrate Mu- 
seum, Shippensburg University, Shippensburg, Pennsylvania 17257. 


Price of this issue $55.00 


COMMITTEE ON SPECIAL 
PUBLICATIONS 


HuGuH H. Genoways, Editor 
Carnegie Museum of Natural History 
5800 Baum Blvd. 
Pittsburgh, Pennsylvania 15206 


TimoTtnuy E. LAWLor, Managing Editor 
Department of Biological Sciences 
Humboldt State University 
Arcata, California 95521 


BIOLOGY OF 
NEW WORLD MICROTUS 


EDITED By 


ROBERT H. TAMARIN 


Department of Biology 
Boston University 
Boston, Masschusetts 02215 


SPECIAL PUBLICATION NO. 8 
THE AMERICAN SOCIETY OF MAMMALOGISTS 
PUBLISHED 12 SEPTEMBER 1985 


iil 


MCZ 
Libsixves. i ¥ 


NOV 20 25 


Library of Congress Catalog Card No. 82-73762 
© 1985 
ISBN No. 0-943612-07-1 


iv 


CONTRIBUTORS 


SYDNEY ANDERSON 


Curator, Department of Mammalogy 

American Museum of Natural 
History 

Central Park West and 79th Street 

New York, New York 10024 


GEORGE O. BATZLI 


Department of Zoology 
University of Illinois 
Urbana, Illinois 61801 


ELMER C. BIRNEY 


Bell Museum of Natural History 
University of Minnesota 
Minneapolis, Minnesota 55455 


Ross E. BYERS 


Winchester Fruit Research 
Laboratory 

Virginia Polytechnic Institute and State 
University 

Winchester, Virginia 22601 


MICHAEL D. CARLETON 


Division of Mammals 

National Museum of Natural History 
Smithsonian Institution 

Washington, D.C. 20560 


ROBERT A. DIETERICH 


Institute of Arctic Biology 
University of Alaska 
Fairbanks, Alaska 99701 


MICHAEL S. GAINES 


Department of Systematics and 
Ecology 

University of Kansas 

Lawrence, Kansas 66045 


LOWELL L. GETZ 


Department of Ecology, Ethology, and 
Evolution 

University of Illinois 

Urbana, Illinois 61801 


ROBERT S. HOFFMANN 


Museum of Natural History 
University of Kansas 
Lawrence, Kansas 66045 


BaRRY L. KELLER 


Department of Biological Sciences 
Idaho State University 
Pocatello, Idaho 83201 


JAMES W. KoEpPL 


Museum of Natural History 
University of Kansas 
Lawrence, Kansas 66045 


CHARLES J. KREBS 


Institute of Animal Resource Ecology 
University of British Columbia 
Vancouver, British Columbia, 


V6T 1W5 Canada 


WILLIAM Z. LIDICKER, JR. 


Museum of Vertebrate Zoology 
University of California 
Berkeley, California 94720 


DALE M. MADISON 
Biology Department 


State University of New York 
Binghamton, New York 13901 


FRANK F. MALLORY 
Biology Department 
Laurentian University 


Sudbury, Ontario, 
P3E 2C6 Canada 


JosEPH H. NADEAU 


The Jackson Laboratory 
Bar Harbor, Maine 04609 


OLIVER P. PEARSON 


Museum of Vertebrate Zoology 
University of California 
Berkeley, California 94720 


CARLETON J. PHILLIPS 


Department of Biology 
Hofstra University 
Hempstead, New York 11550 


ROBERT K. ROSE 


Department of Biological Sciences 
Old Dominion University 
Norfolk, Virginia 23508 


ROBERT W. SEABLOOM 


Department of Biology 
University of North Dakota 
Grand Forks, North Dakota 58201 


Mary J. TAITT 


Institute of Animal Resource Ecology 
University of British Columbia 
Vancouver, British Columbia, 

V6T 1W5 Canada 


vi 


RoBERT M. TIMM 


Field Museum of Natural History 
Roosevelt Road at Lake Shore Drive 
Chicago, Illinois 60605 


JERRY O. WOLFF 


Department of Biology 
University of Virginia 
Charlottesville, Virginia 22901 


BRUCE A. WUNDER 


Department of Zoology and 
Entomology 

Colorado State University 

Fort Collins, Colorado 80523 


RICHARD J. ZAKRZEWSKI 
Sternberg Memorial Museum 


Fort Hays Kansas State College 
Hays, Kansas 67601 


PREFACE AND 
ACKNOWLEDGMENTS 


In 1979, Hugh H. Genoways, Chairman of the Editorial Com- 
mittee of the American Society of Mammalogists, asked me if I 
would be interested in editing a special publication of the society to 
be titled, “Biology of New World Microtus.” Knowing that there 
was an interest in such a volume, and that such a volume could be 
a valuable resource, I was happy to do it. The successful “Biology 
of Peromyscus,” published in 1968 by the society, gave us a model 
from which to work. The expected date of publication was set at 
late 1984. 

There then followed a meeting with the Editorial Committee of 
the Society to establish content and authorship. It was decided that 
the book should be restricted to New World Muicrotus to keep the 
size of the volume to a manageable length. Because we have many 
chapters, there is some repetition and fragmentation, but each sub- 
ject is self-contained and readily available to anyone using the book 
as a reference source. As did John King, editor of the Peromyscus 
volume, I limited my editorial responsibilities to overseeing the 
writing and revising the chapters. I hope that each chapter is an 
up-to-date synthesis of the material in that field, a guideline for 
future research, and a useful reference. Some chapters, such as 
Phillips’ chapter on microanatomy, contain much new information. 

The authors of this book did not take a firm stand on the question 
of Microtus systematics. Anderson, in his chapter on taxonomy and 
systematics, chose to outline the problems and issues in vole tax- 
onomy rather than making premature “definitive” statements. 
Hence, a few authors, such as Zakrzewski, consider Pitymys as a 
valid generic name while most consider it to be a synonym of M:- 
crotus. I think that there is still much to be done in the area of vole 
systematics, but Anderson points us in the right direction. 

Chapters were subjected to anonymous peer review. Although I 
would like to thank individually the many reviewers who put so 
much effort into improving the quality of this volume, I obviously 
cannot and still maintain their anonymity. I thus hope that a gen- 


eral acknowledgment will convey my gratitude. I greatly appreciate 
their efforts. I would also like to thank Hugh H. Genoways and 
Timothy E. Lawlor for the many hours of editorial work that they 
put in after the manuscript for this book left my desk. Lastly, thanks 
to my family, Ginger, David, and Bonnie, for putting up with an 
inordinately long 1983. 


Roe 
16 February, 1984 


vill 


CONTENTS 


THE FOSSIL RECORD Ruchard Ju ZLanr2cwskt ee 1 
PNM S rec Cb soe eer eee Pern ee ee Patent cence noe eee 1 
Introd wctiom ese eee 1 
Systematics and the Fossil Record 5 
@oncluding Remarks sos cesses erecta eee 29 
PCLT OW CGH PENCE S ss a a a acerca aero eee 29 
Selected Bibliognaphy 22 ee 30 
Appendix A. Fossil Faunas Containing Pitymys and Microtus ..... 37 
Appendix B. Localities Containing Pitymys pinetorum, P. ochrogaster, 

amd VMitcrotuse Der reSy CGti CUS cress ere eer eee ee eneeeeeere ee 48 

TAXONOMY AND SYSTEMATICS 52 
ANDS treat ooo sea a aera eae ete 52 
ry terco ch ca cb rn year os eee 58 
Eistory-of Systematics: at the Generic Level 55 
History of Systematics at the Species Level 68 
Discussion of Systematic Viewpoints 0222 74 
Moitenatures Cited ee ee ee 81 

ZOOGEOGRAPHY Robert S. Hoffmann and James W. Koepp. ........ 84 
RS tape Oca ek areata 84 
Introduction 84 
Ecological Zoogeography 85 
Historical Zoogeography 105 
Acknowledgments 113 
Meitenatune® Cited cece re ee bis 

MACROANATOMY 116 
ANS tract eee eek aay cee eee eee geo 116 
Dina tad Ua CO rn ae ete Sete re, ater eesis 117 
Integumcnt 22 118 
Skeleton and External Form 121 
DViuiscurl ature te ge en eee tree ek ta at eee a ee a 136 
Sis tall EO TV SVS ma cage aaa nase A ae 138 
Digestive System ................ 140 
Reproductive System 155 
Discussion ............-.-:::0ssss00 159 
ABUT ACT? CIC Cees ee eee Ba seth Foe el 169 

MICROANATOMY 176 
Abstract 176 
Introduction 177 
Methods 177 
Baier nce ener oat eerie 179 
Anterior Pituitary Gland 179 
TE YC eee ee EEE RE eee ane ep 180 
Tarsal (Meibomian) Gl arnds oie eeeeeeesenneeeeecesennnnneeneeccennnnnennececnnnnnuseneeee 193 
Integumentary Glands 194 
| Ys oT 0) eee ee go soe eyes sie vo Ende eeresne nese 196 


Sallavarjve Gain cl sees eeeeeereereeee 202 


Digestive; Mera ct es se. ee Serer ae ere ee eee oe ee ee 217 
Adrenal Gland sss ee eee 241 
Reproductive Tracts 243 
Acknowledgments ............ 247 
iterate (Cite cere ere eae ee nee 247 
ONTOGENY JOSEP SL, INGO CCU ee cr ae eee eee 254 
Abstract 254 
Introduction 254 
The Prenatal Period 255 
Parturition ee eee 262 
“BhetRostnatal ab eric ee eee 270 
SVT MELL CSS ip came ates A Saas 8 ete ee Se ie 
PS AEH Gg «1 0 geet sent Denne ener DR Ear nee 280 
PACK O Wile rie Tay eres sree ae ee 280 
Piteratures Crit ec yee sere eee ee ee eee 280 


TE tea ba iit ea tig: Ec CS ea eee 
Responses to Habitat Features 220000 
Competitive Exclusion and Habitat Utilization 
Habitat Utilization or [slams occ ceseeeeesseeeeeeeeeeeeesneeeesnneeceeneeseennneeee 
Habitat Configuration and Stability 2.0 
Effects of Human Activities on Microtus Habitats 2200s 302 
Aer cultumall| Ela it cits meee eee eneree cee ee eee ee 304 
Derartersext unre 4 Gi ee cl eee ears ere ee 305 
COMMUNITY ECOLOGY Robert K. Rose and Elmer C. Birney ... 310 
PR DDS Uriel Cae ee Nees an EER nade NA rs eee 310 
Introduction 310 
Communities of Small Mammals with Microtus ........c.cscscsecsssseeesssseeeeeeeeeee 312 
The Influence of Microtus on Communities 2... ccc eeeeeeeceeteeeeee 325 
The Role of Microtus in Small Mammal Communities |... 329 
Conclusions! and! Perspectives 2 eee ccer ee 333 
Acknowledgments 222 2002s. se ee 334 
Teiteraturre Cite ea ea naar re 335 
BEHAVIOR eT OAV Of eee ramen eg 340 
340 
341 
341 
Social Behavior 344 
Literature Cited 366 
ACTIVITY RHYTHMS AND SPACING 373 
Abstract ............... 373 
Introduction .... 374 
Activity Rhythms ........ 374 
SCLIN ae 389 
Generalities and Predictions for Future Testing 22222.2.22.::ccccceccccccccccceseceee 411 
Acknowledgments 
Witeratuce™ Gite ees ee eee re eee ee ee 


DISPERSAL Williaa fam le dick 67am | 1g naeemannenere rere errr eee 420 
Han a Sof 8 2] eee = eee Pape Ae eta eye React PEE SEN 420 
Introduction 2... a 42 


Review of Techniques ............ 422 
A Classification of Dispersal ............ 425 
Characterization of Dispersers w- 427 
Demographic Causes and Consequences 436 
Eivolurtiorvaryy: USS eS cers error see neers 442 
Summary and Conclusions 445 
Meiteraturr es ©: tel eee eneeneeeeeete rete ne eee rete ree eiee reePer eee rese eters eee 448 
455 
455 
456 
457 
472 
478 
481 
482 
484 
503 
Acknowledgments 0.0.0.0... 504 
Literature Cited 2. 504 
Appendix A. Endoparasites 528 
PREDATION Oliver Pm RECT SO 1a aeree aia ater oes eee ee 535 
PANTS C1e ek Cte ices ace ere acres ere ee dere 535 
dra choye AU Yo} w 0) 0 ese Me esse ca eee cea o eng ne Yom Uv Pe EO Cane erUTE oyenc oe 536 
Predation by Birds ......................... 537 
Predation by Mammals 550 
Predation by Fish, Amphibians, and Reptiles 2. 558 
| DD YRS Ss) Vo) o Wess eee eee tener eran feria gr re ote ene bby) 
Conclusions 562 
Literature Cited 563 
POPULATION DYNAMICS AND CYCLES Mary J. Taitt and 
Charles J. Krebs 567 
Abstract 567 
DIOS £0 8 GU Co} a0) lessee eenOeIeS setae terface to eee oe eee rede ere ee 568 
INAfe tht cL Si 0 fi GU hy fees esree etree erences ome eee Ee ee eee 569 
Observed Population Patterms 22.0... 572 
Hypotheses to Explain Population Patterns 588 
MIBSStS0f FAV POtneses: hoirenecpeetre e 593 
Mathematical Model] s 2.0.0.0... eeeeeceeesescccencccncccccccnccccccccceccececeececeeeeeeeeneeeeeeeeeeeeeeeeete 609 
Discussion 610 
Witeratures Cited sotstes oe eer cs RD ee eae 612 
MANAGEMENT AND CONTROL 621 
Alls tra C tj Se 2s ie an SR es SR sols A ep. teen 621 
Introd wet om eee 621 
History of Vole Control in Orchards 623 
Environmental Hazards and Chemical Residues 0c 639 
Concluding Remarks 641 
ME rterertvarce © it el eee a ener eh ee IT a te 642 


LABORATORY MANAGEMENT AND PATHOLOGY Frank 


Po Mallory and Robert A Dictench 647 
TaN EL1 tee are et een een ye 647 
Tnatro ducts Onn oe ee ee 647 
Laboratory Management 652 
| S-Nd 6 (0) (0) 2 657 
ROOD gg a 20 ch geemeence eeepc ned ete near RST PR OO a 676 
Acknowledgments 2.......eccscsssssssssescssscsscccceceeeeeeeseseseessnnsnsnnnsccceeeceeeeeeeensttnsnnssssceneceeeeeeeenesue 676 
Sibert ere Cte sae are ce ee 677 

ENDOCRINOLOGY Robert W. Seabloor wesserssscccccscsssssssesssssvssssssscccessssssessseees 685 
Str Ct pa aa Ne re en eee 685 
Mint reco ea Ct i tee ede re ee ste ee es EO cA ET 686 
Timing of Reproductive Function 686 
Estrus and Ovulation inniccecccecccccccccceeeceeeeeeeeecsssscccceceeeeeeeeeee 693 
Formation and Duration of Corpus Luteum 697 
RGAE a 0 ete es AE ete see et re ore seo oe Rg etn 
Post-partum Events 
Mesticular Activity x25 ee ee ee 
MUBW sy To cd econ corre i ae oh a Seg ead Pen PB, el pecoar 
Adrenal Cortex 222... 

Summary and Conclusions 
Teiterartennee tA 

REPRODUCTIVE PATTERNS Barry ie Keller mee nena nee 125 
Abstract 725 
UG oY ays LOK ot C0) o hema eeeemeareee es re NSNE ES ea SoM Ale ed nace ere RIDES 726 
uengthwotsBreedim eas eas OU ee ee 728 
Breeding Intensity 
MESUGE TS SY ZC eee ese eee ree 
IDISCUSSION (= ee 
Acknowledgments 
Teyateerer unre Cit hse aac ee 

779 
779 
779 
781 
Intake, Forage Quality, and Individual Performance —...222202000 790 
Forage Quality and Population Characteristics 0... 803 
Conclusions 806 
iteratune) Cited eee ee ere eee 806 

ENERGETICS AND THERMOREGULATION Bruce A. 

UATE (C7 pe a i Me BR a ee ee RO ES a ea 812 
Abstract 812 
PERO U CE OTR ee ie Se ice re ee en a 813 
IA Ute 0 Coy (oh eee er Pa RP et einer Ra 815 
PEG yj eA COUNTS 11 Ware eee ee 817 
Emerg cA Cath Ota etc cere cases ne eee sr ee 821 
Energy-Flow Models: Individuals and Populations 22222 837 
Future Studies ovate. ole eee ie el A tet te ene 838 
Wuiterertne Cite css a ee ps 839 


xil 


845 

845 

Delage Color atv ga oeyegece eeee 846 
Cytogenetics 849 
Allozymic Variation ........... 853 
Quantitative Genetics 864 
Relationship between Genetics and Population Regulation .................. 870 
Conclusions 875 
PRGRTIO WEG Sri CIES at ics 878 
ME terra tein: Cite ss cee 878 
| L).() DN OD, ie sence 2 Ne ee ne Ne oY an ee ee eS eae aT 884 


xili 


THE FOSSIL RECORD 
RICHARD J. ZAKRZEWSKI 


Abstract 


EMAINS of fossils assignable to Microtus are known from 241 
R sites in 39 states and provinces in North America. These sites 
range in age from early Pleistocene (Irvingtonian-Aftonian ?) to Ho- 
locene. 

Two groups, based in part on the morphology of the m1, can be 
distinguished: 1) a Pitymys group, wherein the m1 consists of three 
closed triangles; and 2) a Microtus group, wherein the m1 consists 
of four or more closed triangles. 

Pitymys is considered a valid genus. It is represented in the fossil 
record by at least eight extinct species, and two extant species have 
a fossil record. Microtus is represented by two extinct species, and 
10 extant species have a fossil record. 

Both genera probably originated in Asia and migrated across the 
Bering Land Bridge into North America. The first migration ap- 
pears to have taken place about 1.8 m.y.b.p. and is represented by 
primitive species of both genera. Advanced species represent addi- 
tional migrations and/or autochthonous development. 

Both genera had a wider distribution in the past. Ranges of 
various species have retracted, in some cases substantially, since 
mid-Holocene time, probably as a result of climatic change. 


Introduction 


This chapter deals with the fossil record of Microtus in North 
America, fossil record being defined as all Pleistocene and any Ho- 
locene sites wherein any of the recorded taxa are locally extinct. 
Using this definition, I list 241 sites from 39 states and provinces 
in North America (Fig. 1 and Appendix A). Additional Holocene 
records that do not meet this definition can be found in Semken 


Dedicated to the late John E. Guilday. 


1 


2 Zakrzewski 


(in press). The distribution of these sites suggests a sampling bias, 
reflecting both potential deposits and individual interests. 

Although the primary function of this chapter is to update the 
fossil record, I also make some comments regarding systematics. 
The sole basis for the comments is the morphology of the teeth. 
The terminology of the teeth follows, or is modified from, van der 
Meulen (1973) and is shown in Fig. 2. 

I have used a standard format in discussing each taxon. This 
format includes the sites where the taxon is found, the age of the 
sites, characters used to distinguish the taxon, problems in applying 
these criteria, general comments regarding interrelationships, dis- 
tribution, etc. For fossil taxa I have included the type locality and 
the location, number, and nature of the type specimen. 

A number in parentheses follows each site when it is listed under 
a taxon in the text. This number can be used to find the site on the 
distribution maps (Figs. 1, 5, 6, 8), in the appendices, and to refer 
to the pertinent references in the selected bibliography or to per- 
sonal communications listed in the acknowledgments. 

Although Boellstorff (1978) showed that it is no longer reason- 
able to refer to events in the early Pleistocene by the classical gla- 
cial-interglacial terminology, I continue to do so herein (Fig. 3). 
My major rationale is to avoid confusion. Most non-geologists are 
familiar with the terminology and most published records use these 
terms for a time reference. 

In compiling these records I relied on published information (most 
of the citations are primary sources; a few, however, are secondary) 
and the cooperative spirit of a number of colleagues. I examined 
small samples of all the extant taxa and some of the extinct ones. 
I view the results as a “state-of-the-art” statement and as a starting 
point for subsequent work. 

Abbreviations used in text are as follows: 


Institutions 

AMNH—Ame rican Museum of Natural History, New York 

CM Carnegie Museum of Natural History, Pitts- 
burgh 

FGS —Florida Geological Survey, Gainesville 

KU —University of Kansas, Museum of Natural His- 
tory, Lawrence 

UA —University of Alaska, Fairbanks 


DE —University of Florida, Gainesville 


Fossil Record 3 


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Fic. 1. Approximate location of sites from which fossil Microtus and Pitymys 
have been reported. Sites 231 to 241 (Appendix A) are not plotted. 


4 Zakrzewski 


ACC 


Fic. 2. Terminology employed for teeth. Abbreviations are: AC, anterior cap; 
ACC, anteroconid complex; BRA, buccal reentrant angle; b, shortest distance be- 
tween BRA3 and LRA4; c, shortest distance between BRA3 and LRA3; LRA, 
lingual reentrant angle; PL, posterior loop; T, triangle. 


Teeth (see Fig. 2) 


ACC  —anteroconid complex 
AC —anterior cap 
b —shortest distance between BRA3 and LRA4 
c —shortest distance between BRA3 and LRA3 
BRA  —buccal reentrant angle 
LRA -—lingual reentrant angle 
PE —posterior loop 
ai —triangle 
Ages 


B.P.—before present, m.y.b.p.—million years before pres- 
ent, H—Holocene; W—Wisconsin; S—Sangamon; I—Illi- 
noian; Y—Yarmouth; K—Kansan; A—Aftonian; L—Late 


Superscripts with Taxa 
*—taxon extinct locally 
°—_taxon extinct 
nd—nomen dubium 


Fossil Record 5 


STRATIGRAPHIC SELECTED RANGES OF 
GLACIAL STA 
STAGE |oares UNIT LOCALITIES SELECTED TAXA 


HOLOCENE 


+ 


WISCONSIN 


SANGAMON 


ILLINOIAN 


RANCHOLABRE AN 


YARMOUTH i KANOPOLIS 
] PEARLETTE ASH 


HARTFORD ASH 


CUDAHY 


HALL ASH PIT 
KANSAN 


uJ 
2 
uJ 
oO 
Oo 
KE 
12) 
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= 
a 


COLERIDGE ASH 


AF TONIAN 


IRVINGTONIAN 


WELLSCH VALLEY 


Fic. 3. Time chart showing relationships of different units and selected sites 
discussed in text. LMA, land mammal age; PM, paleomagnetic stage. 


Systematics and the Fossil Record 


Microtus is the most advanced of the genera of voles in North 
America. The molars are evergrowing, contain cement in the reen- 
trant angles, the enamel of the occlusal surface is often differen- 
tiated into thick and thin segments, and well-developed dentine 
tracts are present on the sides of a number of loops or triangles. 

Two groups can be distinguished. One consists of taxa that have 
three closed alternating triangles on the m1, herein considered the 
Pitymys group; the other, taxa that have four or more closed alter- 
nating triangles on the m1, herein considered the Microtus group. 
Presently, most workers consider Pitymys a subgenus of Muicrotus; 
however, there is some merit for considering Pitymys a distinct 
genus, a view that I favor and follow herein. 


Pitymys Group 


The Pitymys group can be distinguished from the Microtus group 
by its m1, which consists of a PL, three closed alternating triangles, 


6 Zakrzewski 


and an ACC that varies in its complexity (Fig. 4). Triangles an- 
terior to the first three are generally confluent and appear to be 
added in sets of two, rather than individually. The upper molars 
tend to be less complex, retaining the primitive pattern. The enamel 
on the occlusal surface is inconsistent in its differentiation into thin 
and thick segments. Some specimens exhibit differentiation; others 
do not. 

I would include in this group and place in synonymy under 
Pitymys McMurtrie, 1831, the following taxa: Neodon Hodgson, 
1849; Pedomys Baird, 1857; Phaiomys Blyth, 1863; and Allophaio- 
mys Kormos, 1933. This approach is not novel. One of the more 
recent variations is that of Martin (1974). 

It is nearly impossible to distinguish Pitymys pinetorum (Le Conte) 
from ‘“‘Pedomys” ochrogaster (Wagner) on the basis of dental mor- 
phology (“ ” around generic names signify incorrect usage). Al- 
though an opinion can be reached if large samples are available 
(see Pitymys ochrogaster section below), the criteria cannot be used 
to distinguish taxa above the species level. 

‘“Allophaiomys” is not distinguishable at the generic level from 
‘““Phaiomys” (Martin, 1975). Differences that have been found are 
of the sort that distinguish species, not genera. 

“Allophaiomys” was probably ancestral to Pitymys (van der Meu- 
len, 1973). Although the early members of this lineage are generally 
distinguishable from the later, it is sometimes difficult to assign 
individuals from intermediate populations (Hibbard et al., 1978). 
This lineage is shown by the pattern of the m1, which consists of 
two major “end” morphotypes with intermediates (Fig. 4A—C, F). 
These facts suggest that the taxa should be placed in one genus. 

Some specimens of ‘““Neodon” have two sets of confluent triangles 
(Fig. 4D). However, others have the typical Pitymys pattern (Fig. 
4E) and, therefore, should be retained in that genus. This approach 
is consistent with the approach used in the consideration of other 
genera, including Microtus, that vary in the number of triangles. 

Based on the fossil record, Pitymys had a wider distribution than 
it does now. Hinton (1926) suggested that Pitymys’ present distri- 
bution and habits are a result of competition with Muicrotus. An 
alternative model was suggested by Hibbard (1944), who felt that 
Pitymys may have been forced southward by advancing ice and 
resorted to burrowing for thermoregulation. Where Microtus and 
Pitymys occur together they are not in competition. 


Fossil Record Wl 


fas 
tk 


Fic. 4. Selected morphotypes of m1 in Pitymys. A, P. sp.; B, P. llanensis; (G, JP 
ochrogaster; D, P. meadensis; E, P. quasiater; F, P. pinetorum. See text for additional 
explanation. 


Pitymys is thought to have descended from Mimomys (van der 
Meulen, 1974), probably in Asia. The first appearance in the New 
World is near the beginning of the Pleistocene at Wellsch Valley 
(13) in Saskatchewan (Figs. 1, 3). Later taxa may have resulted 
from speciation in North America or subsequent migration over the 
Bering Land Bridge. 


8 Zakrzewski 


Pitymys sp.—Remains of this taxon are known from Kansas, 
Aries (133), Nash (134), Kentuck (147), Wathena (148), Courtland 
Canal (151); Nebraska, Sappa (154); Saskatchewan, Wellsch Val- 
ley (13); South Dakota, Java (160); and Texas, Fyllan Cave (104) 
(Fig. 5). These sites are considered to be Irvingtonian (Aftonian- 
Kansan) in age. 

The specimens from these sites are at the most primitive grade 
of evolution. The majority of mls can be assigned to morphotype 
la (Fig. 4A). I have listed all the records here primarily for con- 
venience. Future work may show that any or all are distinct. Spec- 
imens from few of the sites have been critically studied and sample 
sizes are generally small. 

Einsohn (1971) assigned specimens from Kentuck, Wathena, and 
Sappa to Microtus llanensis Hibbard on the basis of size and occlusal 
pattern. (Hibbard [1952, Fig. 10] figured a m1 with morphotype 
la and assigned it to M. llanensis.) Martin (1975) referred the 
specimens from Kentuck and Java to “Allophaiomys” pliocaenicus 
Kormos. Van der Meulen (1978) suggested that the specimens from 
these three local faunas represent a species different from “A.” 
pliocaenicus because the degree of confluency between triangles 4 
and 5 and the AC is intermediate in development between “A.” 
pliocaenicus and “‘A.” deucalion Kretzoi. Van der Meulen (1978) 
also pointed out that, although all m1s assignable to morphotype 1 
exhibit enamel differentiation, the American specimens exhibit 
greater differentiation of enamel than does “A.” deucalion. It is 
perhaps for this reason that Churcher and Stalker (in press) are 
placing the finds from the Wellsch Valley, Java, and Kentuck in a 
new species. 

I am not convinced that enamel differentiation is a valid character 
for defining taxa in this group. I have looked at specimens from 
Fyllan Cave, which I (Zakrzewski, 1975) originally assigned to 
Microtus llanensis, and Wathena, but have examined in detail only 
some from Kentuck. I was unable to distinguish any enamel dif- 
ferentiation in the Kentuck specimens. Enamel differentiation is a 
variable character in this group. To learn whether the variability 
is ontogenetic, individual, or species specific will require more study. 
However, the Wellsch Valley specimens may represent a valid 
species because the type series appears to be larger than other spec- 
imens; the possibility of a size cline should also be considered. 

In addition, while I was examining the Kentuck sample, I ob- 
served a number of mls of morphotype 1b (Fig. 4B). This mor- 


Fossil Record 9 


photype is common within samples of more advanced, but extinct, 
species of Pitymys. It can also be found within samples of extant 
taxa, in which the common morphotype is Ic (Fig. 4C, F). Van der 
Meulen (1978) admitted that dividing the taxa at the generic level 
was arbitrary. Because of the chrono-morphocline exhibited, it seems 
more reasonable to place all morphotype 1 specimens in one genus. 

The Wellsch Valley site may have yielded the earliest known 
specimens of Pitymys in North America. Deposits at this site have 
been dated at 1.75 m.y.b.p. on the basis of paleomagnetic studies. 
Only the Nash site could be as old or older. he Nash occurs in 
the upper part of the Crooked Creek formation (fm.) in sediments 
that were channeled into the part of the Crooked Creek that con- 
tains the Borchers Ash dated at 1.96 m.y.b.p. (Fig. 3) (Zakrzewski, 
1981). These deposits are overlain by the Kingsdown fm., which 
contains an ash that has been dated at 1.2 m.y.b.p. (Boellstorff, 
1976). Underlying this ash is the Aries site (Honey, pers. comm.). 
The Coleridge Ash, which is underlain by the Sappa, also has been 
dated at 1.2 m.y.b.p. The other sites are considered to be approxi- 
mately equivalent to the Sappa. 

If the age of the Wellsch is correct, then Pitymys was in North 
America earlier than previously suspected. This occurrence also 
supports the hypothesis that Pitymys and Muicrotus have a long 
independent history because M. paroperarius, a more advanced tax- 
on, is also recorded from this site. 

Pitymys guildayi (van der Meulen, 1978) .—This species is known 
only from Maryland, Cumberland Cave (222) (Fig. 5) of Irving- 
tonian (Kansan) age [see Pennsylvania (235) in Appendix A for 
additional record]. The type (CM 20333) is a right dentary with 
m1-m2. 

Pitymys guildayi is approximately intermediate between Pitymys 
sp. from Kentuck and Wathena and P. llanensis with respect to the 
length of the ACC, the width of the AC, and the width of c (van 
der Meulen, 1978). 

Although he conceded that “Allophaiomys,” “Phaiomys,” and 
‘““Pedomys” could not be distinguished on the basis of tooth mor- 
phology, van der Meulen (1978) placed P. guilday: in ““Pedomys” 
because the enamel on the teeth is differentiated and because ‘‘Pe- 
domys” and ‘“‘Phaiomys” have undergone independent development 
on their respective continents and, therefore, should be considered 
separate genera. 

I have examined the type of P. guildayi, and although I agree 


Zakrzewskt 


10 


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uveq sary sdwdjig jo satsads OUNXa YOIYM WO} $9}e1G pa}luF, SnonSsjuos pue epeuery) UT says JO UOTeD0] JeWIxOIddy 


‘paysodas 
°¢ “Oly 


Fossil Record 11 


with van der Meulen that the teeth exhibit enamel differentiation, 
I do not feel that this character can be used to distinguish ‘“‘Pedo- 
mys’ from any other taxon. Likewise, although the two lineages 
may have undergone some independent development, their mor- 
phology suggests descendancy from a morphotype la ancestor; to 
consistently follow independent development as the sole basis for 
generic rank would quickly result in a number of morphologically 
indistinguishable genera. 

Pitymys cumberlandensis van der Meulen, 1978.—Remains of 
this species have been reported from Arkansas, Conard Fissure 
(173); and Maryland, Cumberland Cave (222) (Fig. 5). Both of 
these sites are considered to be Irvingtonian (Kansan) in age. 

The type (CM 20338, right dentary with m1—m3) is from Cum- 
berland Cave. Van der Meulen (1978) characterized P. cumberlana- 
ensis as showing little enamel differentiation on the teeth, having a 
mi with BRA4 and LRAS that are shallow and rarely contain 
cement, and unreduced third molars. 

Van der Meulen (1978) considered P. cumberlandensis to be an- 
cestral to P. pinetorum, P. parvulus, and P. nemoralis, and judged 
that these four taxa constitute the genus Pitymys, based in part on 
undifferentiated enamel. He felt that P. cumberlandensis was too 
primitive to have been derived from “‘Allophaiomys.” Although these 
relationships may be correct, I don’t think that undifferentiated 
enamel can be used as one of the diagnostic characters. 

Pitymys involutus (Cope, 7877) .—Specimens of this taxon have 
been reported from Pennsylvania, Port Kennedy Cave (228); and 
Maryland, Cumberland Cave (222) (Fig. 5). Both of these sites are 
considered to be Irvingtonian (Kansan-Yarmouth) in age. 

Cope (1871) described P. involutus from Port Kennedy. Subse- 
quently, Gazin (Gidley and Gazin, 1938) referred material from 
Cumberland Cave to the taxon. The species was considered distinct 
on the basis of the development of the reentrants on the ACC and 
its small size. 

Since 1938 the teeth from the type specimen (AMNH 8699a, 
dentary with m1—m3) have been lost (Hibbard, 1955a). The spec- 
imen that Hibbard (1955a, Fig. 2d) suggested might be P. involutus 
appears to be Microtus paroperarius. Van der Meulen (1978) stated 
that he was able to find all three taxa that he recognized from the 
Cumberland Cave among the small sample available to Gazin. Be- 
cause van der Meulen was unable to determine which of the three 


12 Zakrzewski 


would be synonymous with P. involutus, he suggested that the taxon 
be considered a nomen dubium. 

Pitymys dideltus (Cope, 7877) .—Remains of this taxon are only 
known from Pennsylvania, Port Kennedy Cave (228) (Fig. 5). The 
specimens that served as types for P. dideltus (AMNH 8694) and 
its junior synonym P. “sigmodus” (AMNH 8696) have disintegrat- 
ed or are missing (Hibbard, 1955a). If the specimens that Hibbard 
(1955a) considered to pertain to P. dideltus were assigned correctly 
the taxon would be valid. The diagnostic criteria would be that the 
total length of the toothrow falls within the range of P. pinetorum, 
but the length of the m1 exceeds that in either P. pinetorum or P. 
ochrogaster. Hibbard (1955a) listed an m1 (AMNH 8695) as having 
an occlusal length of 3.8 mm. Only P. aratai has the m1 as large, 
but the total length of the toothrow exceeds that of P. pinetorum 
(Martin, 1974). 

Van der Meulen (1978) considered P. dideltus a nomen dubium, 
because the type has been destroyed and the site from which it was 
collected is no longer accessible. 

Pitymys aratai Martin, 1974.—This taxon is known only from 
Florida, Coleman IIA (178) of Rancholabrean (Illinoian?) age (Fig. 
5). The species (type UF 11685, right dentary with ml—m3) can 
be distinguished easily because of the Pitymys pattern on the m1 
and its large size. The m1 is 3.8 mm long, which is at the upper 
end of the range of Microtus xanthognathus (Leach) and M. richara- 
sont (DeKay) (Martin, 1974: Table 3.8). Pitymys dideltus also has 
a ml that measures 3.8 mm (Hibbard, 1955a), but as mentioned 
P. dideltus is best considered as a nomen dubium. Repenning (1983) 
synonymized P. aratai: with P. mcnowni Hibbard. 

Pitymys hibbardi Holman, 1959.—Remains of this taxon are 
known from Florida, Bradenton (175) and Williston (189) (Fig. 
5). Both sites are considered to be Rancholabrean (Sangamon) in 
age. The type (FGS V-5929, left dentary with m1-m3) of P. Azb- 
bardi was described by Holman (1959) from Williston. It was dif- 
ferentiated primarily on the basis of its large size, which is at the 
upper limit of the range of extant taxa. Pitymys hibbardi has a 
reduced capsular process on the dentary and is smaller than P. 
aratai. Martin (1974) thought that P. hibbardi might have evolved 
from P. aratai. 

Pitymys llanensis (Hibbard, 1944) .—Remains of this species have 
been found in Arkansas, Conard Fissure (173); Kansas, Cudahy 
(132), Kanopolis (143), Unnamed (144), Kentuck? (147); and Tex- 


Fossil Record 13 


as, Vera (115) (Fig. 5). ‘These sites are all considered to be Irving- 
tonian (Kansan-Yarmouth) in age. 

Hibbard (1944) described P. llanensis (type KU 6626, left den- 
tary with ml—m2) from the Cudahy and placed it in ““Pedomys.” 
Semken (1966) and van der Meulen (1978) followed this assign- 
ment. 

Pitymys llanensis can be distinguished from other taxa on the 
basis of its m1. The ACC is longer and wider than in P. guildayu. 
The tooth is generally shorter than those of P. pinetorum and P. 
ochrogaster, and narrower than that of the latter. The b in P. dla- 
nensis is wider than that of P. pinetorum. 

The majority of mls belonging to P. llanensis are assignable to 
morphotype 1b (Fig. 4B). Morphotype 1b is intermediate between 
la (typical of P. sp.; Fig. 4A) and Ic (typical of P. ochrogaster [Fig. 
4C] and P. pinetorum [Fig. 4F]). Van der Meulen (1978) stated 
that these morphotypes occur in different percentages within dif- 
ferent fossil populations and used them biostratigraphically. In 
examining the sample from Kentuck, I was unable to determine 
whether two taxa or a highly variable population of one taxon were 
present. This overlapping of morphotypes is one reason that I place 
all taxa with three closed triangles into Pitymys. 

The specimens from the Unnamed site may pertain to Microtus. 

Pitymys mcnowni Hibbard, 1937.—This species is known from 
California, Centerville Beach? (27); and Kansas, Unnamed (149). 
Paleomagnetic dating places the California site in the Irvingtonian, 
whereas the Kansas site is probably Rancholabrean. 

The type (KU 3851, right dentary with m1—m2) is from Kansas. 
Hibbard (1937) considered the taxon distinct on the basis of the 
large size of its m1 (3.3 x 1.3 mm) and the character of the salient 
angles, which he described as being broader and with rounder api- 
ces than in other taxa. 

The measurements, especially the length, are at the upper end 
of the range for P. ochrogaster and P. pinetorum. Only one Pitymys 
specimen that I have measured (Hibbard et al., 1978, text-fig. 6) 
was greater than 3.3 mm. Seven specimens were 1.3 mm or wider. 
I have not examined the type, but suggest that it may represent a 
large P. ochrogaster or P. pinetorum. 

On the basis of size and dental pattern, Repenning (1983) sug- 
gested that P. mcnowni is synonymous with P. aratai and ancestral 
to, if not conspecific with, P. nemoralis (V. Bailey). 

Pitymys ochrogaster (Wagner, 1842).—Specimens of the prairie 


14 Zakrzewski 


vole have been reported from 30 to 63 sites in 14 states (Appendix 
B). These sites range in age from Rancholabrean (Illinoian) to 
Holocene. 

It is very difficult to distinguish P. ochrogaster from P. pinetorum 
on the basis of teeth unless large sample sizes are available. I suspect 
that some of the taxonomic assignments of the fossils are based on 
the geographic location of the site within the range of the particular 
taxon rather than on an analysis of the sample. Some workers have 
accepted the possibility that either one or both taxa might be in 
their fauna. This latter approach accounts for the range in the 
number of sites mentioned above and in the P. pinetorum section 
that follows. 

Criteria that have been used by paleontologists to separate the 
taxa include relative thickness of enamel (van der Meulen, 1978), 
shape of m3 (Hager, 1974), and width of b (Hibbard et al., 1978). 
The latter character seems to be the most reliable, but even in it 
there is some overlap between the taxa. Smartt (1977) was able to 
identify P. ochrogaster in New Mexican sites by means of discrim- 
inant analysis. 

Van der Meulen (1978) stated that ““Pedomys” can be distin- 
guished from Pitymys by the fact that the former has differentiated 
enamel on the occlusal surface, whereas the latter has enamel of 
equal thickness. This difference was one of the reasons he named 
the species P. guildayi and P. cumberlandensis, respectively, and placed 
the former in ‘‘Pedomys” as a subgenus of Microtus. Microtus is 
characterized in part by differentiated enamel. Although I agree 
with this characterization of Microtus and have verified the differ- 
ences in enamel between P. guildayi and P. cumberlandensis, spec- 
imens of P. ochrogaster and P. pinetorum that I have examined 
exhibit both conditions. As mentioned above, whether the variation 
in enamel thickness is a function of the individual’s age, geographic 
location, or some other factor(s) is unknown. 

Pitymys pinetorum (Le Conte, 1830) .—Fossil remains of the pine 
vole are known from 38 to 76 sites in 16 states (Appendix B). All 
of the sites are Wisconsin to Holocene in age and the majority are 
within the present range of the species. 

Pitymys pinetorum has an m1 that is generally longer than that 
of P. llanensis, generally narrower than that of P. ochrogaster, and 
a b that is narrower than in either (Hibbard et al., 1978). 

Pitymys pinetorum appears later in the fossil record than P. och- 


Fossil Record 15 


rogaster. I suspect this is a function of sampling; most sites at which 
it occurs are east of the Mississippi and few of these are older than 
Wisconsin. 

Both van der Meulen (1978) and Repenning (1983) considered 
P. pinetorum nemoralis to be a full species on the basis of size and 
morphological characteristics. If they are correct, the fossil records 
of P. pinetorum will need to be reexamined in terms of this change. 

Pitymys meadensis Hibbard, 1944.—Specimens of this taxon have 
been reported from California, North Livermore Ave. (32), Olive 
Dell Ranch (43); Colorado, Hansen Bluff (70); Kansas, Cudahy 
(132), Tobin (140), Wilson Valley (142) (Fig. 5); and Mexico, El 
Tajo de Tequixquiac (84). With the exception of the site in Mexico, 
considered to be Rancholabrean (Wisconsin), the localities are of 
Irvingtonian (Kansan) age. 

Pitymys meadensis (type KU 6563, left dentary with m1—m2) was 
described by Hibbard (1944) from the Cudahy. The species is char- 
acterized by the fact that triangles 4 and 5 on the m1 are generally 
confluent and closed off from the AC. In addition, LRA5 and BRA4 
are often deeper than in other species so that a sixth and seventh 
triangle develop, which are confluent and open into AC (Fig. 4D). 
This development of the ACC is found in some European taxa and 
in some specimens of the Mexican species P. quasiater (Coues) 
(Repenning, 1983). 

Van der Meulen (1978) placed both P. meadensis and P. quasiater 
in Microtus because they exhibit differentiated enamel on their oc- 
clusal surface. The morphology of the m1 in P. meadensis (Fig. 4D) 
and P. quasiater (Fig. 4E) and its closeness to some specimens of 
P. pinetorum (Fig. 4F) suggests the taxa should be retained in 
Pitymys. 

Pitymys quasiater is a relict population confined to the southeast- 
ern highlands of Mexico, whereas P. meadensis was apparently 
widespread in the past (Fig. 5). Perhaps P. meadensis was ancestral 
to P. quasiater, or the two are conspecific. Additional work will be 
necessary to determine the exact relationship between these two 
taxa. 


Microtus Group 


This group can be distinguished from the Pitymys group by its 
m1, which consists of a posterior loop, four or more closed alter- 


16 Zakrzewski 


nating triangles, and an AC that varies in its complexity. Triangles 
on the ml appear to be added in alternate fashion. The upper 
molars tend to be more complex as well, with a number of species 
developing additional triangles. ‘The enamel on the occlusal surface 
tends to be consistently differentiated into thin and thick segments. 

Within the group it is more difficult to assign isolated specimens 
to individual taxa because of similarities in dentition and the wide 
range of variation expressed in some species. T'wo subgroups can 
be established on the morphology of the m1: a basically four-tri- 
angled group (M. deceitensis, M. paroperarius, M. “‘speothen” and 
M. oeconomus) (Fig. 7A); and a five or more triangled group (the 
remaining taxa) (Fig. 7B). 

Other criteria that can be used are size (M. richardsoni and M. 
xanthognathus are significantly larger), occlusal pattern of M2 (M. 
pennsylvanicus has an extra triangle), M3 (M. chrotorrhinus has 
additional triangles), and shape of the incisive foramina. The latter 
character exhibits a great deal of variation owing to age of the 
individual. Other characters show a great range of variation as well 
and the best approach for correctly assigning specimens may be to 
use some appropriate multivariate analysis as was demonstrated by 
Smartt (1977). 

Microtus and Pitymys are thought to have separately entered North 
America from Asia. The first appearance of Microtus in the New 
World is near the beginning of the Pleistocene and is represented 
by M. deceitensis and/or M. paroperarius. Advanced species appear 
to represent subsequent immigrations (van der Meulen, 1978). The 
genus had a much wider range in the past than it does now. A 
number of species exhibit a significant retraction of range. 

Microtus deceitensis Guthrie and Matthews, 1971.—This taxon is 
known only from its type locality at Cape Deceit (1) Alaska of 
Irvingtonian (pre or early Kansan) age. Remains of this taxon (type, 
UA 866, right dentary with m1l—m3) are considered to represent 
the most primitive species in North America assigned to the genus. 
The absolute age of the deposit is not known and the fauna does 
not correlate well with any other fauna from North America; there- 
fore, it cannot be determined with certainty whether M. deceitensis 
also represents the earliest record of Microtus in the New World. 
M. deceitensis is similar to the extinct M. paroperarius Hibbard and 
the extant M. oeconomus Pallas in the possession of a principally 
four-triangled m1. It differs from the latter two taxa in possessing 


Fossil Record 17, 


a more complex m3, in that the second lingual loop tends to be 
bisected by the LRA2, and a simpler M3, consisting of only two 
alternating triangles as found in Pitymys (Guthrie and Matthews, 
1971). 

Van der Meulen (1978) felt that M. deceitensis represents an 
extinct side branch of Microtus evolution, but also offered the al- 
ternative that it may have given rise to M. xanthognathus. Repen- 
ning (pers. comm.) thinks that M. deceitensis represents an Asian 
relict unrelated to any North American taxon. He places M. 
deceitensis into Lasiopodomys, which he raises to generic status on 
the basis of its Pitymys-like M3. 

Microtus paroperarius Hibbard, 1944.—Remains of M. paroper- 
arius are known from Arkansas, Conard Fissure (173); Colorado, 
Hansen Bluff (70); Iowa, Little Sioux (161); Kansas, Cudahy (132), 
Holzinger (137), Tobin (140), Wilson Valley (142), Unnamed? 
(144), Hall Ash Pit (150); Maryland, Cumberland Cave (222); 
Nebraska, Unnamed (156) and Mullen (157 or 158); Saskatche- 
wan, Wellsch Valley (13); and Texas, Vera (115) [see Pennsylvania 
(235) in Appendix A for additional record]. The ages of these sites 
(Fig. 6) range from Irvingtonian (Aftonian?) to Rancholabrean 
(early Illinoian?). 

The type of M. paroperarius (KU 6587, partial right dentary 
with m1l—m2) was described by Hibbard (1944) from the Cudahy. 
It is characterized by its m1, which generally consists of four closed 
alternating triangles and a fifth triangle that opens broadly into AC 
(Fig. 7A). A small percentage of specimens may have m1s with five 
closed triangles. Similar mls are found in M. speothen (Cope) and 
M. oeconomus. 

Hibbard (1955a) stated that mls of M. paroperarius are smaller 
than those of M. speothen from the Port Kennedy Cave (228). How- 
ever, the few measurements available for M. speothen are just over, 
or within the range of those obtained for M. paroperarius. 

Paulson (1961) pointed out that 50% of the m1s of M. paroper- 
arius contain cement in LRA4, whereas the LRA4 of M. oeconomus 
lacks cement. Van der Meulen (1978) stated that the two taxa 
cannot be distinguished on the basis of tooth morphology. Perhaps 
additional study would show that the taxa are conspecific. If so, a 
range retraction even greater than that seen in M. xanthognathus is 
indicated. 

The Wellsch Valley occurrence is the earliest record of the taxon 


18 Zakrzewski 


(Figs. 3, 6). These specimens were reported as M. deceitensis by 
Kurtén and Anderson (1980). The Mullen occurrence may be the 
latest. Kurtén and Anderson (1980) reported the specimens from 
Mullen I, which is Kansan in age, but Martin (1972) reported that 
they came from Mullen II, which is Illinoian in age, and assigned 
them to M. pennsylvanicus (see Martin, 1972, Fig. 2C) because 
there were no other indicators of Kansan age. Martin (1972) stated 
that M. paroperarius is ancestral to M. pennsylvanicus although he 
presented no evidence, unless it is the fact that some M. paroperarius 
exhibit five closed triangles. The remaining sites are generally con- 
sidered to be Kansan in age. 

Van der Meulen (1978) suggested that M. paroperarius migrated 
to the New World, along with other taxa, just prior to 0.7 m.y.b.p. 
However, if the date of 1.75 m.y.b.p for the Wellsch Valley is 
correct, the migration was much earlier. 

Microtus speothen (Cope, 7877).—The remains of this extinct 
species were known only from the Port Kennedy Cave (228) of 
Yarmouth age from Pennsylvania. Originally described by Cope as 
Arvicola speothen, he (Cope, 1899) subsequently synonymized the 
species A. tetradelta under A. speothen and placed the latter in M:- 
crotus. 

Hibbard (1955a) felt that M. speothen belonged in the M. oecono- 
mus group. He also stated that M. speothen was larger than M. 
paroperarius. However, Cope (1899) listed the length of m1 as 3.0 
mm, which would fall in the range of M. paroperarius m1s (2.6- 
3.4) reported by Paulson (1961). 

Unfortunately, the type of M. speothen (AMNH 86839, left den- 
tary with ml—m3) has been destroyed and the site is no longer 
accessible; therefore, van der Meulen’s (1978) suggestion that all 
of Cope’s taxa from Port Kennedy should be considered nomen 
dubia is a reasonable one. 

Microtus oeconomus Pallas, 71778.—Fossil remains of the tundra 
vole are known only from the Yukon Territories, Old Crow River 
Loc. 11 (10) and 12 (8), as well as Bluefish Cave I (11). These 
sites are Sangamon?, Illinoian, and late Wisconsin, respectively. 
Similar to the extinct M. paroperarius in dental morphology, the 
two taxa may be conspecific (van der Meulen, 1978). The fossil 
records of M. oeconomus are being studied by Brenda F. Beebe 
(Jopling et al., 1981) and are the first reports of this taxon as a 
fossil. 


19 


Fossil Record 


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20 Zakrzewski 


Microtus miurus Osgood, 1907.—Specimens of the Alaska vole 
have been reported from Alaska, Sullivan Pit (2), Fairbanks II (3), 
Fairbanks I (4); and Yukon Territories, Old Crow River Loc. 11 
(10), 12 (8 and 9), 14N (7), Bluefish Cave I (11) [see Iowa (238) 
in Appendix A for additional record]. The sites range in age from 
Illinoian to Holocene, and with the exception of the Sullivan Pit 
(Repenning, pers. comm.), the species is not found near any of them 
today. 

Microtus miurus is distinguished by its narrow cranium with a 
sharp median crest. The former character is used to place M. miurus 
in its own subgenus Stenocranius. Kurtén and Anderson (1980) 
stated that M. miurus has a M1 with five triangles and a m1 with 
a simple trefoil or AC. These two characters could be used to dis- 
tinguish it from M. pennsylvanicus. | found no M. miurus with five- 
triangled Mis and could not distinguish its m1 from that of M. 
pennsylvanicus. 

The earliest record of M. miurus is from Fairbanks I. Brenda F. 
Beebe is studying the remains from Bluefish Cave I. 

Microtus richardsoni (DeKay, 1542).—Fossil remains of Rich- 
ardson’s vole are known from Alberta, Eagle Cave (18); and Mon- 
tana, Warm Springs (19). All of these sites are late Wisconsin in 
age and within the present range of the species. Remains of M. 
richardsoni are relatively easy to recognize. ‘The species is among 
the largest in the genus, being about the same size as M. xantho- 
gnathus. It can be distinguished from that and other taxa by the 
fact that the incisive foramina decrease in size with age, so that in 
some individuals they are nearly closed. In addition, the M1 and 
on occasion the M2 possess an additional small triangle (Fig. 7E), 
although it generally is not closed off from the previous alternating 
triangle as is the triangle on the M2 of M. pennsylvanicus (Fig. 
TE): 

Microtus californicus (Peale, 1845).—Remains of the California 
vole are known from California, Samwel Cave (28), Potter Creek 
Cave (29), cf. Irvington (31), Carpinteria (33), McKittrick (34), 
Rancho La Brea (35), San Pedro (36), La Mirada (37), Emery 
Borrow Pit (38), Zuma Creek (39), Costeau Pit (40), Newport Bay 
Mesa 1067 (41), cf. Vallecito Creek (42), Kokoweef (44); and Ne- 
vada, Tule Springs E, (45), Glendale? (47). These sites range in 
age from Irvingtonian (Kansan) to Rancholabrean (Wisconsin). 

In assigning specimens to M. californicus, some workers (Miller, 
1971) have relied on the shape of the incisive foramina, which are 


Fossil Record 21 


wide and unconstricted, and the fact that the teeth of the species 
seem to be slightly larger than those of other taxa that occur near 
California. Many M2s of the California vole have the LRA2 di- 
rected posteriorly so that it appears a fourth triangle would become 
isolated if the LRA2 lengthened (Fig. 7D-—E). 

The oldest remains (if correctly identified) are from the Vallecito 
Creek and Irvington. In fact one of the specimens from Vallecito 
could be the oldest record for a Microtus. I (Zakrzewski, 1972) 
questionably assigned an edentulous dentary to M. californicus on 
the basis of the presence of a deep masseteric fossa and alveoli that 
showed that the teeth were evergrowing. The specimen is from Loc. 
6683, which is not in the type section, and is associated with re- 
mains of Synaptomys (Metaxomys) anzaenis. Metaxomys is associ- 
ated with faunas of Blancan age, whereas the extant subgenera with 
one exception (Dixon |.f., Kansas) are associated with faunas of 
Irvingtonian and younger age. At that time I suggested two alter- 
native explanations. The specimen represents a genus other than 
Microtus or the Synaptomys represent a relict population. Although 
the former alternative cannot be dismissed, data acquired while 
preparing this manuscript suggest that the latter interpretation may 
be closer to the truth. 

The other sites are Wisconsin in age. The two sites in Nevada 
are outside the present range of the taxon and the Glendale record 
may be M. montanus (Kurtén and Anderson, 1980). 

Microtus mexicanus (Saussure, 1567).—Fossil remains of the 
Mexican vole have been reported from Mexico, San Josecito (85); 
New Mexico, Brown Sand Wedge (72), Dry Cave (73), Burnet 
Cave (74), Muskox Cave (75), Anthony Cave (77), Conkling Cav- 
ern (78), Howells Ridge Cave (82); and Texas, Upper (91) and 
Lower (92) Sloth Cave, Pratt Cave (93). All of the records ascribed 
to this taxon are late Wisconsin to Holocene in age. Likewise, all 
the finds are either in or not substantially distant from the present 
range. 

Smartt (1977) identified the majority of New Mexican records 
using discriminant analysis. Kurtén and Anderson (1980) stated 
that the incisive foramina are short, broad, and truncated poste- 
riorly. ‘This character was highly variable in specimens that I ex- 
amined. In some M1s and M2s the LRA2 is deep and directed 
posteriorly, so that it appears an additional triangle might form 
(Fig. 7D). In addition, I observed an M2 of M. mexicanus that had 
a M. pennsylvanicus pattern. 


22 Zakrzewski 


Microtus longicaudus (Merriam, 1888) .—Specimens of the long- 
tailed vole have been reported from Alberta, January Cave? (17), 
Eagle Cave? (18); Colorado, Chimney Rock Animal Trap? (65), 
Unnamed (69); Idaho, Moonshiner Cave (21), American Falls? 
(24); New Mexico, Dry Cave (73), Burnet Cave (74); and Wyo- 
ming, Agate Basin (62), Little Box Elder Cave (63). They range 
in age from Sangamon? to Holocene. The oldest and only pre- 
Wisconsin record of M. longicaudus could be from American Falls 
(the specimen may actually represent M. pennsylvanicus). The Al- 
berta and Colorado records may represent M. montanus. 

There is nothing diagnostic about the teeth of M. longicaudus. 
Some workers feel that this species can be distinguished by its in- 
cisive foramina, the borders of which are parallel or taper gradu- 
ally. However, this feature is not unique to this taxon. Smartt 
(1977) has used discriminant analysis to identify the long-tailed 
vole in New Mexican sites. 

I have observed an M2 of M. longicaudus with a fourth triangle 
similar to that of M. pennsylvanicus and an m1 with a prism fold or 
‘“‘mimomyskante,” a feature typical of primitive voles of Blancan 
age. 

Microtus montanus (Peale, 1848).—Remains of the mountain 
vole are known from Alberta, Eagle Cave? (18), January Cave? 
(17); Arizona, Salina (52); Colorado, Chimney Rock Animal ‘Trap? 
(65); Idaho, Jaguar Cave (20), Moonshiner Cave (21), Downey 
Dump (23), American Falls (24), Rainbow Beach (25); Kansas, cf. 
Jones (126), Trapshoot (138); Nevada, Glendale? (47); New Mex- 
ico, Anthony Cave (77), Shelter Cave (79), Howells Ridge Cave 
(82); Oregon, Fossil Lake (26); Texas, Navar Ranch #13 (89); 
Utah, Snowville (55), Silver Creek (56); and Wyoming, Little Can- 
yon Creek Cave (58), Prospects Shelter (59), Natural Trap Cave 
(60), Little Box Elder Cave (63), Bell Cave (64). These sites range 
in age from Irvingtonian (Kansan) to Holocene. 

The earliest records of M. montanus are from Downey Dump 
and Snowville (Repenning, pers. comm.). The remaining sites range 
in age from Sangamon to Holocene. The reports from Kansas, 
Texas, New Mexico, Nevada (if not M. californicus), and Alberta 
(if not M. longicaudus) are outside the present range of the taxon. 

Smartt (1977) identified specimens of M. montanus from New 
Mexico by using discriminant analysis to differentiate between 
species that might be present. Davis (1975) recognized the presence 


Fossil Record 23 


of an additional Microtus from the Jones site because a number of 
M2s could not be assigned to M. pennsylvanicus even though all of 
the mls from the site appeared to be pennsylvanicus-like. Davis 
called his unidentifiable taxon, Microtus species Alpha. Stewart 
(1978) suggested that Davis’ species Alpha might be M. montanus 
on the basis of faunal similarities between the Jones and Trapshoot 
sites. 

Kurtén and Anderson (1980) implied that the posterior constric- 
tion of the incisive foramina and an M2 with four closed triangles 
are diagnostic for this taxon. ‘The posterior constriction is in part a 
function of the age of the individual, older individuals showing more 
constriction than younger ones. 

I know of no New World Microtus for which four closed triangles 
on the M2 is as typical as it is for M. pennsylvanicus. Other species 
may have a small percentage of individuals that exhibit four closed 
triangles on M2; however, most non-pennsylvanicus Microtus M2s 
are similar to that shown in Fig. 7C. 

Microtus chrotorrhinus (Miller, 1894).—Specimens of the yel- 
low-nosed vole have been reported from Pennsylvania, New Paris 
#4 (224), Hollidaysburg Fissure (225), Bootlegger Sink (227); 
Québec, Caverne de St. Elzéar (230); Tennessee, Carrier Quarry 
Cave (199), Baker Bluff (200); Virginia, Back Creek #2 (218), 
Clark’s Cave (219), Natural Chimneys (221); and West Virginia, 
Eagle Rock Cave (211), Hoffman School Cave (212), Mandy Wal- 
ters Cave (213), Upper Trout Cave (214). These sites are late 
Wisconsin to Holocene in age. 

Microtus chrotorrhinus is commonly found with M. xanthognathus 
and M. pennsylvanicus in cave faunas of the Appalachians. Microtus 
chrotorrhinus is smaller than M. xanthognathus and differs from M. 
pennsylvanicus in having a distinctive M3, with two additional tri- 
angles. The first and second alternating triangles are generally con- 
fluent; however, Guilday (1982) has shown that this pattern is also 
fairly common in some populations of M. pennsylvanicus. 

Microtus chrotorrhinus occurs today in the eastern subarctic and 
as a relict form at high elevations in the central Appalachians. The 
fossil records with one exception are in or very near to its present 
range. Graham (1976) listed M. chrotorrhinus as a member of the 
Welsh Cave fauna (205) but this is incorrect. 

Guilday et al. (1964) have demonstrated a cline within extant 
populations. Individuals become larger toward the south. The fossil 


24 Zakrzewski 


5 
= = 


Fic. 7. Selected morphotypes of m1 and M2 in Microtus. A, m1 typical of M. 
paroperarius group; B, m1 typical of non-paroperarius group of Microtus; C, M2 
typical of most non-pennsylvanicus species of Microtus; D, M2 seen in some M. 
mexicanus and M. californicus showing incipient development of additional triangle; 
E, M2 of M. richardson: showing further development of additional triangle; F, M2 
typical of M. pennsylvanicus showing additional triangle. 


$ 
S 


specimens from New Paris #4 are equivalent in size to those from 
extant populations of Labrador and Québec. 

Guilday et al. (1977) suggested that M. chrotorrhinus was able 
to survive in the east (in contrast to M. xanthognathus) by moving 
to higher elevations when the climate changed in post-glacial time. 
It was able to extend its range into northeastern Canada after the 
ice melted. 

Microtus xanthognathus (Leach, 18/5).—Fossil remains of the 


Fossil Record D5 


yellow-cheeked vole have been reported from Alaska, Fairbanks II 
(3), Chicken (5); Arkansas, Peccary Cave (172); Illinois, Meyer 
Cave (206); Iowa, Waubonsie (164); Kentucky, Welsh Cave (205); 
Missouri, Bat Cave (170); Pennsylvania, New Paris #4 (224), 
Bootlegger Sink (227); Québec, Caverne de St. Elzéar (230); Ten- 
nessee, Baker Bluff (200), Cheek Bend Cave (203); Virginia, Loop 
Creek Quarry Cave (215), Gillespie Cliff Cave (216), Back Creek 
#2 (218), Clark’s Cave (219), Natural Chimneys (221); West Vir- 
ginia, Eagle Rock Cave (211); Wyoming, Prospects Shelter (58); 
and Yukon Territories, Old Crow River Loc. 44 (6), 12 (8-9), 11 
(10), Bluefish Cave I (11) [see Iowa (238, 239) and Wisconsin (241) 
in Appendix A for additional records]. These sites are all within 
the Rancholabrean stage ranging in age from late IIlinoian [Old 
Crow River Loc. 12 (8)] to Holocene (Caverne de St. Elzéar). 

Microtus xanthognathus can be distinguished from other species 
of Microtus, except for M. richardsoni, by its large size. In addition, 
Hallberg et al. (1974) stated that the BRA3 on the M3 of M. 
xanthognathus lacks cementum, whereas the same reentrant in M. 
pennsylvanicus contains cementum. I have observed cementum in 
the BRA3 of M3s in adult M. richardson: as well as a narrowing 
of the incisive foramina with age. These two characters may be 
useful in separating M. richardson: from M. xanthognathus. How- 
ever, the lack of cementum in the BRA3 should be used with care 
as Guilday (1982) stated that 10.3% (n = 113) of the M. xantho- 
gnathus from Appalachian caves have cementum, whereas 5.2% 
(n = 1,235) of the M. pennsylvanicus lack cementum. 

Although still extant across much of northwestern Canada and 
east-central Alaska, the records of the yellow-cheeked vole from 
conterminous United States and the Gaspe Peninsula (Fig. 8) are 
well outside the present range of the species. Guilday et al. (1977) 
suggested that M. xanthognathus dwelled on the taiga. As the cli- 
mate changed toward the end of the Pleistocene, populations moved 
northwest following the shifting environment. Populations could 
not be maintained in the east because of changes in the vegetation. 
Movement into northeastern Canada was blocked by ice. Biotic 
evidence from the Ozark region suggested to Hallberg et al. (1974) 
that M. xanthognathus lived in more of a parkland than taiga sit- 
uation. 

Microtus pennsylvanicus (Ord, 7875).—Specimens of the mead- 


Zakrzewski 


26 


sag ‘a8ues yuasasd s}t jo apisino ase yey) paodas usaq sey snyspusoyjuvx ‘ YOIYM WO] Sais Jo UONeoo] ayeuTIxo1ddy 


oS? 


00k 


oS6 


f 


000! 


‘panojd you ase (y xtpuaddy) [pz pur “o€z ‘8EZ 


050! 


‘9 ‘Olg 


002! 


oSt 


oS? 


Fossil Record Qi, 


ow vole have been reported from 91 sites in 24 states and four 
provinces (Appendix B) that range in age from Irvingtonian (Yar- 
mouth) to Holocene. M. pennsylvanicus is the most widely distrib- 
uted species of Microtus. Its distribution was even more extensive 
in the past as M. pennsylvanicus has been reported from more than 
two dozen sites in seven states south of its present range. The ear- 
liest record for the meadow vole is from Kansas, Kanopolis (143). 

Microtus pennsylvanicus is closely related to the European field 
vole, M. agrestis. Both taxa have an M2 that exhibits four alternating 
triangles. This character is considered to be diagnostic for the species 
and suggested to some workers an additional invasion of microtine 
stock subsequent to early Kansan time. 

The diagnostic fourth alternating triangle of M2 in M. pennsyl- 
vanicus is much smaller than the other three, in most cases being a 
small nubbin (Fig. 7F). Although I have never observed an M2 of 
a meadow vole that lacked the fourth triangle, I have observed a 
fourth triangle in one specimen each of M. mexicanus and M. lon- 
gicaudus. The only difference between the specimens is that in M. 
pennsylvanicus the fourth triangle appears to be closed off from the 
third, whereas in M. mexicanus and M. longicaudus a very thin strip 
of dentine connects the two triangles. M. mexicanus and especially 
M. californicus have M2s in which LRA2 is directed posteriorly so 
that the third triangle appears to be developing a bud and one can 
visualize how a fourth triangle might develop (Fig. 7D-E). 

Guilday (1982) has shown that enough variation exists within 
the M3s of Microtus species common to Appalachian cave faunas 
that assignment to specific taxa on the basis of a few isolated teeth 
is unwarranted. 

The number of alternating triangles on the ml in M. pennsyl- 
vanicus varies from five to seven. Semken (1966) demonstrated an 
increase in the number of alternating triangles through time for 
fossil sites in Kansas. Subsequent work by Davis (1975) and 
McMullen (1978) confirmed this chronocline. Davis (1975) showed 
that in extant populations, meadow voles with the largest teeth and 
greatest number of triangles occur on the grasslands of the High 
Plains where the grass is coarser. 

Davis (1975) attempted to relate the present distribution of M. 
pennsylvanicus to the distribution and relative abundance of C-3 
and C-4 grasses. Although his results were ambiguous, additional 
study seems warranted. 


28 Zakrzewski 


Microtus sp.—Specimens of Microtus not assigned to species are 
known from Alberta, Medicine Hat M (14) and K (15); Arizona, 
Choate Ranch (48), Murray Springs (49), Murray Springs Arroyo 
(50), Papago Springs (51), Vulture Cave* (53); California, Hawver 
Cave (30); Colorado, Dutton (66), Selby (67); Idaho, Wasden (22); 
Iowa, Little Siouxt/? (161); Kansas, Tobin*’? (140); Nebraska, Un- 
named* (155); Nevada, Tule Springs B,* (46); New Mexico, Dark 
Canyon Cave* (76), Palomas Creek Cave* (81), Baldy Peak Cave*t 
(83); Saskatchewan, Ridell* (12); Texas, Tank Trap Wash #1+ 
(87), Huecos Tanks #1* (88), Dust Cavet (90); and Utah, Crystal 
Ball Cave (54). These sites range in age from Irvingtonian (Kan- 
san) to Holocene. Most of these specimens probably belong to some 
extant taxon living in or near the area of the site as all but the 
Little Sioux and Tobin records are Wisconsin and Holocene in age. 
Some of these specimens are unassignable because of the fragmen- 
tary nature of the material. A few of these records were taken from 
faunal lists where no description or size of sample was noted. 

The oldest records are from the Little Sioux and Tobin. The 
former was reported by Gerald R. Paulson in an unpublished fau- 
nal list for the site. Unfortunately, I could not find the specimens 
in the collections at the University of Michigan. The latter record 
is represented by an isolated m1 with five closed alternating tri- 
angles and a simple anterior cap (Zakrzewski and Kolb, 1982). It 
could represent the earliest record of an extant taxon as it is very 
similar to the teeth assigned to M. pennsylvanicus from the Kano- 
polis (143) site (Hibbard et al. 1978). But as discussed above, iso- 
lated teeth of Microtus, especially m1s, are generally unassignable 
to a species. 

Unless they prove to be of M. mexicanus, the records from Texas 
and New Mexico would substantiate a more extensive range for 
one or more other species. Other significant extensions at the species 
level are represented by the non-pennsylvanicus Microtus reported 
by SkwaraWoolf (1980) from the Ridell and the one from the 
Unnamed site in Nebraska. 

Another record of interest is that from Tule Springs B, (46). 
Mawby (1967) stated that the m1 from this site differed in detail 
with those m1s he examined from site E, and those in the mammal 
collection at the University of California, Berkeley. To learn wheth- 
er the specimen represents a new taxon or an aberrant individual 
of some extant taxon requires additional study. 


Fossil Record 29 


Concluding Remarks 


To gain a better understanding of the interrelationships and early 
history of Microtus the following suggestions are offered. 


1) Additional sites in all areas need to be found, but especially 
in those areas for which there are no records. 

2) Because of the amount of variation within the taxa, studies 
on large samples of extant and extinct (when possible) taxa 
by appropriate multivariate techniques are necessary. 

3) When undertaking a systematic study of an extant species, 
mammalogists should include data that might prove useful 
regarding isolated teeth as well as other aspects of the anat- 
omy. 

4) When dealing with fossils, specimens should not be assigned 
to an extant taxon solely on the basis of present distribution. 


Acknowledgments 


I thank the following individuals for allowing me to examine 
specimens under their care: Jerry R. Choate, Museum of the High 
Plains, Fort Hays State University; Philip D. Gingerich, Museum 
of Paleontology, University of Michigan; Robert S. Hoffmann, Mu- 
seum of Natural History, University of Kansas; Philip Meyers, 
Museum of Zoology, University of Michigan; and Holmes A. 
Semken, Department of Geology, University of Iowa (145). 

I thank the following individuals for sharing their knowledge of 
unpublished records (sites in parentheses; see 145 above) or checking 
the accuracy of the records after compilation: Elaine Anderson (14- 
15, 38-39, 44, 69, 112, 169), Denver, Colorado; Brenda F. Beebe 
(11); James A. Burns (17-18), and Rufus S. Churcher, all of the 
University of Toronto; Walter W. Dalquest, Midwestern Univer- 
sity; Ralph E. Eshelman (134, 150-151), Calvert Cliffs Museum, 
Solomons, Maryland; Shirley Fonda (225), State College, Pennsyl- 
vania; Russell W. Graham, Illinois State Museum; the late John 
E. Guilday (201, 203, 214-216, 235), Carnegie Museum of Nat- 
ural History; Arthur H. Harris (71, 75-76, 81, 83, 86, 90, 92), 
University of Texas at El Paso; James Honey (133), Lakewood, 
Colorado; Ernest L. Lundelius (94, 98, 105-106, 108, 114), Uni- 
versity of Texas; Wade Miller (54), Brigham Young University; 


30 Zakrzewski 


Gerald R. Paulson (161), Ann Arbor, Michigan; Charles A. Re- 
penning (23, 52, 55), U.S. Geological Survey, Menlo Park, Cali- 
fornia; H. A. Semken (164); J. D. Stewart (138, 236), University 
of Kansas; Danny D. Walker, University of Wyoming; and S. Da- 
vid Webb (174-197), University of Florida. In addition I have listed 
four unpublished records (135, 136, 144, 155) based on specimens 
in the Sternberg Memorial Museum. I thank Sydney Anderson, 
American Museum of Natural History, the late J. E. Guilday, and 
C. A. Repenning for their constructive comments on an earlier draft 
of the manuscript. Gwenne Cash drafted the figures and typed the 
manuscript. 


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BoELLsTorFF, J. 1976. The succession of late Cenozoic volcanic ashes in the Great 

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* Numbers in parentheses following citations refer to fossil faunas identified in 
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Fossil Record 31 


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32 Zakrzewski 


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Fossil Record 33 


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Fossil Record 35 


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Fossil Record 37 


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Appendix A. Fossil Faunas Containing Pity- 
mys and Microtus* 


Alaska 


Sullivan Pit (2), Tofty Placer District, H/W 
M. miurus, M. xanthognathus?+ 
Fairbanks II (3), Yukon-Tanana Upland, W, 11,735 + 130 to 40,000 B.P. 
M. miurust, M. xanthognathus 
Chicken (5), Yukon-Tanana Upland, W 
M. xanthognathus 
Fairbanks I (4), Yukon-Tanana Upland, I 
M. miurus 
Cape Deceit (1), Derring Region, K/A 
M. deceitensis° 


Alberta 


Eagle Cave (18), High Rock Range, W, 22,700 + 1,000 B.P. 
M. richardsoni, M. longicaudus or montanust 
January Cave (17), Front Range, W, 23,100 + 860 B.P. 
M. longicaudus or montanus* 
Medicine Hat M (14), Medicine Hat District, W, 25,000 + 800 to 38,000+ B.P. 
M. sp. 
Medicine Hat K (15), Medicine Hat District, S 
M. sp. 
Hand Hills (16), Hand Hills, W/I 
M. pennsylvanicus 


* Dates ending in B.P. are radio-carbon dates; dates ending in m.y.b.p. are fission- 
track dates; dates with no postscript are based on paleomagnetic inferences. Abbre- 
viations and symbols: nd, nomen dubium; °, taxon extinct; +, taxon extinct locally; 
#, records from Webb (pers. comm.) and supercede those in Webb (1974). 


38 Zakrzewski 


Arizona 
Vulture Cave (53), Coconino Co., W, <13,170+ B.P. 
M. sp.* 
Papago Springs (51), Santa Cruz Co., W 
M. sp. 
Choate Ranch (48), Cochise Co., W 
M. sp. 
Murray Springs (49), Cochise Co., W 
M. sp. 
Murray Springs Arroyo (50), Cochise Co., W 
M. sp. 
Salina (52), Navajo Co., W 
M. montanus 
Arkansas 


Peccary Cave (172), Newton Co., W, 16,700 + 250 B.P. 

P. pinetorum, P. ochrogaster+, M. pennsylvanicus+, M. xanthognathust 
Conard Fissure (173), Newton Co., K 

P. llanensis®, P. cumberlandensis°, M. paroperarius° 


California 


La Mirada (37), Los Angeles Co., W, 10,690 + 360 B.P. 
M. californicus 
Rancho La Brea (35), Los Angeles Co., W, 12,650 + 160 to 40,000+ B.P. 
M. calvfornicus 
McKittrick (34), Kern Co., W, 38,000 + 2,500 B.P. 
M. californicus 
Samwel Cave (28), Shasta Co., W 
M. californicus 
Potter Creek Cave (29), Shasta Co., W 
M. californicus 
Hawver Cave (30), Eldorado Co., W 
M. sp. 
Carpinteria (33), Santa Barbara Co., W 
M. californicus 
San Pedro (36), Los Angeles Co., W 
M. californicus 
Emery Borrow Pit (38), Los Angeles Co., W 
M. californicus 
Zuma Creek (39), Los Angeles Co., W 
M. caltfornicus 
Costeau Pit (40), Orange Co., W 
M. californicus 
Newport Bay Mesa 1067 (41), Orange Co., W 
M. californicus 
Kokoweef (44), San Bernadino Co., W 
M. californicus 
North Livermore Ave. (32), Alameda Co., Y, 500,000 
P. meadensis® 


Fossil Record 


Irvington (31), Alameda Co., Y/K 
M. cf. M. californicus 

Vallecito Creek (42), San Diego Co., Y/K 
M. cf. M. californicus 

Centerville Beach (27), Humboldt Co., K/A, >730,000 to <900,000 
P. mcnowni?° 

Olive Dell Ranch (43), San Bernardino Co. 


P. meadensis° 


Colorado 


Chimney Rock Animal Trap (65), Larimer Co., W, 11,908 + 180 B.P. 
M. longicaudus or M. montanus 

Dutton (66), Yuma Co., W 
P. ochrogaster, M. pennsylvanicus, M. sp. 

Selby (67), Yuma Co., W 
M. sp. 

Unnamed (69), Alamosa Co., W 
M. longicaudus 

Mesa De Maya (68), Las Animas Co., S 
P. ochrogaster 

Hansen Bluff (70), Alamosa Co., K, =0.7 m.y.b.p. 
P. meadensis°, M. paroperarius® 


Florida# 


Warm Mineral Springs (174), Sarasota Co., W 
P. pinetorum 

Devil’s Den III (186), Levy Co., W 
P. pinetorum, M. pennsylvanicus 

Waccasassa IIB (187), Levy Co., W 
P. pinetorum, M. pennsylvanicus 

Ichetucknee River (197), Columbia Co., W 
P. pinetorum 

Vero 2 (176) and 3 (177), Indian River Co., W 
P. pinetorum 

Kendrick IA (179), Marion Co., W 
P. pinetorum 

Arrendondo I (190), Alachua Co., W 
P. pinetorum, M. pennsylvanicus 

Arrendondo IB (191), Alachua Co., W 
M. pennsylvanicus 

Arrendondo II (192), HA (193), B (194), and C (195), Alachua Co., W 
P. pinetorum 

Haile XIB (196), Alachua Co., S 
P. pinetorum 

Reddick IA (180), B (181), C (182), D (183), and IIC (184), Marion Co., S 
P. pinetorum 

Mefford I (185), Marion Co., S 
P. pinetorum 

Withlacooche VIIA (188), Levy Co., S 
M. pennsylvanicus 


39 


40 Zakrzewsk1 


Bradenton (175), Manatee Co., S 
P. hibbardi° 

Williston (189), Levy Co., S$ 
P. hibbardi° 

Coleman IIA (178), Sumter Co., I 
P. aratai° 


Georgia 


Ladds (198), Bartow Co., W 
P. pinetorum 


Idaho 


Jaguar Cave (20), Lemhi Co., H/W, 10,370 + 350 to 11,580 + 250 B.P. 
M. montanus 

Rainbow Beach (25), Power Co., W, 21,500 + 700 to 31,300 + 2,300 B.P. 
M. montanus 

Wasden (22), Bonneville Co., W 
M. sp. 

Moonshiner Cave (21), Bingham Co., W 
M. longicaudus, M. montanus 

American Falls (24), Power Co., S 
M. montanus, M. longicaudus or M. pennsylvanicus 

Downey Dump (23), Bannock Co., K 
M. montanus 


Illinois 


Meyer Cave (206), Monroe Co., H 
P. pinetorum, M. pennsylvanicus+, M. xanthognathus* 


Indiana 


Harrodsburg Crevice (207), Monroe Co., S 
P. ochrogaster 


Iowa 


Brayton (162), Audubon Co., W, 12,420 + 180 B.P. 
P. pinetorum, M. pennsylvanicus 
Oakland (163), Pottawattamie Co., W 
M. pennsylvanicus 
Waubonsie (164), Mills Co., W, 14,430 + 1,030 to 14,830 + 1,120 B.P. 
P. pinetorum, P. ochrogaster, M. pennsylvanicus, M. xanthognathus* 
Elkader (238), Clayton Co., W, 20,530 + 130 B.P. 
M. pennsylvanicus, M. xanthognathus*, M. cf. M. miurus* 
Eagle Point (239), Clinton Co., W 
M. pennsylvanicus, M. xanthognathus* 
Craigmile (240), Mills Co., W, 23,200 + 535 B.P. 
P. pinetorum, P. ochrogaster, M. pennsylvanicus 


Fossil Record 


Little Sioux (161), Harrison Co., K, 0.74 m.y.b.p. 
M. paroperarius®, M. sp.*/° 


Kansas 


Robert (125), Meade Co., W, 11,100 + 390 B.P. 
P. ochrogaster, M. pennsylvanicus* 
Jones (126), Meade Co., W, 26,700 + 1,500 to 29,000 + 1,300 B.P. 
P. ochrogaster, M. pennsylvanicus+, M. cf. M. montanus* 
Hill City (236), Graham Co., W 
M. sp. 
Keiger Creek (135), Clark Co., W 
M. pennsylvanicus* 
Trapshoot (138), Rooks Co., W 
P. ochrogaster, M. pennsylvanicus+, M. montanus* 
Jinglebob (127), Meade Co., W 
P. ochrogaster, M. pennsylvanicus* 
Unnamed (152), Smith Co., W/S 
M. pennsylvanicus 
Cragin Quarry (128), Meade Co., S 
P. ochrogaster, M. pennsylvanicus* 
Mt. Scott (129), Meade Co., I 
P. ochrogaster, M. pennsylvanicus* 
Butler Spring (130), Meade Co., I 
P. ochrogaster, M. pennsylvanicus* 
Adams (131), Meade Co., I 
M. pennsylvanicus* 
Unnamed (136), Trego Co., I 
M. pennsylvanicus* 
Duck Creek (139), Ellis Co., I 
P. ochrogaster, M. pennsylvanicus* 
Williams (145), Rice Co., I 
P. ochrogaster, M. pennsylvanicus* 
Sandahl (146), McPherson Co., I 
P. ochrogaster, M. pennsylvanicus* 
Unnamed (149), Brown Co., ? 
P. mcnowni° 
Rezabek (141), Lincoln Co., I 
P. ochrogaster, M. pennsylvanicus* 
Kanopolis (143), Ellsworth Co., Y 
P. llanensis’, M. pennsylvanicust 
Cudahy (132), Meade Co., K, =0.6 m.y.b.p. 
P. llanensis°, P. meadensis°, M. paroperarius® 
Hall Ash Pit (150), Jewell Co., K, 20.74 m.y.b.p. 
M. paroperarius® 
Holzinger (137), Trego Co., K 
M. paroperarius? 
Tobin (140), Russell Co., K 
P. meadensis°, M. paroperarius®, M. sp.*/° 
Wilson Valley (142), Lincoln Co., K 
P. meadensis°, M. paroperarius° 
Unnamed (144), Ellsworth Co., K 
P. llanensis?° or M. paroperarius ?° 


41 


42 Zakrzewski 


Aries (133), Meade Co., K, =1.2 m.y.b.p. 
P. sp.° 

Kentuck (147), McPherson Co., K 
P. sp.°, P. llanensis° 

Wathena (148), Doniphan Co., K 


Po sp. 

Courtland Canal (151), Jewell Co., K 
P. sp.° 

Nash (134), Meade Co., A, >1.2, <1.9 m.y.b.p. 
P. sp.° 


Kentucky 


Welsh Cave (205), Woodford Co., W 
P. pinetorum and/or P. ochrogaster, M. pennsylvanicus, M. xanthognathust 


Maryland 


Cavetown (223), Washington Co., W 
M. pennsylvanicus 
Cumberland Cave (222), Allegany Co., L.K. 


P. guilday®, P. cumberlandensis°, P. involutus’, M. paroperarius® 


Mexico 


Unnamed (86), Chihuahua, W 
M. pennsylvanicus* 

San Josecito (85), Nuevo Leon, W 
M. mexicanus 

El Tajo de Tequixquiac (84), Mexico, W 
P. meadensis° 


Michigan 
Sleeping Bear Dune (208), Leelanau Co., H, 730 + 250 B.P. 


P. pinetorum, P. ochrogaster+, M. pennsylvanicus 
Adams (209), Livingston Co., W 
M. pennsylvanicus 


Missouri 


Brynjulfson Cave #2 (165), Boone Co., H, 1,400 + 200 to 2,260 + 230 B.P. 
P. pinetorum and/or P. ochrogaster, M. pennsylvanicust 

Brynjulfson Cave #1 (166), Boone Co., H/W, 9,440 + 760 to 34,000 + 2,100 B.P. 
P. pinetorum and/or P. ochrogaster, M. pennsylvanicust 

Crankshaft Cave (167), Jefferson Co., H/W 
P. pinetorum and/or P. ochrogaster, M. pennsylvanicus* 

Boney Spring (169), Benton Co., W, 13,700 + 600 to 16,580 + 220 B.P. 
P. pinetorum and/or P. ochrogaster, M. pennsylvanicus* 

Herculaneum (168), Jefferson Co., W 
P. ochrogaster 

Zoo Cave (171), Taney Co., W 
P. pinetorum and/or P. ochrogaster, M. pennsylvanicus* 


Fossil Record 


Bat Cave (170), Pulaski Co., W 
P. pinetorum? and/or P. ochrogaster, M. pennsylvanicus+, M. xanthognathust 


Montana 


Warm Springs #1 (19), Silver Bow Co., H/W 
M. pennsylvanicus, M. richardsoni 


Nebraska 


Unnamed (155), Buffalo Co., W/S 
M. sp.* 
Angus (153), Nuckolls Co., I 
P. ochrogaster, M. pennsylvanicus 
Hay Springs (159), Sheridan Co., I 
M. pennsylvanicust 
Mullen II (158), Cherry Co., I 
P. pinetorum* and/or P. ochrogaster, M. pennsylvanicus 
Mullen I (157), Cherry Co., K 
M. paroperarius° 
Unnamed (156), Valley Co., K 
M. paroperarius° 
Sappa (154), Harlan Co., K, =1.2 m.y.b.p. 
P. sp.° 


Nevada 
Tule Springs E, (45), Clark Co., W 


M. californicus* 

Tule Springs B, (46), Clark Co., W 
M. sp. 

Glendale (47), Clark Co., W 
M. californicus+ or M. montanust 


New Mexico 


The Khulo (80), Dona Ana Co., H 
M. pennsylvanicus* 
Howells Ridge Cave (82), Grant Co., H/W 
P. ochrogaster*, M. pennsylvanicus+, M. mexicanust, M. montanust 
Anthony Cave (77), Dona Ana Co., H/W 
M. pennsylvanicus+, M. mexicanus*+, M. montanus* 
Conkling Cavern (78), Dona Ana Co., H/W 
M. mexicanus* 
Shelter Cave (79), Dona Ana Co., H/W 
M. montanus* 
Burnet Cave (74), Eddy Co., H/W 
M. mexicanus*, M. longicaudus* 
Brown Sand Wedge (72), Roosevelt Co., W, 11,170 + 360 B.P. 
P. ochrogaster*, M. pennsylvanicust, M. mexicanus+ 
Dry Cave (73), Eddy Co., W, 10,730 + 150 to 33,590 + 1,150 B.P. 
P. ochrogaster, M. mexicanus, M. longicaudus+ 
Muskox Cave (75), Eddy Co., W 


P. ochrogaster*, M. pennsylvanicus+, M. mexicanust 


43 


44 Zakrzewski 


Dark Canyon Cave (76), Eddy Co., W 
M. sp.* 

Isleta Cave #1 (71), Bernalillo Co., W 
M. pennsylvanicus* 

Palomas Creek Cave (81), Sierra Co., W 
M. sp.* 

Baldy Peak Cave (83), Luna Co., W 
M. sp.* 


New York 


Dutchess Quarry Cave (229), Orange Co., W, 12,530 + 370 B.P. 
P. pinetorum, M. pennsylvanicus 


Ohio 


Carter (210), Darke Co., W, 10,230 + 150 B.P. 
M. pennsylvanicus 


Oklahoma 
Domebo (121), Caddo Co., W, 11,200 + 500 B.P. 


P. pinetorum, P. ochrogaster 
Bar M #1 (122), Harper Co., W, 21,360 + 1,250 B.P. 
M. pennsylvanicus* 
Doby Springs (123), Harper Co., I 
M. pennsylvanicus* 
Berends (124), Beaver Co., I 
P. ochrogaster, M. pennsylvanicus* 


Oregon 
Fossil Lake (26), Lake Co., W 


M. montanus 


Pennsylvania 


New Paris #4 (224), Bedford Co., H/W, 9,540 to 11,300 + B.P. 
P. pinetorum, M. pennsylvanicus, M. chrotorrhinus*, M. xanthognathus* 
Hollidaysburg Fissure (225), Blair Co., H/W, 10,000 to 12,000 B.P. 
P. pinetorum, M. pennsylvanicus, M. chrotorrhinus* 
Bootlegger Sink (227), York Co., W, 11,550 + 100 B.P. 
P. pinetorum, M. pennsylvanicus, M. chrotorrhinus*, M. xanthognathus* 
Frankstown Cave (226), Blair Co., W 
M. pennsylvanicus 
Port Kennedy Cave (228), Montgomery Co., Y 
P. involutus?/*, P. dideltus?/*, M. speothen®/"4 
Hanover Quarry Fissure (235), Adams Co., A 
P. guildayi°, P. cumberlandensis°, M. paroperarius® 


Québec 


Caverne de St. Elzéar (230), Bonaventure Co., H, 5,110 + 150 B.P. 
M. pennsylvanicus, M. chrotorrhinus, M. xanthognathus* 


Fossil Record 45 


Saskatchewan 


Riddell (12), Saskatoon District, W 
M. pennsylvanicus, M. sp. 

Wellsch Valley (13), Swift Current-S. Saskatchewan Upland, A, 1.75-10° 
P. sp.°, M. paroperarius° 


South Dakota 


Java (160), Walworth Co., K 
P. sp.° 


Tennessee 


First American Bank Site (204), Davidson Co., H/W, 9,410 to 10,034+ B.P. 
P. pinetorum and/or P. ochrogaster 
Baker Bluff (200), Sullivan Co., W, 10,560 + 220 to 19,100 + 850 B.P. 
P. pinetorum and/or P. ochrogaster+, M. pennsylvanicus, M. chrotorrhinust, M. xan- 
thognathus* 
Guy Wilson (201), Sullivan Co., W, 19,700 + 600 B.P. 
M. pennsylvanicus 
Carrier Quarry Cave (199), Sullivan Co., W 
P. pinetorum and/or P. ochrogaster, M. pennsylvanicus, M. chrotorrhinus* 
Robinson Cave (202), Overton Co., W 
P. pinetorum, M. pennsylvanicus 
Cheek Bend Cave (203), Maury Co., W 
P. ochrogaster, M. pennsylvanicus, M. xanthognathus* 
Beartown Cave (237), Sullivan Co., W 
M. cf. M. pennsylvanicus 


Texas 


Kyle Site (108), Hill Co., H, 389 + 130 to 1,389 + 150 B.P. 
P. pinetorum* and/or P. ochrogaster* 

Blue Spring Shelter (232), Randall Co., H, 840 to 1,135 B.P. 
P. pinetorum* and/or P. ochrogaster* 

Barton Springs Road (103), Travis Co., H, 1,015 + 105 to 3,450 + 150 B.P. 
P. pinetorum* and/or P. ochrogaster* 

Deadman Shelter (233), Swisher Co., H, 1,240 to 1,485 B.P. 
P. pinetorum* and/or P. ochrogaster* 

Canyon Country Club Cave (234), Randall Co., H, 1,270-1,650 B.P. 
P. pinetorum* and/or P. ochrogaster* 

Miller’s Cave (106), Llano Co., H/LW, 3,008 + 310 to 7,290+ B.P. 
P. pinetorum* and/or P. ochrogaster* 

Klein Cave (99), Kerr Co., H, 7,683 + 643 B.P. 
P. pinetorum, M. pennsylvanicus* 

Felton Cave (101), Sutton Co., H, 7,700 + 130 B.P. 
P. pinetorum* and/or P. ochrogaster* 

Schulze Cave (100), Edwards Co., H/LW, 9,310 + 310 to 9,680 + 700 B.P. 
P. pinetorum* and/or P. ochrogaster* 

Ben Franklin (110), Delta Co., H/LW, 9,550 + 375 to 11,135 + 450 B.P. 
P. pinetorum* and/or P. ochrogastert, M. pennsylvanicus* 

Lubbock Lake (114), Lubbock Co., H/LW, 9,883 + 350 to 12,650 + 350 B.P. 
P. pinetorum* and/or P. ochrogaster* 


46 Zakrzewski 


Levi Shelter (102), Travis Co., H/LW, =10,000 B.P. 
P. pinetorum* and/or P. ochrogaster* 
Cooper Reservoir (109), Delta and Hopkins cos., H/W 
P. pinetorum* and/or P. ochrogaster* 
Huecos Tanks #1 (88), El Paso Co., H/W 
M. sp.t 
Navar Ranch #13 (89), El Paso Co., H/W 
M. montanus* 
Longhorn (105), Burnet Co., H/W 
P. pinetorum* and/or P. ochrogaster* 
Cave Without A Name (98), Kendall Co., W, 10,900 + 190 B.P. 
P. pinetorum?* and/or P. ochrogaster*, M. pennsylvanicus* 
Howard Ranch (119) = Grosebeck Creek, Hardeman Co., W, 16,775 + 565 B.P. 
P. pinetorum and/or P. ochrogaster*+, M. pennsylvanicust 
Clear Creek (113), Denton Co., W, 28,840 + 4,740 B.P. 
P. pinetorum and/or P. ochrogaster* 
Tank Trap Wash #1 (87), El Paso Co., W, >33,000 B.P. 
M. sp.* 
Dust Cave (90), Culberson Co., W 
M. sp.* 
Rattlesnake Cave (94), Kinney Co., W 
P. pinetorum* and/or P. ochrogaster* 
Montell Cave (95), Uvalde Co., W 
P. pinetorum* and/or P. ochrogaster* 
Zesch Cave (107), Mason Co., W 
P. pinetorum* and/or P. ochrogaster* 
Upper Sloth Cave (91), Culberson Co., W 
M. mexicanus 
Lower Sloth Cave (92), Culberson Co., W 
M. mexicanus 
Pratt Cave (93), Culberson Co., W 
M. mexicanust 
Quitaque (120), Motley Co., W 
P. pinetorum* and/or P. ochrogaster+, M. pennsylvanicus* 
Friesenhahn (96), Bexar Co., W 
P. pinetorum* and/or P. ochrogaster* 
Moore Pit (111), Dallas and Denton cos., W 
P. pinetorum* and/or P. ochrogaster* 
Coppell (112), Dallas and Denton cos., W 
P. pinetorum* and/or P. ochrogaster* 
Sims Bayou (97), Harris Co., W 
P. ochrogaster 
Easely Ranch (116), Foard Co., S 
P. pinetorum* and/or P. ochrogaster*, M. pennsylvanicus* 
Monument (117), Foard Co., S 
P. pinetorum* and/or P. ochrogaster*, M. pennsylvanicus* 
Smith Ranch (118), Foard Co., S 
P. pinetorum* and/or P. ochrogaster* 
South Fish Creek (231), Cooke Co.,-S 
P. pinetorum* and/or P. ochrogaster* 
Vera (115), Knox Co., K 
P. llanensis°, M. paroperarius? 
Fyllan Cave (104), Travis Co., K 
P. sp.° 


Fossil Record 


Utah 


Crystal Ball Cave (54), Millard Co., W 
M. sp. 

Silver Creek (56), Summit Co., W/S, >40,000 B.P. 
M. montanus 

Snowville (55), Box Elder Co., K 


M. montanus 


Virginia 


Strait Canyon (220), Highland Co., W, 29,870 + 1,800-1,400 B.P. 
M. pennsylvanicus 
Loop Creek Quarry Cave (215), Russell Co., W 
M. xanthognathus* 
Gillespie Cliff Cave (216), Tazwell Co., W 
M. xanthognathust 
Early’s Pits (217), Wythe Co., W 
M. pennsylvanicus 
Back Creek #2 (218), Bath Co., W 
M. pennsylvanicus, M. chrotorrhinus+, M. xanthognathus* 
Clark’s Cave (219), Bath Co., W 
P. pinetorum, M. pennsylvanicus, M. chrotorrhinus*, M. xanthognathus* 
Natural Chimneys (221), Augusta Co., W 
P. pinetorum, M. pennsylvanicus, M. chrotorrhinus+, M. xanthognathus* 


West Virginia 


Eagle Rock Cave (211), Pendleton Co., W 
P. pinetorum, M. pennsylvanicus, M. chrotorrhinus, M. xanthognathus+ 
Hoffman School Cave (212), Pendleton Co., W 
P. pinetorum, M. pennsylvanicus, M. chrotorrhinus 
Mandy Walters Cave (213), Pendleton Co., W 
P. pinetorum, M. pennsylvanicus, M. chrotorrhinus 
Upper Trout Cave (214), Pendleton Co., W 
P. pinetorum, M. pennsylvanicus, M. chrotorrhinus 


Wisconsin 


Moscow Fissure (241), Iowa Co., 17,050 + 1,500 B.P. 
P. cf. P. ochrogaster, M. pennsylvanicus, M. xanthognathus* 


Wyoming 


Bush Shelter (57), Washakie Co., H, 9,000 B.P. 
M. pennsylvanicus* 
Little Canyon Creek Cave (58), Washakie Co., H/W, 10,170 B.P. 
M. pennsylvanicust, M. montanus 
Agate Basin (62), Niobrara Co., H/W, 10,430 to 11,450 B.P. 
M. pennsylvanicus*, M. longicaudus* 
Bell Cave (64), Albany Co., H/W, 12,240 B.P. 
P. ochrogaster, M. pennsylvanicus+, M. montanus 
Prospects Shelter (59), Bighorn Co., H/W, 10,000 to 27,000 B.P. 
P. ochrogaster, M. pennsylvanicus+, M. montanus, M. xanthognathus* 


47 


48 Zakrzewski 


Natural Trap Cave (60), Bighorn Co., H/W, 12,000 to 20,000 B.P. 
P. ochrogaster, M. pennsylvanicust, M. montanus 

Sheaman Site (61), Niobrara Co., W 
M. pennsylvanicus* 

Little Box Elder Cave (63), Converse Co., W 
P. ochrogaster, M. pennsylvanicust, M. montanus, M. longicaudus 


Yukon Territories 


Bluefish Cave I (11), Bluefish-Porcupine Upland, H/W, 12,900 + 100 B.P. 
M. miurus*, M. oeconomus, M. xanthognathus 

Old Crow River Loc. 12 (9), Old Crow Basin, W 
M. miurus*, M. pennsylvanicus, M. xanthognathus 

Old Crow River Loc. 44 (6), Old Crow Basin, S?, >54,000 B.P. 
M. xanthognathus 

Old Crow River Loc. 11 (10), Old Crow Basin, S? 
M. muiurus*, M. oeconomus, cf. M. xanthognathus 

Old Crow River Loc. 12 (8), Old Crow Basin, I 
M. muiurus*, M. oeconomus, M. xanthognathus 

Old Crow River Loc. 14N (7), Old Crow Basin, ?age 


M. miurus* 


Appendix B. Localities Containing Pitymys 
pinetorum, P. ochrogaster, and Microtus 
pennsylvanicus 


P. pinetorum 


Arkansas Haile XIB (196) 
Peccary Cave (172) Ichetucknee River (197) 
Florida Georgia 
Warm Mineral Springs (174) Ladds (198) 
Vero 2 (176) Illinois 
Vero 3 (177) Meyer Cave (206) 
Kendrick IA (179) Iowa 


Reddick IA (180) 
Reddick IB (181) 
Reddick IC (182) 
Reddick ID (183) 
Reddick IIC (184) 
Mefford I (185) 
Devil’s Den (186) 
Waccasassa IIB (187) 
Arrendondo I (190) 
Arrendondo II (192) 
Arrendondo IIA (193) 
Arrendondo IIB (194) 
Arrendondo IIC (195) 


Brayton (162) 

Waubonsie?*t (164) 
Kentucky 

Welsh Cave? (205) 
Michigan 

Sleeping Bear Dune (208) 
Missouri 

Brynjulfson Cave #2? (165) 

Brynjulfson Cave #1? (166) 

Crankshaft Cave? (167) 

Boney Spring? (169) 

Bat Cave? (170) 

Zoo Cave? (171) 


Fossil Record 49 


Nebraska Miller’s Cave?* (106) 
Mullen II?+ (158) Zesch Cave?* (107) 
New York Kyle Site?* (108) 
Dutchess Quarry Cave (229) Cooper Reservoir?* (109) 
Oklahoma Ben Franklin? (110) 
Domebo (121) Moore Pit? (111) 
Pennsylvania Coppell ?* (112) 
New Paris #4 (224) Clear Creek? (113) 
Hollidaysburg Fissure (225) Lubbock Lake?* (114) 
Bootlegger Sink (227) Easely Ranch?* (116) 
‘Tennessee Monument?*t (117) 
Carrier Quarry Cave? (199) Smith Ranch?t (118) 
Baker Bluff? (200) Howard Ranch? (119) 
Robinson Cave (202) Quitaque?* (120) 

First American Bank Site? (204) South Fish Creek?* (231) 
Texas Blue Spring Shelter ?* (232) 
Rattlesnake Cave?* (94) Deadman Shelter?* (233) 
Montell Cave?* (95) Canyon Country Club Cave?* (234) 

Friesenhahn? (96) Virginia 

Cave Without A Name?*t (98) Clark’s Cave (219) 

Klein Cave (99) Natural Chimneys (221) 
Schulze Cave?* (100) West Virginia 

Felton Cave?* (101) Eagle Rock Cave (211) 
Levi Shelter?* (102) Hoffman School Cave (212) 
Barton Springs Road?* (103) Mandy Walters Cave (213) 
Longhorn ?* (105) Upper Trout Cave (214) 


P. ochrogaster 


Arkansas Michigan 
Peccary Cavet (172) Sleeping Bear Dune (208) 
Colorado Missouri 
Dutton (66) Brynjulfson Cave #2? (165) 
Mesa de Maya (68) Brynjulfson Cave #1? (166) 
Indiana Crankshaft Cave? (167) 
Harrodsburg Crevice (207) Herculaneum (168) 
Iowa Boney Spring? (169) 
Waubonsie? (164) Bat Cave? (170) 
Kansas Zoo Cave? (171) 
Robert (125) Nebraska 
Jones (126) Angus (153) 
Jinglebob (127) Mullen II? (158) 
Cragin Quarry (128) New Mexico 
Mt. Scott (129) Brown Sand Wedge* (72) 
Butler Spring (130) Dry Cave (73) 
Trapshoot (138) Muskox Cave* (76) 
Duck Creek (139) Howells Ridge Cave* (82) 
Rezabek (141) Oklahoma 
Williams (145) Domebo (121) 
Sandahl (146) Berends (124) 
Kentucky Tennessee 


Welsh Cave? (205) Carrier Quarry Cave? (199) 


50 Zakrzewski 


Baker Bluff? (200) 
Cheek Bend Cave (203) 
First American Bank Site? (204) 


Texas 


Rattlesnake Cave?* (94) 
Montell Cave?* (95) 

Sims Bayou (97) 

Cave Without A Name?* (98) 
Schulze Cave?* (100) 

Felton Cave?* (101) 

Levi Shelter?* (102) 

Barton Springs Road?* (103) 
Longhorn?* (105) 

Miller’s Cave?+ (106) 

Zesch Cave?* (107) 

Kyle Site?* (108) 

Cooper Reservoir?* (109) 
Ben Franklin?* (110) 

Moore Pit?* (111) 


Coppell ?* (112) 

Clear Creek ?* (113) 
Lubbock Lake?* (114) 
Easely Ranch?t (116) 
Monument?* (117) 
Smith Ranch?* (118) 
Howard Ranch?* (119) 
Quitaque?* (120) 

South Fish Creek ?*+ (231) 
Blue Spring Shelter ?* (232) 
Deadman Shelter?* (233) 


Canyon Country Club Cave?* (234) 


Wisconsin 
Moscow Fissure (241) 
Wyoming 
Prospects Shelter (59) 
Natural Trap Cave (60) 
Little Box Elder (63) 
Bell Cave (64) 


M. pennsylvanicus 


Alberta 


Hand Hills (16) 


Arkansas 


Peccary Cave* (172) 


Colorado 


Dutton (65) 


Florida 


Devil’s Den (186) 
Waccasassa IIB (187) 
Withlacoochee VIIA (188) 
Arrendondo I (190) 
Arrendondo IIB (194) 


Idaho 


American Falls? (24) 


Illinois 


Meyer Cavet (206) 


Iowa 


Brayton (162) 
Oakland (163) 
Waubonsie (164) 
Elkader (238) 
Eagle Point (239) 


Kansas 


Robert* (125) 

Jones* (126) 
Jinglebob* (127) 
Cragin Quarry* (128) 
Mt. Scottt (129) 
Butler Spring* (130) 
Adams* (131) 

Keiger Creek* (135) 
Unnamed? (136) 


Trapshoot* (138) 
Duck Creek* (139) 
Rezabekt (141) 
Kanopolis* (143) 
Williams* (145) 
Sandahl* (146) 
Unnamed (152) 
Kentucky 
Welsh Cave (205) 
Maryland 
Cavetown (223) 
Mexico 
Unnamed? (86) 
Michigan 
Sleeping Bear Dune (208) 
Adams (209) 
Missouri 
Brynjulfson Cave #2* (165) 
Brynjulfson Cave #1* (166) 
Crankshaft Cavet (167) 
Boney Spring* (169) 
Bat Cave* (170) 
Zoo Cavet (171) 
Montana 
Warm Springs #1 (19) 
Nebraska 
Angus (153) 
Mullen II (158) 
Hay Springs* (159) 
New Mexico 
Isleta Cave* (71) 
Brown Sand Wedge? (72) 


Muskox Cave* (75) 

Anthony Cave* (77) 

The Khulot (80) 

Howells Ridge Cave* (82) 
New York 

Dutchess Quarry Cave (229) 
Ohio 

Carter (210) 
Oklahoma 

Bar M #1* (122) 

Doby Springs* (123) 

Berends* (124) 
Pennsylvania 

New Paris #4 (224) 

Hollidaysburg Fissure (225) 

Frankstown Cave (226) 

Bootlegger Sink (227) 
Québec 

Caverne de St. Elzéar (230) 
Saskatchewan 

Riddell (12) 
Tennessee 

Carrier Quarry Cave (199) 

Baker Bluff (200) 

Guy Wilson (201) 

Robinson Cave (202) 

Cheek Bend Cave (203) 


First American Bank Site (204) 


Beartown (237) 

Texas 
Cave Without A Name+ (98) 
Klein Cavet (99) 


Fossil Record 


Ben Franklin* (110) 
Easely Ranch* (116) 
Monument? (117) 
Howard Ranch? (119) 
Quitaque* (120) 
Virginia 
Early’s Pits (217) 
Back Creek #2 (218) 
Clark’s Cave (219) 
Strait Canyon (220) 
Natural Chimneys (221) 
West Virginia 
Eagle Rock Cave (211) 
Hoffman School Cave (212) 
Mandy Walters Cave (213) 
Upper Trout Cave (214) 
Wisconsin 
Moscow Fissure (241) 
Wyoming 
Bush Shelter* (57) 
Little Canyon Creek* (58) 
Prospects Shelter* (59) 
Natural Trap Cave* (60) 
Sheaman Sitet (61) 
Agate Basint (62) 
Little Box Elder Cavet (63) 
Bell Cave* (64) 
Yukon Territories 
Old Crow River Loc. 12 (9) 


Symbol: *, taxon extinct locally. 


Dil 


TAXONOMY AND SYSTEMATICS 
SYDNEY ANDERSON 


Abstract 


Des Holarctic arvicoline or microtine rodents have long been 
recognized as a distinct group at the level of family or subfam- 
ily, and are here regarded as a subfamily of the Muridae. The 
genus with the most species is Microtus. 

The methods and results of major taxonomic works (Miller in 
1896, Bailey in 1900, and Hinton in 1926) are compared. The 
taxonomy of North American Microtus has passed through several 
historic phases relating to the availability of specimens, increases in 
knowledge, and changing taxonomic viewpoints. Prior to 1860 scat- 
tered explorations resulted in relatively small series of specimens 
and 34 supposed species were named. From 1860 to 1890 not much 
happened. The decade ending in 1900 was more productive than 
any other decade before or since. Most full species now recognized 
were known by the end of that decade, large series were collected, 
a polytypic concept of species developed, and the number of mono- 
typic species began to decline. From 1900 to 1920 the new trends 
continued but at a slower pace. From 1920 to 1950 was a period 
of further consolidation, the number of recognized species decreased 
rapidly as monotypic species became subspecies, and the number 
of subspecies increased rapidly as geographic variation became bet- 
ter known. The period of alpha taxonomy, which focused on the 
question of what are the species, matured from 1950 to 1980, so 
that the number of recognized species has approached an equilib- 
rium. 

However, if the task of taxonomy is considered to be the eluci- 
dation of relationships at all levels, the taxonomic work needed for 
an adequate understanding of the Arvicolinae lies mostly in the 
future. 

Many natural groups are clustered in ways that give “hollow 
curve” frequency distributions. For example, within the genus M- 
crotus, the subgenus Microtus includes about half of the 25 or so 
North American species and the other half are scattered among six 


By 


Taxonomy and Systematics 53 


other subgenera. The results of the “‘artichoke method” are evident 
in Microtus taxonomy as in that of most other groups. No attempt 
has ever been made to apply numerical taxonomy or contemporary 
cladistic methods to the study of Muicrotus. What we have is an 
eclectic mixture of methods and results. I argue that this is not 
necessarily bad, but that since there is little agreement on systematic 
methods, it is important that authors explain their assumptions and 
procedures as well as presenting data and taxonomic results. 


Introduction 


In this chapter the taxonomic context of arvicoline or microtine 
rodents is presented and the close connection of Old World and 
New World arvicoline faunas is noted, then the history of the clas- 
sification of these rodents at the generic level is summarized, and 
the classification of New World Microtus at the species level is 
reviewed. Finally, some systematic methods are discussed with the 
objective of clarifying what has been done and suggesting needs for 
future work. 

The genus Microtus consists of several dozen species of ‘‘micro- 
tine” or “arvicoline” rodents belonging to the family Arvicolidae or 
subfamily Arvicolinae (within Muridae or Cricetidae). The context 
of the group within the Class Mammalia (as outlined by Simpson, 
1945) is: 


Class Mammalia Linnaeus, 1758 
Subclass Theria Parker and Haswell, 1897 
Infraclass Eutheria Gill, 1872 
Order Rodentia Bowdich, 1821 


The rodents are the most successful order of living mammals as 
measured by numbers of species and individuals. Rodents are gen- 
erally recognized as a monophyletic group based on peculiarities of 
teeth and skulls related to gnawing. Convergent similarities occur 
in other orders, such as the Primates and Marsupialia. Because of 
other characters, however, there is little doubt that the aye-aye is a 
primate or that a wombat is a marsupial. The Rodentia originated 
very early in mammalian evolution and there is no clear evidence 
for the precise relationship of Rodentia among other orders of 
Mammalia. This is one of the major unresolved problems in mam- 
malian taxonomy. 


54 Anderson 


Suborder Myomorpha Brandt, 1855 
Superfamily Muroidea Miller and Gidley, 1918 


Carleton (1980) reviewed the history of major classifications of 
muroid rodents at the familial level. The arvicolines or microtines 
have been treated at various times as both a family and a subfamily. 
Chaline et al. (1977) recognized the family Arvicolidae. Carleton 
and Musser (1984) recognized the subfamily Arvicolinae within 
the family Muridae. The level as such (subfamily vs. family) is not 
so important as are the hypotheses of relationships. More explicit 
diagrams of relationship and more explicit statements of characters 
and rationale for each branching point and lineage are needed. 


Family Muridae Gray, 1821 
Subfamily Arvicolinae Gray, 1821 


The lemmings and voles, the major groups in Arvicolinae, were 
thought by Hinton (1926) to have been derived separately from the 
Murinae. Repenning (1968) analyzed the earliest arvicolines (Plio- 
cene forms not known to Hinton) and likewise noted a possibility 
of polyphyly, as derivatives of Cricetidae. Martin (1979) analyzed 
fossil North American arvicolines and implied polyphyly by stress- 
ing independent developments of various arvicoline dental special- 
izations in different lines and by a drawing showing 16 unconnected 
lineages, thus avoiding the question of relationships. Martin argued 
that, because of the rapidity of changes and similar changes in 
different lines, arvicolines are useful in biostratigraphy in spite of 
uncertainty about details of phylogenetic connections. 

The systematic relationships of both living and fossil North 
American arvicolines in general and the genus Microtus in particular 
involve Old World groups as well as North American groups. The 
following living groups in North America presumably have their 
nearest relatives in Eurasia rather than in North America, and 
perhaps other groups within North American Microtus also do: 


Dicrostonyx torquatus, Lemmus sibiricus, and Clethrionomys rutilis 
inhabit both continents. 

Lagurus curtatus is related to Lagurus lagurus and L. luteus of the 
Old World. 

Microtus miurus and the insular form M. abbreviatus are related to 
M. gregalis of the Old World. All are placed in the subgenus 
Stenocrantus. 

If the subgenus Pitymys is monophyletic, then the New World species 


Taxonomy and Systematics 5 


are related to the Old World species of Pitymys more closely 
than to other New World Microtus. 
Microtus richardsont has been placed in the subgenus Arvicola which 
allies it with Old World species of that subgenus. 
Microtus pennsylvanicus and its close insular relatives in North 
America have been allied with Microtus agrestis of the Old 
World on the basis of a posterior loop on m2. 

Microtus chrotorrhinus has a giant chromosome that suggests a pos- 
sible relationship with Microtus agrestis (Kirkland and Jan- 
nett, 1982). 

Microtus longicaudus and its insular near relative Microtus coro- 
narius have some similarities with the Old World subgenus 
Chionomys. 


Some of these affinities are generally agreed upon, some are very 
tentative hypotheses, and some are controversial. For example, the 
teeth of Microtus richardsoni are more complex than those of the 
Old World species of Arvicola and this leads some paleontologists, 
whose attention is focused on dental traits, to reject the hypothesis 
of monophyly and consider resemblences in other features as con- 
vergences. There is considerable uncertainty about the affinities of 
species of Pitymys, Neodon, and Pedomys, with each other and with 
other species of Microtus. This is good, because it indicates that 
people are reexamining and refining the classification. Much re- 
mains to be done. 


History of Systematics at the Generic Level 


The pivotal study in the systematics of arvicoline rodents at the 
generic level is Miller’s (1896) revision. It is pivotal in the sense 
that no comparably comprehensive study had been done earlier or 
has been done since. In general, prior studies were more limited in 
scope, geographically, taxonomically, or in characters considered. 
Miller considered all arvicolines, both Old World and New World, 
and reviewed and attempted to synthesize all relevant characters. 

The content of the genus Microtus as recognized by Miller (1896) 
was greater than that of most later authors. ‘There has been a 
tendency to elevate Miller’s subgenera to genera. The “essential 
characters” of the genus Microtus (Miller, 1896:44) were consid- 
ered to be as follows. 

1) “Upper incisors without grooves.” Such grooves normally oc- 


56 Anderson 


cur in Synaptomys and Promethiomys and may appear as infrequent 
variants in individuals of other genera including Microtus. 

2) ‘Lower incisors with roots [partly] on outer side of molar 
roots.” Posteriorly, the incisor root passed from the lingual side to 
the labial side of the molar roots between the second and third 
molars. This is the general condition among voles. In the lemmings 
Synaptomys, Myopus, Lemmus, and Dicrostonyx, the root of the in- 
cisor lies medial to the roots of all three lower molars. 

3) ‘“Molars rootless.”” Among the lemmings, this condition of 
persistent growth occurs in all four genera. Among the living New 
World voles, it occurs only in Microtus (as treated by Miller, in- 
cluding Lagurus and Neofiber), not in Phenacomys (including Ar- 
borimus), Clethrionomys (then called Evotomys), or Ondatra (then 
called Fiber). Persistent growth is the final stage in the development 
of hypsodonty, which is found in varying degrees in all Arvicolinae. 

4) “Enamel pattern characterized by approximate equality of 
reentrant angles.” This differs from the condition of the lower mo- 
lars in Phenacomys which have much deeper inner reentrant angles 
than outer reentrant angles. Inequality of depth of angles occurs 
also in the upper molars of Synaptomys, Myopus, and Lemmus, 
which have deeper outer reentrant angles than inner ones, and to 
a lesser degree also in their lower molars, which have deeper inner 
angles. 

5) “First lower molar usually with five closed or nearly closed 
triangles.” Within Microtus the fourth and fifth triangles of m1 are 
confluent rather than closed in subgenera Pitymys, Pedomys, and 
Neodon. This differs from the conditions in lemmings, among which 
Synaptomys, Myopus, and Lemmus have three closed triangles and 
two transverse loops, or four transverse loops and no closed trian- 
gles, and Dicrostonyx has seven closed triangles and two transverse 
loops. 

6) “Upper third molar with one, two, or three closed triangles.” 
Phenacomys has two or three, Clethrionomys has three, Dicrostonyx 
has three or four and two transverse loops, and Synaptomys, My- 
opus, and Lemmus have four transverse loops and no closed trian- 
gles. 

7) ‘Tail nearly always longer than hind foot, terete.” The tail is 
shorter than the hindfoot in Lemmus, Myopus, and Dicrostonyx (and 
in Asiatic Lagurus among Miller’s Microtus). The tail is somewhat 
flattened laterally in Ondatra. 

8) “Feet, fur, eyes, and ears very variable.” All of the other 


Taxonomy and Systematics 57 


genera (about 18) of arvicolines combined contain fewer species 
(about 60) than Muicrotus (about 68; Honacki et al., 1982) and 
exhibit less variation within any one genus in these features. The 
hindfeet of Ondatra are modified for aquatic locomotion and the 
feet of the arctic lemmings, Lemmus and Dicrostonyx, have pecu- 
liarities not seen in Microtus. 

9) “Thumb never with a well-developed ligulate nail.” A nail of 
this sort is present in Lemmus. 

Names of genera and subgenera that have been used for living 
North American species of Microtus at one time or another, and 
that are synonyms by virtue of the fact that their type species belong 
to Microtus, in Miller’s (1896) broadest sense, are as follows. 


Microtus Schrank, 1798, type species Microtus terrestris of Schrank, 
a synonym of Mus arvalis Pallas, now Microtus arvalis, of 
the Old World, and not Mus terrestris of Linnaeus. Miller 
(1896) initiated the wide use of the name Microtus. Prior 
to 1896 Arvicola was used. Microtus is the central genus 
and subgenus in the complex, and the group with the most 
species. 

Arvicola Lacépéde, 1799, type species Mus amphibius Linnaeus, a 
synonym of Microtus terrestris (Linnaeus). The American 
species Microtus richardson has been referred to Arvicola in 
the narrower subgeneric sense by some authors, although 
this referral is not universally accepted. Arvicola includes 
two Old World species. 

Mynomes Rafinesque, 1817, type species Mynomes pratensis Rafi- 
nesque, a synonym of Mus pennsylvanicus Ord, now Mi- 
crotus pennsylvanicus. 

Psammomys LeConte, 1830, type species Psammomys pinetorum 
LeConte, now Mucrotus pinetorum, not Psammomys 
Cretzschmar, 1828, which is a gerbil. 

Pitymys McMurtrie, 1831, type species Psammomys pinetorum 
LeConte. 

Ammomys Bonaparte, 1831, type species Psammomys pinetorum 
LeConte, hence an objective synonym of Pitymys Mc- 
Murtrie. 

Lagurus Gloger, 1841, type species Mus lagurus Pallas, now treated 
as Lagurus lagurus; the genus includes the American species 
Lagurus curtatus. 


58 Anderson 


Pedomys Baird, 1857, type species Arvicola austerus LeConte, now 
a subspecies of Microtus ochrogaster. 

Chilotus Baird, 1857, type species Arvicola oregoni Bachman, now 
Microtus oregont. 

Neofiber ‘True, 1884, type species Neofiber alleni True, now sepa- 
rated from Microtus. 

Aulacomys Rhoads, 1894, type species Aulacomys arvicoloides Rhoads, 
now a subspecies of Microtus richardsont. 

Tetramerodon Rhoads, 1894, type species Arvicola tetramerus Rhoads, 
now a subspecies of Microtus townsendit. 

Orthromys Merriam, 1898, type species Microtus umbrosus Mer- 
riam, proposed as subgenus, later used as genus. 

Herpetomys Merriam, 1898, type species Microtus guatemalensis 
Merriam, proposed as subgenus, later used as genus. 

Stenocranius Kastschenko, 1901, type species Arvicola slowzowi Po- 
liakoff, a synonym of Mus gregalis Pallas, now Muicrotus 
gregalis; valid as a subgenus including Microtus miurus and 
M. abbreviatus of the New World. 

Chionomys Miller, 1908, type species Arvicola nivalis Marins, now 
Mictotus nivalis, Old World; Microtus longicaudus was re- 
ferred to this subgenus by Anderson (1960) but this has 
been generally ignored. 

Lemmiscus Thomas, 1912, type species Arvicola curtata Cope, now 
Lagurus curtatus. 

Sumeriomys Argyropulo, 1933, type species Mus socialis Pallas, now 
Maicrotus socialis; cited here because of its involvement with 
Suranomys; the name Sumeriomys has not been specifically 
applied to any New World Microtus. 

Suranomys Chaline, 1972, p. 142, type species Microtus male: Hin- 
ton, a Pleistocene species. Microtus ratticeps, M. nivalis, M. 
gud, and M. roberti were also assigned to the subgenus. 
Later, M. operarius, M. oeconomus, M. socialis, and M. or- 
egont were also assigned (Chaline, 1974). The type species 
of Chilotus, Chionomys, and Sumeriomys were all assigned 
to Suranomys and all are older names than Suranomys. The 
oldest is Chilotus. 

Arvalomys Chaline, 1974, type species by original designation (Cha- 
line, 1974:450) Microtus arvalis. Arvalomys included Old 
and New World species generally referred to the subgenus 
Microtus and has the same type species as Microtus. Arva- 


Taxonomy and Systematics 59 


lomys is therefore an objective junior synonym of Microtus 
as a subgenus. 


References above that are not included in the Literature Cited 
section may be found in Hall (1981) or Miller (1896). 

In 1912, Miller treated Pitymys and Arvicola as genera separate 
from Microtus in his book on the mammals of western Europe. He 
characterized Microtus as “restricted to the species with normal 
skull, palate, and enamel folding, 8 mammae, 6 plantar tubercles, 
and no special modifications of external form” (p. 659). In the 
“essential characters” of the subgenus Microtus in 1896, Miller also 
had given the following: third lower molar (m3) without closed 
triangles; first lower molar (m1) with five closed triangles and nine 
salient angles; third upper molars (M3) with three closed triangles 
and seven or eight salient angles; sole moderately hairy (contrasting 
with naked in Neofiber, nearly naked in Arvicola, thickly haired 
between heel and tubercles in Pedomys, hairy in Lothenomys, Alti- 
cola, and Hyperacrius, and very hairy in Lagurus and Phaiomys); 
and claws of hindfeet longest (those of forefeet longest in Pitymys, 
very long and about equal on all four feet in Phaiomys). 

In 1926, Hinton published the first volume of a planned two 
volume monograph on the Microtinae (=Arvicolinae as used here). 
The second volume, which would have included Microtus, was nev- 
er published, but the first volume is of interest here for several 
reasons. Repenning (1968) evaluated it as “the most significant 
single contribution to the development of an understanding of the 
evolution of these rodents.” In it the Old World species of Arvicola 
were treated as a distinct genus. Microtus richardsoni of the New 
World was excluded from Arvicola. All of the subgenera recognized 
by Miller in 1896 were raised to genera. The Old World genus 
Ellobius was assigned to the Microtinae. The resemblence of the 
Malagasy genus Brachytarsomys to microtines was described. Hin- 
ton recognized 31 genera and subgenera (including fossil forms) in 
the subfamily. 

The concept of arvicoline rodents as a distinct subfamily origi- 
nated much earlier (Coues, 77 Coues and Allen, 1877; Gray, 1821). 
Hinton (1926:2) related the distinctive features of the microtines to 
diet and burrowing habit. Included as “general characters” (p. 5) 
were the following: 1) robust or thickset build; 2) head broad and 
flattened; 3) muzzle bluntly rounded; 4) eyes small; 5) ears small; 


60 Anderson 


6) skin of trunk largely enclosing moderately long and powerful 
limbs (this contributes to character 1); 7) pentadactyl, but thumb 
reduced in size; 8) tail never very long, reaching two-thirds of the 
length of head and body; 9) fur tending to be soft and dense; 10) 
skull of firm construction (in some cases massive); 11) sagittal su- 
tures between paired frontal, premaxillary, maxillary, and palatine 
bones generally fusing early (before or just after birth); 12) rostrum 
short; 13) eyes forward of vertical plane touching the front edges 
of the anterior molars; 14) zygomatic arches strongly built and more 
or less widely bowed laterally, zygomatic plate stout and obliquely 
oriented to long axis of skull; 15) palatine processes of maxillary 
and palatine bones enormously thickened, in correlation with hyp- 
sodonty of molars and powerful development of the jaw muscula- 
ture; 16) auditory bullae well developed; 17) mandible stout, in 
correlation with the hypsodonty and muscular development noted 
under 15; 18) cheekteeth hypsodont; and 19) worn surfaces of 
cheekteeth displaying a pattern of triangles and transverse loops, 
produced by the truncation by wear of the ends of tall prismatic 
columns. 

The above list is abstracted from detailed discussions of these and 
many related features. Diagnostic characters are here mingled with 
characters that are not peculiar to the subfamily (in the current 
terminology, synapomorphies are mingled with plesiomorphies). 
Hinton was quite aware of the difference between the concepts of 
apomorphy and plesiomorphy (but not the newer words, of course) 
and his discussion of evolution provides many interesting ideas about 
evolutionary changes in the group. On page 26 he summarized the 
most prominent characters that “sharply define” the subfamily as: 
the firm construction of the skull, shortened rostrum, forwardly 
placed orbits, peculiarly formed zygomatic plates, presence of post- 
orbital squamosal crests or processes, the thickened palatal process 
of the maxillaries and palatines, and the hypsodont prismatic cheek- 
teeth. 

Although Hinton (1926) did not draw an explicit diagram of 
phylogenetic relationships of microtine rodents he did discuss them 
in sufficient detail that such a diagram can be drawn, and I have 
done so (Fig. 1). The broader scope of the entire subfamily repre- 
sented by the diagram is helpful in considering the content of the 
genus Microtus alone, because the content is not generally agreed 
upon and because the same principles and characters apply at var- 
ious taxonomic levels. 


HINTON 1926 


Synaptomys 
Myopus 


Lemmus 


Anteliomys 


Eothenomys 


Alticola 


Dolomys 
Arvicola 
Phaiomys 
Phenacomys 
Arborimus 
Ondatra 
Neofiber 
Orthriomys 
Herpetomys 
Pitymys 
Neodon 


C Pedomys 


Microtus 


Lemmiscus 


Lagurus 


Fic. 1. 


Dicrostonyx 


Murine rodents 


Clethrionomys 


Hyperacrius 


Platycranius 


Tyrrhenicola 


HOOPER AND MUSSER 1964 


Ellobius 


Prometheomys 


Dicrostonyx 


7A Eothenomys 


Clethrionomys 
Ondatra 

Lemmus 

Neofiber 
Phenacomys 
Arborimus 
Synaptomys 
Lagurus 

M. montanus 

M. pennsylvanicus 
M. longicaudus 
M. miurus 

M. oeconomus 

M. oregoni 

M. richardsoni 

. californicus 
M. guatemalensis 
M. ochrogaster 
M. mexicanus 


M. pinetorum 


Taxonomy and Systematics 61 


faa rs 
uo 
15B E 
E 
EE 


Cladograms indicating hypothesized branching 


CHALINE 1980 and earlier 


Dicrostonyx 

Synaptomys 

Myopus 

Lemmus 

Ondatra 

Neofiber 

Clethrionomys 

Lagurus 

Arvicola 

Phenacomus 

Dolomys 

Hyperacrius 

Alticola 

Eothenomys 

Anteliomys 

M. duodecimcostatus (Meridiopitymys ) 
. brandti et al. (Lasiopodymys ) 
- Sikimensis et al.(Neodon) 
leucurus (Phaiomys ) 
richardsoni (Aulacomys ) 
guatemalensis (Herpetomys ) 
umbrosus (Orthriomys ) 
nivalis (Chionomys) 
oeconomus 


gud 

roberti 

oregoni (Chilotus) 
socialis (Sumeriomys ) 
malei (Sur. 


guentheri et al.(Iberomys) 
gregalis (Stenocranius) 
middendorffi 
abbreviatus 

miurus 

pinetorum (Pitymys ) 
savii 

pyrenaicus 
lichtensteini 
subterraneus 
agrestis 
pennsylvanicus 
chrotorrhinus 
xanthognathus 
longicaudus 
californicus 
montanus 

canicaudus 
mexicanus 
maximowiczi 
mongolicus 

- montebelli 

cabrerae 

arvalis (Arvalomys) 
- orcadensis 


ERE ER ERE ES ESTER ER ESET ER ER TT ERSTE RES ERE 


sequences (the reader 


should not infer any other meaning from the diagrams) in the evolution of Arvicolinae 
according to Hinton (1926; based on all characters), Hooper and Musser (1964; 
based on anatomy of the glans penis), and Chaline (1980; based on teeth). The lines 
that are labelled are for reference to selected specific characters given in text. Clades 
that coincide in content between the three diagrams are few and are labelled. Current 
authors would generally switch the positions of clades 2A and 6A and thus consider 
the arvicolines to be monophyletic rather than polyphyletic. Extinct lines shown are 
indicated by E; not all extinct lines are shown. The clade(s) labelled M belong to 
Microtus in the broad sense. 


Hinton agreed with his mentor, Forsyth Major, in favoring the 
“multituberculate theory” of eutherian origins. The theory is that 
all orders of eutherian mammals descended from the multituber- 
culates of the extinct order Allotheria and that the major trend in 
evolutionary change in molariform teeth was from longitudinally 


62 Anderson 


complex teeth to simpler teeth. This view was controversial in 1926 
and no one advocates it in exactly this form today. Simplification 
may have occurred in some phylogenetic lineages, of course. Hinton 
(1926:34) reported in a footnote that “As long ago as 1914 Winge 
and I were comparing our views on this subject, and he told me 
that I had got everything upside down. No doubt others will be of 
the same opinion today!” Much of Hinton’s discussion of evolu- 
tionary trends is quite acceptable, but in regard to the trend of 
molar evolution Winge (1941) may have been correct. 

The evolutionary changes that Hinton postulated in each lineage 
of Fig. 1 (or the synapomorphies that are the basis for the hypoth- 
esis of monophyly for the lineage, in current cladistic terminology) 
are outlined here (in the form of a key for convenience, although it 
is not a key and cannot be used to identify specimens). The phy- 
logeny is mostly dichotomous but there are multichotomies in lines 
9A and 20A. Each alternative coincides with the initial lineage of 
a clade in the diagram. A clade is defined as any one line and all 
of its descendent lines. The numbers of living species noted in dif- 
ferent groups are from Corbet and Hill (1980), Hall (1981), or 
Honacki et al. (1982), rather than from Hinton. 


ft: Skull lightly built; rostrum moderately long; temporal 
ridges widely separated; palate thin and flat; medial 
sutures of skull persistent; eyes and ears large; tail 
moderately long; lower incisor inferior or lingual to 
molars, short, not extending back of m3; cheekteeth low- 
crowned, rooted, multitubercular, and longitudinally 
complex; jaw motion transverse or oblique; incisors 
narrow and orthodont or opisthodont; enamel of inci- 
sors pigmented; enamel of cheekteeth even in thickness 
(there is no dichotomy here, these are postulated char- 
acters of primitive ancestral murine rodent) 0. 2 

2(1). A. Skull more heavily built; rostrum shortened; palate 
thickened and concave; medial sutures tending to fuse 
in skull; eyes and ears reduced; tail shortened; molar 
teeth becoming prismatic and occlusal surface flat, 
reentrant folds lacking cement, becoming hypsodont and 
then persistent in growth (never rooted in old age); 
roots of molar capsules extend on labial side of incisor 
TOOt-OL lOWER jaw 2-54 Lemmings, 3 


OE 


4(3). 


5(4). 


6(2). 


7(6). 


Taxonomy and Systematics 63 


B. Molar teeth remaining as in 1 above (no synapo- 
morphic characters; this is what remains after the lem- 
TT Seale LET OVC Ol) Meee cae ee 6 
A. Fur thickened and seasonally variable; limbs and 
tail shortened; ears reduced to mere fold; feet broadened, 
soles furred, pads reduced; claws enlarged, claws of 
manal digits 3 and 4 undergoing seasonal change in 
form; ulna powerfully built; incisors becoming pro- 
odont; skull becoming even heavier 
ee ee ee Genus Dicrostonyx, ten species 
B. Molars simplified longitudinally, cement added in 
reentrant folds, strengthening teeth; incisors and other 
teeth broadened; salient angles of lower molars reduced 
on outer side and those of upper molars reduced on 
HEINEY SC cg eg a 
A. Incisors becoming grooved (regarded as a “memo- 
rial” of primitive cuspidate incisor); palate like that of 
Microtus .......... Genus Synaptomys, two New World species 
B. Build becoming heavier (as in 3A); palate like that 
OF Cleo nom ys =. 5 
arses Lyell eee Nobo Ae ew eae 
peated Genus Myopus (or subgenus of Lemmus), one 
Old World species; recently placed in the genus Lemmus 
B. Size larger; skull much heavier; squamosals tending 
to converge anteriorly; eyes smaller; feet larger and 
broader; thumb nail large and flat; palmar and plantar 
surfaces hairy; bulla not greatly inflated, spongy within 
eas ee Genus Lemmus, three species 
A. Molars simplified longitudinally Murine rodents 
B. Molars becoming prismatic and flat on occlusal sur- 
face, molars becoming hypsodont, eight mammae pres- 
ent (presumably the characteristics of the subfamily 
appear here as well as in 2A, such as heavy skull, short 
rostrum, smaller eyes and ears, shorter tail, thicker pal- 
ates, and fusion of medial cranial sutures) ............... Voles, 7 
A. Posterior palate shelf-like 
B. Posterior palate with sloping median septum and 
lateral pits, at first septum broad and ill-defined, pits 
small and shallow, lateral bridges incompletely devel- 
(0) 3 oft Papas sive een ned fe mee Men ere A e/a ee ar OTe esac careeee 12 


64 Anderson 


8(7). 


O18): 


10(9). 


11(10). 


12@): 


13(12). 


A. Molars becoming persistent in growth 0. 9 
B. Molars rooted in adults (symplesiomorphy only) ... 
Son er ee aes eee ae Genus Clethrionomys, seven species 
A. Reentrant angles wide, teeth appear “drawn out,” 
UV AUER: LIE RSs © DCI ener ee ee 
Penne een Genus Alticola, seven Old World species, 10 
B:- Mammae reduced to four = 2S 
gee ee eee eter Genus Eothenomys, 12 Old World species 
C. Temporal ridges tending to fuse in interorbital area, 
complex “primitive” M3 with five or six salient angles 
on each side, median spine on posterior of palate 
Pee eee ene Genus Anteliomys; now put in Hothenomys 
A. (No synapomorphy postulated) 00 11 
B. Fossorial specialization; m3 reduced in size and 
Simplihed in Structure =. == as 
Subgenus Hyperacrius; recently treated as separate genus 
A. Skull much flattened 00 
ee Subgenus Platycranius, one species 
B. (No synapomorphy postulated) 0 
Si oar eet tae et Subgenus Alticola, three species 
A. Progressive hypsodonty in time; temporal ridges not 
meeting palateas im Avzicolad 2 
BB Ue cai MN PGS OE a act ore oe 
Genus Dolomys, one Old World species; 
now called Dinaromys 
A. (This dichotomy was only vaguely defined by Hin- 
ton, as separate discussions of a Mimomys to Arvicola 
line and another line from Phenacomys-like to Microtus 
and other genera). Eyes and ears moderately large; feet 
normal; tail moderately long; rostrum moderately long; 
interorbital region broad; temporal ridges separate 
(these are all primitive traits listed under initial lineage 


B. Molars growing persistently; palate further devel- 
oped to Microtus-form; temporal ridges meeting; bullae 
developing some internal bony trabeculae; stapedial ar- 
tery enclosed in bone (all of these traits are present also 
in one or more of the branches of 13A) een 24 


14(13). 


15(14). 


16(15). 


17(15). A 


18(14). 


1138) 


20(18). 


D0). 


Taxonomy and Systematics 65 


A. Bullae small and globular, without internal trabec- 
ulae; stapedial artery naked as it nears stapes; m3 not 
displaced by shaft of lower incisor which passes below 


B. Molars becoming persistent in growth ee one 
Rea rr irneeser Sener ae ee Genus Microius in a broad sense, 18 
A. Lower molars with long inner salient angles; groove 
between alveoli of cheekteeth and ascending ramus not 
“pocketed? a a eNOS ee eat 

.. New World Genus Phenacomys in its broadest sense, 16 
B. Palate simple; stapedial artery in bony tube; inter- 
orbital area narrow; nee modifications of feet and 
fur; size large 0. aes hc Re ee DY 
. (No synapomorphies) See: ee eee ee 
eee ae Genus iene one New World species 
B. Arboreal; tail long _. _ 

z . _ Genus Arborimus, two ) New World species 
A. ‘Size larger Dae Genus Ondatra, one New World species 
B. Molars becoming persistent in growth 0. 
ee tia Bt Genus Neofiber, one New World species 
A. Median interorbital crest; m3 has closed triangles; 
m1 with variable number of triangles, three to five; 


> 


inguinal mammae lost ‘*Mexican line,” 19 
Bam without closed triangles. =) 1.42 2. 20 
A. Bullae smaller .. : 

Miss Deane Subgenus (One ‘Microtus “imbrosis only 
B. Bullae larger (derived feature) eee 


_ Subgenus Herpetomys, Microtus guatemalensis only 
A. ml with only three closed triangles, triangles 4 and 
5 are confluent 2 Pitymys generic group, 21 
B. mil with fave closed triangles... 
Bide eee acre see ees et eee Microtus-Lagurus line, 22 
A. Fossorial specialization; eyes small; ears small; tail 
short; large hands; moderately hairy soles; pelage short 
and dense; four or six mammae; skull rather smooth; 
braincase more or less depressed _..... Genus Pitymys 
B. Temporal ridges fused in interorbital region in 
adults; eight mammae; fur full and soft; ears evident 
above fur; bullae moderately large; mastoid not inflated 
.. Genus Neodon, one Old World species 


66 Anderson 


22(20). 


2302) 


24(13). 


C. Temporal ridges fused; six mammae; fur long and 
coarse; ears concealed in fur; bullae small; mastoid in- 
fated 2 ee Genus Pedomys, one New World species 
D. Face long; bullae small _. Extinct genus 7 yrrhenicola 
A. Bullae enlarged, cancellous; reentrant angles lack 
CEMent: S@lES Mali ee ee Genus Lagurus, 23 
B. (No synapomorphies; this is what is left after the 
distinctive Lagurus is removed) ene 
sa reat N IR Genus Microtus (in a restricted sense) 
A. Lemming-like externally, with short tail; m3 with 
four closed triangles and two outer salient angles (syn- 
LPO UOT: PIGS) ase er tee Nae een ee 
peer Subgenus Lagurus, two Old World species; three 
species have been recognized recently and two of these 
have been placed in a separate genus, EHolagurus 
B. Less lemming-like, tail not so short; m3 with 3 closed 
triangles and two outer salient angles nee 
enna .. Subgenus Lemmiscus, one New World species 
A. Size medium to large; skull massive, strongly ridged 
when adult; squamosals approach each other anterior- 
ly; bullae small, few trabeculae within; aquatic modi- 
fications; palms and soles naked eee 
Bas Ls SRO Subgenus Arvicola, two Old World species 
B. Size small to medium; skull less massive; squamo- 
sals well separated; bullae large, dense spongy bone 
within; fossorial modifications; fur long and soft; palms 
and soles densely haired, pads concealed cen 
Genus Phaiomys, one species; placed with Pitymys by 
Corbet and Hill (1980) 


Hinton’s phylogeny has some questionable features, beyond the 
need to add newer knowledge and to reevaluate many of the char- 
acters used. It postulates a polyphyletic derivation of the Arvicolinae 
from murine rodents, ““much later divergence from the primitive 
Murine stock by Microti than by Lemmi” (Hinton, 1926:40). This 
conclusion results from the weight accorded the multituberculate 
theory and results in the necessity of postulating multiple origins 
of various characters, including most of the diverse features that 
characterize the Arvicolinae. This raises the question as to which, 
if any, taxa should be polyphyletic. The development of persistently 


Taxonomy and Systematics 67 


growing molar teeth is postulated to have occurred at least five 
different times (in lineages 2A, 8A, 13B, and 14B). This raises the 
usual questions about relative importance (“‘weighting”’) of different 
characters and about the role of parsimony in classification. Some 
of the taxa recognized are not defined by synapomorphies, but are 
what is left after small monophyletic groups are removed from 
larger monophyletic groups. For example, the genus Microtus (as 
represented by 22B) is merely what is left after Lagurus (22A) is 
removed from 20B; the genus Clethrionomys (8B) is what is left 
after 8A is removed from 7A; and the subgenus Alticola (11B) is 
what is left after 10B and 11A are removed from 9A. These are 
examples of results achieved by what I will describe as the “arti- 
choke method.” 

In 1941, Ellerman published volume 2 in his monumental com- 
pilation on the families and genera of living rodents. In regard to 
names that have been used for North American Microtus, he largely 
followed Hinton in treating the following as separate genera: Neo- 
fiber, Lagurus, Orthriomys, Herpetomys, Pitymys, Arvicola (excluding 
Microtus richardsoni), Pedomys, and Microtus. Ellerman used the 
following as subgenera within the genus Microtus: Microtus, Aula- 
comys (for M. richardsoni), Stenocranius, and Chilotus. Chionomys 
was disregarded in his classification as being poorly defined. 

In 1953, Hall and Cockrum published a synopsis of North Amer- 
ican microtine rodents. They recognized Neofiber, Lagurus, and M:- 
crotus aS separate genera and recognized within Microtus the sub- 
genera Muicrotus, Herpetomys, Orthriomys, Aulacomys, Chilotus, 
Stenocranius, Pitymys, and Pedomys. Subsequent American authors 
have tended to follow this grouping. 

Because of uncertainty as to the limits of the genus, the planners 
of this volume arbitrarily agreed to use the content of the genus 
Microtus in North America as treated by Hall and Cockrum (1953) 
and after them Hall and Kelson (1959) in order that the coverage 
of the different chapters would be comparable. 

Hall subsequently (1981) dropped the use of the subgeneric names 
Herpetomys, Orthriomys, and Chilotus, and changed Aulacomys back 
to synonymy in Arvicola. 

Hooper and Musser (1964) published a phylogenetic diagram 
for arvicolines based on the anatomy of the glans penis alone (mostly 
following Hooper and Hart, 1962). The diagram was drawn rather 
subjectively in order to summarize general clusters and different 


68 Anderson 


degrees of phenetic distinctness as well as branching sequences. ‘The 
characters that were the bases for each detail of the diagram were 
not explicitly listed. For purposes of comparison and discussion I 
extracted the very tentative cladistic relationships implied by the 
branching sequence alone (ignoring lengths of side branches and 
distances between branching points) and compared this cladogram 
with that drawn from Hinton’s work. Other than the terminal twigs 
(mostly genera and subgenera), only one postulated clade coincided 
(7A from Hinton was represented by a common clade for Eothen- 
omys and Clethrionomys, the only twigs examined among the six 
twigs of 7A). 

Kretzoi (1969) outlined a phylogeny for arvicolines but did not 
include any diagram of branching relationships. 

In an essay outlining the evolutionary branching of arvicolines 
based on dental morphology (mostly not described in the essay), 
Chaline (1980) presented a pattern combining anagenesis (in which 
a fossil taxon changes into another taxon without branching) and 
cladogenesis (in which one line branches into two or more, in one 
case about 10 and in another about 15). I drew a branching diagram 
to represent Chaline’s phylogeny based on this and earlier papers 
(Chaline, 1974, 1975a, 19755) and compared it with the diagrams 
drawn from Hinton (1926) and Hooper and Musser (1964). Other 
than the terminal twigs themselves, only four clades coincided (see 
Fig. 1). 

Since there presumably was only one actual phylogeny and since 
we have more than one hypothetical phylogeny and little agreement 
among them, it is clear that more work is needed here. 


History of Systematics at the Species Level 


The pivotal study at the level of species in the systematics of 
North American Microtus was Bailey’s (1900) revision. Bailey used 
the same generic content and subgenera that Miller (1896) used 
and set the stage for a reduction in the number of recognized species 
by defining ten species groups within the subgenus Microtus and 
by recognizing a number of subspecies. Bailey’s own words (1900: 
9) clearly summarized the nature of his contribution to the ad- 
vancement of systematic knowledge of the genus: “It is not many 
years since certain prominent writers treated as mere varieties, or 
subspecies, animals that belong to widely different subgenera, while 


Taxonomy and Systematics 69 


TABLE 1 
THE DEVELOPMENT OF TAXONOMY FOR NORTH AMERICAN Microtus AS DEMON- 
STRATED BY A SERIES OF COMPREHENSIVE SUMMARIES OF NUMBERS OF TAXA* 


Number 
Hall and 
Bailey Miller Cockrum Hall 
Taxon (1900) (1923) (1953) (1981) 
Species 48 52 25 22. 
Monotypic species 37 37 10 8 
Subspecies 2D) 57 122 131 


* Lagurus and Neofiber are excluded. 


others described and named with full specific rank every different 
condition of pelage in a single species. In some cases the original 
type was not preserved, or no type was designated by the describer, 
or still worse, the type locality was not given, so that subsequent 
writers renamed these same species or confounded them with others. 
The resulting confusion can now be cleared up by means of series 
of specimens collected within the past ten years at most of the 
known type localities, and in the general region of those not defi- 
nitely known. The series of specimens available, and the number 
of localities represented, make it possible to define almost every 
North American species from typical specimens, and in most cases 
to give the various changes of pelage due to season and age.” 

For the benefit of the readers who may not be familiar with 
examples of the earlier taxonomic treatments to which Bailey was 
referring, “certain prominent writers” who “treated as mere vari- 
eties, or subspecies, animals that belong to widely different subgen- 
era” probably referred to Coues and Allen (1877). Other writers 
who “described and named with full specific rank every condition 
of pelage in a single species” can be found listed in the synonymy 
(Hall, 1981) of Microtus pennsylvanicus pennsylvanicus where the 
names themselves, such as hirsutus, alborufescens, and fulva, suggest 
that trivial features of the pelage were involved. 

The developing taxonomy for North American Microtus may be 
examined by comparing a series of comprehensive summaries: Bai- 
ley in 1900, Miller in 1923, Hall and Cockrum in 1953, and Hall 
in 1981 (Table 1). 

The number of names that had been proposed as species names 


70 Anderson 


prior to 1900 was 74, of which 26 were reduced to subspecific status 
or synonymized by Bailey (1900). Prior to Bailey’s (1900) revision, 
and mostly in the three years before 1900, 11 names had been 
proposed as subspecies of previously recognized species (not count- 
ing the nominate subspecies created thereby) and one species had 
been reduced to subspecies. Other names had lapsed into complete 
synonymy, not being recognized as subspecies. 

Between 1900 and 1953 the following changes occurred. In Bai- 
ley’s (1900) pennsylvanicus-group of seven species, revisionary 
changes reduced the number of recognized species to three. In 1908, 
Bangs named a new species in this group, M. provectus. New sub- 
species were named in 1901, 1920, 1940, 1948, and in 1951. (The 
taxonomic names, authors, and bibliographic references are readily 
available in Hall, 1981, and other sources and need not be given 
here. The dates are given to provide a general view of the chronol- 
ogy.) Bailey’s montanus-group of five species was reduced to a single 
species, and new subspecies were named in 1914, 1935, 1938, 1941, 
and 1952. Bailey’s californicus-group of three species was reduced 
to one species in 1918 and new subspecies were named in 1922, 
1926, 1928, 1931, 1935, and 1937. In Bailey’s (1900) operarius- 
group of seven species, reductions in recognized species were made 
in 1942 by Zimmermann who regarded it as conspecific with M:- 
crotus oeconomus of the Old World. New subspecies were described 
in 1909, 1932, and 1952. The two species in Bailey’s townsendu- 
group were treated as subspecies in 1936. New subspecies were 
recognized in 1936, 1940, and 1943. In Bailey’s longicaudus-group 
of five species, a reduction in recognized species was made in 1938. 
Several new subspecies were named between 1922 and 1938. In 
1911 a new insular species in this group, M. coronarius, was named. 
In Bailey’s mexicanus-group of three species, a reduction in recog- 
nized species was made in 1932 and new subspecies were named 
in 1902, 1934, 1938, and 1948. Bailey’s xanthognathus-group has 
never included anything except Microtus xanthognathus. His chro- 
torrhinus-group was essentially redundant with his species Microtus 
chrotorrhinus, which included two subspecies. A third subspecies 
was named in 1932. In regard to Bailey’s subgenus Pitymys, we 
note that in 1898 he named Microtus pinetorum nemoralis, but in 
his revision of 1900, perhaps as a lapsus, he used the name Microtus 
nemoralis. In 1916, Howell named Pitymys parvulus. New subspe- 
cies of Pitymys were named in 1941 and 1952. In 1912, Thomas 


Taxonomy and Systematics 71 


removed Lagurus from the genus Muicrotus, and this treatment has 
been followed by other authors since. The three species of Bailey’s 
subgenus Chilotus were treated as subspecies of Microtus oregoni in 
1920. New subspecies were named in 1908 and 1920. Three of the 
four species in Bailey’s subgenus Pedomys were treated as subspe- 
cies of Microtus ochrogaster in 1907. New subspecies of M. ochro- 
gaster were named in 1942 and 1943. 

In 1920, Howell and Harper both used Neofiber as a genus 
separate from Muicrotus as Chapman had done in 1889. Merriam 
(1891) had reduced Neofiber to a subgenus of Microtus. Miller 
(1896) and Bailey (1900) treated Neofiber as a subgenus of Microtus 
and provided diagnostic characters and comparisons. Subsequent 
authors who used Neofiber as a genus (including Harper, 1920; 
Howell, 1920; and Schwartz, 1953) did not state why it should be 
treated as a genus instead of a subgenus. As noted above, Ellerman 
(1941) and Hinton (1926) raised most of Miller’s subgenera of 
Microtus to separate genera, including Neofiber. Martin (1979) did 
not connect the base of the phylogenetic line leading to Neofiber 
with either Microtus or Ondatra. 

In 1901, Osgood named Microtus miurus and in 1907 he named 
a subspecies thereof. New species of similar Microtus from the same 
region (Alaska and vicinity) were named in 1931, 1945, and 1947. 
In 1952, Hall and Cockrum reduced these all to subspecies of M. 
muurus. 

In the years from 1953 to 1981 the following taxonomic changes 
were made. The species Microtus provectus was reduced to a sub- 
species of M. pennsylvanicus in 1954. New subspecies of M. penn- 
sylvanicus were named in 1956, 1967, and 1968. Youngman (1967) 
considered brewer: and nesophilus to be subspecies of M. pennsyl- 
vanicus. The species Microtus canicaudus was separated from M. 
montanus in 1970. New subspecies of M. montanus were named in 
1954. In Microtus californicus a new subspecies was named in 1961. 
In 1966, Goodwin named a new species, Microtus oaxacensis. 

In Microtus townsendu, a new subspecies was named in 1955. 
The species Microtus oeconomus was revised in 1961 by Paradiso 
and Manville. Hall (1981) pointed out that oeconomus may not be 
the correct name for the North American populations now referred 
to Microtus oeconomus. The correct name may be ratticeps or kam- 
tschaticus, but until the question can be resolved it may be desireable 
to continue with oeconomus. In 1960 a new subspecies of Microtus 


72 Anderson 


longicaudus was named. Microtus ludovicianus was reduced to sub- 
specific status in M. ochrogaster in 1972 and in 1977 a new sub- 
species of M. ochrogaster was named. Microtus fulviventer was re- 
duced to subspecific status in M. mexicanus in 1964 and in 1955 a 
new subspecies of M. mexicanus was named. Microtus parvulus was 
made a subspecies of M. pinetorum in 1952. A new subspecies of 
Microtus richardsoni was named in 1959. Microtus miurus was re- 
garded as conspecific with Microtus gregalis of the Old World by 
some authors but was again treated as a separate species in 1970 
by Fedyk. Microtus nemoralis was regarded by Repenning (1983) 
aS a species separate from M. pinetorum and more closely related 
to M. quasiater, M. meadensis (fossil), and Old World Pitymys, 
which was regarded as a genus separate from Microtus. 

The taxonomic history described above and represented in Fig. 
2 exhibits several rather different phases, as follows. 

1) 1815 to 1860. Initial scattered exploration in which about half 
of the full species now recognized were discovered—34 supposed 
species were named; a rather typological view was common; and 
adequate series of specimens to enable workers to escape the typo- 
logical (small sample) perspective were not available. 

2) 1860 to 1890. Not much happened—few new names were 
proposed; and few specimens were obtained. 

3) 1890 to 1900. The most productive decade in the taxonomic 
history of North American Microtus—most of the remaining full 
species now recognized were discovered; the mass produced break- 
back mouse trap was available; the U.S. Government was persuad- 
ed by C. Hart Merriam to launch the great explorations of the 
Biological Survey; large series of specimens were obtained; variation 
within and between populations became obvious; a polytypic con- 
cept of the species supplanted the typological concept; subspecies 
names were used more often; the winnowing process began, the 
number of monotypic species began to decline, and the number of 
recognized species increased noticeably more slowly than the num- 
ber of names being proposed for species. 

4) 1900 to 1920. The new forces initiated just before 1900 con- 
tinued their development but at a slower rate—revisionary work 
continued on a species by species basis; the numbers of proposed 
species increased more slowly than before, and the numbers of rec- 
ognized species increased slowly and then ceased to increase; the 
number of monotypic species did not change; and the number of 


Taxonomy and Systematics 73 


100 


50 


1820 1900 1980 


Fic. 2. Taxonomic history of North American Microtus (excluding Lagurus and 
Neofiber, as most authors have done in recent decades). A, cumulative number of 
recognized subspecies and monotypic species; B, cumulative number of names of 
species proposed; C, number of species recognized as valid at different times; D, 
number of monotypic species recognized at different times; E, cumulative number of 
species proposed among those recognized as valid in 1980. 


recognized subspecies continued to increase rapidly as continued 
field work filled in details of geographic variation within species. 

5) 1920 to 1950. Further consolidation—the number of recog- 
nized species decreased rapidly as monotypic species became sub- 
species of polytypic ones following the discovery of intergradation; 
few new species were proposed and these were quickly synony- 
mized; and the numbers of recognized subspecies continued to in- 
crease rapidly. 


74 Anderson 


6) 1950 to 1980. Maturation of the period of alpha taxonomy— 
fewer distinctive subspecies were discovered and a reaction against 
continued subspecific splitting occurred; only one new species was 
proposed; and the decline in numbers of recognized species contin- 
ued gradually and now approaches an equilibrium. 


Discussion of Systematic Viewpoints 


In this section I examine the systematic approaches that Miller, 
Hinton, and others have used in classifying Arvicolinae, outline 
some needs for future taxonomic research, and discuss the effect 
upon taxonomy of a major pattern of macroevolution. 

Miller (1896:24) rationalized his synthesis of genera in the fol- 
lowing terms: “In the present paper the classification used is based 
on an assemblage of characters. The more important of these, or 
the ones least adapted to the special needs of the different animals, 
and hence least likely to vary, are: Form of skull, structure of bony 
palate, pattern of enamel folding, number of mammae, number of 
plantar tubercles, and presence or absence of musk glands on the 
sides. Characters of less importance, because more readily modified 
to fit a species to the special requirements of its environment, and 
hence more unstable, are: Quality of fur, hairiness of soles, length 
of tail, form of front feet, size of eyes, and form of external ear. It 
is only through careful consideration of all these that a satisfactory 
arrangement of the species can be obtained.” 

This is certainly better than no explanation, which is what many 
authors have provided when creating and changing rodent taxon- 
omy. Nevertheless, Miller’s statement does not provide any explicit 
guidelines on how “careful consideration” will lead to “a satisfac- 
tory arrangement.” The systematic theory was still murky. 

In contrast, Hinton’s (1926) point of view seems almost contem- 
porary in theory. He wrote (1926:5) that “‘if the more or less sub- 
stantial mask of specialization be stripped off from each species one 
finds the primitive core of each animal underneath; if the primitive 
characters so found be used as the bases of comparison there is no 
difficulty either in arranging species, genera, and families in natural 
order, or in conceiving what the essential characters of the ancestor 
common to any given group must have been. That is what I have 
attempted to do in this chapter. The stripping process is, however, 
by no means easy, and it reveals many a disconcerting gap in our 


Taxonomy and Systematics 75 


knowledge.” I take it that “the essential characters of the ancestor 
common to any given group” means about the same as “‘synapo- 
morphies” in much of the current cladistic literature (see Nelson 
and Platnick, 1981, for a comprehensive summary). 

Hinton, however, did not complete his work on the genus M:- 
crotus and he did not apply the theory in order to postulate rela- 
tionships other than the contents of groups recognized by names in 
his formal classification. 

Bailey (1900) dealt with problems of alpha taxonomy. What are 
the species? How do they vary geographically? What are their 
polytypic morphological limits? Exactly where do they occur geo- 
graphically and ecologically? The theory here relates to the nature 
of biological species, whether they exist and, if so, how they may 
be recognized ? These questions have attracted most of the taxonom- 
ic attention in the genus Microtus since 1900. 

Less attention has been given to examining relationships above 
the species level in Microtus or among arvicoline rodents generally, 
either in theory or practice. 

One method commonly used in arvicoline taxonomy (and in most 
other groups for that matter) I call the ‘“‘artichoke method.” The 
analogy is to the fact that the outer leaves of an artichoke are more 
conspicuous than the inner ones and when one takes an artichoke 
apart one usually begins with the most conspicuous part, then takes 
the next most conspicuous leaf, etc. Some taxonomists follow the 
same pattern. For example, if the keys to Murinae or Microtinae 
in Ellerman (1941) are examined, it seems that the most peculiar 
and thus conspicuous form is pulled off first, then the next most 
conspicuous, etc. Since the species that are unusually conspicuous 
morphologically tend to be rare in nature and since the most com- 
mon specimens tend to be of some less conspicuous species, the keys 
are inefficient and frustrating to use for most identifications. There 
is no agreement as to how many successively less conspicuous species 
one should remove from the core of the genus and call subgenera. 
As the degree of distinctness becomes less and less, the decision as 
to which of the remaining species is most distinct becomes more 
and more difficult to make. Eventually, even the most ardent splitter 
usually gives up before the final split is made and complete redun- 
dancy of species and subgenus is reached. 

The artichoke method is generally phenetic in that the most con- 
spicuously different item or small subset of items in the cluster is 


76 Anderson 


singled out for separation. The taxonomist is usually not hypothe- 
sizing a cladistic relationship, although in some cases this is done. 

The existing classification of most groups of mammals, and of 
the genus Microtus in particular, has resulted from an eclectic in- 
teraction of several different procedures: 1) an initial recognition 
and naming of distinctive (and presumably often monophyletic) 
groups at various levels (for example, the subclass Eutheria, the 
order Rodentia, the subfamily Arvicolinae, the genus Microtus); 2) 
the singling out and naming of species (or small groups of species 
that are unusually distinctive in a phenetic sense, without any nec- 
essary hypothesis of cladistic relationship (the artichoke method; for 
example, the subgenera Chilotus, Pedomys, Aulacomys, Orthriomys); 
3) the naming of “left-over groups” for consistency rather than 
because of any clearcut hypothesis of monophyly (for example, after 
the presumably distinctive and mostly monotypic subgenera in the 
genus Microtus are named, what is left, which is most of the species 
in the genus, is called the subgenus Microtus). The tradition of 
“consistency” is practiced at all of the non-obligatory levels of the 
classification. One is not obligated to use subgenera, but if any 
subgenus is recognized in a genus all of the species must be put in 
some subgenus. The “left-over” subgenus may have no distinctive 
features in common except the shared derived features of the genus. 
In this case, the subgeneric arrangement does not necessarily imply 
anything about geneological or cladistic relationships among the 
species within the genus. It indicates only that a few are pheneti- 
cally more peculiar than the others. The left over groups may be 
paraphyletic and in one sense are permitted by our ignorance rather 
than sustained by our knowledge. They are not exactly comparable 
to what have been called “wastebasket” groups, which may be ad- 
mittedly polyphyletic or paraphyletic, but like the “wastebasket” 
groups they are not conceived to be strictly monophyletic (holophy- 
letic). 

There is still much interesting work to be done in refining the 
analyses of geographic variation within species whether or not one 
chooses to use subspecies names. Slightly differentiated but none- 
theless distinct sibling species probably remain to be detected by a 
combination of old and new methods of study. Relationships be- 
tween populations in the Old World and the New World need 
careful examination at the species level. 

The major unfinished taxonomic tasks, however, are above the 


Taxonomy and Systematics 77 


species level in the hierarchy of classification. In my opinion, the 
role of taxonomy should be to describe and interpret relationships 
at all levels from local populations or demes on up. The traditional 
levels such as genus, subgenus, species, and subspecies are some- 
what arbitrary and their existence may lead to unwarranted em- 
phases, such as the idea that something with a name is more im- 
portant than something without a name. This leads either to the 
disregard of important things or to a stultifying and unstable pro- 
liferation of names. If there are 20-25 species of Microtus in North 
America and if that number is not likely to change much, our task 
has not ended. What needs to be done now is to study the relation- 
ships at all levels among these species, a task that has barely begun. 

Many published reports of newly studied biological features are 
sufficiently comparative to have taxonomic implications. ‘The au- 
thors have generally avoided the sort of uncritical enthusiasm for 
single characters that led to some of the classifications proposed for 
arvicolines prior to Miller’s (1896) major revision. There has been 
no major taxonomic synthesis of these fascinating newer develop- 
ments. The needed syntheses may be conducted either among all 
arvicolines or within smaller groups such as Microtus, and should 
integrate a number of different features. It is not possible to do it 
all at once. Any reasonably comprehensive and careful synthesis 
can serve as the hypothesis of relationships for further testing with 
other characters. It will be better if authors do not feel compelled 
to express all of the hypothesized relationships in a formal classi- 
fication. I suspect that knowledge of the fate of earlier single-char- 
acter classification combined with the deplorable idea that only for- 
mal named taxa are important in taxonomy (which is equivalent to 
the current view of some cladists that all hypothesized relationships 
should be expressed in formal classification) may actually inhibit 
progress in arvicoline taxonomy. 

The following is merely a sample of papers on diverse features 
recently studied in rodents that might eventually be used in these 
taxonomic syntheses: myology (Repenning, 1968); male reproduc- 
tive anatomy, including bacula, soft parts, and accessory glands 
(Anderson, 1960; Arata, 1964; Hooper and Hart, 1962); meibo- 
mian glands in eyelids (Hrabé, 1978; Quay, 1954a); skin glands 
(Jannett, 1975; Quay, 1968); diastemal palate (Quay, 19546); be- 
havior (Gray and Dewsbury, 1975; Jannett and Jannett, 1974); 
chromosomes, including gross karyology and finer structure seen in 


78 Anderson 


G- and C-banding studies (Matthey, 1957); cranial foramina 
(Wahlert, 1978); basicranial circulation (Bugge, 1974); stomach 
anatomy (Carleton, 1981); blood chemistry, including enzymes and 
hemoglobin (Nadler et al., 1978); and DNA sequencing. 

Characters used in older classifications need reexamination also. 
Potentially useful systematic information may come from any com- 
parative biological study. 

Since 1950, considerable thought and verbiage have been devoted 
to taxonomic methods and objectives. The ideas of numerical tax- 
onomy burst upon the scene in the 1950s, emanating chiefly from 
the University of Kansas, where I was at the time. The ideas of 
cladistic taxonomy burst upon the scene in the 1970s, emanating 
chiefly from the American Museum of Natural History, where I 
was at the time. My presence was a coincidence, and I was, and 
still am, somewhat skeptical about some of the assumptions, meth- 
ods, and goals of each school. Both schools have contributed im- 
portantly to systematics. In any event, no one has yet published 
applications of the precepts and methods of either numerical phe- 
netics or present day cladistics to the classification of Microtus. 

My taxonomic viewpoint is basically phylogenetic or cladistic, 
but it differs in some ways from other cladistic viewpoints, such as 
those summarized by Cracraft (1981) in a recent discussion of bird 
classification. His references or the book by Nelson and Platnick 
(1981) will lead the interested reader to the chief summaries of the 
cladistic school, so I will not document these sources. A recent study 
by Marshall (1980) of caenolestid marsupials illustrates a useful 
application of the method, in my opinion. 

Assuming that a convincing case for the monophyletic status of 
the genus Microtus can be made, it will be quite valuable to attempt 
to develop a complete phylogenetic hypothesis of the relationships 
of the species. Eventually this will need to include all species, both 
New and Old World. This is a challenging task, but cannot be done 
here. I attempted earlier in this chapter to abstract from Hinton’s 
extended discussions the phylogenetic gist and I found that some 
lines were defined by shared primitive (symplesiomorphic) char- 
acters only. 

A group now defined by shared primitive features may have 
unnoted synapomorphies. If these are discovered, the group may 
then be regarded as monophyletic. The point here is that primitive 
and derived states have different meanings in taxonomy. Other things 


Taxonomy and Systematics 79 


being equal (which they rarely are in reality), it might be better to 
have monophyletic taxa than paraphyletic or polyphyletic taxa, and 
it might be better to postulate a more parsimonious phylogeny than 
one with parallelisms and character reversals. Nevertheless, uncer- 
tainties do exist about character states and directions of evolutionary 
change, and paraphyletic taxa will continue to be recognized. I see 
no way to avoid these problems. What is important is to have a 
reasonably clear understanding of our concepts. If our present con- 
cept of the genus Muicrotus seems to be paraphyletic, we should 
acknowledge this. We can continue to use the concept, at least until 
we have something better. 

In regard to parsimony, I am neither a numerical cladist nor 
numerical pheneticist. I do not think that since it is difficult to 
decide which, if any, characters are more important it is better to 
regard all characters as equally important. ‘The most parsimonious 
phylogeny for a given set of characters may not be the most ac- 
ceptable one. One very peculiar feature may outweigh three simple 
features. 

A nested hierarchy of taxa in biological classification preceded 
any explicit notion of evolution and was not, therefore, conceptually 
dependent upon evolution. The evolutionary idea of a branching 
tree is, however, not only consistent with a nested hierarchy, but 
seems to provide the best general explanation for the occurrence of 
the hierarchy of characters and taxa. The degree to which it is 
possible to hypothesize or to know what the actual phylogenetic tree 
may have been and the degree to which this understanding should 
be or can be expressed in classification are moot points. In the 
classification of mammals (and of arvicoline rodents in particular), 
it is my impression that authors with fairly definite ideas about the 
existence of monophyletic groups have tended to name these groups 
in their classifications, but not all named groups are accompanied 
by explicit hypotheses of monophyly. 

Let us now briefly consider the nearly universal ‘“‘hollow curve” 
frequency distribution found in nature, including the nested sets of 
our biological classifications, and how this relates to the artichoke 
method in taxonomy. 

The prevalence of hollow-curve frequency distributions in taxo- 
nomic data sets was documented in some detail by me earlier (An- 
derson, 1974). In general, if within some larger group the numbers 
of subgroups (at any given level of the hierarchy) containing dif- 


80 Anderson 


ferent numbers of items are plotted as a frequency diagram, a deep- 
ly concave or “hollow” curve will result. For example, if the num- 
bers of genera of living mammals containing different numbers of 
species are plotted, half of the genera contain one species, and most 
of the species are included in a small percentage of the genera. The 
pattern exists in nature; it is not an artifact of the method of clus- 
tering for the same pattern is seen in the results of phenetic study, 
cladistic study, or eclectic study. The pattern is apparent in North 
American Muicrotus where about half the species belong to the sub- 
genus Muicrotus and the other six subgenera share the other half. 
Given the pattern it is possible to predict how many successive 
branching points are likely to be present in a maximally resolved 
cladogram for a group of any size (Anderson, 1975). Given 61 
species of Microtus (New and Old World, and including Pitymys; 
Corbet and Hill, 1980), about 11 categories would be needed be- 
tween species and genus if all branchings in the phylogeny were to 
be expressed in a formal classification. 

To summarize where I think the taxonomy of Microtus should 
go from here, I note the following. To ask whether Pitymys should 
be considered a distinct genus or a subgenus of Microtus is not an 
especially interesting question, to me. Some interesting questions 
are: 1) Do the species of Pitymys share distinctive peculiarities? 2) 
If so, is this because they have descended from a common ancestor 
that had those peculiarities? 3) Or (as an alternative) are the species 
of Pitymys the ends of a number of separate lineages of Microtus 
that have become more fossorial than most Microtus? These may 
or may not be easy questions to answer, but they should be exam- 
ined and answered to whatever degree possible. The focus of the 
investigation should be on the characters and on relationships rather 
than on names or arbitrary categories. After a reasonably well-es- 
tablished hypothesis of relationships exists, nomenclature and clas- 
sification should be addressed. Sometimes, I think, we taxonomists 
get the cart before the horse. 

There will be differences of opinion about what is interesting or 
important, about phenetic versus cladistic criteria for “relation- 
ships,” about the value of stability, and about other matters in this 
entire procedure. I don’t think a general consensus now exists in 
systematic mammalogy in regard to these details. I would not insist 
that everyone agree with me. What I would try to encourage, how- 
ever, as an author, reviewer, and editor, is that assumptions, view- 


Taxonomy and Systematics 81 


points, objectives, and methods be indicated clearly. When this is 
done, a person with a different point of view can at least evaluate 
the author’s accomplishment in terms of the author’s goals and also 
relate the study to different viewpoints. 


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ZOOGEOGRAPHY 


ROBERT S. HOFFMANN AND 
JAMES W. KOEPPL 


Abstract 


HE genus Microtus is less species-rich in the New World than 
TT the Old, perhaps reflecting the origin and longer residence of 
the genus in the Palearctic. While Microtus are usually thought of 
as grassland species, most species are mainly associated with succes- 
sional meadow facies of forest and woodland biomes. The 19 species 
and four insular allospecies occupying the New World may be 
classified ecologically; three are primarily tundra inhabitants; nine 
are primarily taiga species, equally divided among boreal, montane, 
and Pacific coastal sections; two are southwestern chaparral or 
woodland species; one is primarily Great Plains grassland; one east- 
ern deciduous forest; and four are relict species with small ranges 
scattered through cloud forest communities in the Mexican moun- 
tains. Patterns of Pleistocene occurrence of New World Microtus 
are correlated with these ecological patterns. The oldest lineages 
are apparently represented by the Mexican cloud-forest relicts; 
chaparral, grassland, and eastern deciduous forest lineages are 
somewhat more recent; and taiga- and tundra-inhabiting voles rep- 
resent the most recent, late-Pleistocene lineages to appear in the 
New World. Certain allospecies pairs probably diverged only in 
the Wisconsinan—Holocene period, a few thousand years ago. 


Introduction 


Twenty-three species of Microtus currently are recognized from 
the New World (Anderson, this volume). ‘The extratropical portion 
of the New World is termed the Nearctic, a biogeographic region 
first defined by Sclater (1858) and Wallace (1876). The genus M- 
crotus is found throughout much of the Nearctic, and in the New 
World virtually is restricted therein; various species of these voles 


84 


Zoogeography 85 


are important components of most Nearctic mammal faunas. The 
Nearctic often is combined with its Old World counterpart, the 
Palearctic, to form the Holarctic, a circumboreal biogeographic re- 
gion. 

The number of species of Microtus in the Palearctic is greater 
than in the Nearctic. If one includes the species of Pitymys and 
Proedromys, as in the broad generic concept employed in this vol- 
ume, there are 48 species of Old World voles (Honacki et al., 1982). 
The difference is increased if the four species confined to small 
islands in the New World are eliminated; most or all are sometimes 
considered subspecies of closely related mainland species. The three 
insular species of the Palearctic (M. kikuchu, M. montebelli, and M. 
sachalinensis) occupy extensive ranges on large islands—Taiwan, 
Japan (Kyushu, Honshu, Sado; perhaps Shikotan), and Sakhalin, 
respectively—and thus differ from New World insular taxa. 

The difference in species richness—48 versus 19—may be ac- 
counted for in part by the larger area of the Palearctic, approxi- 
mately 14 million square miles as compared to six and a half million 
for the Nearctic. Nevertheless, whereas the Palearctic is about dou- 
ble the area of the Nearctic, it possesses about two and a half times 
as many species of Microtus. Of this total of 67 species, only one, 
M. oeconomus, occurs on both sides of the Bering Strait and thus 
displays a Holarctic, or amphiberingian, distribution. Relation- 
ships between other Palearctic and Nearctic species at higher taxo- 
nomic levels are, in many cases, not well understood. 

Biogeography and its subfield, zoogeography, can be divided into 
two areas of inquiry. Ecological biogeography is concerned with 
present interrelationships of species or higher taxa as members of 
associations of organisms. Historical biogeography examines the 
question of past origins and relationships of species or higher taxa 
as members of biotas (Wiley, 1981). These two approaches are not 
mutually exclusive, but it is convenient to review them separately. 


Ecological Zoogeography 


Biomes and Biogeographic Provinces 


Attempts to classify associations of organisms (communities, life 
zones, biomes, and smaller associations) have a long history (Allee 
et al., 1951; Shelford, 1963; Udvardy, 1969). Voles of the genus 


86 Hoffmann and Koeppl 


TABLE 1 


BIOMES AND BIOGEOGRAPHIC PROVINCES OF THE NEARCTIC IN WHICH 


Microtus OCCUR 


Biome Biogeographic province!’ 


Tundra 


Low Arctic Alaskan Tundra 


Aleutian 
Canadian Tundra 


Alpine — 
Taiga 
Boreal Yukon Taiga 
Canadian Taiga 
Coastal Sitkan 
Oregonian 
Montane?’ Rocky Mountains 


Sierra-Cascade 


Montane Pine-Oak Madrean-Cordilleran 


(part) 
Temperate Grassland Grasslands 
Temperate Deciduous Forest 
Northern-Upland 
Southern-Lowland Austroriparian 
Broad Sclerophyll Californian 


Cold Desert Great Basin 


Mammal province? 


Alaskan 

Western Eskimoan 
Aleutian 

Eastern Eskimoan 
Ungavan 


Yukonian 

Western Hudsonian- 
Canadian 

Eastern Hudsonian- 
Canadian 

Vancouverian 

Oregonian (part) 

Humboldtian (part) 

Montanian 

Coloradan 

Uintian 

Oregonian (part) 

Humboldtian (part) 

Sierran 


Navahonian 
Yaquinian 

San Matean 
Saskatchewanian 
Kansan 

Texan 


Alleghenian 
Illinoian 
Carolinian (part) 
Carolinian (part) 
Louisianan (part) 
Diablan 
Californian 

San Bernardian 
Columbian 
Artemesian 


Zoogeography 87 


TABLE 1 
CONTINUED 
Biome Biogeographic province’ Mammal province? 
Tropical Forest 
Cloudforest Madrean-Cordilleran _ 
(part) 


‘From Udvardy (1975). 

° From Hagmeier (1966). 

> Montane taiga in the Appalachian Mountains is included with Udvardy’s Eastern 
Forest Province and Hagmeier’s Alleghanian Province. 


Microtus occupy particular habitats (Getz, this volume), but these 
habitats occur within biomes (a concept based on climax vegetation) 
or biotic provinces (a concept based on both systematic resemblance 
of the biota and ecogeographic similarity). Microtus can thus be 
considered to occupy not only habitats, but also biomes or biotic 
provinces. 

Biomes have been classified differently by different authors, but 
there is general agreement on the major biomes of North America. 
These include (generally from north to south and from west to east) 
the following: 1) arctic tundra, including polar desert, high arctic 
tundra, and low arctic tundra; 2) alpine; 3) coniferous forest, or 
taiga, including boreal taiga, Pacific coastal taiga, and montane 
taiga; 4) temperate grassland, or steppe, including the northern and 
southern Great Plains; 5) temperate deciduous forest, including a 
northern-upland region and southern-lowland region; 6) broad 
sclerophyll, or chaparral-oak woodland; 7) cold desert; 8) hot desert; 
9) pinyon-juniper-oak woodland; 10) montane pine-oak forest; 11) 
subtropical-tropical deciduous forest; 12) tropical rainforest, in- 
cluding cloud forest (modified from Shelford, 1963). Different per- 
mutations of these elements have been suggested by other authors 
(see Kendeigh, 1961; and Odum, 1971). Biomes are related to biotic 
provinces in a general way: although biomes may be geographically 
discontinuous, biotic provinces are continuous, and usually are con- 
tained within, a given biome. Table 1 lists those biomes (see above), 
biogeographic provinces (Udvardy, 1975), and ‘“‘“mammal provinces” 
(Hagmeier, 1966) in which Microtus occurs in the New World, as 
a guide to terminology employed in this section. All maps are poly- 
conic oblique conic conformal projections. 


88 Hoffmann and Koeppl 


Fic. 1. Distribution of Microtus oeconomus in North America (modified from 
Hall, 1981). Subspecies are: 1, M. 0. amakensis; 2, M. 0. elymocetes; 3, M. 0. innuitus; 
4, M. 0. macfarlani; 5, M. 0. operarius; 6, M. 0. popofensis; 7, M. 0. punukensis; 8, M. 
o. sitkensis; 9, M. 0. unalascensis; 10, M. 0. yakutatensis. 


Voles of the genus Microtus range northward into the tundra 
biome or Western Eskimoan province in Alaska and Canada, and 
southward into montane pine-oak, subtropical deciduous, and cloud- 
forest formations (Madrean-Cordilleran province) in the montane 
highlands of central Guatemala, and inhabit all but the most xeric 
of the biomes enumerated above. In the following section we discuss 
their distribution by major biomes. 

Tundra.—The northernmost records are of the tundra vole, M. 
oeconomus, which is known to occur (Bee and Hall, 1956) on the 
northern slope of the Brooks Range in Alaska to 71°N latitude 
about 50 mi S of Pt. Barrow (Fig. 1). As its North American 
common name implies, this species regularly inhabits the tundra 
biome in mesic meadow habitats (Getz, this volume) of the low 
arctic (in the Palearctic, however, M. oeconomus has a much broader 
distribution both geographically and ecologically). No Microtus in- 
habits the more severe high arctic or polar desert associations that 
are occupied by the lemmings (Lemmus and Dicrostonyx). ‘The only 
other species of Microtus to occur regularly in arctic tundra habitats 


Zoogeography 89 


Fic. 2. Distribution of Microtus miurus (mainland) and its insular allospecies M. 
abbreviatus (modified from Hall, 1981). Subspecies are: 1, M. m. andersoni; 2, M. m. 
cantator; 3, M. m. miurus; 4, M. m. muriei; 5, M. m. oreas; 6, M. a. abbreviatus; 7, M. 
a. fishert. 


(Fig. 2) are the singing vole, M. miurus (and its insular allospecies, 
the St. Matthew Island vole, M. abbreviatus), and the meadow vole, 
M. pennsylvanicus (Fig. 3). Microtus miurus and M. abbreviatus are 
classified in the subgenus Stenocranius together with the Palearctic 
narrow-skulled vole (M. gregalis). Stenocranius has an amphiber- 
ingian distribution, like M. oeconomus, and both taxa are thought 
to have occupied the Bering land bridge during the latest (Wiscon- 
sinan) glacial period until the land bridge was flooded by rising sea 
level about 7,500 years ago (Hoffmann, 1976). The populations of 
voles found on islands in the Bering Strait (M. abbreviatus on St. 
Matthew and Hall islands; M. oeconomus on St. Lawrence, Un- 
alaska, Kodiak, and adjacent small islands) thus represent refugial 
survivors of the late Pleistocene land-bridge populations (Hoff- 
mann, 1981). The singing vole is found in more xeric tundra hab- 
itats than the tundra vole (Getz, this volume), and often is associated 
with dwarf and riparian willow stands (Bee and Hall, 1956). M:- 
crotus pennsylvanicus is found only sporadically in arctic tundra. 
Available distributional records suggest that it may range north- 


90 Hoffmann and Koeppl 


a~ 


Im 
Opa 


alg of miles 
=a 


scale of miles 


Fic. 3. Distribution of Microtus pennsylvanicus and its insular allospecies M. 
brewert (27) and M. nesophilus (28; extinct) (modified from Hall, 1981). Subspecies 
of M. pennsylvanicus are: 1, M. p. acadicus; 2, M. p. admiraltiae; 3, M. p. alcorni; 4, 
M. p. aphorodemus; 5, M. p. chihuahensis; 6, M. p. copelandi; 7, M. p. drummondi; 
8, M. p. enixus; 9, M. p. finitus; 10, M. p. fontigenus; 11, M. p. funebris; 12, M. p. 
insperatus; 13, M. p. kincaidi; 14, M. p. labradorius; 15, M. p. magdalenensis; 16, M. 
p. microcephalus; 17, M. p. modestus; 18, M. p. nigrans; 19, M. p. pennsylvanicus; 20, 
M. p. provectus; 21, M. p. pullatus; 22, M. p. rubidus; 23, M. p. shattucki; 24, M. p. 
tananaensis; 25, M. p. terraenovae; 26, M. p. uligocola; 27, M. [p.] breweri; 28, M. [p.] 
nesophilus; 29, M. p. dukecampbelli. 


ward into the tundra more regularly in the Canadian Arctic east of 
the range of M. oeconomus (Fig. 3), suggesting the possibility of 
competitive interaction between the species. Youngman (1975) re- 
ported both species “utilizing the same runways” in the Yukon. 
Taiga.—South of the arctic tundra in North America extends a 
broad transcontinental belt of northern coniferous forest, or boreal 
taiga. The western and southwestern margin of the boreal taiga 


Zoogeography 91 


merges into the structurally rather similar Pacific coastal taiga and 
Cascade-Sierra-Rocky Mountain montane taiga, whereas in the east 
there is a transition through the mixed coniferous-deciduous forest 
of the Great Lakes-New England region to the montane taiga and 
mixed forests of the Appalachians. The vole with the widest distri- 
bution in the taiga biome of North America is M. pennsylvanicus 
(Fig. 3). Its vernacular name—meadow vole—suggests a contra- 
diction; meadow voles, though widely distributed in taiga, occur 
mainly in grassy meadow habitats within the coniferous forest (Getz, 
this volume). Along the northwestern margin of their range, they 
are syntopic in taiga meadows with M. oeconomus (see above). 
Meadow voles extend southward in the Appalachian (Alleghenian 
province) and Rocky Mountains (Montanian, Coloradan prov- 
inces), and also into the eastern deciduous forest and in the grass- 
lands of the northern Great Plains. In the Pacific coastal taiga 
association, however, there occurs the similar and probably related 
M. townsendu (Fig. 4). Townsend’s vole, like the meadow vole, 
inhabits meadows within the coastal taiga (Getz, this volume) from 
Vancouver Island to northern California (Oregonian, Humboldtian 
provinces), and is completely allopatric with M. pennsylvanicus 
(Cowan and Guiguet, 1956; Dalquest, 1948). 

Two other voles are restricted to the Pacific coastal taiga biome. 
The creeping vole, M. oregoni (Fig. 5), is a species of strongly 
fossorial habits that inhabits forest as well as meadow habitats 
(Getz, this volume). It is sufficiently distinctive to be placed in its 
own monotypic subgenus (Chzlotus), and probably represents a rel- 
ict distribution of a relatively old lineage (see below). In contrast, 
the gray-tailed vole, M. canicaudus, probably is a recently derived, 
peripheral isolate of the widely distributed montane vole, M. mon- 
tanus (Fig. 6); it is restricted to grassy meadows and prairies (Getz, 
this volume) in and around the Willamette Valley in northwestern 
Oregon and perhaps adjacent Washington. This Pacific coastal area 
thus is one center of species richness for the genus; other vole gen- 
era—Arborimus and Clethrionomys—also have species restricted to 
this region. 

The putative parental lineage to the gray-tailed vole is the mon- 
tane vole (M. montanus), which is found in montane taiga through- 
out the Cascade-Sierra and Rocky Mountain ranges and the dis- 
tribution of which also includes the intervening riparian meadows, 
arid grasslands and shrub steppe and semi-deserts (Getz, this vol- 


92 Hoffmann and Koeppl 


| 

| 

| 
AY 


scale of miles 
455 


Fic. 4. Distribution of Microtus townsendu (from Hall, 1981). Subspecies are: 1, 
M. t. cowani; 2, M. t. cummingi; 3, M. t. laingi; 4, M. t. pugeti; 5, M. t. tetramerus; 
6, M. t. townsendit. 


ume) of the Columbia Plateau, Snake River Plains, and northern 
Great Basin (Fig. 6). Another species whose range primarily is 
within the montane taiga biome and cold desert biomes is the long- 
tailed vole, M. longicaudus (Fig. 7). This vole occupies not only the 
area in which the montane vole is found, but also extends westward 
to the Pacific coastal taiga in Oregon and northern California and 


93 


Zoogeography 


N 
N 


(oe) 
t+ 


150 


scale of miles 


LASS 


118 


122 


M. 


regoni (from Hall, 1981). Subspecies are 
rpens. 


egoni; 4, M. o. se 


of Microtus o 
irdi; 3, M. o. or 


ribution 
o. ba 


G.5. Dis 
tus; 2 


t 
cetus; 2, M. 


FI 
d 


SS 
———— 


‘| 


d Koeppl 


94 Hoffmann an 


CS 


o 


Le 
L 


ee ee 


WA | 
= | 
/ 
: > / ) 
ac fs 


Ae 
Se 
: | : 


LEQ 

Ae . R 

5 : DD a — > 
fo*e a on ° sete i 


MAH 
®) 


@5) 


FEWRES-O 


7 


a | 


Zoogeography 95 


northward into the coastal and boreal taiga as far as northeastern 
Alaska. 

Microtus montanus and M. longicaudus thus occupy habitats in 
taiga biomes south and west of the range of M. pennsylvanicus, but 
all three species are geographically sympatric in a considerable por- 
tion of the central and southern Rocky Mountains. Here, then, is 
another center of species richness for the genus. 

The species discussed so far are medium-sized voles that have 
rather general habitat requirements. Another group contains three 
species that apparently are more specialized in their habitat re- 
quirements, and two of the three are large in body size. The taiga 
vole, M. xanthognathus, is known from scattered localities in the 
boreal taiga zone from the west coast of Hudson Bay northwestward 
to central Alaska, and south to central Alberta (Fig. 8) (Western 
Hudsonian and Canadian, Yukonian provinces). From central Al- 
berta southward in the Rocky Mountains to central Utah (Mon- 
tanian, Coloradan provinces), and in the Cascade Mountains (Or- 
egonian province), the almost equally large water vole, M. 
richardsoni, occurs in the alpine and in subalpine taiga stands (Fig. 
9). Finally, in the eastern boreal taiga from northeastern Minnesota 
to Labrador and southward in the Appalachian Mountains to North 
Carolina (Alleghenian province), the smaller rock vole, M. chrotor- 
rhinus, has been found sparingly (Fig. 10). All three of these species 
seem to be specialists, found only where a particular combination 
of habitat conditions are met (Getz, this volume), but their com- 
bined ranges encompass most of the taiga biome. In all, then, nine 
species of Microtus have ranges that are primarily associated with 
the taiga biome in North America. 

South of the taiga biome and its montane extensions, a smaller 
number of species of Microtus is to be found, each occupying sharply 
defined habitats. Moreover, the systematic relationships of these 


—_ 


Fic. 6. Distribution of Microtus montanus and M. canicaudus (16) (modified from 
Hall, 1981). Subspecies of M. montanus are: 1, M. m. amosus; 2, M. m. arizonensis; 
3, M. m. canescens; 4, M. m. codiensis; 5, M. m. dutcheri; 6, M. m. fucosus; 7, M. m. 
fusus; 8, M. m. micropus; 9, M. m. montanus; 10, M. m. nanus; 11, M. m. nevadensis; 
12, M. m. pratincola; 13, M. m. rivularis; 14, M. m. undosus; 15, M. m. zygomaticus. 


d Koeppl 


Zoogeography SH 


scale of miles 


Fic. 8. Distribution of Microtus xanthognathus (from Hall, 1981). 


species are controversial, and many of them have at one time or 
another been affiliated with the genus Pitymys. 

Shrubland and woodland.—Southwestern North America is oc- 
cupied by two allopatric species. The California vole, M. califor- 
nicus, occurs in the broad sclerophyll (chaparral) oak woodlands 
and grassland of the Pacific coast from central Oregon (where it is 
geographically sympatric with several other species of Muicrotus) 
southward to northern Baja California (Fig. 11) (Humboldtian, 


— 


Fic. 7. Distribution of Microtus longicaudus and its insular allospecies M. coro- 
narius (15) (modified from Hall, 1981). Subspecies of M. longicaudus are: 1, M. l. 
abditus; 2, M. l. alticola; 3, M. 1. angusticeps; 4, M. l. baileyi; 5, M. 1. bernardinus; 6, 
M. 1. halli; 7, M. l. incanus; 8, M. 1. latus; 9, M. l. leucophaeus; 10, M. l. littoralis; 11, 
M. 1. longicaudus; 12, M. l. macrurus; 13, M. l. sierrae; 14, M. 1. vellerosus. 


Seo 


ta 


“Sf 


: S| 
\ 
ny 


scale of miles 


myllodontus; 4, M. r. 


i (modified from Hall, 1981). Subspe- 


S 
Cal 
uw 
Ss 
Q 
Ss 
e § 
= 8 
BE 
Si 
Sok 
wy 
eS 
S 
ScariA 
oN 
wy 
— 
= 3 
tw 5 
oS 
g .8 
2e 
fe! 
5 3 
Ey se 
oe ON 
w 
~~. 
Ds 
a 
= 
Dy 
+ fe 
Os 
Hn 
EY 
1S) 


richardson. 


Zoogeography 99 


scale ot miles 


Fic. 10. Distribution of Microtus chrotorrhinus (modified from Hall, 1981). Sub- 
species are: 1, M. c. carolinensis; 2, M. c. chrotorrhinus; 3, M. c. ravus. 


Diablian, Californian, San Bernardinian provinces). ‘The Mexican 
vole, M. mexicanus, occurs from the southern Rocky Mountains 
southward in the Sierra Madre of Mexico to central Oaxaca (Mad- 
rean-Cordilleran province) (Fig. 12). Both species usually inhabit 
grassy habitats within or adjacent to, oak and pine woodlands, re- 
spectively (Getz, this volume). The Mexican vole occupies one of 
the most xeric habitats among Nearctic Microtus, although it also 
may live in cool, moist sites (Getz, this volume). 
Grassland.—Farther east, the prairie vole, M. ochrogaster, is con- 


nd Koeppl 


Hoffmann a 


100 


TERY 


x . 


Zoogeography 101 


tinuously distributed in both mesic and xeric grasslands of the east- 
ern half of the northern and central Great Plains, from the southern 
Prairie Provinces of Canada south to Oklahoma, and eastward 
through the “Prairie Peninsula” to western West Virginia (Fig. 
13) (Saskatchewanian, Kansan, IIllinoian provinces). An isolated 
relict population (M. o. ludovicianus) once inhabitated the Gulf Coast 
prairies of eastern Texas and western Louisiana, but it may now 
be extinct. 

Temperate deciduous forest.—The temperate deciduous forest 
biome provides habitat for the woodland vole, M. pinetorum (Fig. 
14). This is a highly fossorial species that inhabits both meadow 
and forest habitats; M. pinetorum and M. ochrogaster are broadly 
sympatric in the broad ecotone between deciduous forest and grass- 
land biomes. The two species tend to segregate by habitat (Getz, 
this volume), but may use the same runways. A widely disjunct 
relict, the Jalapan woodland vole, M. quasiater, is known only from 
a small area in the Sierra Madre Occidental of central Mexico 
(Fig. 15). It may represent a peripheral isolate of M. pinetorum, or 
a relict of an earlier arvicolid invasion of the New World. Its prin- 
cipal habitat is meadow and grassland within the “oak forest as- 
sociation of tropical vegetation” (Hall and Dalquest, 1963). Thus, 
it may more properly belong to the next biome. 

Cloud forest.—The remaining three species also are poorly known. 
The Oaxacan vole, M. oaxacensis, is known only from evergreen 
“cloud forest” habitat in the vicinity of Vista Hermosa, in the Sierra 
Madre Occidental of Oaxaca (Fig. 16). The Zempoaltepec vole, M. 
umbrosus, is known only from the vicinity of Zempoaltepec and 
Totontepec, also in the mountains of central Oaxaca (Fig. 16). 
Finally, the Guatemalan vole, M. guatemalensis, has been found on 
several isolated mountain ranges from central Chiapas to central 
Guatemala (Fig. 16); both M. umbrosus and M. guatemalensis are 


—_— 


Fic. 11. Distribution of Microtus californicus (modified from Hall, 1981). Sub- 
species are: 1, M. c. aequivocatus; 2, M. c. aestuarinus; 3, M. c. californicus; 4, M. c. 
constrictus; 5, M. c. eximius; 6, M. c. grinnelli; 7, M. c. halophilus; 8, M. c. huperuthrus; 
9, M. c. kernensis; 10, M. c. mariposae; 11, M. c. mohavensis; 12, M. c. paludicola; 13, 
M. c. sanctidiegi; 14, M. c. sanpabloensis; 15, M. c. scirpensis; 16, M. c. stephens; 17, 
M. c. vallicola. 


102 Hoffmann and Koeppl 


S 


Ye 
ies 


Cie 


Fic. 12. Distribution of Microtus mexicanus (modified from Hall, 1981). Sub- 
species are: 1, M. m. fulviventer; 2, M. m. fundatus; 3, M. m. guadalupensis; 4, M. m. 
hualpaiensis; 5, M. m. madrensis; 6, M. m. mexicanus; 7, M. m. mogollonensis; 8, M. 
m. navaho; 9, M. m. neveriae; 10, M. m. phaeus; 11, M. m. salvus; 12, M. m. subsimus. 


found in montane pine-oak and evergreen cloud-forest biomes. None 
of the three shows any obvious close relationship to more northerly 
species of Microtus, and all probably are best regarded as relicts of 
early arvicolid invasions of the New World (see below). 


Zoogeography 103 


Q rm \ 
\ at a 


ee . 
eS 


scale of miles | 
! 


pee ol 


| 
+ 
? 
f 
<) 
\ 


Fic. 13. Distribution of Microtus ochrogaster (modified from Hall, 1981). Sub- 
species are: 1, M. 0. haydenii; 2, M. o. ludovicianus; 3, M. 0. minor; 4, M. o. ochrogaster; 
5, M. o. ohionensis; 6, M. o. similis; 7, M. o. taylori. 


Summary of Ecological Zoogeography 


It is clear from the foregoing that the largest number of species 
of Microtus in the New World (nine) are found in ecological for- 
mations associated with coniferous forest (taiga) biomes. Of these, 
three species occur primarily within boreal taiga (M. chrotorrhinus, 
M. pennsylvanicus, M. xanthognathus), three species within Pacific 
coastal taiga (M. canicaudus, M. oregoni, and M. townsendii), and 


104 Hoffmann and Koeppl 


Fic. 14. Distribution of Microtus pinetorum (from Hall, 1981). Subspecies are: 
1, M. p. auricularis; 2, M. p. carbonarius; 3, M. p. nemoralis; 4, M. p. parvulus; 5, M. 
p. pinetorum; 6, M. p. scalopsoides; 7, M. p. schmidti. 


three species within Rocky Mountain montane taiga (M. longicau- 
dus, M. montanus, and M. richardsoni). The southwestern pine-oak 
forest inhabitant, M. mexicanus, also might be included either here 
or with the three relict species (M. guatemalensis, M. oaxacensis, 
and M. umbrosus) that inhabit montane cloud forest, which includes 
a pine-oak forest aspect; these constitute the next largest ecological 
group. Tundra-dwelling voles comprise two species (M. miurus and 
M. oeconomus), both Beringian in distribution (see below), and re- 
cent entrants into the New World. In contrast, the two deciduous 
forest species (M. pinetorum and M. quasiater) probably are much 
more ancient. Finally, the broad-leaf sclerophyll woodland-shrub- 
land of the Pacific Coast (“‘chaparral’’) and its associated grassland 
harbors one species (M. californicus), as does the temperate grass- 
land of the Great Plains (M. ochrogaster). 

Thus, whereas most species of Microtus inhabit meadows and 


Zoogeography 105 


Fic. 15. Distribution of Microtus quasiater (from Hall, 1981). 


similar grassy habitats (Getz, this volume), in a broader sense most 
are forest and woodland species in terms of the biomes they inhabit. 
From their predominance in taiga biomes it also is possible to infer 
that Microtus long has been associated with northern forest and 
woodland environments. It is this historical dimension that we shall 
examine next. 


Historical Zoogeography 


Early Pleistocene 


“Modern” voles, including Microtus in the broad sense of this 
volume, first appeared in the New World in the early Pleistocene 
(Irvingtonian— Martin, 1979; Repenning, 1980; Zakrzewski, this 
volume), about 1.8—2.0 m.y.b.p. These first modern voles with root- 
less molars are placed in Allophaiomys (=Pitymys; see Zakrzewski, 
this volume), an extinct Holarctic genus thought by some to be 
ancestral either to modern Pitymys (van der Meulen, 1978; Za- 
krzewski, this volume) or to all later rootless cheektoothed voles 
(Chaline, 1974). According to Repenning (1980), these modern voles 
dispersed into the Nearctic from the Palearctic across the Bering 


106 Hoffmann and Koeppl 


O 100 


scale of miles 


oO 
0% 
$25] 

RLY 


OO 
S050 


Fic. 16. Distributions of M. oaxacensis (1), M. umbrosus (2), and Microtus gua- 
temalensis (3) (modified from Hall, 1981). 


land bridge. However, Martin (1979) was more cautious, and sug- 
gested that the earliest records in North America might predate 
those in Eurasia. In any event, the lineages of this early radiation 
probably include the subgenera Phaiomys (now restricted to the Old 
World) and early Neodon (Martin, 1974; Repenning, 1980). Sur- 
vivors of this early radiation in the New World may include M. 
umbrosus (Martin, 1974) and perhaps M. guatemalensis (Repen- 
ning, 1980), both of which exhibit relict distributions in the mon- 
tane cloud forests of Mexico and Guatemala (Fig. 16). 


Middle Pleistocene 


A later dispersal event, about 1.2 m.y.b.p., brought “‘even-more- 
modern-looking forms” (Repenning, 1980), including later Neodon, 
and the subgenus Pitymys (L. W. Martin [1979] and R. Martin 
[1974] placed the first appearance of Pitymys later, around 0.6 


Zoogeography 107 


m.y.b.p.). Survivors of these lineages may include M. quasiater (Re- 
penning, 1980) and M. oaxacensis (Martin, 1974, who also included 
M. guatemalensis here). Again, these are species with relict montane 
distributions at the southern extreme of the range of the genus (Fig. 
16). The Pitymys lineage in North America subsequently differ- 
entiated into at least two others, leading to M. (Pitymys) pinetorum, 
the temperate deciduous forest species (Fig. 14), and M. (Pedomys) 
ochrogaster, the temperate grassland species (Fig. 13) (see Martin, 
1974; van der Meulen, 1978; and Kurtén and Anderson, 1980). 

The earliest appearance of Microtus (sensu stricto) in the New 
World is controversial. Until recently, this was thought to be in the 
Middle Irvingtonian (M. paroperarius; Martin, 1979; van der Meu- 
len, 1978), but Repenning (1980) claimed that not only M. paro- 
perarius but also M. californicus first appeared around 1.8 m.y.b.p., 
at the beginning of the Pleistocene (see Zakrzewski, this volume). 
Another controversial, possibly early, date is for Microtus deceiten- 
sis, first described from Alaska (Guthrie and Matthews, 1972) and 
later from Saskatchewan (Harington, 1978), but referred to M. 
paroperarius by Zakrzewski (this volume). These faunas also are 
considered early Pleistocene by some (Kurtén and Anderson, 1980) 
or even late Pliocene (Repenning, 1980). That it is a Microtus with 
a primitive dental pattern is agreed, but whether it is a “side branch” 
(Kurtén and Anderson, 1980), or an early evolutionary stage ‘‘pos- 
sibly leading to M. xanthognathus” (van der Meulen, 1978), is not 
(see Zakrzewski, this volume). 

In either event, species of Microtus (sensu stricto) are common, 
either as immigrants or autochthons, in the late Pleistocene. Re- 
penning (1980) spoke of a “dispersal wave about 0.47 m.y.b.p., 
[when] Microtus pennsylvanicus floods North America east of the 
Rocky Mountains ....” Subsequently, all other living species are 
found as fossils, except M. canicaudus, M. oregoni, M. townsendit, 
and insular forms (Zakrzewski, this volume). 

If M. californicus did indeed appear in North America at the 
beginning of the Pleistocene, its restricted, possibly relict, distri- 
bution (Fig. 11) and its unusual habitat (broad-leafed sclerophyll 
vegetation) are understandable. However, its phylogenetic relation- 
ships to other Microtus, New or Old World, remain obscure. The 
same is true of another Pacific coast endemic, M. oregoni (Fig. 5). 
It has been placed in the subgenus Chilotus, which usually is re- 


108 Hoffmann and Koeppl 


garded as monotypic, though Ognev (1950) proposed a close rela- 
tionship between M. oregoni and the Old World M. socialis. Given 
its restricted range, ecological specialization, and isolated position 
among New World Microtus, it probably represents an early im- 
migration or evolutionary divergence. 

Another species possibly related to an otherwise Old World sub- 
genus is M. longicaudus which, with its insular allospecies, M. [/.] 
coronarius (Fig. 7), has been allocated to Chionomys (Anderson, 
1960). The subgenus Chionomys also includes M. nivalis, M. gud, 
and M. robert: of the western Palearctic, eastward to the Kopet Dag 
Mountains, and Lawrence (1982) implied that the eastern Pale- 
arctic M. millicens and M. mussert also might be related to this 
group. These latter two probably are relict species now restricted 
to the mountains of western China (Lawrence, 1982), but their 
ranges might be evidence of a biogeographic track (Wiley, 1981) if 
they and M. longicaudus do belong to Chionomys. Such a relation- 
ship would imply a fairly early dispersal of the ancestor of M. 
longicaudus across Beringia into the New World, but an alternative 
hypothesis is that M. longicaudus is convergent with Chionomys and 
evolved more recently from a New World lineage. 

The history of the New World water vole, M. richardsont, is 
plagued by similar uncertainty. Hooper and Hart (1962), Jannett 
and Jannett (1974), and others allocated this species to the genus 
(or subgenus; see Hall, 1981) Arvicola. However, it is difficult to 
account for M. richardsoni as a late Pleistocene immigrant from the 
Old World Arvicola lineage, and it may be an evolutionary lineage 
paralleling Arvicola but from an early Blancan Mimomys-like New 
World lineage (Hoffmann, 1980). A third alternative is that rich- 
ardsoni represents a “long independent history [and] separate der- 
ivation from Allophaiomys ...” (Martin, in Honacki et al., 1982). 
Finally, it has been suggested (Repenning, in litt.) that M. richard- 
sont 1s a late Pleistocene peripheral isolate of the M. xanthognathus 
lineage. Of these different possibilities, the last one now seems to 
us to be most likely. If so, and if M. xanthognathus is derived from 
M. deceitensis, then the three species of taiga-inhabiting voles (M. 
chrotorrhinus, M. richardsoni, and M. xanthognathus) that are now 
allopatric (Figs. 8-10) may represent a lineage that has been evolv- 
ing in North America since at least mid-Pleistocene, and perhaps 
earlier. 


Zoogeography 109 
Late Pleistocene 


The most widespread species of New World Muicrotus is M. penn- 
sylvanicus (Fig. 3); its history goes back to late mid-Pleistocene, 
about 500,000 years ago. It may be a descendant of M. paroperarius 
(Guthrie, 1965; Martin, 1972), an earlier immigrant and one of 
the first Microtus (sensu stricto) in North America (see above). This 
lineage in turn may have given rise to other lineages adapted to 
taiga meadows, such as M. montanus-M. canicaudus in the Rocky 
Mountains-Sierra-Cascade (Fig. 6), M. mexicanus in the southern 
Rocky Mountains-Sierra Madre (Fig. 12), and M. townsendii in 
the Pacific coastal taiga (Fig. 4). The superspecies Microtus [penn- 
sylvanicus| has a distribution characterized by several insular allo- 
species, M. [p.] brewer1 on Muskeget, and M. [p.] nesophilus on 
Gull Island (extinct); M. [p.] provectus on Block Island sometimes 
has been given species rank, and several insular subspecies have 
been named. In addition, a series of geographically isolated popu- 
lations occur along the margin of the species’ range, south to Florida 
(Fig. 3) (Woods et al., 1982) and Chihuahua (Bradley and Cock- 
rum, 1968). According to Repenning (1980), M. pennsylvanicus, 
although apparently abundant and widely distributed in the late 
Pleistocene, was found only east of the Rocky Mountains (see also 
Martin, 1968). Presently, an isolated relict population (M. p. kin- 
caidi) is found at Moses Lake in central Washington (Fig. 3). 

Farther west and south, taiga meadows are inhabited by the 
allopatric M. townsendu (Fig. 4). Rand (1954) was the first to 
suggest that Pleistocene isolation in taiga refugia south of the con- 
tinental ice might have led to divergence of an ancestral M. penn- 
sylvanicus, thus giving rise to M. townsend by peripheral isolation. 
The karyotype of living M. pennsylvanicus is 2n = 46 (FN = 50), 
whereas that of M. townsendu is entirely uniarmed with 2n = 50 
(FN = 48). The two karyotypes are derivable from one another by 
a combination of fusion/fission and inversion mechanisms (Gaines, 
this volume). 

Microtus mexicanus, which inhabits montane coniferous forest 
meadows to the south of the range of M. pennsylvanicus, has a 
distribution that suggests it also might have diverged from the an- 
cestral lineage through Pleistocene isolation (Fig. 12). The Mexican 
vole has a karyotype of 2n = 44 (FN = 54), and thus has six biarmed 


110 Hoffmann and Koeppl 


autosomal pairs as compared with three in M. pennsylvanicus 
(Gaines, this volume). It has diverged considerably from M. penn- 
sylvanicus and M. townsend in its habitat relationships, being 
adapted to more xeric conditions than the other two (Getz, this 
volume), and this suggests an earlier divergence. 

Of the small taiga meadow-dwelling voles, the one exhibiting the 
greatest amount of range overlap with M. pennsylvanicus is M. 
montanus (Fig. 6). The two species are geographically sympatric in 
the central and southern Rocky Mountains, but are segregated eco- 
logically. The meadow vole, where it co-occurs with the montane 
vole, usually is restricted to mesic grassland, whereas the latter is 
found in more xeric situations (Getz, this volume). Where M. mon- 
tanus lives in the absence of M. pennsylvanicus, it regularly inhabits 
mesic habitats as well (intermountain basins, Cascade-Sierra ranges). 
This habitat segregation probably is due to a combination of habitat 
selection and competitive interaction (Koplin and Hoffmann, 1968; 
Murie, 1969, 1971). Its present distribution is completely allopatric 
to that of M. townsendi; only where it takes the mesic habitat does 
it slightly and marginally overlap with M. mexicanus (Findley, 
1969). 

The montane vole also possesses one of the most derived karyo- 
types found among New World Microtus, with 2n = 24 (FN = 44), 
and a completely biarmed complement (Gaines, this volume). ‘This, 
plus the extent of sympatry, suggests that M. montanus has had a 
long and independent history. Whether it represents an early off- 
shoot of the M. paroperarius-M. pennsylvanicus lineage, or perhaps 
instead is derived from another New World lineage, is not presently 
resolvable. 

Microtus canicaudus has been regarded as a subspecies of M. 
montanus, but differs karyotically, electrophoretically, and morpho- 
logically (Hsu and Johnson, 1970). Its allopatric distribution (Fig. 
6) and the fact that it shares a highly derived (though slightly 
different) karyotype with M. montanus indicates that it is a recently 
diverged allospecies that probably evolved as a result of peripheral 
isolation in the late Pleistocene. 

The two lineages of New World Microtus (Figs. 1, 2) yet to be 
discussed are tundra specialists, M. oeconomus and M. muurus (to- 
gether with its insular allospecies, M. abbreviatus). Both are re- 
stricted to the northwestern corner of North America, and are not 
known to occur in suitable lowland tundra or alpine habitats to the 


Zoogeography 111 


east or south of their present ranges, even though no obvious phys- 
iographic barriers restrict their distribution. In the Old World, M. 
oeconomus has a much wider range, both geographically and eco- 
logically. It occurs throughout Siberia, southward into Mongolia 
and China, and westward through eastern Europe to the Baltic, 
Scandinavia, and Hungary, with an isolated relict population in the 
Netherlands (Honacki et al., 1982; Saint Girons, 1973). Within 
this range it occupies not only tundra, but also wet meadow and 
marsh habitats throughout the taiga, mixed forest, and forest-steppe 
zones. 

The Palearctic sister species of continental M. miurus is the nar- 
row-skulled vole, M. gregalis, and until recently the two often were 
considered conspecific (Rausch, 1964; Rausch and Rausch, 1968). 
Fedyk (1970) demonstrated chromosomal and morphological dif- 
ferences, and discussed the evolutionary history of the group. In the 
Old World, M. gregalis has a large range, being found throughout 
Siberia, south to Mongolia, China, and ‘Tadzhikistan, and west to 
the Ural Mountains and the White Sea. Within this area it is found 
in upland tundra and rocky, montane habitats, but also occupies 
forest meadows, forest steppe, various grassland-steppe habitats, 
and even semi-arid steppe (Ognev, 1950). 

Thus, the New World representatives of these Holarctic taxa are 
much more limited in habitat than Old World representatives, and 
restricted geographically to within or near the limits of the ice-free 
refugium of East Beringia. New World populations of M. oecono- 
mus have differentiated little from eastern Siberian populations 
(Nadler et al., 1976, 1978), and their occurrence on St. Lawrence 
Island (a surviving part of the Bering land-bridge) suggests that the 
species is a recent immigrant to the New World, probably within 
Wisconsin time (about 70,000 years ago; but see Zakrzewski, this 
volume). The New World narrow-skulled voles exhibit greater dif- 
ferentiation, and this might indicate a somewhat earlier divergence, 
perhaps during late Illinoian time (about 170,000 years ago). Nar- 
row-skulled voles are reported from pre-Wisconsinan glacial de- 
posits in Beringian Alaska (Kurtén and Anderson, 1980; Zakrzew- 
ski, this volume). 


Summary of Historical Zoogeography 


A clear relationship between evolutionary history, ecological as- 
sociation, and systematic position 1s indicated by the foregoing anal- 


112 Hoffmann and Koeppl 


yses. The earliest appearance of Microtus in the New World was 
in the early Pleistocene; these were primitive voles represented by 
surviving lineages of species with relict distributions in montane 
cloud forests at the southern edge of the Nearctic. They either are 
referred to monotypic subgenera (Orthriomys, Herpetomys) within 
Microtus, or are members of the subgenera (or genera) Pitymys or 
Neodon (Martin, 1974). 

The appearance in the middle Pleistocene of more modern lin- 
eages also may be related to other montane relict species surviving 
in central and southern Mexico (M. oaxacensis and M. quasiater) 
that also have been placed in Pitymys or Neodon. However, these 
pitymyine lineages also gave rise to the temperate deciduous forest 
vole, M. (Pitymys) pinetorum, and to the grassland vole, M. (Pe- 
domys) ochrogaster. Microtus californicus, a broad sclerophyll relict, 
also may have appeared at this time. 

The late Pleistocene saw repeated appearance (immigrations) of 
Microtus lineages. The first of these, about half a million years ago, 
was associated with Kansan glaciation. Paleogeographic evidence 
suggests that, at that time, taiga covered at least part of the Bering 
landbridge (Hoffmann, 1976), whereas more temperate vegetation 
may have been present earlier. The lineage leading to the taiga- 
dwelling specialists—M. xanthognathus, M. chrotorrhinus, and M. 
richardsoni—probably appeared then, as did the lineage leading to 
the less specialized M. pennsylvanicus. Other vole species found in 
taiga biomes also might have appeared about this time, such as M. 
(Chilotus) oregont and M. (Chionomys) longicaudus. 

Later in the late Pleistocene, climatic conditions on the Bering 
landbridge became more severe (Hoffmann, 1976), and only cold 
tundra and steppe-tundra species probably were able to survive 
Beringian conditions. There is evidence that, in the Ilinoian glacial 
period, the lineage leading to M. (Stenocranius) miurus reached East 
Beringia but no farther. Finally, in the Wisconsinan glacial period 
M. oeconomus also crossed Beringia. 

These last two or three major glacial periods were also charac- 
terized by displacement and fragmentation of taiga biomes south of 
the glacial ice (Hoffmann, 1976, 1981). This resulted in isolation 
and subsequent speciation in one or more of the Microtus lineages 
already present in North America, and to the evolution of M. mon- 
tanus and M. mexicanus in the Rocky Mountains-Sierra-Cascade- 
Great Basin and the Madrean-Cordilleran provinces, respectively, 


Zoogeography 113 


probably in the Illinoian. It also resulted in isolation and speciation 
of M. townsend and M. canicaudus in the Oregonian Province, 
probably in the Wisconsinan. Also during (or at the end of) the 
Wisconsinan, the several insular allospecies probably evolved: M. 
abbreviatus from M. miurus, M. coronarius from M. longicaudus, and 
M. breweri and M. nesophilus from M. pennsylvanicus. 

The above scenario is a testable evolutionary hypothesis in that 
it predicts the time and place of occurrence of the various lineages 
as fossils; it also makes certain predictions concerning phylogenetic 
relationships. 


Acknowledgments 


Research upon which this review was based in part was sup- 
ported by National Science Foundation grants DEB 80-04148 and 
80-07246 as part of a joint research project co-sponsored by the 
Academies of Sciences of the U.S. and U.S.S.R., and the bilateral 
Environmental Protection Agreement (Project 0.2.05-7104). Assis- 
tance in field and laboratory was provided by R. R. Patterson, R. 
L. Rausch, T. Pearson, J.-P. Airoldi, P. B. Robertson, C. F., N. 
W., C., R., and C. F. Nadler, Jr.; S. A., J. F., D. R., and B. E. 
Hoffmann, H. Levenson, L. R. Heaney, A. E. Kozlovskii, V. N. 
Orlov, V. E. Sokolov, M. N. Meier, A. Gill, M. Johnson, M. 
Gaines, and L. Deutsch. We also acknowledge the cooperation of 
the several state and provincial game departments in granting us 
permission to collect. 


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MACROANATOMY 


MICHAEL D. CARLETON 


Abstract 


UR basic knowledge of the morphology of Microtus has accu- 
mulated incidentally in the pursuit of greater taxonomic un- 
derstanding of the genus, its morphological limits, and its position 
within the web of kinship to other Arvicolidae. Although system- 
atists have focussed by far their greatest attention on variation in 
the dentition and cranial skeleton of Muicrotus, a rich amount of 
information is available for less traditional character complexes, 
such as the musculature, alimentary canal, and reproductive tract. 
In this chapter, that morphological information is reviewed under 
the headings of six organ systems—Integument, Skeleton and Ex- 
ternal Form, Musculature, Circulatory System, Digestive System, 
and Reproductive System—and presented within both a functional 
context and a phylogenetic framework. Many aspects of Microtus 
anatomy, particularly the cranial skeleton, associated masticatory 
musculature, and dentition, have been linked directly or indirectly 
to selection for exploitation of a herbivorous trophic niche, and 
species of Microtus are generally viewed as among the more derived 
of Arvicolidae with respect to character state development of such 
features. Curiously though, the genus Microtus as currently recog- 
nized seemingly lacks any uniquely derived traits that serve to un- 
ambiguously distinguish it from other Arvicolidae. Of the approx- 
imately 71 characters that have been distilled from various 
morphological and taxonomic investigations of Arvicolidae, the 
character states exhibited by specimens of Microtus are either prim- 
itive for Muroidea (22) or Arvicolidae (27), or variously shared 
with other arvicolid genera (22). Instead, the identification of Mz- 
crotus historically has been defined polythetically. These observa- 
tions lend support to the viewpoint that Microtus is at best a para- 
phyletic taxon. 


116 


Macroanatomy 117 


Introduction 


Perhaps no other group of rodents within Muroidea, an assem- 
blage numbering some 250 genera and over 1,000 species, possesses 
so distinctive a form as the Arvicolidae. Whether one considers 
species so disparate as the muskrat and bog lemming, the quality 
of “‘microtineness” is nonetheless penetrative: robust animals with 
short legs and tails, blunt muzzles, diminutive pinnae, and small 
eyes. The prismatic, hypsodont cheekteeth are definitive. Despite 
the priority of the family-group name Arvicolidae, voles of the genus 
Microtus, by their speciosity and ecological abundance, qualify as 
the morphotypical representatives of the family. This chapter ex- 
plores the macroanatomy of that genus. 

Mere description of form, the repetition of morphological terms 
and facts, is an unenlightening, not to mention boring, exercise. 
Morphology finds its heuristic expression in the taxonomic and 
functional insights that it provides to systematic biology, and it is 
this dualistic quality that keeps the study of morphology fresh and 
dynamic. As this chapter demonstrates, much of our knowledge of 
the gross anatomy of Muicrotus was incidentally generated in the 
pursuit of greater taxonomic comprehension of the group. Function, 
as a separate consideration, more often seemed to emerge as an 
afterthought from such taxonomically motivated discovery of mor- 
phological variety. Accordingly, in reviewing the morphological lit- 
erature on Muicrotus, I seek to present information within both a 
phylogenetic framework and a functional context. Several hierar- 
chical levels of relationship are pertinent to our morphological con- 
ception of the taxon Muicrotus. Of particular interest here are the 
anatomical variation exhibited by species constituting the genus, the 
diagnostic properties of Microtus with respect to other genera of 
Arvicolidae, and the distinctive attributes shared by Microtus and 
other Arvicolidae as members within the broader sphere of the vast 
and diverse Superfamily Muroidea. 

The cranial and dental illustrations that grace these pages were 
rendered by Janine Higgins, whose careful work and attention to 
detail I much appreciate. The figures are based on specimens housed 
in the National Museum of Natural History. Jean Smith patiently 
typed the various drafts of the manuscript. I dedicate this chapter 
to David J. Klingener, former major professor, who first introduced 


118 Carleton 


me to the delights of rodent anatomy through a manuscript for a 
chapter he had written on Peromyscus anatomy. The invitation to 
author this chapter on Microtus was consequently received and ac- 
cepted with pleasure and a sense of somehow coming full circle. 


Integument 


Species of Microtus are a rather sombre-colored lot. The pelage 
of most matches some shade of brown, varying from light, some- 
times grayish, to very dark, almost blackish. Bright splashes of color 
are primarily limited to the yellow or rust-colored noses observed 
in M. chrotorrhinus and M. xanthognathus. The fur texture is like- 
wise unremarkable, being moderately thick, long, and lax in the 
majority of species. The longer guard hairs and dense, wooly un- 
derfur of the water vole (M. richardsonz) and the short, finely-dense, 
‘“molelike” pelt of species of the subgenus Pitymys, constitute the 
prinicipal textural variants within the genus. Unlike pelage texture 
and color, more systematic attention has been focussed upon other 
cutaneous features, namely skin glands, the Meibomian glands of 
the eyelids, and the plantar footpads. 


Skin Glands 


Differences in pelage texture, color, density, and length usually 
indicate the location of hypertrophied sebaceous glands, which ex- 
ude an odiferous, lipidic substance. The glands undergo rapid dif- 
ferentiation coincident with puberty, are typically better developed 
in males but may be equally pronounced in both sexes, are highly 
sensitive to androgen levels, and function in dispersing scents that 
mediate many crucial aspects of arvicolid behavior (for example, 
individual recognition, territory, social dominance, reproductive 
condition, and breeding status). 

Early students of arvicolid systematics, such as Bailey (1900) and 
Miller (1896), accorded taxonomic significance to the presence— 
absence and location of the skin glands and incorporated this vari- 
ation into their identification keys, a variation still used in taxo- 
nomic keys (Hall, 1981). Howell (1924) detailed the size, age, and 
sexual variation of the hip glands in a population of Microtus mon- 
tanus. 

Quay (1968) provided the first exhaustive collation of sebaceous 


Macroanatomy 119 


patches in Arvicolidae. He identified four zones on the posterolater- 
al region of a vole’s trunk where the glands occur: caudal, rump, 
hip, and flank. Caudal glands exist only in Dicrostonyx and rump 
glands in Lemmus and Myopus (Claussen, 1975; Quay, 1968). Oth- 
er arvicolid genera have either flank (most) or hip glands or lack 
posterolateral glandular development altogether (Ondatra, Ellobius, 
and Prometheomys). Microtus encompasses species in each of the 
last three categories, but the glandular occurrence does not accord 
with current subgeneric alignments. Quay documented hip glands 
in Pitymys and some Microtus; flank glands in Aulacomys, Steno- 
cranius, some Microtus, and possibly Herpetomys and Pedomys; but 
discovered no posterolateral glands in Chilotus, Orthriomys, and cer- 
tain Microtus. Quay reported that, at high latitudes, all adult male 
and female M. oeconomus possessed well developed hip glands; yet, 
at more southern localities, the percentage of voles with highly 
developed glands decreased, especially among females. Quay sug- 
gested that this cline may generally apply to North American M:- 
crotus at the specific and populational levels. Jannett (1975), how- 
ever, cautioned that, in view of the responsiveness of cutaneous 
glands to hormonal titres, variation in their development within 
species could relate to populational differences in the timing and 
extent of reproductive activity. 

The question of the polarity of evolution of glandular zones in 
Arvicolidae is an interesting one. Quay (1968) reasoned that the 
breadth of representation of skin glands among arvicolids argues 
for their early acquisition, probably as flank patches, during their 
evolution. While the presence of some sebaceous zone in the ances- 
tral arvicolid seems probable, the decreasing histological complexity 
of the posterior glands and the occurrence of caudal and rump 
glands only in lemmings, forms otherwise thought to be primitive, 
suggest that a transformation series from caudal to rump to hip to 
flank is a plausible alternative. The diverse anatomical locations of 
the glandular zones presuppose different postures and motions as- 
sumed when animals dispense their scents (see, for instance, Jannett 
and Jannett, 1974; Quay, 1968; Wolff and Johnson, 1979) and 
may reflect the radiation of arvicolids into dissimilar structural hab- 
itats (for example, open tundra, boreal forest floor, grass runways, 
subterranean tunnels, and river banks). The absence of skin glands 
in some Microtus is considered a derived trait (Jannett, 1975; Quay, 
1968). Jannett (1975) stimulated an atypical differentiation of hip 


120 Carleton 


glands in M. longicaudus and M. pennsylvanicus, species which nor- 
mally lack such glands, by administering large dosages of exogenous 
testosterone. He interpreted these results as additional proof that 
the progenitors of these two voles possessed skin glands and that 
the cutaneous target zones had lost their sensitivity to physiologi- 
cally normal androgen levels. His study also underscores the pos- 
sible evolutionary plasticity of these glandular features and the po- 
tential for reversals and convergences. Recently, Boonstra and 
Youson (1982) and Tamarin (1981) have found hip glands in field 
populations of M. pennsylvanicus. 


Meibomian Glands 


The eyelids of arvicolids, like those of other mammals, contain 
modified sebaceous glands, called Meibomian or tarsal glands. Sev- 
eral authors have revealed differences among arvicolids involving 
the number, size, and position of these glands, differences which do 
not correlate with season of capture, sex, or age of the animals 
(Dearden, 1959; Hrabé, 1977, 1978; Quay, 1954a). Quay’s (19542) 
study is the broadest taxonomically and encompasses most subgen- 
era of North American Microtus. In the primitive condition, the 
glands are smaller, more evenly spaced, and numerous; species of 
Dicrostonyx, Lemmus, Synaptomys, Clethrionomys, Lagurus, and 
Phenacomys fall into this category (Dearden, 1959; Quay, 1954a). 
Fewer Meibomian glands with large, uneven gaps between them 
characterize the progressive condition, as observed in Arvicola, On- 
datra, and species of Microtus. The reduction in glandular number 
seems to be compensated by an increased size of those that remain, 
especially the posterior ones which extend beyond the eyelid margin 
(=extrapalpebral glands). Microtus species are surprisingly uniform 
and generally average between three and six tarsal glands; M. 
(Stenocranius) miurus is the most divergent, having a mean of nine 
glands. The functional or ecological correlates of this reductional 
trend remain obscure. 


Plantar Footpads 


The number, size, and position of plantar pads or tubercles have 
been used in taxonomic keys of Arvicolidae (Bailey, 1900; Dukelski, 
1927; Hinton, 1926; Miller, 1896). Most genera have either five 
or six metatarsal pads, but the densely furry soles of Dicrostonyx 


Macroanatomy 121 


apparently lack pad definition. The maximum number of six pads, 
probably the plesiomorphic state, consists of four interdigitals, sit- 
uated near the phalangeal bases, and the thenar and hypothenar, 
set closer to the heel. Although most genera exhibit a constant 
number of plantar pads, Microtus contains species with either five 
or six. Miller (1896) and Bailey (1900) employed this variable at 
the subgeneric level in Microtus, identifying Aulacomys, Chilotus, 
Herpetomys, Orthriomys, Pedomys, and Pitymys as having five pads, 
and Microtus and Stenocranius as having six. The stability of this 
character within Microtus should be more thoroughly documented. 
Howell (1924), for instance, reported substantial variation in a 
single population of M. montanus, whereas Dukelski (1927) con- 
cluded that plantar pad morphology was appropriately conservative 
for application at lower taxonomic levels. In addition to their ob- 
vious functional connotation with respect to locomotion and type of 
substrate, the plantar pads are sites where sweat glands are local- 
ized (Griffiths and Kendall, 1980). 


Skeleton and External Form 


Cranial and External Morphometrics 


Mensural data on the skull and external form of Microtus is 
diffusely spread through the literature. The compilation in Table 
1 is intended only to introduce the more comprehensive studies that 
contain tabulations of cranial and external variables; many more 
sources of measurements exist, particularly in faunistic accounts. 
Earlier studies often provided measurements of individual speci- 
mens but lacked sample statistics. Although many dimensions have 
been used historically, only some dozen have been consistently re- 
corded (Table 1). Perhaps the preeminence of these variables fol- 
lowed the precedent set by their employment in early studies (for 
example, Howell, 1924; Kellogg, 1918). More likely, their popu- 
larity stems from their repeatability and the ease of positioning the 
caliper’s jaws about the anatomical landmarks which characterize 
the arvicolid skull (Figs. 1, 2). 

Morphological heterogeneity between and within population 
samples generally has been partitioned into geographic and non- 
geographic sources of variation, the latter subdivided into variation 
associated with age, secondary sexual dimorphism, seasonal influ- 


122 Carleton 


TABLE 1 
CRANIAL DIMENSIONS AND SOURCES OF MENSURAL DATA FOR 
New Wor_pb Microtus 


Dimension Literature source and species* 


Lengths 


an 


Alveolobasilar 
Angular process 
Basilar 


mW 


Bony palate 


2 

2 

1 

1 
Condyloalveolar 3 
Condylobasal 1 
Condylobasilar 1 
Condyloincisive 3 
2 

2 

1 

3 

2 


Condylopalatal 
Condylozygomatic 
Dentary 

Diastema 

Incisive foramen 


> 


Maxillary toothrow 
(alveolar) 1 
Nasal 1 
Occipitonasal 1 
Palatilar 4, 
Rostral 7, 
Total toothrow 
(11-M3) 13 
Widths 


Alveolar (across 
toothrows) 
Braincase 


Nt CO W 


Interorbital poe 4s 0, 70,95 10 e121 S14 
Interparietal 
Lambdoidal 
Mastoid 
Postpalatal 
Prelambdoidal 


Rostral 


, 3, 6, 8,9, 10, 11, 14 
4.5 oy 12,13 


me hOA MRK HN KH HB ANIN 


8,1 
8, 1 
Zygomatic Do ADs. 0. fabs Oo LOS Ie 28 Se 


Miscellaneous 
Cranial capacity 250 
Depth of braincase 6, 14 
Height of skull 128 See Seale 14 
Palatofrontal height 8 


* 1. Kellogg (1918): M. californicus. 
2. Howell (1924): M. montanus. 


Macroanatomy 123 


ences, and a vague category usually labelled “individual.” There 
are other ways to categorize and view biological variation (see, for 
example, Mayr, 1969; Yablokov, 1974), but the above divisions 
illustrate the approach commonly adopted by systematists who have 
interpreted continuous variation of the skull and external form of 
Microtus. For an appreciation of the evolving treatment of popu- 
lation variation in taxonomic studies of Microtus, the reader should 
consult Anderson (1959), Howell (1924), Snyder (1954), and Choate 
and Williams (1978). Howell’s (1924) exhaustive exposition of 
variation in a population of M. montanus yosemite warrants special 
mention and, although antiquated in some regards, could serve in 
any mammalogy course as a didactic introduction to sources of vari- 
ation in a mammalian species population. 

Cranial changes during growth are frequently striking in muroid 
rodents and especially so in arvicolids. The authors above have 
qualitatively described the suite of ontogenetic changes in Microtus: 
the skull loses its rounded, fragile conformation and becomes heavi- 
er and “squared”; bony processes and ridges, especially the post- 
orbital process and lambdoidal ridge, become strongly expressed 
and cranial sutures disappear; as the skull enlarges, the propor- 
tional relationship of the facial and cranial regions shifts from rel- 
atively short rostrum and wide braincase to an elongate, narrower 
configuration; the weak, narrow zygoma expand and bow laterally; 
the dorsal curvature of the skull progressively flattens. To reduce 
age-related biases, investigators have grouped skulls into growth- 
age cohorts. Because the molars of Microtus continuously erupt, 
stages of tooth wear, used as age indices in other muroid studies, 


3. Goin (1943): M. pennsylvanicus. 

4. Hall (1946): M. longicaudus, M. montanus. 

5. Durrant (1952): M. longicaudus, M. mexicanus, M. montanus, M. richardson. 

6. Anderson (1954, 1956, 1959): M. montanus, M. pennsylvanicus. 

7. Snyder (1954): M. pennsylvanicus. 

8. Bee and Hall (1956): M. miurus, M. oeconomus. 

9. Jones (1964): M. ochrogaster, M. pinetorum, M. pennsylvanicus. 

10. Rausch (1964); Rausch and Rausch (1968): M. abbreviatus, M. miurus. 

11. Armstrong (1972): M. longicaudus, M. mexicanus, M. montanus, M. ochrogas- 
ter, M. pennsylvanicus. 

12. Kirkland (1977): M. chrotorrhinus. 

13. Choate and Williams (1978): M. ochrogaster. 

14. Wilhelm (1982): M. mexicanus. 


124 Carleton 


pmx 


Fic. 1. Lateral view of cranium of male Microtus (Stenocranius) miurus, Alaska. 
The key that follows defines abbreviations that appear in this figure and in Figs. 


2-4. 
Foramina and Fossae 


alc—alisphenoid canal 
eam—external auditory meatus 
fm—foramen magnum 
fo—foramen ovale 
foa—foramen ovale accessorius 
hg—hypoglossal 

icf—internal carotid fissure 
inc—incisive 

ioc—infraorbital canal 
ipm—interpremaxillary 
jg—jugular 

ml—middle lacerate 
mpf—mesopterygoid fossa 
ms—masticatory 
nlc—nasolacrimal canal 
op—optic 

pg—postglenoid 
plpp—posterolateral palatal pits 
ppf—parapterygoid fossa 
ppl—posterior palatine 
smx—sphenomaxillary 
sph—sphenoidal fissure 
spv—sphenopalatine vacuities 
ss—subsquamosal 
st—stapedial 
stm—stylomastoid 


Bones and Processes 


als—alisphenoid 
alst—strut of alisphenoid 
bo—basioccipital 
bs—basisphenoid 


fr—frontal 
ip—interparietal 
ju—jugal 


lbr—lateral bridge 
Ir—lambdoidal ridge 
mb—mastoid bulla 
mr—median ridge 
mx—maxilla 
na—nasal 
os—orbitosphenoid 
pa—parietal 
pl—palatine 
pmx—premaxilla 
pop—postorbital process 
ps—presphenoid 
pt—pterygoid 
sq—squamosal 
tp—tympanic bulla 
tr—temporal ridge 
ts—transverse shelf 
zya—zygomatic arch 
zyp—zygomatic plate 


Macroanatomy 125 


4 
_ ) 4 ——, zya 
| A 
/ | 
/ me ‘ 
| oe \ a | ~ | 
i ae “ \ 
| | # \ 
“hava [| 


alc 9 - 1p ‘ ml 
ee qe ‘ j 
b: FA ay icf 
Va { F ( 
eam \ \ 
e ‘eto 
a <¢ yo 4 
WwW i> 
Ev 
. - ' 
fm 


Fic. 2. Ventral view of cranium of male Microtus (Stenocranius) miurus, Alaska. 
For abbreviations, see Fig. 1. 


cannot be assigned. As a result, systematists have relied upon cranial 
dimensions (Howell, 1924), ratios compounded therefrom (Ander- 
son, 1959), or suture closure and ridge development (Choate and 
Williams, 1978; Klimkiewicz, 1970; Snyder, 1954) in their recog- 
nition of age classes. Snyder (1954) and Anderson (1959) construct- 
ed ratio diagrams of several cranial variables to portray the amount 
of age-related change and to identify which variables most quickly 
attain “‘adult” dimensions. Cranial breadth, prelambdoidal breadth, 
height of skull, and interorbital width undergo relatively little mod- 
ification with age, while rostral, condylobasilar, and alveolobasilar 
length and zygomatic breadth change dramatically. Gebczynska 


126 Carleton 


(1964) monitored growth in cranial dimensions using laboratory- 
raised M. agrestis and verified the same pattern of allometric changes. 

Engels (1979) nicely elucidated these allometric properties in the 
skull of M. arvalis by tracing the growth of individual bones. Using 
discriminant function and canonical variate analyses, he demon- 
strated that the growth rates of the toothrows and bones of the 
braincase, orbits, and bullae abate by the postnatal day 22; conse- 
quently, their dimensions are comparatively age-invariant following 
weaning. In contrast, facial bones (nasals, premaxillae, and max- 
illae) and those of the basicranial axis continue growth over a longer 
period, contributing a significant age factor to their variability in 
populations. An axis of decreasing duration of growth exists from 
anterior to posterior for the dermal roofing bones. The interaction 
of these developmental tendencies imparts the proportional read- 
justments that contrast the skulls of juvenile and adult voles as 
described above. 

Secondary sexual differences in size are not conspicuous in M:- 
crotus, but where such disparity exists, males are the larger sex. 
Slight size dimorphism has been recorded in M. chrotorrhinus 
(Kirkland, 1977), M. longicaudus (Findley and Jones, 1962), M. 
mexicanus (Findley and Jones, 1962), M. miurus (Bee and Hall, 
1956), M. montanus (Anderson, 1959; Howell, 1924), M. oeconomus 
(Bee and Hall, 1956), and M. pennsylvanicus (Goin, 1943; Snyder, 
1954). Although males consistently average larger than females, the 
hiatus is usually insignificant statistically, leading investigators to 
combine measurements of the sexes for analytic purposes (Ander- 
son, 1959; Choate and Williams, 1978; Findley and Jones, 1962; 
but see Snyder, 1954, for an exception). In addition to averaging 
larger, authors have commented that males exhibit greater extremes 
of development, an observation supported by the higher coefficients 
of variation derived for most cranial variables of the male gender 
in M. montanus and M. pennsylvanicus (Anderson, 1959; Goin, 
1943; Howell, 1924). In view of the size differences observed in 
other species, it is interesting that Choate and Williams (1978) 
discovered no significant sexual dimorphism in M. ochrogaster, nor 
did either sex average consistently larger among their samples. The 
degree or presence of sexual dimorphism in size should be verified 
for other species of Microtus, and the association of species’ mating 
systems with the extent of dimorphism should be explored. 

The contribution of seasonal effects to non-geographic hetero- 


Macroanatomy 127 


geneity of population samples has been addressed infrequently but 
may account for appreciable inter- and intralocality variation, es- 
pecially among species having northern distributions. Bee and Hall 
(1956) substantiated remarkable seasonal differences in cranial size 
and shape for populations of M. oeconomus and M. miurus inhab- 
iting the arctic slope of Alaska. Microtus miurus born in spring and 
summer possess the narrow braincase and elongate skull character- 
istic of the subgenus Stenocranius, whereas individuals born in late 
fall and winter resemble the nominate subgenus in cranial confor- 
mation. Bee and Hall (1956) attributed these dissimilarities to the 
rapid growth of spring- and summer-reared animals, fostered by 
the richer diet and less stressful climate, and cautioned that under- 
standing variation in these northern Microtus requires equal as- 
sessment of seasonal and geographic effects. Conceivably, the im- 
portance of seasonal influences diminishes in more southern and 
presumably more equable environments, a relationship that could 
be evaluated by comparing locality samples of a species such as M. 
pennsylvanicus, which has a broad latitudinal distribution. 

The residual population variation not explained by age, sexual 
dimorphism, or season of capture is characterized as “individual,” 
and the sample statistic Coefficient of Variation is often used to 
convey the amount of this variation. Coefficients of variation for 
cranial dimensions are usually less than 10.0 and frequently fall 
between 2.5 and 6.0, but those for external measurements are typ- 
ically greater (Choate and Williams, 1978; Goin, 1943; Howell, 
1924; Snyder, 1954; Wilhelm, 1982). These values fit the broad 
pattern of variability of linear skeletal measurements distilled from 
studies of numerous kinds of mammals (Yablokov, 1974). The in- 
vestigations of Goin (1943) and Snyder (1954) employed the same 
locality sample of M. pennsylvanicus but disclosed quite different 
magnitudes of individual variation. Snyder noted that this discrep- 
ancy probably arose from his use of more restricted age classes and 
the consequent elimination of some age-related size increases. Rath- 
er than an explanatory source of population heterogeneity, variation 
termed “individual” is more often an all-other category tailored to 
the convenience and purpose of a specific study and cannot be as- 
sumed to reflect the underlying genetic variability intrinsic to the 
population. Still other factors, either procedural or biological, may 
be contributive. 

The number of subspecies recognized for most species of Microtus 


128 Carleton 


bears testimony to the occurrence of geographic variation (see Hoff- 
mann and Koeppl, this volume). In his study of Californian M. 
montanus, Kellogg (1922a) observed that his samples are recogniz- 
able colonies whose center of differentiation corresponds to separate 
marshy areas. Fortunately, he concluded that formal identification 
of each variant would only create a nomenclatural morass. Snyder 
(1954) performed analyses of variance on samples of M. pennsyl- 
vanicus pennsylvanicus and demonstrated significant locality effects 
for most external and cranial measurements within a restricted 
geographic area of northwestern Pennsylvania. Furthermore, sam- 
ples of several subspecies of M. pennsylvanicus from northeastern 
North America collectively exhibited the range of variation docu- 
mented for just the localized samples of M. p. pennsylvanicus, a 
result which led Snyder to question the purpose of so many sub- 
species. Findley and Jones (1962) examined patterns of variation 
among disjunct populations of M. longicaudus, M. mexicanus, and 
M. montanus from montane regions of the southwestern U.S. and 
observed a positive correlation between the amount of geographic 
variation within a species and the degree of geographical or ecolog- 
ical restriction of its constitutive populations. Snell and Cunnison 
(1983) assessed patterns of interpopulational cranial variation of 
M. pennsylvanicus from throughout its range and found that phe- 
netic distances among populations did not correspond to geographic 
distances. They concluded that geographic proximity is not a good 
estimate of isolation of populations, but that other factors (for ex- 
ample, topographical complexity, intervening unfavorable habitats, 
and sensitivity to local selection pressures) probably account for the 
disruption of genetic continuity and maintenance of morphological 
differences among geographically close populations of M. pennsyl- 
vanicus. 

These four cases, drawn from different times and exemplifying 
different methods and perspectives, are cited not to revive debate 
on the subspecies concept but to emphasize the demic nature of 
geographic variation that characterizes populations of Microtus and 
that is expressed in the subtle but demonstrable differences in size 
and shape between those populations. 

As is true for the subspecific category as applied to other mam- 
mals, the recognition of geographic races of Microtus species rests 
primarily on differences in size, proportion, and pelage color. Few 
taxonomic studies, however, have attempted to quantify broad geo- 


Macroanatomy 129 


graphic trends and objectively delimit subspecific boundaries. An- 
derson (1959) qualitatively scored coat color in M. pennsylvanicus 
using an exemplar method, mapped the distribution of mean color 
values, and discerned geographical groupings that aided his delin- 
eation of subspecies. Reflectance analyses of pelage color in M. 
ochrogaster from the central Great Plains, however, disclosed no 
meaningful trends or patterns of racial differentiation (Choate and 
Williams, 1978). In M. montanus, Anderson (1959) detected a geo- 
graphic trend toward larger-bodied voles from the southern part of 
its range, a reversal of Bergmann’s generalization on ecophysiolog- 
ical affects on body size. Choate and Williams (1978) noted a sim- 
ilar body-cline in M. ochrogaster. Snell and Cunnison (1983) more 
thoroughly explored the relationship of climate and cranial varia- 
tion in M. pennsylvanicus, using several multivariate techniques to 
assess the effects of 15 climatic variables. They too noted an inverse 
correlation of size and temperature, extreme low temperature and 
mean annual number of days with frost being two of the most 
significant climatic factors explaining cranial variation. 

The studies of Choate and Williams (1978), Snell and Cunnison 
(1983), and Wilhelm (1982) constitute the first extensive use of 
multivariate methods in collating geographic variation of morpho- 
metric variables used to describe Microtus populations. 


Qualitative Cranial Features 


Besides size and shape, other aspects of cranial morphology have 
commanded attention in systematic studies of Microtus, among them 
the condition of the posterior palatal area, the occurrence of cranial 
foramina, and the septal development of the bullar chambers. Al- 
though the variation observed in these traits is described as discon- 
tinuous, especially as dogmatically used in binary keys, extensive 
examination has revealed intermediate stages at some hierarchical 
level of comparison. Some of this heterogeneity fits Berry and Searle’s 
(1963) picture of epigenetic polymorphism, in which variation is 
realized during ontogeny, perhaps as a result of developmental 
thresholds for character expression that result in discrete adult phe- 
notypes. Such epigenetic traits may be constant in some species, or 
even in certain populations of a species, but they exhibit polymor- 
phic variation in others. Hilborn (1974) surveyed the occurrence of 
some cranial foramina in M. californicus and concluded that the 


130 Carleton 


SPV 


Fic. 3. Ventral view of two common palatal arrangements observed in Arvi- 
colidae: left, simple condition as exemplified by Clethrionomys gapperi, Virginia; 
right, complicated configuration as exhibited by Microtus pennsylvanicus, Wisconsin. 
For abbreviations, see Fig. 1. 


prevalence of such traits could be used to measure genetical differ- 
ences between local populations. 

In their pioneering studies of arvicolids, Hinton (1926) and Mil- 
ler (1896) attached particular taxonomic import to the bony archi- 
tecture of the posterior palatal region. Bailey (1900:10) gave palatal 
development as a trenchant generic character in his diagnosis of 
Microtus: ““Palate with median ridge, distinct lateral pits, complete 
lateral bridges (not terminating in posterior shelf in any American 
species).”” His description characterizes the more prevalent of the 
two basic anatomical plans recognized in Arvicolidae (Fig. 3). In 
the other, the palate terminates as a transverse shelf, with or with- 
out a median spine, and the palatal pits extend anteriorly and above 
the palatal shelf. This arrangement is seen in Clethrionomys, Eoth- 
enomys, and, to a lesser degree, in Lemmus. Although the palatal 
types seem clearly defined, assignment of genera, species, and some- 
times individuals to one condition or the other is sometimes equiv- 
ocal. Thus, Hooper and Hart (1962) stated that all degrees of 
intermediacy are found within Arvicolidae, and Rausch (1964) il- 
lustrated gradations between the extreme palatal configurations once 
thought to distinguish Old World M. gregalis from New World M. 
miurus. Hinton (1926:16) drew attention to the thick processes of 


Macroanatomy 131 


the maxillary and palatine bones and emphasized this feature as an 
integral characteristic of arvicolids. The degree of thickness varies 
within Arvicolidae, however, and this variation seemingly relates to 
posterior palatal development. As recognized by Hinton, the thick- 
ness of the palatal extensions of the maxillaries and palatines cor- 
relates with the hypertrophied alveolar cavities of the high-crowned 
molars. And like the incremental development of hypsodonty ob- 
served between genera of arvicolids, it is not surprising that a cor- 
responding gradation in palatal structure exists also. 

The incisive foramina in Microtus are either broad and oval- 
shaped at both ends or constricted posteriorly. Anderson (1959) 
recognized seven states of foraminal shape bridging these extremes 
and tabulated their frequency of occurrence in 11 species repre- 
senting five subgenera of Microtus. Most species’ histograms spanned 
several character states but always displayed a clear-cut modality. 
Quay (19545) demonstrated that the posterior constriction is con- 
fined to the maxillary portion of the incisive foramina and may 
become expressed strongly in older animals. In M. (Aulacomys) 
richardsoni, the posterior closure is so complete that the absolute 
length of the incisive foramina decreases with age; a slight increase 
in length represents the normal growth pattern in other Microtus. 
Quay did not speculate on the functional significance of this phe- 
nomenon. 

The patency of foramina that pierce the base of the alisphenoid 
bone varies among arvicolids (terminology follows Wahlert, 1974). 
In the hypothesized primitive state, a strut of the alisphenoid de- 
marcates a medial masticatory foramen, which transmits the mas- 
ticatory and buccinator branches of the trigeminal nerve (V3), and 
a posterolateral foramen ovale accessorius, which conducts other 
branches of V3. This condition obtains in Ellobius, Eothenomys, and 
the lemmings Lemmus, Myopus, and Synaptomys. In the remaining 
genera, including most species of Muicrotus, the base of the ali- 
sphenoid has a single, spacious opening (Fig. 4), presumably de- 
rived by loss of the alisphenoid strut. Berry and Searle (1963) scored 
the double-foramina condition in 83% of the Lemmus lemmus ex- 
amined, but in only 1% of one population of Microtus agrestis and 
none of another. In conformance with Berry and Searle’s results, I 
discovered that a single opening prevails in most Microtus (32 of 
35 species examined). Nevertheless, two Old World species, M. 
majort and M. montebelli, generally possess discrete masticatory and 


132 Carleton 


Os 


fo 


Fic. 4. Ventrolateral view of orbital and alisphenoid region of Microtus oecono- 
mus, Alaska (top), and M. oregoni, Oregon (bottom), illustrating occurrence of fo- 
ramina. For abbreviations, see Fig. 1. 


Macroanatomy 133 


ovale foramina, and one trans-Beringean species, M. oeconomus (Fig. 
4), commonly exhibits both, but I did not assay frequencies in detail. 

Some uncertainty has attended the identity of another cranial 
foramen, a small one situated between the maxillary and alisphe- 
noid bones and ventral to the sphenoidal fissure. This foramen 
transmits a branch of the internal maxillary artery, its continuation 
in the lower orbit evidenced by a faint groove across the maxillary 
bone. Within Arvicolidae, the foramen occurs in Myopus, Synap- 
tomys, Lagurus (Lemmiscus), Arvicola, and most species of Microtus. 
Among North American Microtus, it is uniformly lacking in M. 
oeconomus (Fig. 4) and variable in M. pinetorum and M. quasiater. 
The variable extent of contiguity between the alisphenoid and max- 
illary bones that encircle this foramen suggests a plausible trans- 
formation series associated with the degree of hypsodonty and com- 
plementary height of the molar alveolar capsules (Fig. 4). Both 
Guthrie (1963) and Hinton (1926) observed that the space enclosed 
by the maxillary-alisphenoid junction is homologous with the ven- 
trolateral portion of the sphenoidal fissure in those arvicolids which 
lack this accessory foramen. The dorsal extension of the alveolar 
capsules that accompanied the evolution of extreme hypsodonty re- 
sulted in contact of the maxillary palisades with the alisphenoid, 
thereby sequestering the ventrolateral part of the sphenoidal fissure 
as a new foramen. Howell (1924) termed the opening the foramen 
rotundum, but Hill (1935) noted the incorrectness of Howell’s des- 
ignation and instead called it the alisphenoid foramen. Because the 
latter name invites confusion with the alisphenoid canal, because 
the opening is not strictly homologous with the anterior end of the 
alisphenoid canal of other rodents, and because the foramen ap- 
parently evolved as a neomorphic trait only in certain arvicolids, I 
suggest the positional term sphenomaxillary foramen. 

The auditory bullae of arvicolids are globose structures (Fig. 2), 
appearing moderately inflated compared to most cricetines but not 
matching the outsized proportions seen in many gerbillines. Hooper 
(1968) examined serial cranial sections of Lemmus, Synaptomys, 
Clethrionomys, Neofiber, and three species of Microtus, and dis- 
cerned three types of middle ear systems, termed the open, inter- 
mediate, and closed. In examples of the first (for example, Cleth- 
rionomys), a large accessory tympanum is present, and the walls of 
the mastoid and tympanic bullae lack osseous internal septa and 
spicules, thus presenting an open bullar chamber. In forms exhib- 


134 Carleton 


iting the closed system (for example, Lemmus), an accessory tym- 
panum is absent, and the interior walls of the mastoid and tympanic 
capsules bear thick masses of spongy bone that greatly restrict the 
free space of the chambers. Microtus possesses the intermediate type, 
in which the accessory tympanum consists of a minute arc between 
the dorsal lamina of the tympanic bone, and the bullar walls have 
moderate amounts of cancellous partitions and struts. Even within 
the “intermediate” category, species of Microtus vary appreciably 
in the density and completeness of these bony projections: sparse in 
the subgenus Orthriomys; moderate in Aulacomys, Herpetomys, Pe- 
domys, and some Microtus; and high in Chilotus, Pitymys, Steno- 
cranius, and many Microtus. 

The bony meshwork of the bullae reduces the unobstructed space 
behind the tympanic membrane. Simkin (1965) postulated that the 
cancellous bone functions as an acoustic filter, dampening out bio- 
logically unimportant frequencies from the animal’s environment. 
His suggestion seems compatible partially with Fleischer’s (1978) 
idea that the cancellous network acts to suppress undesirable res- 
onances in a middle ear with a reduced cavity volume. Simkin 
(1965) associated the spongy bullae with mammals living in close 
habitats, such as the bogs, grassy tunnels, and subnivean galleries 
occupied by arvicolids; however, Hooper (1968) concluded that the 
ecological correlates of arvicolids with dissimilar middle ear anat- 
omies were ambiguous. The presence of an accessory tympanum 
augments the receptor surface of the tympanic membrane and prob- 
ably enhances the middle ear transformer ratio. Comparative stud- 
ies of auditory sensitivity using Clethrionomys, Microtus, and Lem- 
mus, may offer some insight to these variations. 

Two configurations of the malleus, denoted as the parallel and 
perpendicular types, have been documented in Muroidea (Cockerell 
et al., 1914; Fleischer, 1978). The two anatomical plans derive their 
names from the parallel or perpendicular orientation of the blade 
of the manubrium to the rotational axis of the malleus-incus com- 
plex. The parallel type characterizes New World cricetines and 
murines, whereas the perpendicular morphology occurs in gerbil- 
lines and arvicolids. Cockerell et al. (1914) considered the parallel 
malleus as primitive, but Fleischer (1978) derived both kinds from 
a state called the “ancestral type,” which resembles the parallel 
morphology except for the lack of an orbicular apophysis. The 
conformational rearrangements that define the perpendicular mal- 


Macroanatomy 135 


leus, such as found in Microtus, lessen the tortional stiffness of the 
malleus-incus complex, suggesting a middle ear complex better at- 
tuned to low frequency sounds (Fleischer, 1978). 


Postcranial Skeleton 


Compared to the cranium the postcranial skeleton of arvicolid 
rodents has attracted less attention in systematic and functional 
studies. Carleton (1980) found that M. pennsylvanicus possess 13 
thoracic and 6 lumbar vertebrae, a count typical of other arvicolids 
and Old and New World cricetines, and suggested that this ratio 
represents the primitive condition in Muroidea. The numbers of 
thoracics (and associated ribs) and lumbars in other muroids range 
from 12 to 15 and 6 to 7, respectively. The reason for this diversity 
in vertebral and rib number has not been explored. Another feature 
of the axial skeleton shared by all arvicolids is the lack of a pro- 
nounced vertebral spine on the neural arch of the second thoracic 
vertebra (Carleton, 1980). An hypertrophied spine arises from the 
second thoracic vertebra in other muroids and serves as the origin 
of the nuchal ligament and part of the splenius muscle, which in- 
serts along the lambdoidal ridge of the skull. The loss of this spine 
in Microtus and other arvicolids intimates changes in posture and 
mobility of the head. 

Investigators have demonstrated the utility of the pelvis for iden- 
tifying, sexing, and aging Muicrotus recovered from owl pellets 
(Brown and Twigg, 1969; Dunmire, 1955; Guilday, 1951; Hecht, 
1971). Brown and Twigg (1969) and Dunmire (1955) were able 
to discriminate adult male and female Microtus using dimensions 
and ratios of the innominate bones, which undergo slight modifi- 
cations at sexual maturity in males but change dramatically in 
females as a result of resorption and remodelling at the pubic sym- 
physis. Mensural overlap and consequent uncertainty of gender 
were restricted to prepubertal individuals. The pelvic changes that 
signal pregnancy and parturition allowed Brown and Twigg (1969) 
to define non-parous, uniparous, and multiparous female cohorts. 
Brown and Twigg also identified several pelvic features that distin- 
guish British Muridae from Arvicolidae. 

Carleton (1980) noted that Microtus pennsylvanicus lack an ent- 
epicondylar foramen on the humerus. All arvicolids examined (14 
genera, including 22 species of Microtus) support this observation, 


136 Carleton 


suggesting that foramen loss is characteristic of the family. Its oc- 
currence in other Muroidea is sporadic: present in gerbillines, most 
Old World cricetines, most North American cricetines, and many 
murines; absent in arvicolids, South American cricetines, and many 
murines. Anatomists have debated whether the foramen protects 
the filiform structures (median nerve and sometimes the brachial 
artery) that traverse it, or whether its occurrence reflects muscular- 
skeletal changes affecting the distal humerus. Landry (1958) re- 
jected both notions and argued that the foramen acts as a retinac- 
ulum, which restrains the median nerve from sagging across the 
elbow joint, especially in mammals with a deep, loose axilla. Al- 
though his explanation may account for the foramen’s variation in 
some mammals, it inadequately accommodates the Muroidea, species 
of which generally have a loose investiture of skin about the axilla 
but nonetheless vary in foramen occurrence. 

Stains (1959) examined the calcanea of M. pennsylvanicus, M. 
ochrogaster, and M. pinetorum, and remarked on the distal place- 
ment of the trochlear process, a shelf-like buttress for the peroneus 
longus tendon, in arvicolids as compared to other muroids. The 
distal shift of the trochlear shelf intimates adjustments in the lever 
action of the peroneus longus, an important flexor of the foot. 


Musculature 


Studies of arvicolid musculature have emphasized the branchio- 
meric complex because of interest in masticatory accommodations 
associated with a herbivorous trophic niche. Howell (1924) provid- 
ed brief descriptions of the jaw muscles in Microtus montanus and 
concluded that adult cranial morphology mirrors the mechanical 
forces exerted during ontogenetic development of muscular attach- 
ments, which in turn are related to the animal’s food and feeding 
mode. Repenning (1968) presented a more detailed picture of the 
masticatory musculature of M. longicaudus. In particular, he noted 
that the insertion of the masseter medialis, pars anterior, onto the 
ascending mandibular ramus imparted a conspicuous depression, 
which he designated the “arvicoline groove.” Repenning stressed 
the importance of this character as a marker to discriminate early 
microtines from dentally progressive cricetines in the fossil record. 
The bulk of our knowledge of myological variation in the Arvicol- 
idae issues from the work of Kesner (1977, 1980). 


Macroanatomy 137 


In his functional analysis of jaw muscles, Kesner (1980) identi- 
fied correlates of the propalinal mastication (motion of the mandible 
primarily in an anterior-posterior direction) so highly evolved in 
arvicolids. In contrast to a generalized cricetine pattern, he con- 
cluded that the anterior vector component of the superficial mas- 
seter, masseter lateralis profundus, and internal pterygoid and the 
vertical component of the medial temporalis are strongly pro- 
nounced. These differences in muscle action, achieved through 
changes in fiber orientation and muscle bulk, shifts in origins and 
insertions, and remodeling of the cranium and dentary, synergisti- 
cally operate to enhance the longitudinal grinding of the dental 
batteries in arvicolids. Kesner highlighted the role played by the 
central tendon of the medial temporalis in propounding his “pro- 
palinal swing” hypothesis of arvicolid feeding mechanics. The cen- 
tral tendon attaches to the postorbital process, a bony crest on the 
squamosal of arvicolids; muscle fibers originating from this tendon 
insert into the temporal fossa of the dentary. He postulated that the 
postorbital-crest tendon of the temporalis functions as a suspensory 
sling for the mandible, uniformly transmitting vertical compressive 
forces throughout the arc of mandibular excursion, while other 
muscles (superficial masseter, masseter lateralis profundus, and in- 
ternal pterygoid) supply the major protrusive action of the lower 
jaw. Species of Microtus, as well as Ondatra and Neofiber, have a 
long, well-developed postorbital-crest tendon compared to the short- 
er condition observed in Phenacomys and Lagurus. 

The attachment of the hyoid apparatus to the cranium occurs by 
two basic kinds of suspensory arrangements among Muroidea, al- 
though some intermediate conditions have been described (Kesner, 
1977; Klingener, 1968; Rinker, 1954; Sprague, 1941). In the ple- 
siomorphic state, a stylohyal cartilage forms a ligamentous connec- 
tion to the wall of the stylomastoid foramen, a discrete jugulohyoi- 
deus muscle inserts upon the end of the stylohyal, and the 
stylohyoideus originates broadly from the same cartilage. This con- 
figuration typifies Clethrionomys, Phenacomys, Lemmus, Synapto- 
mys, and Dicrostonyx within Arvicolidae (Kesner, 1977). In the 
derived state, the stylohyal is absent or greatly reduced, as is the 
jugulohyoideus, and the stylohyoideus muscle originates from the 
paroccipital process and a fascial sheet that now supports the hyoid 
complex. This morphology is exemplified by Ondatra, Lagurus, and 
Microtus. The functional consequences of these evolutionary trans- 


138 Carleton 


formations are unknown; one can only surmise that they relate to 
powers of vocalization or perhaps to mastication and deglutition. 

In his study of generic affinities, Kesner (1977) sampled myolog- 
ical diversity of the jaw, hyoid, and pectoral limb regions. He de- 
termined character state polarities for 47 muscles in Microtus (three 
North American species) and nine other arvicolid genera and per- 
formed several multivariate analyses. Compared to representative 
cricetines, arvicolids possess synapomorphies in the presence of a 
medial insertion of the masseter lateralis profundus, development 
of the postorbital-crest tendon of the temporalis, a robust internal 
pterygoid, reduction of the tendinous arcade of the digastric, and 
the insertion of the pectoralis minor onto the coracoid process. Of 
the species of Microtus examined (pennsylvanicus, pinetorum, and 
richardsoni), M. richardsoni is the most differentiated and Kesner 
supported its transfer to Arvicola. He further recommended that the 
complexity of relationships suggested by muscular variation is best 
conveyed by a multitribal classification of Arvicolidae. 


Circulatory System 


Our comparative anatomical knowledge of the circulatory system 
in Muroidea is mostly limited to the cephalic arterial blood supply, 
probably a reflection of the desire to establish homologies and func- 
tions of the cranial foramina often employed as taxonomic charac- 
ters in studies of Rodentia. Variations in carotid circulatory pat- 
terns, particularly the branching of the stapedial artery, critically 
bear on the occurrence of some cranial foramina as detailed in the 
studies of Bugge (1970) and Guthrie (1963). 

A complete carotid circulation is thought to represent the ances- 
tral muroid condition. The stapedial artery separates from the in- 
ternal carotid near the tympanic bulla, which it enters via the sta- 
pedial foramen. Inside the bulla, the stapedial bifurcates: the 
opthalmic branch crosses the inner surface of the squamosal bone, 
its pathway marked by a faint groove, and enters the orbit through 
the sphenofrontal foramen; the internal maxillary branch emerges 
from the bulla at the petrotympanic fissure, reenters the skull 
through the alisphenoid canal, and passes into the orbit through the 
sphenoidal fissure. This circulatory arrangement characterizes Old 
World cricetines, many New World cricetines, and some neso- 
myines. For a thorough depiction of the intricate carotid circulation, 


Macroanatomy 139 


the reader should consult Bugge (1970), Guthrie (1963), and Klin- 
gener (1968). 

Reductions of the stapedial artery occur in the Arvicolidae, Ger- 
billinae, Murinae, and some New World Cricetinae. Guthrie (1963) 
portrayed the carotid circulation of Microtus pennsylvanicus, and 
Bugge (1970) dissected M. agrestis plus examples of Lemmus, Cleth- 
rionomys, and Arvicola. In all, the proximal portion of the opthalmic 
artery is absent and so too are the sphenofrontal foramen and squa- 
mosal groove. Instead, the distal part of the opthalmic originates 
from the internal maxillary and exits the cranium through the lower 
part of the sphenoidal fissure. The stapedial artery and foramen 
remain large since the internal maxillary constitutes the continua- 
tion of the stapedial outside of the tympanic bulla. Examination of 
skulls of other arvicolids suggests that this pattern is found in all 
except Synaptomys, Myopus, and Lemmus. These lack a stapedial 
foramen and may therefore have an arterial configuration resem- 
bling that reported in Szgmodon (Bugge, 1970), in which both the 
opthalmic and internal maxillary anastomose with the internal ca- 
rotid but still emerge via the sphenoidal fissure. In this condition, 
the importance of the stapedial artery to the orbital circulation is 
greatly diminished. 

No other mammalian order exhibits variation in carotid circu- 
lation like that encountered in the Rodentia (Bugge, 1970), but the 
reason for this diversity is poorly understood. Guthrie (1963) im- 
plicated the freer movement of the mandible in the glenoid fossa 
and the consequent stress this masticatory innovation applied to the 
primitive carotid arrangement. His explanation focussed on varia- 
tion in the origin of the internal maxillary artery across all Rodentia 
and seems inapplicable to the patterns observed in Muroidea. How- 
ever, his account of the probable mechanism whereby this diversity 
was realized phylogenetically is pertinent. In rodents, the embryonic 
carotid vessels consist of remnants of the primitive aortic arch cir- 
culation. Interspecific variation in the adult circulatory pattern partly 
results from the persistence of certain embryonic connections and 
the atrophy of others (Bugge, 1970; Guthrie, 1969). Thus, the ex- 
istence of alternative pathways permits some developmental plas- 
ticity in the configuration of the blood circuit. In this light, it is 
instructive to remember that selection for propalinal mastication 
and bullar hypertrophy, as exemplified by Microtus, has produced 
major restructuring of the cranium, particularly involving those 


140 Carleton 


skull regions where bifurcation of the carotid arteries occurs. The 
enlarged pulp cavities of the hypsodont teeth, the excavation of the 
parapterygoid fossae for the internal pterygoid muscles, and the 
expansion of the tympanic bullae have profoundly affected the mor- 
phology of the alisphenoid and otic regions, which contain the crit- 
ical foramina for several primary carotid branches. Perhaps the 
search for a functional explanation for the variability in carotid 
circulation among Muroidea will lie in the specific skeletal and 
muscular adaptations peculiar to each group and the circulatory 
accommodations such evolutionary changes have imposed. 

A large venous plexus continuous with veins of the nasal chamber 
occupies the maxillary (posterior) portion of the incisive foramina. 
Quay (19546) termed this network the nasopalatine venous plexus 
and noted that its branches penetrate the incisive papillae, which 
elevate the openings of the nasopalatine ducts. The nasopalatine 
complex is drained by the posterior palatine veins, which course 
along furrows on the bony palate and conjoin the internal maxillary 
via the posterior palatine foramina. Modification of the nasopala- 
tine venous plexus is suggested for those Microtus (for example, 
richardsoni and montanus) with posteriorly constricted incisive fo- 
ramina. 


Digestive System 


Dentition 


Whether viewed from a paleontological or neontological per- 
spective, the meristic quality of cheektooth variations has contin- 
ually appealed to students of arvicolid evolution and early estab- 
lished this character suite as the szne qua non of their systematics. 
Hinton (1926:22) succinctly catalogued the dental features that in- 
vestigators have relied upon, to one degree or another, over the past 
century: 


The difference in the number, form, and relative size of the 
triangles and salient angles, the degree to which the dentinal 
spaces are open to or closed off from each other, the greater or 
less complexity of the anterior loop in M, and of the posterior 
loop in M?, the distribution and nature of the enamel sheet in 
different parts of the periphery, the presence or absence of ce- 
ment, and above all the circumstance whether the cheek-teeth are 


Macroanatomy 141 


of persistent or of limited growth 7.e., rooted or rootless;—all 
these, when used with discretion, afford excellent characters for 
the distinction of genera and species. 


With regard to each of these characters, Microtus is among the more 
progressive genera in the family. 

The molar teeth of Arvicolidae stand as the foremost example of 
hypsodont development within the Muroidea. Their hypsodonty 
involves a vertical elongation of the entire crown (denoted coronal 
hypsodonty) in contrast to a pronounced extension of the individual 
cusps, or tubercular hypsodonty. The transformation from a rooted, 
high-crowned tooth to an “evergrowing” one, in which the pulp 
cavity of the root retains its generative function throughout an in- 
dividual’s lifetime marked a major threshold in the evolution of the 
arvicolid molar. The few arvicolids that now possess rooted molars, 
generally viewed as an indicator of primitiveness, include Cleth- 
rionomys, Dinaromys, Ellobius, Ondatra, Phenacomys, and Prome- 
theomys; some of these develop closed roots only as old adults. The 
remaining taxa, including all species of Mucrotus, have continu- 
ously growing, “rootless” cheekteeth. Early fossil arvicolids lacked 
cement in the reentrant folds, a condition which persists in several 
extant genera (for example, in Dicrostonyx and Lagurus); however, 
prominent cement buttresses line the reentrant angles of Microtus 
molars. For discussion of the complex histological rearrangements 
that necessarily accompanied selection for persistently-growing, 
hypsodont molars, see Phillips (this volume). 

The occlusal surfaces of the molars consist of dentine basins en- 
closed by enamel triangles, the number, shape, and completeness of 
which have been stressed in studies of arvicolid relationships. Gen- 
erally a tooth has an anterior loop (also called the “‘trefoil”’), a series 
of alternating salient angles and reentrant folds, and a posterior 
loop (Fig. 5). If the enamel border of a salient angle extends across 
the tooth to contact its opposite member, the wholly enclosed enamel 
prism is termed a closed triangle; if the dentine of contiguous salient 
angles remains confluent, those prisms are designated open trian- 
gles. The metameric nature of arvicolid cheekteeth has discouraged 
attempts to homologize cusps following the Cope-Osbornian tritu- 
bercular system. Instead, an alphanumeric system has been em- 
ployed to designate the molar components and to facilitate compar- 
isons (Hinton, 1926; Klimkiewicz, 1970; Koenigswald, 1980; 
Martin, 1973; Oppenheimer, 1965). Most meristic conventions have 


142 Carleton 


Fic. 5. Occlusal view of the upper right (left) and lower left (right) molar 
toothrows of Microtus pennsylvanicus (from Virginia) illustrating one possible alpha- 
numeric labelling scheme. Abbreviations are: AL, anterior loop; PL, posterior loop; 
TLs, transverse loops; a-g, reentrant folds; 1-5, salient angles of closed triangles; 6- 
7, salient angles of open triangles. 


followed Hinton’s (1926) scheme for labelling the triangles, salient 
angles, and reentrant angles from anterior to posterior in the upper 
molars and from posterior to anterior in the lowers, after first in- 
dicating the anterior and posterior loops (Fig. 5). 


Macroanatomy 143 


Variation in the upper third and lower first and second molars 
broadly defines two occlusal patterns among North American M:- 
crotus. One pattern, as exemplified by the subgenera Herpetomys, 
Orthriomys, Pedomys, and Pitymys consists of two closed and one 
open triangle in M3, only three closed triangles in m1, and two 
closed and two open triangles in m2 (Table 2). The subgenera 
Aulacomys, Microtus, and Stenocranius, on the other hand, are char- 
acterized by at least three closed triangles in M3, usually five entire 
triangles in m1, and four closed triangles in m2 (Table 2). In each 
pairwise comparison, the presumably homologous elements are 
identifiable for each tooth (Fig. 6). These two patterns represent 
the primary foci of dental variation in the genus and were used 
traditionally to delineate the subgenera (Bailey, 1900; Miller, 1896). 
Still other molar configurations have been recognized as taxonom- 
ically important, especially the presence of two closed triangles in 
the m3 of Orthriomys and Herpetomys, the development of a pos- 
teromedial loop in the M2 of some Microtus, and the greater com- 
plexity of the M3 of M. chrotorrhinus (Table 2, Fig. 6). The pres- 
ence of poorly developed triangles has been cited frequently for the 
separate generic status of Pitymys, a taxonomic opinion more often 
espoused by paleontologists and European workers (for example, 
Corbet 1978; Zakrzewski, this volume) than by North American 
mammalogists (for example, Anderson, this volume; Hall, 1981). 
However, the gradational character of dental variation in the group 
complicates such a diagnostic yardstick for generic limits, for it at 
once brings to issue the status and relationship of other subgenera 
(for example, Chilotus, Herpetomys, and Pedomys) and even species 
of typical Microtus (for example, M. oeconomus), whose dentition 
exhibits comparable degrees of divergence. 

In view of the taxonomic weight traditionally accorded arvicolid 
dental morphology, it appears somewhat incongruous that every 
author who has scrutinized their dentition has remarked upon the 
tremendous individual variation, sometimes seen bilaterally on an 
individual, and the fine structural gradations within and between 
populations. Nonetheless, species and populations display a sharp 
modality in occlusal configuration, and the conspicuous variation 
typically involves only particular areas of two molars. Hinton’s 
(1926) claim that the dental pattern of an individual’s cheekteeth 
became altered with age and wear was disproved by Oppenheimer 
(1965), who found no appreciable difference in the pattern of a 


Carleton 


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146 Carleton 


Fic. 6. Occlusal view of principal molar variants in species of Microtus (see also 
Table 2). M? (=M2): a, M. (Pedomys) ochrogaster; b, M. (Microtus) pennsylvanicus. 
M? (=M3): a, M. (Pedomys) ochrogaster; b, M. (Microtus) pennsylvanicus; c, M. 
(Microtus) chrotorrhinus. M, (=m1): a, M. (Orthriomys) umbrosus; b, M. (Muicrotus) 
oeconomus; c, M. (Microtus) pennsylvanicus; d, M. (Stenocranius) miurus. M, (=m2): 
a, M. (Pedomys) ochrogaster; b, M. (Microtus) pennsylvanicus. M, (=m3): a, M. 
(Microtus) pennsylvanicus; b, M. (Orthriomys) umbrosus. 


Macroanatomy 147 


single tooth abraded to simulate various stages of wear. In his sem- 
inal classification of voles and lemmings, Miller (1896) estimated 
that 75 percent of the individuals of a given species conform to a 
“normal” pattern. Figures and frequency tabulations of molar vari- 
ation are available for M. chrotorrhinus (Guilday, 1982; Martin, 
1973), M. longicaudus (Kellogg, 19226), M. montanus (Howell, 1924; 
Kellogg, 1922a), M. pennsylvanicus (Goin, 1943; Guilday, 1982; 
Guthrie, 1965; Klimkiewicz, 1970; Miller, 1896; Oppenheimer, 
1965), and M. xanthognathus (Guilday, 1982) among New World 
Microtus. 

The notion of a polarity of variation has emerged from these 
studies, as witnessed by the greater variability repeatedly affirmed 
for the lower first and upper third molars. Thus, an axis of increas- 
ing variation exists from front to back in the upper toothrow and 
from back to front in the lower one; in addition, the same direction 
of variation obtains for the anterior and posterior moieties of the 
individual molars composing the toothrows. The magnitude of these 
polarities was exhaustively verified by Guthrie (1965), who mea- 
sured 42 dimensions of the molars in M. pennsylvanicus. He re- 
corded higher variation coefficients for the posterior halves of the 
upper molars and anterior halves of the lowers, and found those of 
the posterior part of M3 and front part of m1 to be extraordinarily 
high. Guthrie concluded that the extreme variation is confined to 
those molar segments experiencing the most phylogenetic change 
and hypothesized that such variation is exposed as a result of di- 
rectional selection breaking up previously balanced, polygenic link- 
age systems. Hinton (1926) opined that the greater variability of 
m1 and M3 correlated with their terminal position in the toothrows, 
but his explanation failed to account for the stability of M1 and 
m3 at the opposite ends. Guthrie (1965) modified Hinton’s surmise 
by observing that it is the inherently labile primordia of m1 and 
M3 which remain unobstructed, whereas the homologous sections 
of the other molars abut the stable loop of the contiguous teeth. 
Niethammer (1980) shifted the causal explanation to a functional 
basis, noting that the surfaces of m1 and M3 do not continuously 
occlude during a chewing orbit; as a result of less masticatory in- 
volvement in use of these teeth, their terminal portions are, in some 
sense, functionally unencumbered and more sensitive to selection 
for increased complexity and length. 

Several studies have documented clinal variation in molar pat- 


148 Carleton 


tern. In the Eurasian vole M. arvalis, Stein (1958) showed that 
northern populations have a greater frequency of simpler upper 
third molars (fewer salient angles) compared to southern popula- 
tions, where a relatively complex pattern dominates. He related the 
geographic trend to habitat quality, the northern populations oc- 
cupying more forested areas and the southern ones mostly inhab- 
iting grassland biomes. Jorga (1974) observed greater molar vari- 
ation in populations of M. oeconomus from the southern periphery 
of its range, where one might presume the habitat to be suboptimal. 
Semken (1966) discovered that the incidence of M. pennsylvanicus 
with six closed triangles is less in samples from the northeastern 
United States than in those from the Great Plains. The apparent 
association of dental complexity, and perhaps variability, with eco- 
logical setting needs to be rigorously evaluated, a seemingly trac- 
table study given the abundance of M. pennsylvanicus deposited in 
North American collections. 

In light of the undisputed origin of arvicolids from some brachy- 
odont cricetid stock, there exists an unexpected amount of disagree- 
ment over the direction of evolution of arvicolid molars. Hinton’s 
(1926) commitment to a multituberculate origin of the Rodentia 
persuaded him to view simplification (that is, the loss of enamel 
loops and triangles) as the major trend of dental modification in 
Arvicolidae. His conclusions apparently influenced others in their 
interpretations of patterns of variation at lower taxonomic levels. 
For example, Goin (1943) considered the M3 of M. pennsylvanicus 
as undergoing reduction and that of M. chrotorrhinus as resembling 
the primitive state. Klimkiewicz (1970), Oppenheimer (1965), and 
Zimmermann (1956) similarly affirmed that the variation in their 
species’ samples validated the reductional trend in size and com- 
plexity of arvicolid cheekteeth. The alternative hypothesis of molar 
evolution, that is, augmentation of enamel loops and triangles, rests 
on more substantial evidence (Guthrie, 1965, 1971; Koenigswald, 
1980; Phillips and Oxberry, 1972). For example, Pleistocene forms 
of Microtus exhibit weaker triangulation, suggesting phyletic in- 
crease in enamel complexity leading to Recent species (Guthrie, 
1965; Semken, 1966). Moreover, straightforward outgroup com- 
parisons and examination of early Pliocene fossils confute the idea 
of dental simplification as the derivative morphology. That arvicolid 
molar diversification historically followed a trend of multiplication 
of enamel folds and angles does not eliminate the possibility of 


Macroanatomy 149 


reversal to a simpler state in some lineages. However, identification 
of such evolutionary reversals will require more definitive corrob- 
oration than has been marshalled to date. 

The syndrome of dental innovations that appeared in arvicolids 
is believed to enhance propalinal grinding and thereby to allow 
greater utilization of the harsh, siliceous grasses that compose the 
bulk of their diet (Guthrie, 1965, 1971; Hinton, 1926; Koenigs- 
wald, 1980; Phillips and Oxberry, 1972; Vorontsov, 1979). The 
longitudinal orientation of wear scratches on the enamel (Guthrie, 
1971) and the erosional profile etched into the dentine basins 
(Greaves, 1973) substantiate the dominant propalinal motion of the 
mandible. Although authors have referred to the grinding surface 
of arvicolid toothrows as a plane, close inspection reveals that their 
longitudinal occlusal outlines trace gentle curves that are convex in 
the uppers and concave in the lowers. Kesner (1980) demonstrated 
that the degree of toothrow curvature varies—pronounced in Micro- 
tus, for example, and flatter in Phenacomys—and correlates with the 
length of the postorbital-crest tendon of the temporalis muscle. The 
latter relationship supports his propalinal hypothesis, indicating 
that the excursion of the mandible during propalinal chewing de- 
scribes an arc whose limits and curvature are constrained by the 
postorbital-crest tendon. 

Guthrie (1971) viewed the origin and elaboration of the arvicolid 
cheektooth as meeting two general requirements for comminution 
of abrasive foods: prolonged resistance to crown wear and increased 
complexity of the grinding surface. ‘The maintenance of an effective 
grinding surface was advanced by the attainment of continually 
growing molars, as demonstrated by Koenigswald and Golenishev 
(1979), who measured eruption rates using fluorescent tetracycline 
as a growth marker. In M. fortis and M. mandarinus, the M1 and 
M2 erupt 0.5-0.7 mm per week, and the whole vertically elongate 
crown can regenerate in eight to twelve weeks. As remarked by 
Guthrie (1971), resistance to dental abrasion is incidentally achieved 
through increased complexity of the occlusal plane. Nevertheless, 
the enhanced coronal complexity also relates to masticatory efh- 
ciency because it augments the number of enamel cutting blades. 
Guthrie enumerated the derived features that constitute the “greater 
complexity” of dentally advanced arvicolids such as Microtus: in- 
crease in degree of penetration and decrease in width of reentrant 
angles; increase in acuteness of the salient angles; addition of angles; 


150 Carleton 


more pronounced alternation of salient angles; and redistribution 
of enamel thickness. ‘These modifications, in concert with a pro- 
palinal mode of chewing, create a system of opposing, interdigitat- 
ing shearing blades, neatly designed for slicing and cutting coarse 
food items. Koenigswald (1980) considered the conformation of ar- 
vicolid molars from the aspect of biomechanical stresses imparted 
during propalinal mastication and observed the predictable orien- 
tation of enamel structures perpendicular to the direction of jaw 
motion. In species with apomorphic dentitions, the leading edge of 
an enamel triangle is thicker and convex, whereas the trailing edge 
is thinner and concave. He further noted that the deepening of 
reentrant angles until they abut the opposite enamel border appre- 
ciably lengthens the shearing edges without broadening the molar 
rows. In M. chrotorrhinus, Martin (1973) found that third molars 
with more convoluted posterior loops are absolutely longer than 
those with simpler configurations and may indicate that the phy- 
logenetic formation of more triangles materially increased the length 
of the dental batteries as well as their complexity. Guthrie (1971) 
discussed the influence of competition, habitat, and other selective 
pressures controlling the extent of dental complexity and variation. 

The enamel face of the incisors of Microtus lacks longitudinal 
grooves as found in some other arvicolid genera (for example, in 
Synaptomys). The absence of incisive sulci has been considered so 
diagnostic of the genus that individual exceptions have been deemed 
noteworthy (Fish and Whitaker, 1971; Jones, 1978). In most species, 
the upper incisors are orthodont or opisthodont; only M. (Aulaco- 
mys) richardsoni has noticeably proodont incisors (Bailey, 1900). 
The earlier recognition of the lemming and vole divisions within 
Arvicolidae was based partly on the length and course of the lower 
incisors (Hinton, 1926; Miller, 1896). In the Lemmi, the lower 
incisors terminate before or at the level of the m3 and lie to the 
lingual side of the molar row; in the Microti, the incisors extend 
dorsally into the condylar process and pass between the bases of the 
m2 and m3 to cross from the lingual to the labial side of the man- 


dible. 
Oral Cavity 


Quay (19546) studied the diastemal palate in Arvicolidae (in- 
cluding 12 species of New World Microtus) and documented vari- 


Macroanatomy 151 


ation in the development of furred infoldings of the upper lip (in- 
flexi pelliti labii superioris) in relation to the occurrence of the 
anterior longitudinal ridge and other palatal rugae and to the po- 
sition of the nasopalatine openings. The inflexed lobes of the upper 
and lower lips presumably function to obstruct extraneous material 
from the masticatory area of the mouth when the animal is gnaw- 
ing. The inflexi of Microtus are moderately extensive, abutting at 
the diastemal midline but not fusing as in Ellobius, the most fos- 
sorially adapted arvicolid. Arvicolids with small medial folds of the 
upper lip (for example, Dicrostonyx, Clethrionomys) have a keel- 
like ridge of palatal epithelium, the anterior longitudinal ridge, 
which protrudes between the widely separated inflexi. In conjunc- 
tion with their extensive labial inflexi, Microtus lack an anterior 
longitudinal ridge. Quay (19544) discerned a posterior displace- 
ment of the nasopalatine ducts relative to the length of the diastemal 
palate. Most species of Microtus are intermediate in the position of 
the nasopalatine apertures, but M. (Aulacomys) richardsoni is ex- 
treme in its posterior location of these openings. ‘The nasopalatine 
canals pass dorsally through the premaxillary portion of the incisive 
foramina and into the floor of the nasal chambers, where they are 
anatomically closely associated with the vomeronasal, or Jacobson’s, 
organ (Meredith, 1980; Wohrmann-Repenning, 1980). The prob- 
able function of Jacobson’s organ as an extra-oral gustatory site 
and the dominating importance of chemical communication in me- 
diating much of rodent behavior (Eisenberg and Kleiman, 1972) 
make the variable position of the nasopalatine ducts an attractive 
morphological and behavioral system for investigation. 

Vorontsov (1962, 1979) surveyed the kinds and distribution of 
sensory papillae on the tongue, and in particular, circumvallate 
papillae. Gerbillines, sigmodontines, cricetines, murines, and all 
arvicolids possess a single circumvallate papilla, centrally located 
behind the elliptical prominence of the tongue. Nesomyines and 
cricetomyines are the only muroids known to have three circum- 
vallate papillae, a condition thought to be primitive because it is 
shared with Sciuromorpha and some Hystricomorpha. Golley (1960) 
stated that the tongue of M. pennsylvanicus lacks foliate papillae. 

Spacious internal cheek pouches, like those found in Old World 
hamsters (Cricetinae) and African pouched rats (Cricetomyinae), 
are lacking in Microtus and other arvicolids. 


152 Carleton 


Mideut 


The ancestral gastric morphology in muroids has been inter- 
preted as a simple, single-chambered sac having approximately equal 
distributions of glandular and cornified mucosal linings (Carleton, 
1973; Vorontsov, 1962, 1979). Such a hemiglandular gastric plan 
occurs in numerous species and all major groups of Muroidea, even 
characterizing entire subfamilies (for example, Gerbillinae), but is 
known only in the lemmings (Lemmus, Myopus, and Synaptomys) 
within Arvicolidae. 

Compared to the unilocular-hemiglandular condition, the stom- 
ach of Microtus displays many derived features. As Toepfer (1891) 
and Tullberg (1899) noted for Old World M. arvalis and M. agres- 
tis, the glandular area in Microtus consists of a small circular patch 
restricted to the greater curvature opposite the esophageal orifice 
(discoglandular type following Carleton, 1973). Carleton (1981) 
substantiated the uniformity of Microtus (including 18 North Amer- 
ican species representing all subgenera except Orthriomys) with re- 
spect to the discoglandular pattern of their gastric mucosae and the 
persistence of a thin strip of glandular tissue at the pylorus. A 
bordering fold of cornified epithelium (=Grenzfalten of Toepfer, 
1891; pediculated squamous flap of Dearden, 1969) surrounds the 
discoglandular zone. The left rim of this bordering fold is fimbriat- 
ed, a condition peculiar to Microtus and some other arvicolid genera 
(Carleton, 1981; Vorontsov, 1979). Externally, the stomach of spec- 
imens of Microtus is bilocular. This appearance results both from 
the elaboration of the incisura angularis, a muscular fold on the 
lesser curvature, and the expansion craniad of the left half of the 
stomach. The latter forms a thin-walled, highly distensible fornix 
(=esophageal sac; forestomach; fornix ventricularis of Vorontsov, 
1979), capable of accommodating large amounts of food. The an- 
atomical modifications associated with the bilocular-discoglandular 
stomach seen in Microtus reflect changes in the composition of the 
digestive glands and the architecture of the smooth musculature, 
which in turn imply profound differences in gastric digestion and 
motility (see, for example, Dearden, 1966, 1969; Golley, 1960; 
Luthje, 1976). 

Two functional themes have been reiterated to explain the trend 
of keratinization and glandular reduction observed in muroid stom- 
achs. Bensley (1902) and Tullberg (1899) emphasized the mechan- 


Macroanatomy 153 


ical effect wrought by abrasive foodstuffs, such as the chitinous 
exoskeleton of insects or the siliceous fibers of grasses. Toepfer 
(1891) and Vorontsov (1962, 1979), on the other hand, interpreted 
the modifications as adaptations for symbiotic digestion of cellulose- 
rich foods. The latter hypothesis, with its obvious analogy to ru- 
minant digestive processes, seems more intuitively logical, especially 
in light of the herbivory demonstrated for many arvicolids, partic- 
ularly Microtus. Nevertheless, much basic data on gastric histology, 
motility, physiology, and microbial symbionts must be gathered be- 
fore one of these hypotheses, or yet other plausible interpretations 
(see Carleton 1973, 1981), can be accepted. 

All arvicolids examined have a discrete saccular gall bladder, but 
it is sporadically absent in other muroid assemblages (Carleton, 
1980; Vorontsov, 1979). Why some rodents lack a gall bladder is 
unclear. Vorontsov (1979) speculated that a gall bladder should be 
expected in forms that feed opportunistically and infrequently on 
foods high in protein and fat to ensure that a large supply of bile 
is in reserve and can be mobilized quickly, whereas in species that 
feed more frequently and regularly, bile secretion occurs more or 
less continuously, obviating the need for large volumes of concen- 
trated bile and an organ for storage. The largely herbivorous reg- 
imen and polyphasic activity patterns of Microtus seem to refute 
this hypothesis. The liver in species of Microtus is divided into seven 
lobes, which Vorontsov (1979) interpreted as derived from the eight- 
lobed state characteristic of some other arvicolids and muroids. 


Hindgut 


Species of Microtus, and arvicolids in general, possess a short 
small intestine in relation to the length of the large intestine and 
caecum. Mean relative lengths of the small intestine, large intestine, 
and caecum (expressed as a percentage of total intestinal length) 
are 45, 37, and 18, respectively, for eight Old World species of 
Microtus (Vorontsov, 1962, 1979). In contrast, muroid species whose 
diet predominantly consists of insects or seeds exhibit a compara- 
tively long small intestine and short large intestine and caecum, 
generally in the range of 62, 28, and 10 percent of total length 
(Vorontsov, 1962). 

As cautioned by Barry (1977), these simple proportions do not 
reflect accurately the available surface area for nutrient absorption 


154 Carleton 


in the hindgut. In terms of mucosal surface area, the small intestine, 
with its villous projections and submucosal folds, is still the primary 
section for nutrient assimilation among the small mammals exam- 
ined, including Microtus ochrogaster and M. pennsylvanicus. Thus, 
in M. ochrogaster, the small intestine, large intestine, and caecum 
constitute 44, 35, and 21 percent, respectively, of total intestinal 
length, but the three compose 73, 14, and 13 percent of the total 
absorptive surface of the hindgut. Although the ratios do not ac- 
curately convey their potential importance for absorption within a 
species, differences between species, whether in relative lengths or 
surface areas, are in the direction predicted by their food habits. 
The mucosal surface area of the caecum in Microtus, for instance, 
substantially exceeds that observed in Peromyscus; in fact, the dif- 
ference in caecal capacity suggested by relative surface areas (about 
3.9 times) is more impressive than that (about 2.5 times) calculated 
from relative lengths (Barry, 1977: Table 1). The greater length 
and capacity of the caecum in Microtus and other arvicolids assume 
functional significance in view of the large amount of herbaceous 
matter they consume and the documented role of the caecum as the 
hindgut site for cellulose fermentation (Moir, 1968). 

Aside from relative intestinal lengths, other structural modifica- 
tions undoubtedly affect absorptive surface area. Barry (1976) ob- 
served that the small intestinal villi of M. pennsylvanicus and M. 
ochrogaster are characteristically short, broad, and less dense than 
those of Peromyscus and Mus. He also derived a positive correlation 
between mucosal surface area of the small intestine and the percent 
animal material in the diet, a finding consistent with the activity of 
the duodenum in absorbing amino acids and the low-protein fare 
of Microtus. The proximal section of the large intestine is coiled 
upon itself to form a tapered series of loops, which number 10 to 
12 coils in Lemmus and Ondatra but only three to five in species of 
Microtus; most muroid species either lack colic loops or have only 
one or two (Vorontsov, 1979). Compared to other Arvicolidae, the 
caeca found in Microtus are moderately sacculated, but they easily 
surpass in complexity the shorter, smooth-walled caeca observed in 
most cricetines, murines, and gerbillines. Long villi occur in the 
caecum of Phenacomys and Dicrostonyx but have not been discovered 
in the one species of Microtus examined (californicus) nor in Cleth- 
rionomys, Lagurus, Ondatra, Lemmus, and Synaptomys (Voge and 
Bern, 1949, 1955). Coprophagy has been documented for M. penn- 


Macroanatomy 155 


syluanicus (Ouellette and Heisinger, 1980). The prevalence of this 
nutritional strategy within the genus and the possible correspon- 
dence to morphological specializations of the hindgut, such as colic 
loops or caecal sacculae, should be explored. 


Reproductive System 


Male 


The architecture of the baculum and glans penis has received 
considerable attention from systematists in their assessments of re- 
lationships within Arvicolidae. Hamilton (1946) examined four 
North American species of Microtus, but subsequent investigators 
have increased that number to seventeen, representing all North 
American subgenera except Orthriomys (Anderson, 1960; Burt, 1960; 
Dearden, 1958; Hooper and Hart, 1962; Martin, 1979). This rep- 
resentation, together with those Old World genera and species ex- 
amined (Askenova and Tarasov, 1974; Didier, 1954; Ognev, 1950), 
establishes the Arvicolidae as the most thoroughly surveyed group 
of muroids in regard to phallic morphology. 

The baculum in Microtus generally consists of four parts, a prox- 
imal bony shaft tipped distally with three cartilaginous digits or 
processes. Arata et al. (1965) characterized the junction between 
the shaft and distal processes as a synovial joint. Species of Microtus 
differ in the occurrence and development of the lateral bacular 
processes: they are conspicuous in the subgenera Chilotus and Her- 
petomys and most species of the nominate subgenus; diminutive in 
the subgenera Aulacomys, Pedomys, Pitymys, and Stenocranius; and 
absent in M. (Microtus) californicus and M. mexicanus (Anderson, 
1960; Hamilton, 1946). Anderson (1960) constructed a key to North 
American arvicolids based on bacular traits, but cautioned that 
species of Microtus were especially difficult to accommodate because 
of the variable pronouncement of the lateral bacular digits. 

Arata et al. (1965) traced the ontogenetic development of the 
baculum of Microtus montanus from week-old neonates to adults. 
They found that the proximal shaft is true bone, a perichondral 
ossification formed from dense aggregations of mesenchyme cells in 
the manner described for the rat (Ruth, 1934). However, the re- 
puted “ossifications” of the distal bacular digits mentioned by pre- 
vious authors are in fact calcifications of hyaline or fibrocartilage, 


156 Carleton 


a process appearing first in the medial bacular digit and later in 
the lateral ones. Marked expansion of the proximal shaft and cal- 
cification of the distal elements proceeded rapidly after day 35, 
approximately coincident with the threshold of reproductive ma- 
turity in M. montanus. The ontogeny of bacular morphology in M. 
montanus basically conforms to that observed in other arvicolids 
with trident bacula (Artimo, 1969; Tarasov, 1974). These studies 
reveal the large variation in bacular conformation associated with 
age and physiological state of the animal and emphasize the need 
for cautious taxonomic interpretation of differences between sam- 
ples consisting of few specimens and incomparable age profiles. 

As demonstrated by Hooper and Hart (1962), the interspecific 
variability of the soft parts of the glans penis surpasses that seen in 
the bacular infrastructure. Species of Microtus have a short, broad 
glans with a moderately deep terminal crater, the ventral rim of 
which is usually papillose. The ornate appearance of the glans is 
enhanced further by other soft tissue structures that project from 
the floor of the crater into its interior: the dorsal papilla; the ure- 
thral process; and the medial and lateral bacular mounds. Hooper 
and Hart (1962) sorted the species of Microtus into two groups 
based upon the structure of the dorsal papilla, the length of the 
lateral bacular mounds, and lobulation of the urethral process, and 
recommended that M. (Aulacomys) richardsoni be allocated to Ar- 
vicola. At a higher taxonomic level, they arranged Microtus with 
Lagurus and Arvicola in a tribal assemblage. The data from both 
bacular and penile morphology favors a multitribal classification of 
the arvicolids, a major departure from the traditional dual tribal 
system (Lemmi and Microti) adopted by Hinton (1926) and Miller 
(1896). 

The trident baculum, glans penis with a crater and assorted 
crater embellishments, and intricate phallic vascular supply found 
in Microtus and other arvicolids characterize a fundamental mor- 
phological plan termed the “complex” type by Hooper (1960). At- 
tributes of the contradistinctive “‘simple” phallic scheme, which oc- 
curs in relatively few muroid genera, include a baculum consisting 
of a single element, the absence of a terminal crater and crater 
processes, and an uncomplicated vascular system (Hooper and 
Musser, 1964). Possession of a complex phallus broadly allies ar- 
vicolids with such muroid groups as Old World cricetines, South 
American cricetines, gerbillines, and murines (Hooper and Hart, 
1962; Hooper and Musser, 1964). Anderson (1960) and Hooper 


Macroanatomy 157 


and Hart (1962) considered the well-developed bacula and rela- 
tively ornate glandes penes of Clethrionomys and Phenacomys, voles 
with rooted molars, to represent the primitive condition of the phal- 
lus in Arvicolidae, and viewed absence of lateral bacular digits and 
a comparatively simple glans penis as derived morphologies. ‘Their 
hypotheses agree with the conventional interpretation of the com- 
plex to simple transformation of the phallus, as advocated for the 
Muroidea as a whole (Hershkovitz, 1966; Hooper and Musser, 
1964). 

The male accessory reproductive glands of muroid rodents con- 
stitute a richly variable organ-system, typically consisting of five 
sets of glands: preputial, bulbourethral, ampullary, vesicular, and 
prostate. Three pairs of prostates are conventionally recognized and 
designated by their position with respect to the urethra: anterior, 
dorsal, and ventral; the last pair usually is subdivided into lateral 
ventral and medial ventral lobes. A complete array of accessory 
reproductive glands is believed to represent the plesiomorphic ar- 
rangement in Muroidea (Arata, 1964; Carleton, 1980; Voss and 
Linzey, 1981). 

Such an array typifies the accessory reproductive glands in species 
of Microtus examined to date. Hamilton (1941) described and fig- 
ured the tract of M. pennsylvanicus, and Arata (1964) included M. 
ochrogaster and M. pinetorum. In addition, the 12 Old World M:- 
crotus reported conform to the hypothesized primitive complement 
(Askenova, 1973; Indyk, 1968), although Askenova (1973) did de- 
tect slight but consistent differences in size and form of the pre- 
putials and lateral ventral prostates among nine species studied. 
Except for the larger size of their preputial glands, the accessory 
reproductive glands found in arvicolids are indistinguishable from 
those characteristic of many New World cricetines, murines, and 
some gerbillines (Arata, 1964; Voss and Linzey, 1981). The ho- 
mogeneity in accessory gland morphology exists primarily among 
forms with a complex penis and presents a stark contrast to the 
elaborate modification or loss of particular accessory glands docu- 
mented for forms with a simple phallus (Arata, 1964; Linzey and 
Layne, 1969). 


Female 


The number and distribution of mammary glands have been 
applied taxonomically at the subgeneric level in Microtus and con- 


158 Carleton 


sidered suitably diagnostic to employ in keys (Bailey, 1900; Miller, 
1896). Indeed, species of Microtus collectively exhibit the gamut of 
variation recorded in the entire family. The common number of 
mammae, eight (two pectoral pairs and two inguinal pairs), occurs 
in the subgenera Aulacomys, Chilotus, Stenocranius, and most M:- 
crotus, as well as the majority of other arvicolid genera. Niethammer 
(1972) interpreted this as the primitive number and pattern in 
Arvicolidae and viewed reductions in mammary count as deri- 
vations. Two distributional patterns have been described for M:- 
crotus with six nipples: one pectoral pair and two inguinal pairs in 
Pedomys, and two pectoral pairs but just one inguinal pair in Her- 
petomys. Three arrangements are known for Muicrotus having only 
four mammae: two inguinal pairs in Pitymys, one pectoral pair and 
one inguinal pair in M. (Microtus) mexicanus, and two pectoral 
pairs in Orthriomys. Voles that have fewer than eight nipples but 
that retain the pectoral pairs constitute an interesting exception 
among muroid rodents to the conventional trend, which involves 
loss of the anterior pairs and retention of the inguinal ones (Arvy, 
1974). This condition raises questions about the position of the 
female when nursing and the tenacity of nipple-clinging by the 
young. Niethammer (1972) demonstrated a positive correlation be- 
tween number of mammae and average litter size for species of 
Arvicolidae and commented that species with fewer nipples occupy 
the southern periphery of the global arvicolid distribution, a gen- 
eralization which holds for North American Microtus. 

Aside from variation in the mammary gland formula, the female 
reproductive system has received scant attention in systematic in- 
vestigations. Ziegler (1961) documented the presence of a baubel- 
lum (os clitoridis) in some individuals of M. longicaudus and M. 
californicus and suggested that it was not as uniform in appearance 
and occurrence as the baculum. Arata et al. (1965) failed to discover 
a baubellum in 21 M. montanus but demonstrated the presence of 
three cartilaginous lobes of the clitoris, presumably homologous to 
the distal processes of the complex penis. Hamilton (1941) illus- 
trated the female urogenital tract of adult M. pennsylvanicus, noting 
the duplex uterine structure characteristic of most Rodentia. ‘The 
need for detailed comparative studies of the female reproductive 
tract complementary to those performed on the male tract is readily 
apparent. 

The need to augment our understanding of function associated 
with variations in both male and female reproductive morphologies 


Macroanatomy 159 


is similarly indicated. The role of preputial gland secretions in 
advertising reproductive status and modulating agonistic and ter- 
ritorial behavior is well established (Brown and Williams, 1972), 
but the purposes of the other male accessory reproductive glands 
are less easily interpretable. The probable interaction of accessory 
glands in the formation of copulatory plugs, which have been re- 
ported for species of Microtus, and the hypothesis of copulatory 
plugs as a mechanism of chastity enforcement offer exciting research 
opportunities linking morphology and breeding systems in muroid 
rodents (see Hartung and Dewsbury, 1978; Voss, 1979). In dis- 
cussing the adaptive significance of the baculum of the hamster, 
Callery (1951:206) allowed that “‘. .. detailed studies of copulation 
may show that this structure is of significance in reproduction.” 
While this prediction may seem vacuous, it nonetheless conveys our 
very elementary appreciation of function in regard to phallic mor- 
phology, especially those variations which define the simple versus 
complex penes of muroid rodents. Hershkovitz (1966) advanced a 
lock and key hypothesis to explain muroid phallic diversity, and 
Long and Frank (1968) related the structure of the baculum to 
facilitation of vaginal penetration and stimulation. Dewsbury and 
colleagues (see review by Dewsbury, 1975) have revealed a corre- 
spondence of penile shape and certain aspects of copulatory pat- 
terns, but their correlation pertains only to muroids with a simple 
phallus. Except in a most general sense, these hypotheses offer little 
insight toward understanding the functional importance of details 
of muroid penile morphology (for example, the dorsal papilla, ure- 
thral flaps, bacular mounds) to copulatory behavior and female 
reproductive anatomy. Blandau (1945), on the other hand, metic- 
ulously verified that the bacular mounds of the glans penis of the 
lab rat are reciprocally oriented to engage similar lappets guarding 
the vaginal cervix and described how their contact during copula- 
tion stimulated cervical relaxation and exposure of the uterine ori- 
fices just prior to ejaculation. Investigations of this kind, together 
with further elucidation of female neuroendocrine mechanisms as- 
sociated with ovulation and pregnancy initiation, will provide great- 
er illumination of muroid reproductive adaptations. 


Discussion 


The morphological attributes surveyed in the preceding sections 
compose the known phenotypic landscape of the genus Microtus 


160 Carleton 


and may be viewed from the standpoint of their antiquity. Hennig 
(1966) spoke of the “Age of Origin” of a group of organisms, and, 
in an analogous sense, I am looking at the relative age of origin of 
the various anatomical features exhibited by living species of Mr- 
crotus. To review the morphology of Microtus from this perspective 
involves both an assessment of the characters’ evolutionary polarity 
and some estimate of their initial appearance in phylogeny. My 
rationale for determining the ancestral or derived nature of the 
various traits (see Table 3) may be found in the previous discussions 
or the literature sources cited. Only certain characters are of interest 
here. The observation that all Microtus possess hair, are viviparous, 
and have evergrowing incisors attests to past evolutionary events 
(cast in our taxonomic hierarchy as the Class Mammalia, Subclass 
Theria, and Order Rodentia, respectively) so distantly removed as 
to be inappropriate to a discussion of this volume’s subject. Within 
Rodentia, four hierarchical levels, presumably corresponding to ma- 
jor adaptive radiations, seem pertinent to an understanding of the 
heritage of characters seen in extant Microtus. These levels are the 
Muroidea, the Arvicolidae, a tribal-level clade including Microtus, 
and the cladogenesis of species assigned to the genus Microtus itself. 

The Superfamily Muroidea embraces some 250 genera and 1,100 
Recent species, or about one-quarter of all living mammals. Their 
speciosity, virtually world-wide distribution, and immense ecologi- 
cal diversity qualify them as the most successful radiation of con- 
temporary rodents. Although many of the Recent muroid groups 
may not have differentiated until the late Oligocene or Miocene, 
muroids certainly appeared by early Oligocene times, over 40 
m.y.b.p. The late Eocene form Simimys may be the earliest known 
muroid; however, this enigmatic genus has been variously shuffled 
between Muroidea and Dipodoidea (see Emry, 1981, for an over- 
view). The voles and lemmings, Family Arvicolidae, constitute one 
of the more recently evolved assemblages of the 13-15 that are 
conventionally recognized within Muroidea (see Carleton, 1980, for 
a review of muroid classifications). The earliest indisputable arvic- 
olids, Microtoscoptes and Paramicrotoscoptes, date from the latest 
Miocene (early Hemphillian) of North America, about 6-8 m.y.b.p. 
(Martin, 1975; Repenning, 1980). Despite the comparative recency 
of their appearance, arvicolids have radiated explosively into some 
17 genera representing approximately 125 species, much of this 
diversification occurring from the late Pliocene or early Pleistocene 


Macroanatomy 161 


onwards. Sometime during this period, the ancestor of Microtus and 
related genera emerged. Formal tribes have been erected for the 
genera of Arvicolidae, but I have refrained from specifying one that 
embraces Microtus because disagreement exists over the content of 
such a tribe. Nevertheless, the differentiation of a tribal-level group 
including Microtus and some unspecified number of other genera 
probably transpired in the upper Pliocene, about 2.5—4.0 m.y.b.p. 
The genus Muicrotus, which contains over half of the 125 living 
species of arvicolids, arose comparatively recently. The transition 
from its putative antecedent Allophaiomys is recognized as very early 
Pleistocene, 1.6 to 1.8 m.y.b.p. (Chaline, 1966, 1977; Repenning, 
1980). 

Consideration of the antiquity of the characters of Microtus from 
these four taxonomic ages of origin imposes the stratification pre- 
sented in ‘Table 3. Several points of clarification are warranted 
regarding interpretation of the table. I was obviously constrained 
in assigning a character to one of the four taxonomic levels which 
I initially deemed pertinent to include. Consequently, the placement 
of a trait under a particular column connotes its appearance at least 
at that given taxonomic level; the trait’s origin may have been ear- 
lier. For instance, the smooth-faced upper incisors observed in M:- 
crotus may antedate Muroidea and probably characterized the an- 
cestral myomorph or even the primordial rodent. In instances where 
several character states are found among species of Microtus, I listed 
only the plesiomorphic condition and indicated the existence of more 
apomorphic states by an arrow. The extent of these derived mor- 
phologies is addressed in the preceding anatomical review. I do not 
mean to imply that a character is necessarily uniquely derived for 
the taxonomic level at which it is listed, only that it must have 
originated at that level at least once in the genealogical pathway 
leading to extant Microtus. Numerous examples of suspected par- 
allelism may be cited among the characters surveyed. 

The literature covering various aspects of arvicolid anatomy en- 
compasses six major organ systems and some 71 characters. Of these 
71, most states (49) exhibited by Microtus are interpreted as ances- 
tral either at the level of the Muroidea or Arvicolidae (Table 3), 
and therefore are inappropriate for assessing the near generic rel- 
atives of Microtus or the basis of its generic recognition. A super- 
ficial appraisal of the 22 traits listed under the tribal-level clade 
(Table 3) suggests that many of them cladistically affiliate Microtus 


Carleton 


162 


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166 Carleton 


with Arvicola and Lagurus (Lemmiscus), a notion which received 
support in some studies (for example, Hinton, 1926; Hooper and 
Hart, 1962) but not others (Dearden, 1959; Koenigswald, 1980). 
At this stage of our understanding, however, the morphological 
similarity of Microtus to other genera cannot be reliably segregated 
into that due to parallelism and that consequent to descent from a 
common ancestor. A surprising paradox emerges from this exercise: 
given the currently accepted contents of Microtus, the genus itself 
seemingly lacks any uniquely derived character states that unam- 
biguously diagnose it from other genera of Arvicolidae (Table 3). 
This finding indirectly acknowledges that the derived features ob- 
served in Microtus may have been independently acquired in mul- 
tiple lineages of arvicolids or may indeed represent synapomorphies 
uniting Microtus in a tribal group. Whatever the case, the existence 
of synapomorphic features that circumscribe Microtus to the exclu- 
sion of other arvicolids is not eminently apparent. 

What attributes, then, lend identity to Microtus? Miller’s (1896) 
synopsis of the arvicolids (then viewed as the subfamily Microtinae) 
stressed (p. 24) a “‘.. . classification ... based on an assemblage of 
characters.” In this attitude, his systematic approach was decidedly 
more enlightened than that of his predecessors, such as Blasius and 
Lataste, who erected their systems of classification largely around 
single morphological features (Miller [1896] reviewed the early his- 
tory of Microtus taxonomy). Miller (1896:44) enumerated nine “‘es- 
sential characters” for Microtus (see also Anderson, this volume): 


1) upper incisors without grooves; 

2) lower incisors with roots on the outer side of molar series; 

3) molars rootless; 

4) enamel pattern characterized by approximate equality of 
reentrant angles; 

5) m1 usually with five closed or nearly closed triangles; 

6) M3 with one, two, or three closed triangles; 

7) tail nearly always longer than hindfoot, terete; 

8) feet, fur, eyes, and ears very variable; 

9) thumb never with a well-developed ligulate nail. 


Characters 1, 4, 7, and 9 are symplesiomorphies and attest to noth- 
ing more than the common heritage of species of Microtus as mu- 
roids. In effect, these attributes separated species of Microtus from 
some anatomically distinctive forms which Miller retained as gen- 


Macroanatomy 167 


era, namely Dicrostonyx, Lemmus, Synaptomys, and Ondatra. Char- 
acters 2, 3, 5, and 6 stand as apomorphies relative to their condition 
in the ancestral arvicolid, yet they are shared by several genera. 
Moreover, the variable definition of numbers 5 and 6 renders them 
difficult to apply in specific cases. And condition 8 cannot really be 
considered a diagnostic character, but rather Miller’s (1896) ac- 
knowledgement of the immense variation of these features within 
the genus as he perceived it. In his revision of North American 
Microtus, Bailey (1900) repeated most of Miller’s generic charac- 
ters, namely 1-4, 7, and 9. Bailey, however, deleted characters 5, 
6, and 8 from his generic definition and added one other: palate 
with median ridge, lateral pits, and complete lateral bridges. The 
topography of the palatal region in Microtus is considered derived, 
but like the apomorphic states which compose parts of Miller’s 
diagnosis, it characterizes several genera of arvicolids. 

The recognition of Microtus, therefore, has traditionally rested 
upon a mixture of ancestral and derived features, the latter derived 
only relative to the ancestor or early representatives of Arvicolidae 
but not strictly synapomorphic for Microtus. The taxon’s cohesive- 
ness issues not from the joint possession of uniquely derived features 
but from the unique combination of traits exhibited by most of its 
members, a property which qualifies it as a polythetic entity (sensu 
Sneath and Sokal, 1973). This observation provides some credence 
to the viewpoint that Micvotus is at best a paraphyletic taxon (sensu 
Ashlock, 1972); that is, not all descendants of the most recent com- 
mon ancestor of the genus Microtus are contained within it. Wheth- 
er the genus is polyphyletic also remains a possibility. One may 
argue that evaluation of the status of Microtus based upon the an- 
tiquated (presumably) studies of Bailey (1900) and Miller (1896) 
presents a specious perspective; after all, the generic limits of Mz- 
crotus have changed substantially since the year 1900. This is true. 
Of the 14 subgenera allocated to Microtus by Miller (1896) and 
Bailey (1900), six are currently established as genera (Alticola, Ar- 
vicola, Eothenomys, Hyperacrius, Lagurus, and Neofiber) and one is 
considered synonymous with another genus (Anteliomys of Eothen- 
omys). Yet despite the restriction in generic scope, the characters 
used today (see, for example, Hall, 1981; Ognev, 1950) are re- 
markably the same basic ones set forth by Miller and Bailey, a 
realization which further strengthens the interpretation of Microtus 
as (at best) a paraphyletic group. 


168 Carleton 


What this observation portends for future phylogenetic studies of 
Microtus is unclear. Further analyses may result in division of the 
taxon, identifying smaller and, ideally, monophyletically delineated 
groups. In fact, investigators subsequent to Miller and Bailey fol- 
lowed this course and raised most of their subgenera to genera. 
Thus, Hinton (1926) and Ellerman (1941) treated Chilotus, Her- 
petomys, Orthriomys, Pedomys, and Pitymys as genera distinct from 
Microtus, together with the six now recognized as valid, and even 
Miller later accorded generic status to several forms which he orig- 
inally had arranged as subgenera in 1896 (Miller, 1912, 1924; 
Miller and Kellogg, 1955). Alternatively, pursuance of the criterion 
of monophyly may recommend the subordination of certain genera 
to their former rank as subgenera of Microtus, a course which holds 
a certain attraction. The distant phyletic affinity perceived today 
for some former subgenera of Miller’s (1896) Microtus (that is, 
Alticola, Eothenomys, Hyperacrius, and Neofiber) seems to ratify 
maintenance of their generic separateness, but the isolation of Ar- 
vicola and Lagurus deserves reappraisal in this light. Possibly, the 
unequivocal establishment of a monophyletic concept for Microtus 
will prove to be an elusive goal. The genus may remain a poly- 
thetically defined assemblage whose cladistic stature relative to oth- 
er genera of Arvicolidae is always suspected of being paraphyletic. 
Such a pragmatic taxonomic stance may be inescapable in view of 
the rife parallelism that has apparently attended the radiation of 
arvicolids and the difficulty of distilling synapomorphic traits in a 
complex of persistent sister species. These evolutionary circum- 
stances apply particularly to Microtus, a genus in which parallelism 
seemingly represents an historical fact of the group’s cladogenesis 
(Chaline, 1966, 1974), and one whose period of differentiation oc- 
curred as recently as the early Pleistocene (Chaline, 1977; Repen- 
ning, 1980). 

Any of the systematic courses outlined above will hinge on careful 
and rigorous analysis of the characters which form the essence of 
our phylogenetic inference and classificatory reference system. Such 
analysis must include the continued exploration of other anatomical 
systems and discovery of new characters, potentially valuable for 
testing current estimates of relationship. And there exists a need to 
extend character surveys of non-traditional anatomical systems that 
have received cursory attention to date. For example, the muscular 
and reproductive systems of too few species of Microtus have been 


Macroanatomy 169 


examined, disallowing definitive assessments of a character’s ubiq- 
uity within the genus and its value as a synapomorphy. Throughout 
the chapter, I have referred somewhat casually and dogmatically to 
“characters” as if their basis and recognition are intrinsically self- 
evident. The documentation of correlation among and unsuspected 
variation of several hallowed “characters” used in arvicolid system- 
atics reveals the weakness of any such assertion. Perhaps the num- 
ber of triangles is less important than some term that simultaneous- 
ly conveys the shape of those triangles and the orientation of their 
cutting surfaces. The former difference is countable and easily ex- 
pressed; the latter lacks familiarity and a formulated language of 
comparison. Therefore, in addition to searching out other taxonom- 
ically useful features and augmenting previous anatomical studies, 
the primacy of character analysis to the construction of phylogenies 
and classifications obligates us to continually refine our character 
definitions. 


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MICROANATOMY 
CARLETON J. PHILLIPS 


Abstract 


(Nore selection of tissues from species of New World Microtus 
have been investigated in detail at the light microscopic level; 
at the ultrastructural level Muicrotus is virtually unknown. Most 
previous histological studies have been in conjunction with analyses 
of the evolutionary process, systematics, populations, and ontogeny. 
In particular, light microscopic data are available in the literature 
for such features as the dentition, integumentary glands, tarsal 
glands, adrenal glands, ovaries and testes, and digestive tracts. Mi- 
croanatomical studies of the dentition have revealed likely steps or 
phases and preadaptive characteristics involved in the evolution of 
evergrowing molars. The histology, histochemistry, and actual pres- 
ence or absence of both tarsal and integumentary glands have been 
used successfully in systematic investigations. The adrenal glands 
of Microtus have been shown to undergo histological changes in 
correlation with population density and reproductive status. Ovar- 
ian microanatomy has allowed for estimation of prenatal mortality; 
histology of both ovaries and testes has been used previously to 
demonstrate the effects of variables such as light intensity, photo- 
period, and crowding on sexual maturation. Previously unavailable 
ultrastructural descriptions of the retinal pigment epithelium and 
photoreceptor cells, the parotid and submandibular salivary glands, 
and the esophagus, stomach, and small intestine are provided in 
this chapter. The eye in Microtus has approximately 10% cone and 
90% rod photoreceptors; ultrastructurally the retina resembles that 
found in fossorial pocket gophers, Geomys. ‘The parotid salivary 
gland is serous and has secretory intercalated ducts, whereas the 
submandibular has mucous acini, secretory intercalated ducts, and 
granular intralobular ducts. The ultrastructure of the esophagus, 
gastric mucosa, and small intestine generally resembles that of lab- 
oratory rodents. Although Microtus is not known to have a symbiotic 
microbial relationship, rod-type bacteria nevertheless are found at- 
tached to the keratinized, non-glandular surface of the forestomach. 


176 


Microanatomy 177 


Introduction 


With three major exceptions, organ systems in species of New 
World Microtus have not been described in detail at either the light 
microscopic or transmission electron microscopic levels. ‘The excep- 
tions—dentition, stomachs, and certain skin glands—previously have 
been described and discussed in considerable histological (light mi- 
croscopic) detail with reference to systematics, evolution, and ecol- 
ogy. The light microscopic histology of several other organs—es- 
pecially adrenal glands and ovaries and testes—has been used fairly 
frequently, particularly in the course of ecological and populational 
studies. Somewhat surprisingly, however, these tissues never have 
been described qualitatively or quantitatively to the point where 
intergeneric or interspecific histological comparisons can be made 
with precision. 

The absence of complete, descriptive, microanatomical data for 
Microtus, and other microtines as well, is not particularly surprising 
in view of the fact that microanatomical compendia are available 
only for laboratory mice (Mus), rats (Rattus), and golden hamsters 
(Mesocricetus). The amount of previously published descriptive mi- 
croanatomical data for Microtus necessitated that this chapter be 
somewhat limited in scope. Consequently, not all organ systems are 
represented here and, among those that are, some are described and 
illustrated at the ultrastructural level for the first time. 

The main goals of this chapter are: 1) to help establish a data 
base that will allow for comparisons between Microtus and other 
genera of rodents; 2) to stimulate further study by illustrating the 
sparseness of current knowledge; 3) to summarize the existing mi- 
croanatomical data and sources of information; and 4) to present 
structural information useful to those engaged in other areas of 
research in which knowledge of microanatomy, particularly at the 
ultrastructural level, could be valuable to analysis and interpreta- 
tion of data. 


Methods 


Both light and electron microscopic techniques were used to ob- 
tain microanatomical data that are presented for the first time in 
this chapter. New data are based on five specimens of Muicrotus 
pennsylvanicus (two males, three females) collected in Franklin and 


178 Phillips 


Aroostook Counties, Maine. Voucher specimens from these locali- 
ties are deposited in the collection at the Carnegie Museum of 
Natural History. 

The standard light micrographs of molar dentition were taken 
with an Olympus Vanox photomicroscope with Nomarski interfer- 
ence-contrast optics (IOC). The jaws were fixed in 10% non-buff- 
ered formalin and decalcified in Decal (Scientific Products); a cal- 
cium precipitant test (Lillie, 1965) was used to determine total 
decalcification. The jaws then were embedded in Paraplast and 
sectioned and stained according to routine, widely used techniques 
(see Humason [1972] and Lillie [1965] for detailed descriptive in- 
formation). 

Cellular ultrastructure, as studied with transmission electron mi- 
croscopy (TEM), is heavily emphasized in this chapter. Although 
much remains to be learned from light-level histochemistry, ultra- 
structure probably will prove to be a better basic source of infor- 
mation suitable for comparative investigations. ‘The techniques em- 
ployed for TEM analysis are less well standardized than are 
histological techniques, and for that reason I present here a reason- 
ably complete description of methodology. I found trialdehyde fix- 
ative to be very well suited to ultrastructural analysis of microtines 
and, with minor changes in protocol, it can be used easily under 
field conditions (Phillips, in press). 

Specimens were anaesthetized with 0.25 cc of sodium pentobar- 
bital (50 mg/ml) and intubated by means of polyethylene tubing 
that was passed via the mouth and esophagus into the stomach. ‘The 
primary fixative (based on Kalt and Tandler, 1971) consisted of 3% 
glutaraldehyde, 2% formaldehyde (made fresh each day from para- 
formaldehyde powder), 1% acrolein, 2.5% dimethyl sulfoxide 
(DMSO), and 1 mM CaCl, in 0.05 M cacodylate buffer at pH 7.2 
with 0.1 M sucrose. For digestive tract tissues, fixative was intro- 
duced to the lumina by attaching a 1 cc syringe to the free end of 
the tubing. Meanwhile, other tissues, such as eyes and salivary 
glands, were removed and either hemisectioned (eyes) or diced in 
fixative. After 5 min the digestive tract tissues were removed from 
the visceral cavity and diced in fixative. All tissues were stored in 
primary fixative for 20 h and then placed in fresh buffer with 3% 
glutaraldehyde and stored at 4°C. For processing, tissues were 
washed for 1 h in 0.05 M cacodylate buffer (pH 7.2) with 0.1 M 
sucrose (three changes, 10 min each) and post-fixed for 1 h in 1% 


Microanatomy 179 


OsO, with cacodylate buffer and sucrose. Tissues then were dehy- 
drated in an ETOH series (50, 70, 90, and 95%) for 20 min each 
followed by three changes in 100% E’TOH (10 min each) and then 
three changes (10 min each) in propylene oxide. Lastly, tissues were 
left overnight in a propylene oxide-Epon 812 mixture (1:1) and 
vacuum infiltrated for 6 h in fresh Epon 812. The resin was allowed 
to polymerize for 48 to 60 h at 60°C. Thin sections were studied 
and micrographed with a Philips TEM 201 operated at 60 KV. 
“Thick” sections (0.5 um) of Epon-embedded tissue were stained 
with toluidine blue and micrographed with an Olympus Vanox and 
Nomarski IOC. 


Brain 


Histological study of the brain of any mammal is extremely com- 
plex and requires not only careful fixation but also careful orien- 
tation. Indeed, stereoscopic histological atlases are available only for 
common laboratory rodents such as rats and golden hamsters (for 
example, see Knigge and Joseph, 1968). Insofar as Muicrotus is 
concerned, the brain has not been described at either the light or 
electron microscopic level and, therefore, nothing definitive can be 
said about the microanatomy of the brain. However, Quay (1969) 
reported that he sectioned and examined histologically the brains 
of 12 specimens of Microtus pennsylvanicus. Quay’s investigation 
was a follow-up of an earlier study of the collared lemming (Quay, 
1960) and dealt with the occurrence of colloid deposits in the brains 
of microtine rodents collected in western Canada. Although Quay 
(1969) did not find birefringent colloid deposits in the brain of any 
of the specimens of Microtus, 12 of 16 captive specimens of Dicros- 
tonyx and one wild-caught specimen of Phenacomys did exhibit 
these unusual, possibly pathological, features in their brain tissue. 


Anterior Pituitary Gland 


The ultrastructure of the anterior pituitary gland has been stud- 
ied and described only for an Old World species, Microtus agrestis 
(Charlton and Worth, 1975), but deserves mention here because of 
Hinkley’s (1966) earlier investigation of the effects of plant extracts 
on cell types in the anterior pituitary of M. montanus. In the study 


180 Phillips 


by Charlton and Worth (1975), the pituitary cell types were iden- 
tified by fine structural criteria and comparisons were made to ho- 
mologous cells in laboratory rats. Prolactotrophs, somatotrophs, go- 
nadotrophs, corticotrophs, thyrotrophs, and follicular cells were all 
found to be very similar to the presumably homologous cells in 
Rattus, even after a series of experimental manipulations (Charlton 
and Worth, 1975). One unusual feature, which possibly is unique 
to the anterior pituitary of Microtus, was an “organelle” of un- 
known function found in the adenohypophysial cells. The authors 
(Charlton and Worth, 1975) described the structure as a complex 
array of closely appressed granular endoplasmic reticulum (GER) 
located adjacent to the Golgi complex. From this discription it seems 
likely that the structure is related to protein synthesis. Although the 
gonadotrophic cells from sexually mature individuals most com- 
monly contained this “organelle,” it also was found in all of the 
other types of granular cells. The discovery of an unusual feature 
in gonadotrophs is especially noteworthy in terms of Hinkley’s 
(1966) report that in male Microtus montanus, gonadotrophic (delta) 
cells increased by 41% following a diet of acetone-ether extract from 
sprouted wheat. 


Eyes 


The structure of the eye in Microtus previously has been inves- 
tigated only superficially (for example, Chase, 1972); and because 
the following account covers only the retinal pigment epithelium 
(RPE) and neural retina, many relatively basic questions will re- 
main unanswered. Even though microtines have not been studied 
in detail, enough other species of rodents have been subjects of 
developmental, functional, histological, and ultrastructural investi- 
gations for one to conclude that probably no other mammalian order 
approaches the Rodentia in structural diversity of the eye. This 
should not be particularly surprising because the behavioral and 
ecological diversity among rodents clearly sets them apart from oth- 
er orders. Indeed, it is for these very reasons that attention is called 
to the eye in species of Microtus. 

A basic assumption in constructing an understanding of the evo- 
lution of visual-system microanatomy is, of course, that Microtus 
relies on visual cues as well as on olfactory and auditory input. 


Muicroanatomy 181 


Although the eyes in Microtus are small in comparison to the bulg- 
ing eyes that are so obviously characteristic of most nocturnal cri- 
cetids, it nevertheless is safe to assume that vision is an important 
component of the total sensory system in microtines. Particularly 
significant in this regard is the finding that Microtus pennsylvanicus 
uses a Sun-compass system in orientation, at least in homing females 
(Fluharty et al., 1976). They demonstrated that experimental shifts 
in photoperiod would alter orientation in a predictable, clock-wise 
fashion. Thus, the eyes in M. pennsylvanicus apparently serve as 
the receptors in a fundamentally important, integrated behavioral- 
physiological process that includes some type of “biological clock.” 
The level of visual activity in Microtus is unknown, but it possibly 
is significant that most, or perhaps all, of the species are highly 
susceptible to predation by owls. Consequently, future studies in 
which different roles of the visual system (for example, integrated 
sensory receptors in comparison to “‘sight’’) can be analyzed and 
then compared will be of special interest. 

Microanatomical examination of the eye of light-adapted indi- 
viduals reveals that the choroid layer and retinal pigment epithe- 
lium are relatively thick in Microtus. The stroma of the choroid is 
compact, densely pigmented, and contains relatively few macro- 
phages (Fig. 1). The prominent chorio-capillary zone is highly in- 
nervated (Fig. 1) in Microtus and is set in a dense matrix of con- 
nective tissue fibers. When viewed in a plane perpendicular to the 
RPE, Bruch’s membrane has a compressed, dense appearance with 
elastic fibers scattered throughout. A complex network of interlaced 
individual collagen fibers and reticular fibrils is readily apparent 
in oblique views (Fig. 2). 

The retinal pigment epithelium (RPE) is a monolayer of cells 
that developmentally are derived from the neuroectoderm. The 
function, role, and cytochemistry of the RPE have been investigated 
fairly intensively in vertebrates and presently these cells are known 
to: 1) serve as a blood-retina barrier; 2) interact with the photore- 
ceptor cells through phagocytosis and degradation of age membrane 
discs at the tips of the outer segments; 3) produce pigment granules 
in varying numbers; and 4) serve in ocular defense through their 
immunophagocytic capacity (Elner et al., 1981; Nguyen-Lagros, 
1978; Young, 1971). Among these roles, the best known and most 
studied is that of phagocytosis and degradation of outer membrane 
discs. 


182 Phillips 


Fic. 1. Top: light micrograph showing several principal retinal components in 
Microtus. Note extreme abundance of melanolysosomes (arrow) in the retinal pig- 
ment epithelium (RPE). Area enclosed in box is roughly equivalent to the area 
shown below. Abbreviations are: OS, outer segments of photoreceptors; IS, inner 


Muicroanatomy 183 


The RPE cells in Microtus are characterized by their unusual 
height, extreme abundance of spherical and ovoid melanin granules, 
and by the presence of osmophilic droplets that are not membrane- 
bound and apparently lipid in nature (Figs. 1, 2). The RPE basal 
membrane is complexly infolded; coated vesicles commonly are found 
within the adjacent cytoplasm but other cytoplasmic constituents, 
such as free polyribosomes and smooth endoplasmic reticulum 
(SER), are virtually absent from this area. The remaining cyto- 
plasm, however, is densely filled with tubular SER and polyribo- 
somes (Figs. 2, 3). Lamellar Golgi complexes also are common 
constituents of the middle zone of RPE cytoplasm (Fig. 2). The 
RPE mitochondria are found throughout the cell; the mitochondrial 
profiles either are elongate or nearly round and have both tubular 
and lamellar cristae. 

Given the role of RPE in degradation of outer disc membranes, 
it is not at all surprising that the cytoplasm of the RPE cells in 
Microtus contains large numbers of phagosomes (Fig. 2), lysosomes, 
and pigment granules. The pigment granules, which more accu- 
rately can be termed “‘melanolysosomes” because of their acid phos- 
phatase activity (Leuenberger and Novikoff, 1975), are extremely 
abundant in the RPE cell cytoplasm in Microtus (Fig. 1). Analysis 
of TEM micrographs of Microtus RPE provides ultrastructural 
data that seem to both support and correspond well with the cyto- 
chemical studies of Novikoff et al. (1979). Examples of continuity 
between tubular SER and plasma membranes encasing melanoly- 
sosomes, particularly in mature forms of the latter, are fairly com- 
mon (Fig. 2). Additionally, in instances in which membrane sur- 
rounding melanolysosomes is sectioned within about 30° of a 
perpendicular plane, the surrounding plasma membrane can be 
demonstrated to be unusually thick and apparently tripartite. In 
the example illustrated in Fig. 2, the melanolysosomes are in the 
physical proximity of a Golgi complex and tubular SER, which 
can be characterized as GERL. The GERL in turn apparently is 
directly involved in production of RPE lysosomes. Cytochemical 


a 

segments; C, cone photoreceptor; ONL, outer nuclear layer. Scale bar = 3.5 um. 
Bottom: transmission electron micrograph (TEM) of choroid showing melanin gran- 
ules and choroidal innervation (N). Scale bar = 0.5 um. 


Phillips 


184 


a 
. 
¥ 
= 


Microanatomy 185 


studies of this organelle have shown it to be both rich in hydrolase 
and the site of tyrosinase and acid phosphatase activity as well 
(Eppig and Dumont, 1972; Novikoff, 1976; Novikoff et al., 1979). 
Microperoxisomes also are abundant in Microtus RPE cell cyto- 
plasm. These small spherical bodies are encased in thick, electron 
dense membrane and internally have a granular appearance (Fig. 
2). Previous catalase cytochemical analysis of Mus RPE cells has 
revealed frequent continuity between microperoxisomes and SER 
(Leuenberger and Novikoff, 1975), and the same sort of TEM 
images can be found in Microtus. 

The RPE apical microvilli are highly elaborate and contain 
abundant ovoid pigment granules (Fig. 1) that are interspersed 
among the tips of the photoreceptor cell outer segments (Fig. 3). 
The RPE lateral cell membranes are straight and unspecialized 
except in the apical zone where adjacent cells have a dense terminal 
web and desmosomes that form a circumferential ring-like structure 
within the cytoplasm (Fig. 3). 

The neural retina of Microtus contains both rod and cone pho- 
toreceptor cells (approximately 10% cones, 90% rods). The cells are 
extremely numerous and densely packed as evidenced by the fact 
that the outer nuclear layer is 11-14 nuclei deep. According to 
Chase (1972), in M. ochrogaster the RPE, bacillary layer, and outer 
nuclear layer measure, respectively, 13, 30, and 34 um. 

The cone photoreceptors can be distinguished from the rods by 
virtue of: 1) their larger inner segments (both in height and width); 
2) slightly paler cytoplasm (both in TEM thin sections and in 
toluidine blue-stained “‘thick”’ sections); 3) significantly larger and 
paler mitochondria; 4) their large, spherical, euchromatic nuclei, 
and 5) their complex pedicle-type synaptic bases (Figs. 1, 4, 5). 
Additionally, the cone photoreceptors in Microtus are of particular 
interest because of the extremely large and broad calyx that extends 


— 


Fic. 2. Top: cell cytoplasm in retinal pigment epithelium (RPE) of Muicrotus. 
Note relationship between smooth endoplasmic reticulum and developing melano- 
lysosomes (see arrows). Abbreviations are: P, phagosome; MP, microperoxisome; G, 
Golgi complex; M, mitochondrion. Scale bar = 0.25 um. Middle: lipid droplets (L) 
in RPE. Scale bar = 0.5 wm. Bottom: Bruch’s membrane (BM) and capillary (cap) 
adjacent to basal surface of an RPE cell. Note pore-like fenestrae in the capillary 
wall (arrows). Scale bar = 0.25 um. 


186 Phillips 


Fic. 3. A slightly oblique cut through the apical surface of a retinal pigment 


epithelial (RPE) cell showing the relationship between RPE microvilli (MV) and 
photoreceptor outer segments (OS). Note also the cell junction with dense fibrils 


Microanatomy 187 


well beyond the ciliary stalk and appears to cradle the entire basal 
portion of the outer segment (Fig. 5). In at least some examples the 
calyx clearly forms a type of cytoplasmic bridge so that the inner 
and the outer segments of a given cell have a continuity that is 
additional to the non-motile cilium (Fig. 5). Without serial sections 
it is impossible to determine whether or not such cytoplasmic bridg- 
ing is characteristic of all the individual cone photoreceptor cells in 
Microtus. In a previous report of cytoplasmic bridging (Richardson, 
1969), it was concluded that such bridges were a regular feature of 
both cones and rods in the thirteen-lined ground squirrel (Sper- 
mophilus tridecemlineatus). 

In contrast to the cones, the abundant rod photoreceptors in Mi- 
crotus are narrow in outline, and the nuclei are somewhat ovoid 
and characteristically nearly filled with heterochromatin and the 
synaptic terminals are of the spherule type (Figs. 4, 5). As in the 
cone photoreceptors, cytoplasmic bridging also is found in the rods 
but probably because the rods are so narrow, examples are more 
scarce than they are among the cones. The potential importance of 
cytoplasmic bridging between the inner and outer segments of rods 
and cones lies in the question of how new membrane discs are 
formed by the photoreceptors and how these discs come to contain 
visual pigment. The most widely accepted model for origin of disc 
membranes is one in which new discs are thought to originate from 
invagination of plasma membrane of the outer segment (Sjéstrand 
and Kreman, 1979). Originally it was assumed that opsin was syn- 
thesized in the cytoplasm of the inner segment and then transported 
directly to the outer segment in membranous vesicles. Such a model 
viewed membrane as “fixed,” and thus proposed that opsin-con- 
taining vesicles moved through the cytoplasm and would of necessity 
use the ciliary stalk as an access route to the outer segment (Fig. 
4). Therefore, the presence of cytoplasmic bridging (Fig. 5) would 
seem to be particularly important because it would result in in- 
creased cytoplasmic contact between inner and outer segments (see 
Richardson, 1969). However, in our more current view of mem- 


—_— 

(arrow), the large, coated vesicle (CV), tubular smooth endoplasmic reticulum (SER), 
sparse granular endoplasmic reticulum (GER), and melanolysosomes (ML). Scale 
bar = 1 um. 


Phillips 


188 


Microanatomy 189 


brane structure the possibility of compartmentalized zones within 
the membrane, as well as constituent flow, allows for non-cyto- 
plasmic transport to the outer segment discs. Such a view is sup- 
ported by findings from freeze-fracture studies (Besharse and Pfen- 
ninger, 1980; Rohlich, 1975; Sjéstrand and Kreman, 1979). 
Presently it is known that visual pigment apoprotein originates in 
the GER and Golgi complex of the inner segment, passes through 
the ellipsoid in association with membrane, is incorporated into the 
inner segment plasmalemma in the periciliary region, and flows 
over the cilium into the outer segment where it is incorporated into 
newly formed discs (Besharse and Pfenninger, 1980; Papermaster 
et al., 1975; Rohlich, 1975; Young and Droz, 1968). Fundamental 
structural changes in the plasma membrane take place when the 
discs actually form from the outer segment membrane (Sjéstrand 
and Kreman, 1979). It also has been speculated that lipid synthesis 
takes place in the narrow “growth” zone where discs arise from 
the outer segment membrane (Sjéstrand and Kreman, 1979). In 
view of our current understanding of the disc renewal process, the 
significance of the cytoplasmic bridges found in Microtus, and some 
other rodents as well, could well be the fact that mitochondria are 
a common feature of the bridges (Fig. 5). 

Although membrane flow and the freeze-fracture data per se do 
not require cytoplasmic continuity between inner and outer seg- 
ments and do not restrict exchange to the internal portion of the 
cilium, fundamental alterations in membrane structure and synthe- 
sis of lipids would require energy and thus could be facilitated by 
the immediate presence of mitochondria. Lastly, it is of particular 
interest that typical mitochondrial profiles located within the cyto- 
plasmic bridges usually are associated physically with tubular SER 
that sometimes is organized in layers similar to those that charac- 
terize a Golgi complex (Fig. 5). The details of the entire renewal 
process obviously remain to be elucidated and the possibility of 
species-specific differences also must be considered. 


, mel 


Fic. 4. Top: junction of outer segment (OS) and inner segment (IS), showing 
cilium (c) and associated basal body (b) in the neural retina of Microtus. Note also 
the membrane (arrows) associated with the cross-striated fibril (r). Scale bar = 0.25 
um. Bottom: cross-sections through rods (R) and cone (C) photoreceptors. Compare 
the mitochondria (m) and note cross-striated fibril (arrow). Scale bar = 1 um. 


Phillips 


190 


Microanatomy 191 


The inner segment in both types of photoreceptor cells contains 
abundant polyribosomes but only a few vesicles and relatively little 
SER. Both types of photoreceptor cells have cross-striated fibrils 
that are prominent near the base of the ciliary stalk (Fig. 4). The 
cross-striated fibrils usually are associated with membrane that either 
is smooth or, occasionally, studded with ribosomes (Fig. 5). These 
fibrils are structurally similar to those found in other rodents, such 
as the guinea pig (Cavia), and presumably extend from the cilium 
to the synaptic terminal as they do in Cavia (Spira and Milman, 
1979). The exact function of cross-striated fibrils remains unknown, 
although their morphology and non-random associations with mi- 
tochondria and with membrane systems certainly implies that they 
are more than a ciliary anchoring system. Perhaps cross-striated 
fibrils aid in propagation of changes in membrane potential or serve 
as part of a system with contractile capability (Spira and Milman, 
1979); 

The synaptic layer in Microtus retina is vascularized. Broad- 
based cone pedicles can be distinguished readily from the rod spher- 
ules. The cone pedicles are characterized by numerous invading 
processes from bipolar and horizontal cells; the latter two kinds of 
cells have a much paler cytoplasm than do the photoreceptors. The 
similar rod spherules usually contain two to four pale profiles (Fig. 
5). Both rod and cone terminals typically contain at least one mi- 
tochondrial profile and one or more synaptic ribbon (Fig. 5). Elec- 
tron dense zones denote synaptic junctions within the terminals as 
well as between adjacent cones and rods (Fig. 5). 

In summary, microanatomical analysis of the retinal pigment 
epithelium and neural retina in Microtus reveals a complex, mixed 
cone-rod photoreceptor system suggestive of both scotopic and phot- 
opic vision. In comparison to other studied rodents, Microtus ap- 


_ 


Fic. 5. Top left: synaptic layer in the neural retina of Microtus showing rod 
spherules filled with synaptic vesicles (sv). The pale profiles (n) are sections through 
connecting bipolar and horizontal neurons. Note the single mitochondrial profile (m) 
and pairs of synaptic ribbons (sr). Scale bar = 0.5 wm. Top right: Bases of outer 
segments of rod (left) and cone (right) photoreceptors. Scale bar = 1 um. Bottom: 
longitudinal sections comparing rod and cone photoreceptors. Compare the mito- 
chondrial profiles (m) and note the ribosomes (arrow) attached to membrane asso- 
ciated with the rootlet fiber; b, basal body. Scale bar = 1 um. 


192 Phillips 


pears to be unique in a number of ways. Firstly, the RPE not only 
is thick but also densely filled with melanolysosomes that occupy 
the apical zone of cytoplasm. Although such comparisons have not 
been made previously, examination of micrographs published in 
Kuwabara (1979) and elsewhere clearly indicate that melanoly- 
sosome abundance is far greater in Microtus than in Rattus, Mus, 
Cavia, and Mesocricetus. The greatest morphological similarity is 
between Microtus and the diurnal ground squirrels, Spermophilus, 
and the fossorial plains pocket gopher, Geomys bursarius (Feldman 
and Phillips, 1984; Jacobs et al., 1976; Kuwabara, 1979). How- 
ever, Microtus differs from even these species; in light-adapted M:- 
crotus the melanolysosomes are confined to the apical RPE cyto- 
plasm and the microvilli are relatively short, whereas in the other 
two genera the long microvilli contain most of the granules. One 
possible explanation is that this apparent difference is the result of 
light or dark adaptation prior to sacrifice, but the data presently 
are inadequate for such a determination. 

The relative percentages of rods and cones (90/10) places M:- 
crotus toward the nocturnal end of a broad category of rodents 
possessing mixed retinas. In nocturnal rodents such as Norway rats 
(Rattus norvegicus), pigmented laboratory mice, and the eastern 
woodrat (Neotoma floridana) the retinas essentially are all rod (99%), 
whereas in diurnal ground squirrels (Spermophilus and Cynomys), 
cones comprise about 95% of the photoreceptor cells (Cohen, 1960; 
Feldman and Phillips, 1984; Jacobs et al., 1976; West and Dow- 
ling, 1975). Overall, Mzcrotus joins a group of species that includes 
the gray squirrel (Sciwrus carolinensis), which has about 60% cones, 
and the plains pocket gopher (Geomys bursarius), which has about 
25% cones (Feldman and Phillips, 1984; West and Dowling, 1975). 
Indeed, from a purely morphological point-of-view, Microtus is clos- 
est to Geomys. If additional study upholds these apparent similar- 
ities, the likelihood is that either both of these species share some 
common features because their eyes are less derived from the early 
ancestral state, or that the similarities are indicative of convergent 
evolution toward a fossorial or a semi-fossorial behavior. Indeed, 
Microtus pennsylvanicus spends considerable time in dark burrows 
and seems to prefer light intensities ranging from twilight to total 
darkness (Kavanau and Havenhill, 1976). Future study of the mi- 
croanatomy of rodent eyes undoubtedly will be valuable in eluci- 
dation of systematic relationships and evolutionary patterns. 


Microanatomy 193 


Future study will be required to determine such salient aspects 
of Microtus as visual acuity, spectral sensitivity, and the details of 
the inner nuclear and inner plexiform layers. The latter aspect in 
particular is totally unknown as of this writing and represents a 
topic that cannot easily be inferred from other work and, thus, will 
require considerable primary research. 


Tarsal (Meibomian) Glands 


The eyelids of mammals consist of an integumentary covering 
over a dense connective tissue support (called a “tarsal plate”) and 
skeletal muscle fibers from the orbicularis oculi muscle. Typical 
sebaceous glands are associated with the hair follicles and, in both 
the upper and lower lids, hypertrophied sebaceous glands referred 
to as tarsal, Meibom, or Meibomian glands are positioned within 
the dermis (see Carleton, this volume). Tarsal glands in the eyelids 
of a variety of microtine rodents (both New and Old World species) 
have been described by several authors (Hrabé, 1974; Quay, 1954; 
Sulc, 1929; Vesely, 1923). 

Quay (1954) found interspecific differences among the microtines 
and suggested that the distribution and abundance of tarsal glands 
might be of taxonomic value. Hrabé (1974) agreed with this as- 
sessment and with the idea that the evolutionary trend was one of 
reduction (that is, the more “primitive” microtines might be ex- 
pected to have more glandular units). Both authors (Hrabé, 1974; 
Quay, 1954) found that although the tarsal glands were reduced in 
number in some microtines (including Microtus), the individual 
glands nevertheless were significantly larger in size than in those 
species having more glands. Quay (1954) hypothesized that the 
apparent evolutionary decrease in numbers of individual glands was 
related to the trend toward reduction in size of the eye evidenced 
by many microtines, whereas the increase in size of the individual 
glands could be correlated with an increased need for protective 
secretions during burrowing and other activities associated with a 
semi-fossorial life. 

Histologically, the tarsal glands essentially are hypertrophied se- 
baceous glands that secrete a substance rich in lipids. Apparently 
the glands found in Microtus do not differ notably from homologous 
glands in other rodents or mammals in general. Quay (1954) did 
note, however, that within the upper eyelid the lateral-most tarsal 


194 Phillips 


gland was not only larger than the others but also had an excretory 
duct that followed the course of the extraorbital lacrimal gland. He 
referred to this particular tarsal gland as an extrapalpebral seba- 
ceous gland (Quay, 1954). 


Integumentary Glands 


Many species of microtine rodents are characterized by localized 
pads of hypertrophied glandular tissue that underly the epidermis 
in specific areas of the posterior integument. Although the exact 
positions of these integumentary glands can vary both generically 
and specifically, the glands nevertheless always seem to be restricted 
to four limited areas: 1) the dorsal base of the tail; 2) the rump; 3) 
bilaterally on the hips and upper thighs; and 4) bilaterally on the 
flanks (Quay, 1968). Histologically, these glands may be described 
as ‘“‘sebaceous”’ and, thus, at the light microscopic level they resem- 
ble or perhaps are identical with much smaller, less concentrated, 
glandular units normally associated with mammalian hair follicles. 
Although neither electron microscopic data nor complete biochem- 
ical analysis of the secretory product(s) presently are available, lip- 
ids clearly are one major product of the microtine skin glands (Quay, 
1968). Insofar as function is concerned, there is general agreement 
that these integumentary glands have a communicative role not only 
in microtines but also in the other mammals that possess them (see 
Eisenberg and Kleiman, 1972; Miiller-Schwarze, 1983; Ralls, 1971; 
Wolff and Johnson, 1979). 

In Microtus, hypertrophied sebaceous glands are particularly in- 
teresting for several reasons. Firstly, within the genus these glands 
apparently do not occur naturally in all of the many recognized 
species (Quay, 1968). Based on specimens that he examined, Quay 
(1968) identified a provisional group of seven nominal species in 
which skin glands had not been found. Among these, the common 
and widespread M. pennsylvanicus is noteworthy because recently 
Boonstra and Youson (1982) reported the common occurrence of 
these glands in voles of both sexes. This discovery suggests the 
possibility of an ontogenetic component to the presence or apparent 
“absence” of integumentary glands in some species of Microtus. 

Secondly, it is noteworthy that microtine skin glands can be in- 
fluenced by androgens (Jannett, 1975). In a series of experiments, 
Jannett (1975) investigated the responses of both male and female 


Microanatomy 195 


specimens of M. longicaudus and male M. pennsylvanicus to either 
injections or subcutaneous implants of testosterone. His experimen- 
tal animals included both wild-caught and laboratory progeny and 
were either castrated or ovariectomized. Although neither M. lon- 
gicaudus nor M. pennsylvanicus “normally” has skin glands in the 
wild (excepting Boonstra and Youson’s [1982] report discussed 
above), nearly all of the males and all of the females developed 
glands following administration of testosterone (Jannett, 1975). Left 
unanswered by these experiments is the question of why skin glands 
would develop after stimulation with exogenous testosterone but 
not as a consequence of endogenous androgens. Quay (1968) earlier 
had hypothesized a role for androgens and suggested that differ- 
ential androgen levels or tissue sensitivity might account for species 
or population differences in the presence or absence of the integu- 
mentary glands. Jannett (1975) mentioned the possibility of “‘dif- 
ferent” androgens and the role of other interacting sebotrophic hor- 
mones. Regardless of the reasons for specific differences, it seems 
clear that although some species of Microtus seem to lack glands, 
they nevertheless actually possess the capacity for glandular hyper- 
trophy if given an appropriate stimulation. This finding in itself is 
significant because it illustrates that the mere absence of a structural 
feature does not prove that the feature has been “‘lost” in a genetic 
or evolutionary sense. 

Lastly, the presence or absence and distribution of skin glands 
in Microtus and other microtines clearly has a taxonomic usefulness. 
Indeed, in his classic revision of voles and lemmings, Miller (1896) 
not only introduced the subject but set the stage for continuing 
interest in these unusual integumentary features. Quay (1952, 1968) 
and Jannett (1975) both have added substantially to the subject. 

Histologically, the best description of integumentary glands at 
the light level may be found in Quay (1968). Using M. oeconomus 
as an example, Quay reported as follows. In comparison with the 
sebaceous glands of typical hair follicles, the individual sebaceous 
gland units of the hypertrophied integumentary glands are greatly 
increased in size and cell count and are branched and multi-lobed. 
The epidermis that overlies the gland is thickened irregularly, es- 
pecially in the center of the glandular area. Hair follicles and hair 
growth itself seem to be reduced or distorted. In association with 
this finding, the arrector pili muscles within the area of a typical 
gland either are absent or, at least, difficult to find. The gland ducts 


196 Phillips 


within the central area of the gland frequently become cystic and 
contain keratin that has been sloughed off from the surface as well 
as cellular debris. Lastly, lipid droplets detected through staining 
with Sudan Black B (without acetone extraction) tend to increase 
in both number and size from the periphery of the gland toward 
the center. 

Many questions remain unanswered even though previous stud- 
ies of integumentary glands have provided a sound foundation. 
Biochemiocal analysis of secretory product would provide one set 
of data crucial to additional interpretation of the functional role of 
the glands. Detailed study of the ontogeny of the glands as well as 
comparisons between typical hair follicle glands and hypertrophied 
glands might also be valuable. For example, it would be interesting 
to know whether or not the sebaceous secretory cells undergo changes 
when stimulated by testosterone. Either M. longicaudus or M. penn- 
sylvanicus would be valuable as a model for such research. 


Dentition 


Microtus is characterized by having both evergrowing incisors 
and molars. Although the microanatomy of the incisors has not been 
investigated specifically, the complex molars have been the subjects 
of histological, histochemical, autoradiographic, and genetic studies 
(Gill and Bolles, 1982; Koenigswald and Golenishev, 1979; Ox- 
berry, 1975; Phillips and Oxberry, 1972). The evolutionary history 
of the molars in Microtus is fairly well documented in the fossil 
record (see Carleton, this volume; Zakrzewski, this volume); indeed, 
microtine dentition in general has been used as an index for both 
Eurasian and North American Pleistocene deposits (Hibbard, 1959; 
Kowalski, 1966). 

The crowns of Microtus molars consist of a series of salient and 
re-entrant angles that result in an extremely complex, nearly flat, 
grinding surface (Fig. 6). The occlusal pattern, extreme crown height 
(hypsodonty), cementoid buttressing, and continuous growth that 
characterize the molars, all have been associated with an evolution- 
ary shift to an abrasive diet (Guthrie, 1965, 1971; Phillips and 
Oxberry, 1972; White, 1959). According to Zimmerman (1965), 
even interspecific differences in degree of occlusal complexity can 
be correlated with relative percentage of grasses in the diets of M. 
pennsylvanicus and M. ochrogaster. 


Microanatomy 197 


Fic. 6. Diagrammatic representation of an evergrowing molar; transverse sec- 
tions A, B, and C on right correspond to dotted section lines on the molar shown at 
left. The overview shows the relationship between molars and periodontal ligaments 
(pl), gingivum (g), and alveolar bone (ab). Section A: intra-oral “crown.” Abbrevi- 
ations are: ac, thin layer of acellular cement; e, mature enamel; d, mature dentin; cc, 
cellular cement (major point of attachment); rd, reparative dentin; cb, cementoid 
buttress. Section B: middle, mature segment of the molar that serves as a “root.” 
Abbreviation: p, pulp. Inset shows histological features of enclosed area, including 
periodontal ligaments (pl), fibroblasts (1), pulpal blood vessels (2), odontoblasts (3), 
and cementoblasts (4) on mature enamel (e). Section C: formative apical end of 
“rooted” portion. Abbreviations are: ie, immature enamel; id, immature dentin; ip, 
immature pulp; c, cementoblasts; iee, inner enamel epithelium; oee, outer enamel 
epithelium. Inset shows histological details of enamel epithelium, including amelo- 
blasts (1), stratum intermedium (2), stellate reticulum (3), and outer enamel epithe- 
lium. 


Microanatomical analyses of evergrowing molars have proven 
useful in elucidating structural features and in formulating a the- 
oretical concept of evolutionary mechanisms involved with their 
origin (Phillips and Oxberry, 1972). The major difference between 
evergrowing molars and typical rooted molars is that crown for- 
mation is continuous in the former. Essentially, therefore, the mo- 


198 Phillips 


lars in Microtus are examples of a morphogenetic system in which 
the developmental process never ceases (although the rate may 
change). Histologically, the “rooted” portion of the molar crown 
concurrently resembles the proliferation, morphodifferentiation, 
histodifferentiation, and apposition “‘stages” (Fig. 6) found sequen- 
tially in development of typical rooted teeth (Bhaskar, 1976; Phil- 
lips and Oxberry, 1972). 

Two of the key questions in the evolution of evergrowing molars 
are: 1) how can a continuously growing crown be held in place; 
and 2) why is it that attrition from abrasion and thegosis (tooth to 
tooth contact) does not eventually expose the pulpal chamber? 

The first question was investigated in detail by Oxberry (1975), 
who demonstrated variability in the morphology of the coronal sur- 
faces of the molars. He pointed out that each molar had “major 
points of attachment” where enamel was lacking and “‘minor points 
of attachment” where enamel was present. In the former, the pri- 
mary dentin is covered by a thick layer of cellular cement that in 
turn is connected to adjacent alveolar bone by dense periodontal 
ligaments having an extensive indifferent fiber plexus (Figs. 6, 7). 
In the latter, the mature enamel is covered by a thin layer of acel- 
lular cementum that is deposited shortly before eruption (Phillips 
and Oxberry, 1972) and which allows for attachment of principal 
fiber bundles of the periodontal ligaments (Fig. 7). 

In addition to special attachment points, the evergrowing molars 
also are “buttressed” by cellular cement that “grows” within their 
interstices. This cement has not yet been analyzed histochemically, 
but its decalcified histological appearance differs from that of typical 
cellular cement by having dense arrays of collagenous fibers (Figs. 
7, 8). One implication of an obvious fibrous appearance under such 
circumstances is that the ground substance is sparse. The fact that 


~ 


Fic. 7. Top: transverse section through rooted portion of an upper molar. Note 
the cellular cement (CC) serving as a major point of attachment in an area of the 
tooth lacking enamel (E). Other abbreviations are: D, dentin; P, pulp; PL, perio- 
dontium; AC, thin, acellular cement covering enamel; CB, cementoid buttress. En- 
closed area is shown at higher magnification below. Nomarski interference-contrast 
optics; scale bar = 30 wm. Bottom: a major point of attachment showing cellular 
cement (CC) over dentin (D). Note how periodontal ligaments are invested into the 
cementum (arrows). Nomarski interference-contrast optics; scale bar = 11 um. 


Microanatomy 199 


200 —~Phillips 


Fic. 8. Top: Nomarski interference-contrast optics view of cellular cementoid 
buttress (CB) invested by collagen fibers (arrows) of periodontium. Scale bar = 11 


Mucroanatomy 201 


the buttresses “grow” from a basal zone where cementoblasts pro- 
liferate and become incorporated within the cementum also is unique 
(Oxberry, 1975; Phillips and Oxberry, 1972). Typically, cementum 
(both cellular and acellular) is deposited as a layer on freshly min- 
eralized surfaces (either dentin or enamel) rather than as a perio- 
dontal deposit having directional growth (see Bhaskar, 1976). ‘Tri- 
tiated glycine has been used to monitor incorporation of an amino 
acid and thus demonstrate the growth zone of the cementoid but- 
tresses (Oxberry, 1975). Within 15 min after injection, Oxberry 
(1975) found reduced silver grains at the base of the buttresses and 
after 2 h he found the glycine within newly formed cement. ‘he 
porous structure of the cementoid buttresses results in the absorp- 
tion of saliva, oral microflora, and food debris, which give the intra- 
oral coronal surfaces of Microtus molars their characteristicially 
dark-stained appearance. 

As the occlusal surfaces of molars are worn away, dentinal tu- 
bules become exposed to the oral cavity, fill with debris (Fig. 8), 
and the associated odontoblasts either die or, at least, have impaired 
function. Exposure of the cytoplasmic processes of the odontoblasts 
might be one mechanism that triggers a repair response. Although 
attrition is difficult to measure, tetracycline-stained molars in two 
Old World species (M. fortis and M. mandarinus) have been shown 
to erupt at between 0.5 and 0.7 mm per week (Koenigswald and 
Golenishev, 1979). The extreme attrition of evergrowing molars 
might be expected to also expose the soft dental pulp but does not 
because of production of reparative (irregular) dentin (Fig. 8) that 
plugs the coronal pulpal chamber (Oxberry, 1975; Phillips and 
Oxberry, 1972). Oxberry (1975) demonstrated incorporation of tri- 
tiated glycine into newly formed reparative dentin at 1 h after 
injection, thus suggesting that the process of formation of reparative 
dentin is fairly rapid. Whether or not the reparative dentin is elab- 
orated solely by odontoblasts is as yet unknown, but possibly other 
pulpal cells (such as fibroblasts) also are involved. 

In summary, microanatomical analysis of the molars in Microtus 


pase 
um. Bottom left: debris-filled dentinal tubules (arrows) exposed to the oral cavity 
because of attrition of the occlusal surface of a molar. Nomarski interference-contrast 
optics; scale bar = 29 ym. Bottom right: primary dentin (D) and adjacent irregular, 
reparative dentin (RD). Nomarski interference-contrast optics; scale bar = 29 um. 


202 Phillips 


has enabled development of a model for understanding the evolution 
of evergrowing molars in rodents. 


Salivary Glands 


Among the variety of major and minor salivary glands in Micro- 
tus, microanatomical data presently are available for the parotid 
and submandibular glands, which are only two of the three major 
glands located outside of the oral cavity. None of the numerous 
minor salivary glands, located within the lining of the oral cavity 
and within the tongue, has been studied. No histochemical data 
presently are available for any microtine salivary glands so knowl- 
edge of the chemical composition of the secretory products can be 
inferred only by comparison of structural features and histological 
staining reactions to comparable features in salivary glands of lab- 
oratory rodents on which more detailed sudies have been under- 
taken. Presumably, salivary glands have the same roles in Microtus 
as in other mammals and, therefore, they most certainly not only 
secrete digestive enzymes but probably also secrete IgA, hormones, 
and lubricating mucoid substances (Dawes, 1978; Hand, 1976; 
Phillips et al., 1977). It also is likely that salivary glands in rodents 
have some additional, presently unknown, biological roles. For ex- 
ample, sexual dimorphism in the morphology of secretory portions 
of the submandibular intralobular duct system has been reported 
in both Mus and Rattus (Junqueira et al., 1949; Srinivasan and 
Chang, 1975). Sexual differences in mucins have been described in 
the hamster, Mesocricetus (Shackleford and Klapper, 1962), and 
sexual differences in rates of enyzme biosynthesis have been dem- 
onstrated in Mus (Calissano and Angeletti, 1968). 

Limited dynamic interpretations of static ultrastructural images 
of Microtus salivary glands can be developed because the secretory 
process and general physiology of salivary glands have been inves- 
tigated in considerable detail in recent years (for a summary, see 
Tandler, 1978). For example, pulse-chase experiments, often using 
tritiated leucine, have been employed to develop an understanding 
of serous secretory cells. It has been demonstrated that protein syn- 
thesized in the cisternae of the granular endoplasmic reticulum 
(GER) is assembled into immature product at the Golgi complex 
following energy-requiring transfer from the GER (Bogart, 1977; 
Castle et al., 1972; Palade, 1975). Although details of secretory cell 


Muicroanatomy 203 


BAN \ i rs 
ne ( 


Za, 
OE vi ats Sasi ae treet? 
Sz 


Sy. 
Cade “00 | 


P ve) 


ff 
oy) @ yy, alge 
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Fic. 9. Diagrammatic representation of parotid (A) and submandibular (B) sal- 
ivary glands. Abbreviations are: ac, acinar cells; icd, intercalated duct; gd, granular 
duct; sd, striated duct. 


membrane synthesis and membrane recycling processes have re- 
mained somewhat elusive, it is known that membrane enclosing 
secretory granules arises de novo concomitantly with the product 
and differs biochemically from other membrane (Amsterdam et al., 
1971). Secretory granules are exported in an orderly, chronological 
fashion; the granule membrane fuses to the outer cell membrane 
just prior to release of secretory product into the adjacent lumen 
(Satir, 1974; Tandler and Poulsen, 1976). Excess membrane sub- 
sequently is resorbed in the secretory cell (Amsterdam et al., 1971). 

The small parotid salivary gland in Microtus is positioned at the 
base of the ear. It consists of bulbous serous secretory acini, short 
secretory intercalated ducts, and non-secretory intralobular (striat- 
ed) ducts (Fig. 9). The pyramidal serous cells are characterized by 


Phillips 


204 


Microanatomy 205 


large, spherical euchromatic nuclei cradled by abundant lamellar 
granular endoplasmic reticulum (GER). The basal plasma mem- 
brane is relatively smooth, whereas the basal one-half of the lateral 
membrane typically is slightly interdigitated with that of adjacent 
secretory cells (Fig. 10). Nerve terminals are associated with these 
membrane surfaces, being positioned in shallow indentations on the 
basal surface as well as wedged between adjacent cells (Fig. 11). 
The apical one-half of the lateral membranes of the serous cells 
include intercellular canaliculi and, immediately adjacent to the 
lumen, a zona adherens. The apical membrane, when secretory 
product is released, is irregular and has short microvilli (Fig. 10). 

The serous-cell Golgi complexes are prominent cytoplasmic fea- 
tures; at the inner face of the flat lamellar structures are found 
coated vesicles and immature secretory granules containing mod- 
erately electron dense material (Fig. 10). 

The intercalated ducts in parotid salivary glands of Muicrotus 
apparently are secretory. Although the product has not been chem- 
ically categorized, its appearance in the TEM differs significantly 
from the appearance of the serous granules; intercalated duct cell 
secretory product is only moderately electron dense and the images 
suggest that individual granules can coalesce into larger, irregularly 
shaped granules. Although the coalesced images might be artifac- 
tual, they nevertheless are not found in serous cells processed in the 
same way and therefore can be taken as indicative of some physi- 
ochemical difference between secretory granules. Additionally, the 
intercalated duct cells are characterized by elongate euchromatic 
nuclei, have very little GER relative to that found in the serous 
cells, and the Golgi complexes are inconspicuous (Fig. 11). Secre- 
tory intercalated ducts also have been reported in the hamster par- 
otid (Shackleford and Schneyer, 1964); however, in this species the 
product is said to be extremely electron dense. 

The intralobular (striated) parotid ducts in Microtus are non- 


—_— 


Fic. 10. Top: secretory acinar cell from the parotid salivary gland. Note the 
extensive Golgi complex (G), associated condensing vesicles (cv), and mature secre- 
tory granules (sg). Other abbreviations are: L, lumen; N, nucleus; ger, granular 
endoplasmic reticulum. Scale bar = 1 wm. Bottom: higher magnification of lumen 
(L), secretory granules (sg), and apical and apico-lateral cell surfaces. Note apical 
microvilli (mv) and adjacent cell junctions (arrows). Scale bar = 0.25 um. 


206 Phillips 


Fic. 11. Top: innervation (N) of a serous secretory cell (basal margin) of the 
parotid salivary gland. Abbreviations are: GER, granular endoplasmic reticulum; 


Muicroanatomy 207 


secretory, at least to judge from their histological and ultrastructural 
appearance. At least two ultrastructurally distinctive cell types are 
found in these ducts; each might represent different functional states 
of the other. The most prominent image is one of a large columnar 
cell with a spherical, centrally placed euchromatic nucleus. With 
the trialdehyde fixative and processing techniques used by me, these 
cells have an extremely pale cytoplasm. Indeed, the cytoplasm is so 
pale that cytoskeletal features such as microtubules and fibrils that 
ordinarily are difficult to discern among other cytoplasmic constit- 
uents, are seen easily and their relationships to organelles are ap- 
parent (Fig. 12). The basal cytoplasm of these pale cells contains 
large mitochondrial profiles and the basal plasma membrane in- 
vaginates deeply into the cell (Fig. 12). The second cellular profile 
is one in which the cells appear to be a somewhat condensed version 
of the pale cells, differing from the latter in being smaller, typically 
wedged between pale cells, and in having a darker cytoplasm and 
an irregularly shaped nucleus. The luminal membranes of both cell 
types are characterized by irregular, pleiomorphic microvilli (Fig. 
12), and neither contains secretory product, although in both the 
apical cytoplasm does contain a variety of pale vesicles (Fig. 12). 
The submandibular salivary gland in Microtus is much larger 
than the parotid, more complex in structure, and apparently more 
complex in function as well. The submandibular has large, bulbous 
acini containing mucous secretory cells (Fig. 9). These mucous cells, 
which are a large and prominent feature of the gland, are charac- 
terized by pale coalescing secretory granules containing flocculent 
material (Fig. 13). The nuclei tend toward being heterochromatic, 
are basally positioned, and are irregular or flattened in appearance. 
The peripheral cytoplasm of the mucous cells is filled with lamellar 
GER and has a dark, condensed appearance. Coated and smooth 
vesicles, which are a common feature of serous cells, essentially are 
lacking in the mucous cells. ‘The Golgi complexes are prominent. 
The cell outer plasma membrane generally is smooth except at the 
luminal surface, where a few small microvilli typically are found. 


—_— 

M, mitochondrion; CG, intercellular collagen; BL, basal lamina. Scale bar = 0.12 um. 
Bottom: secretory intercalated duct adjacent to acinus (lower right). Abbreviations 
are: sg, secretory granules; G, Golgi; L, lumen; N, nerve terminal. Scale bar = 1 um. 


208 ~—~Phillips 


Microanatomy 209 


The short intercalated duct is of special interest because it consists 
of low, cuboidal cells that typically are packed with electron dense 
secretory granules (Fig. 13). These granules differ from typical 
serous granules in that they have an irregular rather than spherical 
shape. The intercalated duct cells have ovoid, basally restricted nu- 
clei containing moderate amounts of heterochromatin. The GER, 
Golgi complexes, and mitochondria in the intercalated duct cells 
are sparse but apparently scaled to the overall small size of the cell 
(Fig. 13). The granular intralobular duct system in the subman- 
dibular is secretory in Microtus as it is in most other rodents (Fig. 
9). The ultrastructure of the granular duct cells somewhat resem- 
bles that seen in the intercalated duct cells of the parotid salivary 
gland of Microtus. The cytoplasm is packed densely with round or 
ovoid secretory granules, many of which are coalesced into larger, 
more irregularly shaped granules (Figs. 13, 14). One or more large 
Golgi complexes are in a supranuclear location; the ovoid nucleus 
itself is not restricted to the basal ergastoplasm, is euchromatic, and 
is cradled in extensive lamellar GER. The basal and apical cell 
membranes are unspecialized; the basal membrane is relatively 
smooth, whereas the apical membrane, which borders on the lumen 
of the duct, generally is smooth with only a few microvilli (Fig. 
14). The lateral membranes are characterized by a prominent gap 
junction (Fig. 14). The chemical composition of the secretory prod- 
uct produced in the granular duct is unknown. The ultrastructure 
of the cells, however, might be categorized as sero-mucoid (Shackle- 
ford and Wilborn, 1968) because the granules are pale and appear 
to coalesce, whereas the organellar arrangement and morphology 
are more nearly similar to that associated with serous secretory cells. 

The intralobular striated ducts, to which the granular ducts lead 
(Fig. 9), are characterized by large, pale cells having spherical, 
centrally placed euchromatic nuclei (Fig. 15). Unlike the homolo- 
gous cells of the parotid, the striated duct cells in the submandibular 


—_ 


Fic. 12. Top: basal portion of parotid striated duct cell showing infolded basal 
membrane (arrows), associated mitochondrial profiles (M), and characteristically 
euchromatic nucleus (N). Scale bar = 1 wm. Bottom: apical surface of striated duct 
cell. Note microvilli (MV) and collection of vesicles (V) in adjacent cytoplasm. Other 
abbreviations are: L, lumen; M, mitochondrial profile; mt, microtubule; arrows, 
cytoskeletal fibrils. Scale bar = 0.25 ym. 


210 Phillips 


Microanatomy 211 


salivary gland frequently have accumulations of electron-dense 
granules in a cytoplasmic zone immediately adjacent to the lumen 
(Fig. 15). These granules possibly suggest that the striated duct 
cells in the submandibular are secretory; however, the ultrastruc- 
tural data in themselves are not unequivocal and, therefore, it also 
is possible that the granules are associated with an absorptive func- 
tion of these cells (Rhodin, 1974). 

The parotid salivary gland in mammals generally is more con- 
servative in structure than is the submandibular (Phillips et al., 
1977). This principle is underscored by Muicrotus, in which the 
parotid is similar to that found in Rattus, Mus, and other species, 
whereas the submandibular appears to be considerably different 
from that of other rodents for which data are available. Serous 
acinar cells such as those found in Microtus appear to be typical of 
rodent parotid glands (Hand, 1976; Shackleford and Schneyer, 
1964). Comparisons among rodents are hampered somewhat by 
differences in fixation technique. In the early (1950-1960) TEM 
literature on rodent salivary glands, most micrographs were of ma- 
terial fixed with osmium tetroxide and the secretory granules had 
a pale appearance. The more recent aldehyde fixation techniques 
preserve cellular proteins and glycoproteins to a different extent 
and typically the granules appear as illustrated for Microtus (Fig. 
10). The extreme electron density of the serous secretory granules 
in aldehyde-fixed tissue samples thus is indicative of the highly 
proteinaceous nature of the parotid acinar product. 

Pulse-chase radioautographic analyses have demonstrated that 
synthesis and assembly of product of acinar serous cells in rabbits 
are similar to that found in the zymogen-producing pancreatic cells, 
with the exception that the process is slower in the parotid cells 
(Castle et al., 1972). In the absence of data for Microtus and other 
rodents, it only can be inferred that their parotid serous cells are 
similar functionally to those of rabbits. 

The submandibular salivary gland in rodents has attracted far 


— 


Fic. 13. Top: survey view of three types of secretory cells found in submandib- 
ular salivary gland. Compare the secretory product of the sero-mucous acinar cells 
(sg1), the small intercalated duct cells (sg2), and the granular duct (sg3). Other 
abbrevations are: L, lumen; G, Golgi complex; cv, condensing vesicle. Scale bar = 1 
um. Bottom: higher magnification of intercalated duct cells. Scale bar = 0.5 um. 


212 ~——~Phillips 


Fic. 14. Cross-section through a granular duct of submandibular salivary gland. 
Note unusual zones of occluded cell junction (arrows) positioned on lateral cell 
surfaces. Abbreviations are: sg, secretory granule; G, Golgi complex; cv, condensing 
vesicle. Scale bar = 0.5 um. 


Microanatomy 213 


more attention than has the parotid. In large measure this is due 
to: 1) its size and location, which make it convenient for develop- 
mental studies (for example, see Spooner, 1973); 2) its tendency in 
rodents to be sexually dimorphic (for example, see Srinivasan and 
Chang, 1975); and 3) its well-known capacity to produce a variety 
of compounds, including nerve growth factor (NGF), epidermal 
growth factor (EGF), renin, and kallikrein, which one would not 
expect to find in saliva (Hand, 1976; Murphy et al., 1980). 

The acinar secretory cells of the submandibular in Microtus are 
similar, ultrastructurally, to those of all other rodents for which 
comparative data are available. Such secretory cells are described 
as mucous or, occasionally, seromucous, depending upon selection 
of ultrastructural criteria and fixative (Hand, 1976; Shackleford 
and Wilborn, 1968; Simson et al., 1978; Tamarin and Sreebny, 
1965). Given the ultrastructural characteristics of these cells, it is 
not surprising that the acinar cell product differs from that secreted 
by the parotid in a number of ways, including having a lower level 
of amylase (Shackleford and Schneyer, 1964). Functional differ- 
ences between parotid and submandibular acinar cells were dem- 
onstrated by Bogart (1977), who used tritiated leucine to investigate 
intracellular kinetics in Rattus. The major kinetic difference was in 
the greater time spent by the developing product in the vicinity of 
the Golgi complex (Bogart, 1977), which probably is reflective of 
the “mucoid” nature of the secretory product. A number of cyto- 
chemical studies have provided data that demonstrate that sugar 
moieties and sulfate can be incorporated into secretory cells and 
added to a protein secretologue directly at the Golgi complex (Berg 
and Austin, 1976; Bogart, 1977). 

The secretory intercalated duct and granular duct are the most 
notable features of the submandibular salivary gland in Microtus. 
At sexual maturity in all studied species of rodents, except ground 
squirrels (Spermophilus), a segment of intralobular duct positioned 
between the intercalated duct and the typical “striated” duct under- 
goes a specialized differentiation and develops into a “granular” 
duct that secretes a complex product (Hand, 1976; Shackleford and 
Schneyer, 1964; Srinivasan and Chang, 1975). Androgenic hor- 
mones influence development of the granular duct, which generally 
is much larger in males than it is in females (Calissano and An- 
geletti, 1968; Hand, 1976; Junqueira et al., 1949). Recent histo- 
chemical investigations have established that nerve growth factor 
(NGF) and epithelial growth factor (EGF) are two of the secretory 


Phillips 


214 


t* 
ie 
a 


are 


ee 
oO 
a 
az 


Microanatomy 215 


products of these granular ducts (Murphy et al., 1980). Unlike the 
submandibular acinar secretory product, export of growth factors 
is not triggered by cholinergic secretagogues. Indeed, both alpha 
and beta adrenergic agents stimulate the release of NGF and EGF 
into the ductal lumen (Wallace and Partlow, 1976). Because the 
granular duct serves as an exocrine rather than an endocrine organ 
(Byyny et al., 1974), one significant question is: how do the growth 
factors reach the blood? One plausible answer is that the salivary 
growth factors are swallowed and absorbed in the gastrointestinal 
tract (Murphy et al., 1980). A second question, which is directly 
applicable to Microtus, is: what are the functions of such growth 
factors in adult animals? Although essentially all of the research so 
far has been done with Mus as the experimental animal, it is not 
unreasonable to assume that the granular duct in Microtus also 
secretes NGF or EGF or both. One hypothesis, applicable at least 
to EGF, is that the capacity to produce considerable quantities of 
this protein is somehow linked to evergrowing teeth. Previous stud- 
ies have demonstrated that EGF promotes early eye-opening in 
young mice (Mus) when given orally (Taylor et al., 1972) and, 
furthermore, stimulates eruption of incisors (Hand, 1976). Al- 
though for now we can only speculate, it seems clear that future 
investigations of the relationships among EGF, salivary glands, and 
growth could cast light on the basic mechanisms that allowed for 
evolution of evergrowing teeth. 

The apparent microanatomical and ultrastructural differences 
between the submandibular of Microtus and those of other studied 
rodents is of special interest. Microtus is the only rodent genus 
(among those studied) in which a secretory intercalated duct is 
interposed between the acinus and granular duct; in other rodents 
the intercalated duct consists of non-secretory, low cuboidal cells. 


ne 

Fic. 15. Striated duct of submandibular salivary gland. Compare with Fig. 12 
and note differences in apical surfaces (a). In submandibular striated duct cells, 
apical microvilli and cytoplasmic vesicles are lacking; instead, the apical surface is 
smooth and the apical cytoplasm contains small, electron-dense bodies (arrows). Also 
notice the fixed formative saliva within the lumen. Abbreviations are: m, mitochon- 
drial profile; cv, coated vesicles; ger, granular endoplasmic reticulum. Scale bar = 1 
um. 


216 —~Phillips 


~~ — 


Fic. 16. Diagrammatic view of locations in the digestive tract of M. pennsylvan- 
icus from which tissues were taken for EM analysis: A, esophagus; B, cardiac ves- 
tibule; C, non-glandular forestomach; D, glandular stomach; E, junction of pylorus 
and duodenum; F, small intestine. 


Additionally, the ultrastructure and secretory product of aldehyde- 
fixed submandibular intercalated duct cells in Microtus (Fig. 13) 
are similar to granular duct cells in Mus (see Murphy et al., 1980). 
On the other hand, the granular duct cells in the Microtus sub- 
mandibular are similar in appearance to the intercalated duct cells 
in Microtus parotid salivary glands (Figs. 11, 14). Taken together, 
all of these ultrastructural differences demonstrate the well-known 
evolutionary plasticity of salivary glands (Phillips et al., 1977). 
Unfortunately, however, such structural and organizational differ- 
ences in themselves tell us relatively little about similarities and 
differences in secretory product. 

The possibility that heterochrony has occurred is yet another 


Microanatomy Ziv, 


aspect that deserves consideration when making comparisons be- 
tween the submandibular of Microtus and that of other studied 
rodents. In the developmental dynamics of the submandibular sal- 
ivary gland in Rattus, the morphology and secretory products of 
several different cell “types” undergo significant transitions before 
reaching a final, presumably fully differentiated and stable config- 
uration (Chang, 1974; Srinivasan and Chang, 1975). There is some 
evidence that in neonate rats the formative intercalated duct cells 
(whose morphology is generalized) serve as a “‘stem”’ cell population 
from which “striated” and possibly even acinar cells can develop 
(Chang, 1974). Furthermore, Chang (1974) also found that no 
fewer than three different cell types (acinar, proacinar, and termi- 
nal tubule), each with its own morphology and histochemically 
distinctive product, participate chronologically in a differentiation 
pattern that results in the single type of mucous acinar cell char- 
acteristic of the submandibular of adult rats. Such developmental 
data certainly provide the theoretical basis for explaining the strik- 
ing organizational differences between Muicrotus, Rattus, Mus, and 
other rodents. If morphological differentiation were to stop pre- 
maturely in any of the progenitor cell types, the “mature” gland 
would appear to have two rather than one secretory cell type in the 
terminal acinar-intercalated duct zone in the gland. Such is the case 
in Microtus, and the presence of an “extra” type of secretory cell 
that appears to be a part of the intercalated duct thus may be a 
result of a heterochronic alteration in developmental sequence. 


Digestive Tract 


The microanatomy of the digestive tract has been examined his- 
tologically in a surprising variety of wild rodents including Microtus 
and several other microtine genera. I review the available infor- 
mation in the following paragraphs and describe and illustrate many 
ultrastructural features of the digestive tract of M. pennsylvanicus 
for the first time. The locations from which tissues were obtained 
for TEM analysis are shown diagrammatically in Fig. 16. 

An understanding of diet and nutritional requirements is a key 
component in interpretation of microanatomical features of the 
digestive tract. Because of the broad interest in ecology, energetics, 
and population dynamics of Microtus, considerable ancillary data 
are available on feeding habits. Although more detailed information 


218 Phillips 


relative to nutritional requirements can be found elsewhere (Batzli, 
this volume), several aspects bear repeating here. 

All species of Microtus can be categorized as herbivores; for ex- 
ample, in M. ochrogaster, more than 90% of the diet by volume is 
herbaceous (Zimmerman, 1965). Given the variability in digest- 
ibility of grasses and seeds (Batzli and Cole, 1979), the efficiency 
of the digestive system in Microtus is remarkable; in a 46-g M. 
pennsylvanicus with a daily intake of 28.1 g, the total fecal weight 
was 2.8 g, giving an efficiency of 90% (Golley, 1960). Actual com- 
position of the average diet of individual species varies considerably, 
however, in accordance with habitat and geography. Additionally, 
different species of Microtus have significantly different nutritional 
requirements. Batzli and Cole (1979) found that prairie voles (M. 
ochrogaster) could digest grasses as well as could M. californicus, but 
when fed on a strict grass diet, the prairie vole lost weight and 
eventually died. These rather striking interspecific differences prob- 
ably are reflected also in the microanatomy of the digestive tract. 
Hints of such differences certainly are found in the histological 
studies of Dearden (1966, 1969) and Barry (1976). 


Esophagus 


The histology of the esophagus at the gastro-esophageal junction 
has been described and discussed by Dearden (1966). In Microtus 
the abdominal esophagus is characterized by a moderately keratin- 
ized, thin lamina mucosae that thickens appreciably at the junction 
of the cardiac vestibule (Dearden, 1966). The presence of keratin 
in the stratified squamous epithelium seems to be typical of rodents; 
generally it is thought that keratinization of the esophagus and 
cardiac stomach are correlated with a harsh type of diet (Forman, 
1972; Horner et al., 1964). Two ultrastructurally distinct types of 
basal cell are found in the stratum germinativum of the esophagus 
in Microtus; one cell type is characterized by a slightly irregular, 
largely euchromatic nucleus, whereas the other, which overall has 
a dark, condensed appearance, is characterized by an extremely 
irregular, largely heterochromatic nucleus. Hemi-desmosomes are 
common along the basal plasma membrane in both types of basal 
cell. Extracellular aggregations of glycogen granules appear to fill 
pouch-like pockets between adjacent basal cells. These granules 
apparently are incorporated into the basal cell cytoplasm prior to 
cellular migration into the stratum spinosum. The stratum spinos- 


Microanatomy PANS) 


um itself is very thin (only 2-3 cells deep) and gives way abruptly 
to a stratum granulosum. 

The esophageal epithelial cells undergo a profound transition 
between the basal layer and the luminal surface. Dense aggrega- 
tions of tonofilaments, degrading mitochondria, and clumps of gly- 
cogen granules become the most conspicuous features of the cyto- 
plasm (Fig. 17). Membrane-coating granules (multi-lamellar bodies) 
and keratohyalin granules are present but not particularly abun- 
dant in the esophageal epithelium (Fig. 17). The outer cell mem- 
brane in the superficial cells take on a thickened, electron-dense 
appearance that possibly results from deposition of material from 
the membrane-coating granules (Rhodin, 1974). A somewhat amor- 
phous, osmophilic material fills the intercellular spaces between 
adjacent squamous cells (Fig. 17). On occasion this material ap- 
pears to be organized into a fibrillar formation that extends from 
the outer surface of one cell to the outer surface of another (Fig. 
17). Although keratin filaments are found in the esophageal epi- 
thelium in Microtus, this protein never attains abundance adequate 
for formation of a true stratum corneum. Consequently, although 
keratohyalin granules and clumps of glycogen disappear, the out- 
ermost layers of cells (7-10 deep) never become electron dense and 
the cytoplasm clearly contains bundles of tonofilaments (Fig. 17). 
It is of additional interest that the outermost cells appear to retain 
enough cell-to-cell adherence so that the layers are not disrupted 
by fixation-preparation techniques and thus a stratum disjunctium 
is lacking in the esophagus (Fig. 17). 

The esophageal lamina propria in Microtus (and other micro- 
tines) has been described histologically as a “narrow zone of rather 
loose connective tissue containing numerous elastic fibers” (Dear- 
den, 1966). One particularly interesting feature of the lamina pro- 
pria in Microtus is the presence of interlacing ligament-like bundles 
of collagen that underly the basal lamina of the stratum germina- 
tivum (Fig. 18). Such esophageal structures apparently have not 
been described previously in mammals. In 1-wm “thick” sections 
cut in a plane oblique to the epithelium, the ligament-like bundles 
are clearly visible because they stain intensely with toluidine blue. 
Ultrastructural analysis reveals that they consist of highly orga- 
nized, twisted bundles of collagen and reticulum (Fig. 18). The 
intense staining reaction cannot be attributed to these visible com- 
ponents alone because in typical loose connective tissue neither one 


220 —~Phillips 


Microanatomy fen 


normally stains so intensely. In addition to these ligament-like fiber 
bundles, the connective tissue of the lamina propria also contains 
fibroblasts, macrophages, and elastic fibers. Mucus-secreting esoph- 
ageal glands, which have been reported in the lamina propria of a 
variety of mammalian species (Rhodin, 1974), are lacking in M:- 
crotus (Dearden, 1966). 

The esophageal musculature is of particular interest in Microtus. 
Three layers of muscles—an inner-striated circular, outer-striated 
longitudinal, and a smooth circular layer—compose the lamina 
muscularis externa and lamina muscularis mucosae (Fig. 18). In 
Microtus the outer-striated muscle layer extends from the esophagus 
to the stomach, terminating in the corpopyloric fold (Dearden, 1966). 
In two other microtines, the collared lemming (Dicrostonyx groen- 
landicus) and the steppe vole (Lagurus lagurus), it is the inner- 
striated layer that has continuity with the corpopyloric fold (Dear- 
den, 1966). The overall anatomical design of the gastro-esophageal 
junction in Microtus and other microtines suggested to Dearden 
(1966) that a variety of cardiac valves or sphincters are found in 
mammals. The exact relationship of such valve-like structures in 
Microtus to feeding habits is as yet unclear but should be a focal 
point for future work. 


Stomach 


Histologically, the stomach of Microtus consists of three distinc- 
tive zones (Fig. 16): one, the forestomach, is characterized by non- 
glandular keratinized squamous epithelium; the second is an area 
of glandular mucosa; and the third, the pylorus, also is non-glan- 
dular and is lined with keratinized squamous epithelium (Dearden, 
1969; Golley, 1960). Non-glandular gastric mucosa is typical of 
rodent stomachs but varies considerably in extent among different 
species (Ito, 1967). The presence of non-glandular epithelium ap- 
parently is correlated with diets that include large quantities of food 


a 

Fic. 17. Top: top five layers of epithelial cells lining the esophagus. Note keratin 
filaments (kf) and intercellular layers (arrows); L, esophageal lumen. Scale bar = 
0.12 um. Bottom: Cells in an early stage of the keratinization process. Note degen- 
erating mitochondria (M), glycogen (g), and abundant tonofilaments (tf). Scale = 
0.25 um. 


222 ~—~Phillips 


14 


7 


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righ, LF ote ry 
bid TPLPESS ee) Po 
ERO ET ag 


TPS 
AEG 


Muicroanatomy 223 


having low nutritional value (Ito, 1967). Probably the most extreme 
example is in the grasshopper mouse, Onychomys, in which the 
bilocular stomach is almost totally lined with stratified squamous 
epithelium (Horner et al., 1964). Among studied microtines, the 
glandular-nonglandular ratio varies considerably; Lemmus has the 
most extensive glandular zone, whereas Dicrostonyx has the most 
extensive non-glandular zone (Dearden, 1969). In Muicrotus the 
glandular gastric mucosa is restricted to a narrow zone of the great- 
er curvature (Fig. 16), which is surrounded by keratinized epithe- 
lium and bordered by pediculated squamous flaps (Dearden, 1969). 

The ultrastructure of the non-glandular and glandular stomach 
in Microtus has not been described previously. The following de- 
scription is based on M. pennsylvanicus. 

Although the non-glandular gastric epithelium is relatively uni- 
form at the histological level and generally is described simply as 
“cornified” (Dearden, 1969; Golley, 1960), subtle differences are 
detectable at the ultrastructural level. Both the cardiac vestibule 
and remaining non-glandular stomach differ from the squamous 
epithelium of the esophagus at the gastro-esophageal junction. Un- 
like the esophagus, the stratified squamous epithelium of the stom- 
ach is heavily keratinized and thus characterized by both a stratum 
corneum and a stratum disjunctum (Fig. 19). A typical stratum 
spinosum is lacking in the non-glandular stomach (Fig. 19). In- 
stead, irregularly-shaped basal cells are overlaid by layers (5-7 cells 
deep) of flattened cells having elongate nuclei and abundant tono- 
filaments, keratohyalin granules, and membrane-coating granules. 
Also in the non-glandular stomach, lipid-like droplets accumulate 
in the intercellular spaces between the outermost cells of the stratum 
granulosum and dark inner cells of the stratum corneum. These 
droplets also are found between cells composing the stratum cor- 
neum (Fig. 19). Although these foregoing structural and organi- 
zational differences in esophageal and gastric epithelium are not 


— 


Fic. 18. Top left: light microscopic survey showing esophageal basal cell layer 
(bc) and ligament-like fibers (arrows) attached at base of the epithelium. Boxed area 
is similar to that shown in TEM view at top right. Scale bar = 13 um. Top right: 
braided collagen ligament found in lamina propria of esophagus. Scale bar = 0.25 
um. Bottom: skeletal muscle of esophagus, with prominent Z and M bands. Other 
abbreviations are: g, glycogen; m, mitochondrial profiles. Scale bar = 0.25 wm. 


224 Phillips 


obvious except with the transmission electron microscope, they 
nevertheless are not particularly surprising. The stratified squa- 
mous epithelium of this portion of a digestive tract appears rela- 
tively uniform (except in thickness) at the light microscopic level, 
and one easily can have the impression that the non-glandular stom- 
ach is a continuation of the esophagus. However, developmental 
and comparative studies have shown that the non-glandular gastric 
epithelium is derived from the same source as is the glandular 
mucosa and, therefore, is not a continuation of esophagus (Ito, 1967; 
Kammeraad, 1942). 

The cardiac vestibule differs from the non-glandular forestomach 
in that the epithelium clearly is closely associated with smooth mus- 
cle of the muscularis mucosa (Figs. 20, 21, 22). Epithelial basal 
cells of both the non-glandular forestomach and esophagus overlie 
loose connective tissue, whereas in the cardiac region these cells are 
only narrowly separated from the smooth muscle by densely packed 
collagen, elastic fibers, and fibroblasts (Fig. 20). These differences 
in the positional relationships between smooth muscle and stratified 
squamous epithelium probably are reflective of different functional 
roles. As pointed out by Dearden (1966), the thick smooth muscle 
layer associated with the gastro-esophageal junction is consistent 
with the idea that this zone is capable of serving as a valve. 


— 


Fic. 19. Top: survey view of cardiac vestibule epithelium of the stomach, show- 
ing outer, keratinized, stratum corneum (1), a granular layer (2) containing kera- 
tohyalin (kh), the basal layer (3), and stratum disjunctum (outermost thin layers at 
upper left). Scale bar =17 um. Bottom: TEM view of junction between stratum 
corneum and stratum granulosum. Note the densely packed keratin filaments (area 
within the rectangle), lipid-like intercellular material (arrow), and the keratohyalin 
granule (kh). Scale bar = 0.25 um. 


Fic. 20. Top: transition from basal cells (left) to granular cells (right) in the 
stomach. Note the dense accumulation of glycogen (g), small keratohyalin granules 
(kh), and tonofilaments (tf). Other abbreviations are: m, mitochondrial profile; d, 
desmosome; N, nucleus. Scale bar = 1 wm. Middle: subepithelial components of car- 
diac vestibule. Note unusual presence of a cilium (arrow) on a fibroblast. Scale bar = 
1 um. Bottom: hemi-desmosomes (arrows) on basal cells. Note the basal lamina (BL). 
Scale bar = 0.25 um. 


Fic. 21. Top: keratinization process in the non-glandular stomach, showing large 
keratohyalin granules (kh), glycogen (g), and masses of tonofilaments (tf). Scale bar = 
0.25 um. Bottom: high magnification view of a membrane coating granule (such as 
the one shown in the rectangle at top). Scale bar = 0.10 um. 


226 ~—~Phillips 


me 
M&S 


REN a4 
fe REN 


Microanatomy 227 


228 ~~ Phillips 


Microanatomy 229 


The forestomach in Microtus is of special interest because light 
microscopic analysis of 1-mm “thick” sections as well as TEM 
views, typically reveals rod-type bacteria within this area (Fig. 22). 
The fact that these bacteria nearly always (about 90%) are attached 
and oriented with their long axes perpendicular to the outermost 
layer of the stratum disjunctium suggests the existence of an asso- 
ciation with this portion of the stomach. Symbiotic microbial rela- 
tionships are relatively common in herbivorous mammals; generally 
such bacteria are involved in pregastric fermentation of otherwise 
undigestible plant polymers such as cellulose (for example, see Ito, 
1967). Davis and Golley (1963) earlier expressed doubts about 
microbial fermentation in Microtus because “the contents from the 
esophageal stomach are usually fresh and do not give any evidence 
that digestion or fermentation has taken place.” Although the oc- 
currence of rod-type bacteria in the forestomach of M. pennsylvan- 
icus does not in itself prove that microbial fermentation takes place, 
the microscopic data certainly are consistent with a symbiotic re- 
lationship and reflect the importance of future study. 

The glandular gastric mucosa in Microtus is similar histologically 
to that found in a variety of other rodents, including laboratory 
species as well as wild species for which data are available (Dear- 
den, 1969; Horner et al., 1964; Hummel et al., 1966; Ito, 1967). 
According to Dearden (1969) the gastric pits in Microtus are shal- 
low and the gastric glands consist of only parietal (=oxyntic) cells 
and chief (=peptic) cells. The gastric glands are relatively uniform 
in depth with chief cells being found in the basal portion and pa- 
rietal cells occupying the middle region and extending to just below 
the overlying epithelium (Dearden, 1969). Although parietal and 
chief cells are indeed a prominent feature of the gastric glands (Figs. 
23, 24), two other cell types—mucous neck cells and entero-endo- 
crine cells—also are found within the glands, albeit in smaller num- 


_ 


Fic. 22. Top left: survey view of keratinized epithelium of the forestomach. Note 
the “spiny” nature of the basal cells and presence of keratohyalin granules (kh), 
including some within a nucleus. Capillaries (cap) are found directly below the basal 
layer. Scale bar = 1 um. Top right: light microscopic view of the forestomach showing 
bacteria attached to the surface. Scale bar =17 um. Bottom: TEM view of two 
bacteria; area shown corresponds to area outlined in micrograph of top right. Scale 
bar = 0.25 um. 


Phillips 


230 


Microanatomy 231 


bers. Additionally, both light microscopic and ultrastructural views 
do not necessarily support the idea that chief cells are restricted to 
the basal portion of the gland (Fig. 23). 

Ultrastructurally, the chief cells in Microtus are characterized by 
large, round, basally positioned euchromatic nuclei, abundant GER, 
prominent Golgi complexes, and immature and mature stored se- 
cretory product (Fig. 24). Chief cells synthesize and export pepsin- 
ogen which is altered to pepsin in the presence of HCL produced 
by the parietal cells. The high protein content of the fully developed 
chief cell product is reflected by its electron dense appearance (Fig. 
24). Other granules, presumably immature product, also are a com- 
mon feature of chief cell cytoplasm. These immature granules are 
large and pale, contain clumps of electron-dense material, and often 
are found adjacent to the forming face of the Golgi. The appearance 
of the immature granules as well as their tendency to coaelesce (Fig. 
24) probably partly are due to the primary trialdehyde fixation 
followed by OsO, post-fixation used for the present investigation 
(Simson et al., 1978). 

The secretory function of parietal cells has been studied in con- 
siderable detail and, consequently, it is possible to estimate levels 
of activity as well as functional states of parietal cells from static 
TEM micrographs of the glandular gastric mucosa in Microtus 
(Black et al., 1980; Forte et al., 1977; Ito and Schofield, 1978; Ito 
et al., 1977; Schofield et al., 1979). In the animal illustrated (Fig. 
23), most of the visible parietal cells were actively secreting HCL 
as evidenced by the presence of extensive intracellular canaliculi. 
The canaliculi typically invade deeply into the parietal cell cyto- 
plasm and are easily recognizable by their irregular, loosely orga- 
nized microvilli and by their thick plasma membrane (Fig. 23). 
Abundant parietal cell mitochondrial profiles usually are restricted 
to a zone of cytoplasm immediately around the nucleus and to 
another zone peripheral to the canaliculi. Parietal cells in Microtus 
typically are situated among chief cells and mucous neck cells (Fig. 


= 

Fic. 23. Top left: light microscopic survey view of glandular stomach showing 
parietal cells (P) and chief cells (C). Area within the rectangle is similar to area 
show in TEM view at right. Scale bar = 17 wm. Top right: smooth muscle cell (s) 
adjacent to parietal cell. Note the intracellular canaliculi (ic) in the parietal cell. 
Scale bar = 1 wm. Bottom: Innervation of parietal cells (p). Scale bar = 0.5 wm. 


232 ~—-~Phillips 


Fic. 24. Top: TEM view of a mucous neck cell from the glandular gastric 
mucosa. Scale bar = 1 wm. Bottom: TEM survey of a typical chief cell. The pale 
granules presumably are immature; the electron-dense granules represent mature 
secretory product. Scale bar = 1 um. 


Microanatomy 233 


23). The basal surfaces of parietal cells are in contact with both 
smooth muscle cells and nerve terminals, although no specialized 
morphological interrelationship is obvious with the latter (Fig. 23). 
Inhibition and stimulation of HCL production are noteworthy as- 
pects of parietal cell physiology that have not been explored fully 
in rodents or in other mammals. However, EGF, which is produced 
by rodent submandibular salivary glands (see section on Salivary 
Glands), has been shown to inhibit acid secretion by affecting pa- 
rietal cell cytoskeleton (Gonzalez et al., 1981). Kusumoto et al. 
(1979) demonstrated that somatostatin-producing entero-endocrine 
cells (D cells) are found in juxtaposition with parietal cells in dog 
stomachs. Somatostatin is an inhibitory molecule that can block 
gastric acid secretion. In Microtus, and apparently other studied 
rodents as well, such entero-endocrine-cell and parietal-cell rela- 
tionships have not been found. Instead, only glucagon-producing A 
cells have been seen thus far in Microtus and, although these entero- 
endocrine cells are not common, the ones examined by me were 
located among both parietal and chief cells. Because glucagon also 
has been demonstrated experimentally to inhibit acid secretion while 
promoting glucose-6-phosphate dehydrogenase activity in the mu- 
cous neck cells in humans (Stachura et al., 1981), it seems possible 
that A cells have a dual role in Microtus. 

Mucous neck cells in Microtus are found interspersed among the 
parietal cells. Ultrastructurally they are characterized by accumu- 
lations of coalescing secretory granules that mostly contain moder- 
ately electron-dense material, although many granules also contain 
small amounts of electron-dense product (Fig. 24). The GER typ- 
ically is sparse; the nucleus is euchromatic and basally positioned. 
The large Golgi complexes are unusual in that they are positioned 
in peripheral cytoplasm and from a lateral perspective appear as 
layers of membrane-bound electron-dense material (Fig. 24). The 
surface mucous cells differ from the mucous neck cells in having a 
more electron-dense secretory product within the apical cytoplasm 
and in having short microvilli with sparse glycocalyx. 


Small Intestine 


The pylorus in Microtus is non-glandular, consisting instead of 
a muscular sphincter that Dearden (1969) thought would have an 
almost symmetrically circular action. The proximal portion of the 
duodenum is characterized by glands of Brunner, which are con- 


234 —~Phillips 


Fic. 25. Top: survey of junction between pylorus and duodenum. Note variety 
and abundance of secretory cells including goblet cells (g), mucus-producing cells of 
Brunner’s gland (B), and cells containing a dark-staining product (arrows). Scale 


Microanatomy 235) 


sidered as the source of protective alkaline mucins. In Microtus the 
typical secretory cells composing this glandular mass at the junction 
between “‘stomach” and “intestine” are mucus-producing but differ 
ultrastructurally from mucus-producing goblet cells and surface ep- 
ithelial cells also found in this region (Figs. 25, 26). Cells of the 
glands of Brunner have large euchromatic nuclei, lamellar GER 
with swollen cisternae filled with strands of electron-dense material, 
and large numbers of spherical (sometimes coalescing) pale secre- 
tory granules containing a dispersed flocculent secretion product 
(Figs. 25, 26). The Golgi complexes in these cells are extraordinary; 
newly formed granules of a variety of sizes are found at the concave 
face. The outer, convex surface is characterized by flattened saccules 
containing electron-dense material similar to that found within the 
GER cisternae (Fig. 26). Numerous mitotic figures within the glands 
of Brunner in Microtus are interesting because they suggest a turn- 
over of secretory cells in these glands. Additionally, in most exam- 
ples the dividing cells contain at least some secretory product within 
their cytoplasm (Fig. 25). One type of cell occasionally found within 
the glands of Brunner is distinctive in that it contains a product 
that has an electron-dense core with a less dense surrounding halo 
(Fig. 26). The surface epithelium of the proximal duodenum con- 
sists of absorptive cells, goblet cells, and occasional “surface mucous 
cells” resembling those found in the glandular mucosa of the stom- 
ach (Fig. 27). The latter cells probably reflect a slight interdigita- 
tion between “gastric” and “intestinal” epithelium. 

The small intestine in Microtus is characterized by low, broad 
villi, which is a morphology commonly associated with herbivorous 
diets (Barry, 1976). The villar pattern, perpendicular to the long 
axis of the intestine, probably enables the villi to slow the transport 
of chyme and thus contributes to the high digestive efficiency re- 
ported for meadow voles (Barry, 1976; Golley, 1960). A relatively 
narrow lamina propria is the most striking microanatomical feature 
of the small intestine in Microtus (Fig. 28) and possibly is related 


_ 


bar = 17 um. Bottom: dividing cell (note chromatin, C) with secretory product (ar- 
rows). Presumably this is a mucus-producing cell in the Brunner’s gland (B). Scale 
bar = 1 um. 


236 Phillips 


Fic. 26. Top: a comparison of secretory products of Brunner’s gland cells (SG 
on left) and the electron-dense type (SG on right) also found in the duodenum. Note 
relatively small Golgi (G) and sparse granular endoplasmic reticulum (GER) in the 


Microanatomy 237 


to villar morphology. Two other considerations are the low intes- 
tinal surface area, body-weight ratio and relative uniformity of the 
absorptive surface as demonstrated in an analysis of mucosal surface 
area per cm serosal length (Barry, 1976). Barry (1976) thought 
that in Microtus less absorption takes place at the small intestine 
than in the colon and caecum, which have comparatively great sur- 
face areas. Another aspect is the fact that Microtus eat large amounts 
(volume) of food having relatively low nutritional value; possibly 
passage is slow enough that nutrients can be absorbed gradually 
over the length of the intestine (Barry, 1976). 

Ultrastructurally, the absorptive cells (enterocytes) in the prox- 
imal small intestine of M. pennsylvanicus are very similar to those 
of other rodents such as laboratory strains of the Syrian hamster 
(Mesocricetus auratus), house mouse (Mus musculus), and Norway 
rat (Rattus norvegicus) (for example, see Buschmann and Manke, 
1981a, 19816; Rhodin, 1974). The mid-region of a villus is the 
most appropriate location for interspecies comparison because lower 
on the villus the absorptive cells presumably are less fully differ- 
entiated (at least in ultrastructural morphology), whereas toward 
the villar apex the cells undergo radical changes as they are about 
to be extruded from the epithelium (Potten and Allen, 1977). Mid- 
region absorptive cells in Microtus are columnar and have an ex- 
tensive brush-border of elongate microvilli (Figs. 28, 29, 30). The 
apices and sides of the apical microvilli have a sparse glycocalyx 
coating (Fig. 28). Lateral borders of adjacent absorptive cells are 
characterized by junctional complexes apically and wide intercel- 
lular spaces basally (Figs. 28, 29, 30). As illustrated in Fig. 28, 
from the apical margin the absorptive cell junctional complexes 
typically are: 1) zonula occludens; 2) zonula adherens; and 3) mac- 
ula adherens (Fig. 28). The basal intercellular space is interesting 
in that in non-fasted specimens of Microtus, the space nearly always 
contains accumulations of chylomicrons (Figs. 29, 30) representing 
the results of lipid absorption in the proximal intestine (Sabesin 
and Frase, 1977). The mid-lateral region of many active absorptive 


—_— 

second cell type. Scale bar = 0.5 wm. Bottom: Golgi complex in a Brunner’s gland 
cell. Note immature granules forming along inner face of the Golgi (arrows). Mi- 
tochondrial profiles (M) are abundant in this region of the cell. Scale bar = 0.25 um. 


238 —-~Phillips 


cells also is characterized by complex infoldings of the plasma mem- 
brane that result in a zone that can be described as a shallow 
intracellular canaliculus. ‘The abundance in this zone of coated ves- 
icles both isolated within the cytoplasm and fused on the inner face 
of the plasma membrane suggests that this is a primary site for 
exocytosis leading to chylomicron formation. The large amount of 
chylomicrons (Fig. 30) typically found in non-fasted Microtus is 
significant in view of the general belief that relatively little absorp- 
tion takes place in the proximal small intestine. It should be noted, 
however, that the animals illustrated in this chapter had been fed 
ad libidum on a Purina rodent laboratory chow. 

The cytoplasm of absorptive cells clearly is organized into com- 
partments. Apically, mitochondrial profiles, vesicles, and flattened 
strands of GER are the major components. This is followed by a 
distinctive Golgi zone, another region of mitochondria and GER, 
the euchromatic nucleus, and, basally, a third region of mitochon- 
dria, GER, and free ribosomes (Figs. 28, 29). 

With the exception of goblet cells, which are illustrated here (Fig. 
28), the other cellular components of the proximal intestine, as well 
as all of the colon and caecum, are as yet microscopically unstudied 
in Microtus. Future ultrastructural analysis of the caecum in Mi- 
crotus, particularly interspecies comparisons, could prove to be ex- 
tremely interesting because Lombardi (1978) showed that the cae- 
cum has a significant physiological role in osmoregulation. This 
particularly is true in M. brewert, which occurs on Muskeget Island, 
Massachusetts, where available water cannot be used because of its 
mineral content. According to Lombardi (1978), the caecum is sig- 
nificantly more elaborate (it has a relatively greater surface area) 
in M. brewer: than it is in specimens of M. pennsylvanicus from 
adjacent mainland populations where water is readily available. 
Whether or not such differences carry through to the fine structure 
of the epithelial cells remains to be learned. 


~ 


Fic. 27. Top: surface mucous cell found in the proximal duodenum. Note sparse 
glycocalyx (Gly). Scale bar =0.5 wm. Bottom: high magnification TEM view of 
goblet cell mucus (MUC) being released into the duodenal lumen. Note apparent 
fusion (isolated arrow) of secretory granule membrane (SGM) and the cell mem- 
brane (CM) and microvilli (MV) on the adjacent cell. Scale bar = 0.12 um. 


Microanatomy 239 


240 —~Phillips 


Muicroanatomy 241 


Adrenal Glands 


The adrenal glands are complex components of the mammalian 
endocrine system. Structurally they consist of two histologically rec- 
ognizable zones, the outer cortex and the inner medulla. The cortex 
can be subdivided into three zones that are characterized by cellular 
and, to some extent, functional differences: 1) the outermost is the 
zona glomerulosa, consisting of a thin layer of epithelial cells; 2) 
the middle layer is the zona fasciculata, consisting usually of cells 
rich in cytoplasmic lipid droplets; and 3) the inner, juxtamedullary, 
layer is the zona reticularis (Rhodin, 1974). Corticosteroids are 
synthesized within the cortex, whereas epinephrine and norepi- 
nephrine are produced by cells of the medulla. 

Insofar as Microtus is concerned, most of the interest in the mi- 
croanatomy of the adrenal gland has resulted from efforts to un- 
derstand the well-documented population cycles that characterize 
at least some of the species. A complete review of this particular 
subject may be found elsewhere (Taitt and Krebs, this volume) and, 
thus, only relevant histological aspects are described in this brief 
section. 

Christian and Davis (1966) provided fairly detailed data on his- 
tological changes in the adrenal glands of female specimens of M. 
pennsylvanicus in response to both population density and repro- 
ductive status. These authors were particularly interested in the 
adrenal cortex and undertook a quantitative analysis of the areas 
of each of the cortical zones by projecting drawings and using plan- 
imetry (Christian and Davis, 1966). Changes in adrenal weight in 
Microtus were found to result from increases or decreases in size of 
the potentially hyperplastic zona fasciculata and zona reticularis. 
During an increase in size of these zones caused by adrenal stim- 
ulation, cells of both contained abundant lipid (Chitty and Clarke, 
1963; Christian and Davis, 1966). One interesting histological 


mel 


Fic. 28. Top: light microscopic survey of small intestine showing typical mid- 
villous enterocytes (E), their microvilli (MV), a goblet cell (G), and the lamina 
propria (LP). Scale bar = 17 wm. Bottom left: TEM view of area outlined in rec- 
tangle at top. Note typical goblet cell secretory granules (sg). Scale bar = 1 mum. 
Bottom right: typical enterocyte cell junctions. Abbreviations are: ZO, zonula occlu- 
dens; ZA, zonula adherens; MA, macula adherens. Scale bar = 0.12 um. 


242 Phillips 


Fic. 29. TEM survey of typical enterocytes in small intestine of Microtus. Note 
also the small infiltrating lymphocyte (Lymp). Scale bar = 1 um. 


Microanatomy 243 


question that has arisen from this work is whether or not an X-zone 
is found in the adrenal glands of Microtus. Christian and Davis 
(1966) concluded that such a zone is lacking, at least in mature 
female Microtus. However, more recently, To and Tamarin (1977) 
reported finding histological evidence of a transitory X-zone in some 
nulliparous female M. brewer and in subadult, non-breeding males 
of both M. brewer and M. pennsylvanicus. Although the functional 
significance of the X-zone remains unknown, its presence or ab- 
sence is regarded as important in making comparisons of adrenal 
weights in animals. 

In summary, although the adrenal glands of Microtus have not 
been described in such a way as to make possible microanatomical 
comparisons with the same glands in other mammals, the histology 
of the glands nevertheless has been used as an indicator of popu- 
lation stresses and reproductive status. Additionally, Microtus pos- 
sibly could serve as a useful model for future studies of the transi- 
tory nature of the X-zone. 


Reproductive Tracts 


Reproduction and ontogeny in many species of microtine rodents 
(both Old and New World Species) have been studied from a va- 
riety of perspectives. In general, the reproductive biology of micro- 
tines is an unusually complex and extremely interesting story that 
is made even more significant by the tendency of populations to 
cycle or fluctuate and by the economic importance of some micro- 
tines to agriculture. Insofar as the microanatomy of the reproductive 
tracts is concerned, neither males nor females have been described 
histologically in such a way as to facilitate comparison with other 
types of rodents or with other mammals in general. Nevertheless, 
histology of both testes and ovaries frequently has been employed 
as an adjunct to investigations of reproductive biology and some 
published light-level micrographs are available in the literature (see 
Schadler [1980] for examples of testes and ovaries of Microtus pi- 
netorum). Reproduction and ontogeny are discussed in considerable 
detail elsewhere in this book (Keller, this volume; Seabloom, this 
volume; Nadeau, this volume), and, therefore, only a few examples 
of the use of histology are offered here as a brief introduction to 
the microanatomy of reproductive tracts. 

Even though most microtine species spend significant amounts of 


Phillips 


244 


Microanatomy 245 


time in dark burrows and seem to prefer either twilight or complete 
darkness (Kavanau and Havenhill, 1976), light intensity neverthe- 
less is inversely related to reproductive performance, at least in 
Microtus pinetorum (Geyer and Rogers, 1979). Several investigators 
have studied the possible effects of light intensity and photoperiod 
on both development of the gonads and onset of puberty. Basically, 
a lengthened photoperiod can increase the rate at which puberty is 
attained, at least in M. montanus (Vaughan et al., 1973). Addition- 
ally, in two Old World species, M. agrestis and M. arvalis (Breed 
and Clarke, 1970a; Clarke and Kennedy, 1967), increased photo- 
period was shown to both accelerate puberty and enhance glandular 
development. In regard to onset of puberty, Schadler and Butter- 
stein (1979) presented some useful histological data for Muicrotus 
pinetorum. According to these authors, in animals maintained at a 
photoperiod of 12L:12D, testes from 6-week-old animals lacked 
sperm, whereas those from 8-week-old males had mature sperma- 
tozoa in both the testes and the epididymides. Insofar as females 
are concerned, Schadler and Butterstein (1979) found that in 8- 
week-old animals the ovaries contained occasional tertiary ovarian 
follicles but lacked pre-ovulatory follicles and corpora lutea. At 12 
weeks, however, 89% of the examined ovaries showed either corpora 
lutea or ovarian follicles. 

Reproductive patterns and comparative fertility have been inves- 
tigated by histological analysis of ovaries. For example, Hagen and 
Forslund (1979) used ovarian histology to compare female Microtus 
canicaudus of different age classes. They found that the fetus-corpus 
luteum ratio was significantly higher in young (18-day) females 
than in old (70+ days). The apparent value in using ovarian mi- 
croanatomy in this instance is that it allows one to estimate prenatal 
(embryonic) mortality. Consequently, comparisons can be made to 
determine relative success rates among species or age classes. For 
example, in one study of Microtus californicus the corpora lutea were 


—_— 


Fic. 30. TEM survey of basal portion of Microtus enterocytes showing elaborate 
granular endoplasmic reticulum (GER) and cytoskeletal tonofilaments (Tf). Note 
accumulation of chylomicrons (Chy) in the intercellular space. Other abbreviations 
are: M, mitochondria; BL, basal lamina; FB, fibroblast; CAP, fenestrated capillary. 
Scale bar = 1 um. 


246 Phillips 


found to greatly exceed the embryo count (Greenwald, 1956), 
whereas in the Old World M. agrestis the corpora lutea did not 
greatly outnumber embryos during the course of pregnancy (Breed 
and Clarke, 19706). 

As with the case of adrenal gland histology, reproductive-tract 
microanatomy has been studied in relation to crowding (Schadler, 
1980). In this interesting investigation, Schadler (1980) compared 
a group of crowded and uncrowded individuals of Microtus pine- 
torum and used the histological criteria of Clermont (1972) and 
Grocock and Clarke (1974) to analyze germinal elements and to 
determine sperm indices (SI) in the testes. For the ovaries she fol- 
lowed Pederson and Peters (1968) in measuring follicle size. Under 
crowded conditions, male M. pinetorum matured significantly more 
slowly than did animals kept in less crowded quarters. For example, 
among crowded males, the following histological features were not- 
ed (Schadler, 1980). In 7% the SI was 1 and testes contained mostly 
sertoli cells with some spermatogonia and occasional spermatocytes. 
In 12% the SI was 2, the tubules were “small,” and secondary 
spermatocytes and round spermatids were found. Additionally, in 
this grouping Schadler (1980) also reported finding large eosino- 
philic cells with pyknotic nuclei. In 39% of the crowded males the 
SI was 3 and the testes contained elongated spermatids but not 
spermatozoa. Among the remaining animals, 32% were SI = 1 and, 
although the testes contained spermatozoa, the tubules were “small”; 
only 9% were SI = 5. In uncrowded males, 85% were SI = 5 and 
only 15% were SI = 4. Insofar as the females were concerned, none 
of those kept in crowded conditions had ovulated and no corpora 
lutea were found (Schadler, 1980). On the other hand, 21% of 
uncrowded females had corpora lutea. 

The relationship of diet and reproductive performance is yet 
another example of an area of research in which reproductive or- 
gans have been studied histologically. In this intance, the number 
of maturing ovarian follicles has been shown to increase signifi- 
cantly when green plant food is added to the diet of Microtus mon- 
tanus (Negus and Pinter, 1966; Pinter and Negus, 1965). Gonadal 
hypertrophy also has been demonstrated in relationship to diet (Ne- 
gus and Berger, 1971). 

In summary, although the histological details of the reproductive 
tracts in Microtus have not been described in a traditional sense, 
reproductive tract histology nevertheless frequently has been used 


Microanatomy 247 


to measure a variety of environmental variables and physiological 
parameters. 


Acknowledgments 


Financial support for the original research reported in this chap- 
ter came from the Department of Biology, Hofstra University, and 
an HCLAS grant (Hofstra University) to the author. Several per- 
sons, in particular Dr. Gary W. Grimes, Nadine M. Sposito, and 
Keith Studholme, offered me their time, ideas, and technical assis- 
tance with various aspects of this project. My daughter, Kathrin N. 
Phillips, collected the specimens of Microtus from which the pub- 
lished electron micrographs were made. Lastly, I thank the Hofstra 
University Special Secretarial Services, headed by Stella Sinicki, for 
their outstanding assistance with this manuscript. 


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Microanatomy 249 


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Microanatomy 251 


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ONTOGENY 
JosEPH H. NADEAU 


Abstract 


G fis literature on growth and development from conception to 
sexual maturity of New World Muicrotus is reviewed. The 
following characters and processes are described: 1) the prenatal 
period—spermatozoa, ova, ovulation, fertilization, pre- and post- 
implantation growth and development, implantation, trophoblastic 
giant cells, and mortality; 2) parturition—gestation period, stage of 
development, weight and length of neonates, litter size, sex ratio, 
and parental behavior towards neonates; and 3) postnatal period— 
growth, development, mortality, molting, and sexual maturation. 
The contribution of these ontogenetic attributes to a species’ “‘eco- 
logical strategy” is evaluated. 


Introduction 


It could be argued that ontogeny occupies a central position in 
the description of the biology of any species. The basis for this 
argument is that growth and development are the processes whereby 
genetic information is translated into the anatomy, physiology, and 
behavior of adults. Changes that alter the patterns of ontogeny 
produce inherited variation in the ways of life of an organism. By 
studying the ontogeny of particular morphological, metabolic, or 
neurological attributes, an understanding can be gained not only of 
the causes and consequences of ontogenetic variation but also of the 
ways in which phylogenetic diversity is achieved. Indeed, the de- 
pendence of phylogenetic diversity on ontogenetic variation was one 
of the most important rules that Darwin recognized. 

The variation in anatomy, physiology, and behavior exhibited by 
New World Microtus makes these species particularly well-suited 
for ontogenetic studies. The ontogeny of New World Microtus, how- 
ever, has been studied unevenly. For example, a considerable lit- 
erature exists on litter size (reviewed by Innes, 1978; Krebs and 


254 


Ontogeny 255 


Myers, 1974; Stenseth and Framstad, 1980). In addition, Hasler 
(1975) reviewed the literature on gestation period, ovulation, litter 
size, and sexual maturation, as well as several other aspects of 
reproduction. Most aspects, however, have hardly been studied. For 
example, Ozdzenski and Mystkowska’s (1976a, 19766) studies of 
Clethrionomys glareolus represent the only published descriptions of 
the stages of prenatal development of any New World or Old World 
microtine rodent. 

The purpose of this chapter is to review the literature on growth 
and development from conception to sexual maturation of New 
World Microtus. I have tried to include all relevant observations, 
but I have not tried to include every reference for each observation. 


The Prenatal Period 


Of the various aspects of the ontogeny of New World Microtus, 
the prenatal period is least studied. As a result, the following de- 
scriptions are sketchy. To compensate for these deficiencies, relevant 
information for Old World Microtus is occasionally included. 


Spermatozoa 

Spermatozoa in New World Microtus have not been described in 
the published literature. In Old World Microtus such as M. agrestis, 
spermatozoa are hooked and have a strongly recurved head (Austin, 
1957). The mean length of spermatozoa is 103.5 um, mean head 
length 6.9 wm, and mean neck and midpiece length 27.4 wm. 


Ova 


The diameter of the ovum ranges from 65 to 70 um at ovulation 
in M. californicus (Greenwald, 1956) and is 60 wm in M. montanus 
(Cross, 1971). 


Fertilization 


In Old World Microtus such as M. agrestis, there are an average 
of 4.1 ova in the oviduct at fertilization of nulliparous females 
(Austin, 1957). The mean number of spermatozoa in the ampulla 
of the oviduct is 124 (range 28 to 360). An average of 82% of ova 
are fertilized and only 2% of fertilized ova are polyspermic. ‘The 


256 Nadeau 


TABLE 1 
PRE-IMPLANTATION DEVELOPMENT IN Microtus. TIME Is MEASURED FROM COPULA- 
TION 
Day of 
development Stage of development 
Day 0 Oh Copulation. 
<15h Ovulation in M. californicus (Greenwald, 
1956). 
Meiotic divisions begin after ovulation. 
15-18 h Two-celled ova (Greenwald, 1956). 
Day 2 48-72 h In M. californicus, most ova have 16 cells 
(Greenwald, 1956). 
Day 5 Implantation occurs in M. pennsylvanicus 


(Mallory and Clulow, 1977). 


second maturation division in M. californicus is completed after fer- 
tilization (Greenwald, 1956). 


Pre-implantation Growth and Development 


The age of embryos is usually measured from the time of copu- 
lation (day 0, hour 0), and presence of spermatozoa in vaginal 
smears is considered evidence for recent copulation. The error in- 
volved is usually no more than 12-24 h. A summary of pre-im- 
plantation growth and development is provided in Table 1. Cleav- 
age divisions begin about 40 h after copulation. Cells multiply rap- 
idly and in some cases three to four cell divisions have occurred 
within 48 h. The average rate of cell division is therefore less than 
one division every 2-3 h. 


Post-implantation Growth 


Mallory and Clulow (1977, fig. 13) provide a key to the changes 
in uterine size and shape during gestation in M. pennsylvanicus. 
The average embryonic growth rate in M. pennsylvanicus is 0.25 to 
0.40 g/day (Barbehenn, 1955). 

The patterns of post-implantation growth of representative small 
rodents from day 10 to parturition are presented in Fig. 1. Before 
day 10, the embryo is too small and embedded too deeply in ex- 
traembryonic and uterine membranes to permit ready measure- 


Ontogeny 257 


C. glareolus 


M. pennsylvanicus 
Mus musculus 


CROWN-RUMP LENGTH (mm) 


iO lt2 14 6 I8 20 22 
DAY OF PRENATAL DEVELOPMENT 


Fic. 1. Relation between crown-rump length and day of prenatal development 
in Microtus pennsylvanicus, Mus musculus, and Clethrionomys glareolus. Data are from 
Mallory and Clulow (1977), Theiler (1972), and Ozdzenski and Mystkowska (1976a), 
respectively. 


ment. Data for Clethrionomys glareolus and Mus musculus are in- 
cluded for comparative purposes. Crown-rump length was used as 
a measure of size because more published data were available for 
crown-rump length than for body weight in Microtus, Mus, and 
Clethrionomys. However, crown-rump length and weight are highly 
correlated (M. brewer: r = 0.97, n = 6; M. pennsylvanicus: r = 0.98, 
n = 6; J. H. Nadeau, P. H. Kohn, and R. H. Tamarin, pers. 
comm.). 

The rates of growth in M. pennsylvanicus, C. glareolus, and Mus 
musculus are lower and less variable between species during the 
early portion of prenatal development than during the late portion 
(Fig. 1). For example, the average growth rates between day 10 


258 Nadeau 


and day 16 for M. pennsylvanicus, C. glareolus and Mus musculus 
are 1.6, 2.0 and, 1.9 mm per day, respectively, whereas the average 
rates after day 16 for these three species are 2.0, 4.0 (after day 15), 
and 3.0 mm per day, respectively. The latter rates are 1.25- to 2- 
fold higher and relatively more variable than the former. These 
patterns of growth suggest that rates of embryonic growth for the 
early portion of prenatal development are highly conserved during 
rodent evolution and that the neonatal size (weight) characteristic 
of each species are realized only during the late portion of prenatal 
development. 

The stage in development at which the rate of growth changes 
does not appear to be related to the appearance of any particular 
developmental feature. For example, the change in growth rate in 
Mus musculus occurs after most of the major external morphological 
features have appeared, whereas in C’. glareolus the change occurs 
at a slightly earlier stage of morphological development. 

The growth rates characteristic of each species show the expected 
high correlation with both the length of gestation and neonatal 
weight. Of the three species, C. glareolus has the highest growth 
rate, the lowest neonatal weight and the shortest gestation period, 
whereas M. pennsylvanicus has the lowest growth rate, the highest 
neonatal weight, and the longest gestation period. It is not known 
which, if any, of these three parameters is the independent variable. 
Despite these differences in growth rates, neonatal weights, and 
gestation periods, however, fetuses of these three species are born 
at about the same developmental stage; there is no evidence for 
precocity. 


Post-implantation Development 


I am not aware of any published description of post-implantation 
development in New World Microtus and therefore have included 
a summary of Ozdzenski and Mystkowska’s (1976a, 19766) de- 
scription of development in C. glareolus. Their description focuses 
on external morphological characters primarily. Neither organo- 
genesis nor the development of sexual characters appear to be de- 
scribed in the literature. Although C. glareolus is not a New World 
Microtus, the two are closely related and their ontogenies should be 
comparable. Moreover, although rates of development sometimes 
vary between species, the sequence in which developmental features 


Ontogeny 259 


appear is highly conserved, at least among rodents. Thus, post- 
implantation development in C. glareolus, a summary of which is 
provided in Table 2, may be representative of most microtine ro- 
dents. 


Trophoblastic Giant Cells 


In contrast to the corresponding cells in Mus musculus, the tro- 
phoblastic giant cells of Microtus agrestis (Copp, 1980), M. arvalis 
(Disse, in Copp, 1980), Arvicola amphibius (Sansom, 1922), and 
Clethrionomys glareolus (Ozdzenski and Mystkowska, 1976a) can 
be found at all levels of the endometrium, including the implanta- 
tion site. In addition, microtine trophoblastic giant cells are of two 
types: non-migratory cells that remain at the implantation site and 
migratory cells of which there are in turn two types, small migra- 
tory cells and large migratory cells. One function of non-migratory 
cells is to anchor Reichert’s membrane to the decidua. Reichert’s 
membrane is an extraembryonic membrane covering the outer layer 
of trophectoderm and is secreted by the parietal endoderm (Snell 
and Stevens, 1966). Small migratory cells are not highly polypoid 
as are non-migratory cells and large migratory cells in Microtus and 
trophoblastic giant cells in Mus. The function of migratory giant 
cells is unknown. It is tempting to speculate that these cells might 
be related to the dispersed alkaline phosphatase activity observed 
in the endometrium of certain microtine rodents but not in other 
rodents such as Mus (Mohi Aldeen and Finn, 1970). 


Prenatal Mortality 


Pre-implantation mortality is usually measured as the difference 
between the number of corpora lutea and the number of implan- 
tation sites (including resorbing embryos) and is expressed as this 
difference divided by the number of corpora lutea (100). It is 
assumed that all ova ovulated are fertilized. Other potential biases 
in the estimation of mortality rates include corpora lutea that are 
difficult to identify, accessory corpora lutea, polyovular follicles, 
twinning, and loss of entire litters. Hoffmann (1958) presents a 
thorough discussion of the problems associated with measurement 
of pre-implantation mortality. 

A summary of the data on pre-implantation mortality is pre- 
sented in Table 3. The average percentage of ova lost prior to 


260 Nadeau 


TABLE 2 
POST-IMPLANTATION DEVELOPMENT OF Clethrionomys glareolus (DATA FROM OZ- 
DZENSKI AND MystTkowska, 1976a, 19766) 


Day of 
develop- 
ment Stage of development 

Day 4 Blastocyst elongates and implants. Decidual reaction occurs at site of 
attachment. Inner cell mass orients towards mesometrium. Egg cy]l- 
inder divides into embryonic and extraembryonic portions. Migrat- 
ing giant cells appear. Swelling is visible at implantation site. Am- 
nionic cavity forms. Trophoblastic giant cells appear. 

Day 5 Ectoplacental cone forms. Endoderm differentiates into embryonic 
and extraembryonic portions. 

Day 6 Primitive streak forms. Mesodermal cells begin to migrate. Amnion 
and chlorion form. Implantation site is round and embryo is visible 
through uterine wall. 

Day 7 Allantois forms and joins with chorion to form chorio-allantoic pla- 
centa. 

Day 8 Embryo inverts germ layers to assume shape characteristic of most 
mammalian embryos. Brachial arches are visible. Eye, auditory 
vesicles, and heart are visible. Forelimb buds appear as small 
swellings. There are 13 to 21 somites. 

Day 9 In some cases eye lens is visible. Forelimb bud is paddle-shaped. 


Hindlimb bud swelling is apparent. Trunk and tail are segmented. 


Day 10 Maxillae are separated from head. Fore- and hindlimb buds begin to 
divide into limbs and feet. Retinal pigment is barely apparent. 
Digits begin to demarcate but are not yet separated. 


Day 11 Retinal pigment is obvious. Pinnae are visible. Umbilical hernia ap- 
pears. Limbs elongate. 


Day 12 Eyelids partly cover eyes. Rudiments of vibrissae are visible. Digits 
are well demarcated. 


Day 13 __Pinnae cover auditory openings. Limb joint rudiments are apparent. 


Day 14 _—_ Hair follicles are widely distributed over body. All digits are separat- 
ed. 


Day 15 _—_ Eyelids completely cover eyes. Pinnae attaches to skin opposite audi- 
tory meatus. Claws are visible. Pigment on head and dorsum is 
deposited. Umbilical hernia is lost. 


Day 16 Skin folds are prominent. Secondary fusion of digits is complete. 
Day 17 _ Fetuses are larger and skin folds are more prominent. 


Day 18 _ Parturition. 


Ontogeny 261 
TABLE 3 
PRENATAL MORTALITY (NOT INCLUDING Loss OF ENTIRE LITTERS) IN NEW WORLD 


Mucrotus 


Percent of ova lost 


Post-im- 
Pre-implantation _ plantation 
Species mortality mortality References 
Microtus breweri 10.9 8.1 Tamarin (1977) 
M. californicus — 7 Greenwald (1957) 
= 4.7 Lidicker (1973) 
M. montanus 5.9 2.6-3.9 Hoffmann (1958) 
M. ochrogaster 11.0 — Corthum (1967) 
6.6 7.0 Keller and Krebs (1970) 
(range 3.4-12.9) 
9 1.6 Rose and Gaines (1978) 
M. pennsylvanicus 13 8.4 Beer et al. (1957) 
i — Corthum (1967) 
9 6.4 Keller and Krebs (1970) 
(range 4.7-45.5) 
6.1 yp Tamarin (1977) 
— 3.6 Innes (1978) 


implantation is 8.14% (SD = 2.00). The highest reported rate of 
mortality is in Microtus ochrogaster, the lowest in M. montanus. 

Post-implantation mortality is usually measured as the difference 
between the number of resorptions and number of living and re- 
sorbing embryos and is expressed as the number of resorptions 
divided by the number of living and resorbing embryos (100). At 
least three factors represent potential biases in comparison of the 
numbers of ovulated eggs and litter size. These factors include 
transmigration of pre-implantation embryos from one uterine horn 
to the other, ovulation of more than one ovum from a single ovarian 
follicle, twinning, and loss of entire litters. In M. pennsylvanicus, 
the average number of transmigrated ova per litter is 0.07, the 
average number of embryos resulting from multiple ovulation per 
litter is 0.05, and the average number of twins per litter is 0.02 
(Beer et al., 1957). 

A summary of the data on post-implantation mortality is pre- 
sented in Table 3. The average percentage of embryos lost after 


262 Nadeau 


implantation but before parturition is 5.42% (SD = 2.53). Among 
New World Microtus the highest reported rate of mortality occurs 
in M. pennsylvanicus, the lowest in M. ochrogaster. In M. town- 
sendit, 68.2% of unsuccessful litters are lost during gestation or at 
parturition (Anderson and Boonstra, 1979). 

The rate of prenatal mortality depends on parity. In some species 
(M. breweri, for example), the rate is correlated negatively with 
parity (Tamarin, 1977), whereas in other species (M. arvalis, for 
example) the rate is correlated positively with parity except for the 
smallest females (Pelikan, 1970). 


Parturition 


Gestation Period 


The average length of gestation in New World Mucrotus and 
other representative rodents is given in Table 4. The average period 
is 21.4 days (SD = 1.29). The shortest gestation periods are less 
than 20 days in some populations of M. ochrogaster (Fitch, 1957), 
the longest about 24 days in both M. oregon: (Cowan and Arsenault, 
1954) and M. pinetorum (Kirkpatrick and Valentine, 1970). In 
some species (M. agrestis and Dicrostonyx groenlandicus, for exam- 
ple), gestation can be prolonged if the female is lactating (Breed, 
1969; Manning, 1954). This effect, however, does not increase the 
length of gestation considerably. In most cases, it is not clear wheth- 
er the delay results from delayed post-partum mating, delayed im- 
plantation, or decreased post-implantation growth. 


Stage of Development 


Neonatal Microtus are hairless and unpigmented, their eyes and 
ears are closed, their teeth have not erupted, their anus is not patent, 
but their vibrissae are apparent. These descriptions apply to neo- 
natal M. brewer: (Rothstein, 1976), M. californicus (Hatfield, 1935; 
Selle, 1928), M. montanus (Bailey, 1924), M. ochrogaster (Kruck- 
enberg et al., 1973; Richmond and Conaway, 1969), M. pennsyl- 
vanicus (Innes and Millar, 1979; Lee and Horvath, 1969), and M. 
oregont (Cowan and Arsenault, 1954). There is no evidence that 
fetuses of these species are born at different stages of development. 


Ontogeny 263 


TABLE 4 
LENGTH (Days) OF GESTATION IN NEW WoRLD Microtus* 


Mean 
Species (SD) References 
Microtus abbrevi- 
atus 2AeS Morrison et al. (1976) 
M. californicus 21 Greenwald (1956); Hatfield (1935); Selle (1928) 
M. muiurus 21 Morrison et al. (1976) 
M. montanus 21 Bailey (1924); Hoffmann (1958) 
M. ochrogaster <20 Fitch (1957) 
21 Morrison et al. (1976); Richmond and Cona- 
way (1969) 
22.8 Kenny et al. (1977) 
M. oeconomus 20.5 Dieterich and Preston (1977); Morrison et al. 
(1976) 
M. oregoni 24 Cowan and Arsenault (1954) 
M. pennsylvanicus 21 Lee and Horvath (1969) 
21 Lee et al. (1970); Mallory and Clulow (1977) 
21.0 (0.2) Kenny et al. (1977) 
20 Innes and Millar (1981) 
M. pinetorum 24 Kirkpatrick and Valentine (1970) 
M. townsendit 22 MacFarlane and Taylor (1982) 


* Further data can be found in Hasler (1975). 
+ Twenty-four days in lactating females. 


Weight and Length of Neonates 


Weights of neonatal Microtus are given in Table 5. Little variation 
in weight is observed in species such as M. californicus (range 2.7 
to 2.8 g) and M. ochrogaster (range 2.8 to 3.1 g). By contrast, 
average weight of M. pennsylvanicus varies by more than one g 
among samples (range 1.9 to 3.2). Few data are available for other 
species. 

Neonatal weight often depends on litter size and maternal weight. 
In some populations of M. pinetorum, weight of the entire litter is 
correlated with maternal weight and therefore, because litter size 
is independent of maternal weight, weight of each neonate in a 
litter depends on maternal weight (Paul, 1970). In other popula- 
tions of M. pinetorum, correlations have not been found between 


264 Nadeau 


TABLE 5 


WEIGHT (G) AT BIRTH IN NEW WORLD Microtus 


Mean weight 


Species (SD) 
Microtus breweri 35 
M. californicus Dei 
2.8 
M. muiurus Pa) 
M. montanus 25 
3:9 
M. ochrogaster 2.8 
2.9 (0.1) 
2.8 (0.4) 
Sal 
M. oeconomus 3.0 
M. oregoni 1.7 
(range 1.6-2.2) 
M. pennsylvanicus 19 
Dal 
(range 1.6-2.9) 
2a 
(range 1.6-3.0) 
23) OF 
2.0-3.0 
23 
3225 
M. pinetorum 2.0 
Qed, 


* Pups were weighed 0-3 days after parturition. 


Stage of 
develop- 


ment 


Neonate 


Neonate 
Neonate 


Neonate 


Full term 
Neonate 


Neonate 


Neonate 
Neonate 


Neonate 


Neonate 


Full term 
Neonate 


Neonate 


Neonate 
Neonate 
Neonate 
Neonate 


Neonate 
Neonate 


References 

J. H. Nadeau, P. H. Kohn, and 

R. H. Tamarin (pers. comm.) 
Selle (1928) 
Hatfield (1935) 
Morrison et al. (1977) 
Hoffmann (1958) 
Bailey (1924) 
Richmond and Conaway (1969) 
Fitch (1957) 
Martin (1956) 
Kruckenberg et al. (1973) 
Morrison et al. (1977) 
Cowan and Arsenault (1954) 


Hamilton (1937) 
Hamilton (1937) 


Hamilton (1941) 


Innes and Millar (1981) 
Lee and Horvath (1969) 
Innes and Millar (1979) 
Morrison et al. (1977) 


Lochmiller et al. (1982ca) 
Hamilton (1938) 


litter size (weight) and maternal weight, or between litter size 
(weight) and neonatal weight (Lochmiller et al., 1982a). In M. 
ochrogaster, total litter weight increases linearly with increasing lit- 
ter size from litters of one to four, whereas litters of five and six do 
not weigh significantly more than litters of four (Richmond and 


Conaway, 1969). 


By comparison, individual pup weight is inversely dependent on 
litter size. Here, the mean weight of pups in litters of size one to 


Ontogeny 265 


t 120 oe! 
—~ 
=, 100 35 : 
KF go 39 W 
© = 
ou 
> 60 25 > 
a 
Wi 40 20 4 
ts > 
= ras 
~ 20 is > 
(a) 
Zz. 


| 2 3 4 5 6 
LITTER SIZE 


Fic. 2. Relations between litter weight, individual pup weight, and litter size in 
Microtus ochrogaster. Data are from Richmond and Conaway (1969). 


six was calculated by dividing total litter weight at 21 days by litter 
size at parturition. The results summarized in Fig. 2 show that the 
heaviest pups were found in the smallest litters whereas the lightest 
pups were found in the largest litters. This relationship is not linear 
as would be expected if mothers invested similar amounts of energy 
in each pup regardless of the number of pups in the litter. Instead, 
the observed relationship between the weight of the entire litter and 
of individual pups (Fig. 2) suggests that reproductive efficiency is 
optimized with litters of size 4. In fact, in the population from 
which these data were collected, the mean litter size was 3.8 (Rich- 
mond and Conaway, 1969). Unfortunately, most studies do not 
present the necessary data to determine whether such variation in 
neonatal weight is a general pattern. 


266 Nadeau 


Species 
Miucrotus abbreviatus 


M. breweri 


M. calvfornicus 


M. chrotorrhinus 


M. longicaudus 
M. muurus 


M. montanus 


M. ochrogaster 


M. oeconomus 


M. oregoni 


M. pennsylvanicus 


Mean 
(SD) 


3.0 
3.4 (1.1) 
4.7 (0.1) 


4.6 (0.5) 


3.6 (0.1) 


4.0 
4.9 


3.9 
8.2 


6.0 
6.0 (0.4) 


3.9 (0.4) 


3.5 (0.4) 


4.0 (0.1) 
6.6 (1.0) 


3.3 (0.7) 


4.4 (0.9) 


TABLE 6 
LITTER SIZE IN NEW WorLD Microtus 


Range Origin 


1-8 


1-9 


Lab 
Field 
Lab 


Field 


Field 


Lab 
Field 


Lab 
Field 


Lab 
Field 


Lab 


Field 


Lab 
Field 


Lab 


Lab 


References 


Morrison et al. (1976) 
Tamarin (1977) 


Colvin and Colvin (1970); 
Selle (1928) 
Greenwald (1956, 1957); Hoff- 
mann (1958); Lidicker (1973) 
Timm et al. (1977); Coven- 
try (1937); see also references 
in Timm et al. (1977) 


Colvin and Colvin (1970) 
Hoffmeister (1956) 


Morrison et al. (1976) 
References in Hoffmann (1958) 


Colvin and Colvin (1970) 
Hoffmann (1958); How- 
ell (1924); Negus and Pin- 
ter (1965); Negus et 
al. (1977); Vaughan (1969) 


Colvin and Colvin (1970); Ken- 
ney et al. (1977); Richmond 
and Conaway (1969); Thom- 
as and Birney (1979) 

Jameson (1947); Martin (1956); 
Fitch (1957); Layne (1958); 
Corthum (1967); Keller and 
Krebs (1970); Cole and Bat- 
zli (1978); Rose and 
Gaines (1978); see also refer- 
ences in Hoffmann (1958) 


Morrison et al. (1976) 
Whitney (1977); references in 
Hoffmann (1958) 


Colvin and Colvin (1970); 
Cowan and Arsenault (1954) 


Beer et al. (1957); Colvin and 
Colvin (1970); Lee and Hor- 
vath (1969); Kenney et 
al. (1977); Morrison et 
al. (1976); Poiley (1949) 


Ontogeny 267 


TABLE 6 
CONTINUED 
Mean 
Species (SD) Range Origin References 


4.9(0.6) 1-11 Field Corthum (1967); Coven- 
try (1937); Hamilton (1941); 
Innes and Millar (1981); 
Keller and Krebs (1970); 
Kott and Robinson (1963); 
Storm and Sanderson (1968); 
Tamarin (1977) 

3.1 (0.1) — Field Cowan and Arsenault (1954); 
references in Hoff- 
mann (1958) 


M. pinetorum 1.9(0:2) 1-3 Lab Gentry (1968); Kirkpatrick and 
Valentine (1970) 
2.1(0.2) 1-5 Field Gentry (1968); Glass (1949); 
Goertz (1971); Kirkpatrick 
and Valentine (1970); Lins- 
dale (1928) 


22} — Lab Lochmiller et al. (1982a); 
Paul (1970) 
3.1 (0.1) —_— Lab Schadler and Butterstein (1979) 

M. richardsoni 6.0 — Field Anderson et al. (1976) 

i) 7-8 Field Anderson and Rand (1943) 
M. townsend 4.8 2-6 Lab MacFarlane and Taylor (1982) 

5.4 2-7 Field MacFarlane and Taylor (1982) 
M. xanthognathus 8.4(0.6) 6-13. Field Wolff and Lidicker (1980); 


Youngman (1975) 


Litter Size 


Mean litter sizes for fifteen species of New World Microtus are 
given in Table 6. The mean litter size (field samples only) was 4.9 
(SD = 2.0). Some species have exceptional litter sizes: M. pinetorum 
has an exceptionally small litter size, M. miurus (field sample) and 
M. xanthognathus exceptionally large litter sizes (Table 6). 

Litter size in microtine rodents depends on a number of factors 
including parity, age, season, year, and conditions in the mating 
colony (Innes, 1978; Stenseth and Framstad, 1980). Usually the 
first litter is the smallest. Few other generalizations are possible, 
however. Litter size increases with age and parity in some species 
(M. montanus [Negus and Pinter, 1965], M. californicus [Green- 


268 Nadeau 


wald, 1957; Hoffmann, 1958]), but not in others (M. pennsylvanicus 
[Keller and Krebs, 1970; Poiley, 1949; Storm and Sanderson, 1968], 
M. ochrogaster [Keller and Krebs, 1970; Rose and Gaines, 1978], 
and M. townsendi [Anderson and Boonstra, 1979]). Litter size de- 
pends on parity in some populations of a species (Negus and Pinter, 
1965), but not in others (Hoffmann, 1958). Litter size often in- 
creases in the first few litters and then declines, such as in M. 
oregont (Cowan and Arsenault, 1954) and M. ochrogaster (Rich- 
mond and Conaway, 1969). Litter size sometimes varies consider- 
ably between field and laboratory estimates. For example, M. oec- 
onomus in laboratory colonies has a mean litter size of 4.0 pups 
(SD = 0.1), whereas in natural populations mean litter size is 6.6 
($D = 1.0). Another striking example is M. miurus, which has a 
mean litter size of 3.9 pups in laboratory colonies and 8.2 pups in 
natural populations. Clearly, litter size is subject to a variety of 
influences. 


Sex Ratio 


With four exceptions the sex ratio among species of New World 
Microtus 1s approximately 1:1 (Table 7). The first exception in- 
volves M. montanus in which there is a significant deficiency of 
males born in laboratory colonies (Vaughan et al., 1973). The or- 
igin of the deficiency has not been determined. The second exception 
occurs in at least one population of M. pennsylvanicus (J. H. Na- 
deau and R. H. Tamarin, pers. comm.). Pregnant females in sam- 
ples of live-trapped mice from a low-density population near Na- 
tick, Massachusetts, were autopsied and the morphological sex of 
the fetuses determined. There were significantly more males among 
fetuses than among adults (Table 8). At least two factors affect sex 
ratio in the Natick population; the first results in an excess of males 
among fetuses and the second restores an equal sex ratio among 
adults. Two other populations in southeastern Massachusetts had 
a 1:1 sex ratio among both fetuses and adults. An important im- 
plication of these data is that the usual assumption that an even sex 
ratio at recruitment reflects an even primary sex ratio may not be 
supported. Because sex ratio is not usually estimated among fetuses, 
it is impossible to determine whether skewed prenatal sex ratios are 
exceptional. 

The third and fourth (possible) exceptions are found in M. agres- 


Ontogeny 269 


TABLE 7 
ADULT SEX RATIOS (46:92) IN NEW WorRLD Microtus 


Stage of 
develop- 
Species Sex ratio ment Origin References 
Microtus brewert 12221 Adult Field Tamarin (1977) 
M. californicus 0.6:1 Neonate Lab Selle (1928) 
itaih Fetus and — Greenwald (1957) 
neonate 
tl Adult Field Lidicker (1973) 
M. montanus 0.40:1* _ Lab Vaughan et al. (1973) 
M. oregoni 1.1:1. | Neonate Lab Cowan and Arsenault 
(1954) 
M. pennsylvanicus 1.1:1 Adult Field Myers and Krebs (1971); 
J. H. Nadeau and R. 
H. Tamarin (pers. 
comm.); Tamarin (1977) 
M. xanthognathus 1:1 Juvenile Lab and Wolff and Lidicker (1980) 
field 
M. agrestis 1:1 Fetus and Field Myllymaki (1977) 
adult 


*P<0.05. 


tis (Myllymaki, 1977) and in M. richardson (Anderson et al., 1976) 
in which the sex ratio at recruitment of the first litters of the breed- 
ing season are skewed towards females, whereas the ratio was 1:1 
later in the year. There are two explanations for these observations: 
either the primary sex ratio is uneven, or weanling males emigrate 
or die more often than weanling females early but not late in the 
season. Because the primary sex ratio in the populations studied by 
Myllymaki (1977) was even, the explanation for the biased sex ratio 
must involve differential emigration or mortality. In the study by 
Anderson et al. (1976), the primary sex ratio was not measured 
and as a result these explanations were not evaluated. 

The sex ratios observed in natural populations of New World 
Microtus do not support Stenseth’s (1977) contention that sex ratios 
are biased slightly towards females in low-density populations and 
are biased heavily towards females in high-density populations be- 
cause of inbreeding effects. On the contrary, in the examples given, 
an even sex ratio or an excess of males are found in both low- and 
high-density populations (‘Tables 7, 8). 


270 Nadeau 


Some autosomal genotypes are associated with biased sex ratios: 
certain transferrin genotypes are associated with an excess of males 
in M. pennsylvanicus (Myers and Krebs, 1971). The mechanism by 
which transferrin, or loci linked to transferrin, and sex ratio are 
associated is unknown. 


Parental Behavior at Parturition and during 
Postnatal Development 


In M. ochrogaster, both parents clean up afterbirth and groom 
young (Fitch, 1957; Thomas and Birney, 1979). In some cases, 
post-partum breeding, which is common in some microtine rodents 
(Gustafsson et al., 1980; Kirkpatrick and Valentine, 1970; Lee and 
Horvath, 1969; Lee et al., 1970; Morrison et al., 1976), occurs 
before parturition is complete (Richmond and Conaway, 1969). 

Wilson (1982) demonstrated that M. ochrogaster pups receive 
more bodily contact than M. pennsylvanicus pups. She hypothesized 
that these differences in social environments during early develop- 
ment could have important effects on adult social systems (for re- 
views, see Madison, 1980; Thomas and Birney, 1979). 


The Postnatal Period 


Postnatal Growth 


Hoffmeister and Getz (1968) provided a detailed description of 
growth and age-classes in M. ochrogaster. The descriptions included 
five external, eleven cranial, and two limb measurements, eye-lens 
weight, and closure of sutures. Most growth and development oc- 
curs in the first 2 months. A summary of growth patterns from 
birth to 1 year of age in laboratory colonies of M. pennsylvanicus, 
M. oeconomus, M. miurus, and M. abbreviatus is provided by Mor- 
rison et al. (1977). 

The average rate of growth between parturition and day 21 of 
postnatal development is 1.1 g/day in M. calzfornicus (Selle, 1928) 
and 1.0 g/day in M. montanus (Bailey, 1924); the mean adult weight 
for these two species are 50.1 g (Selle, 1928) and 50.0 g (Bailey, 
1924), respectively. Lochmiller et al. (19825) found that between 
days 22 and 46, M. pinetorum gained an average of 0.8 g/day; they 
concluded that the metabolic efficiency of M. pinetorum was high 


Ontogeny 271 


TABLE 8 
PRENATAL SEX RATIOS (64:22) IN NATURAL POPULATIONS OF Microtus breweri AND 
M. pennsylvanicus IN EASTERN MASSACHUSETTS 


Expected 

Species Observed ratio ratio* pet 
Microtus brewert 

Muskeget 

Island 41:25 (1.64:1) 36:30 1531 PF > 0.05) 

M. pennsylvanicus 

Plymouth Lod? (33i1) Los 0.14 (P > 0.05) 

Natick 22:4 (5:5:1) 14:12 9.90 (P < 0.005) 


* Expected ratios were based on number of adult males and females. For M. 
breweri, 54.5% of live-trapped voles were males (Tamarin, 1977), and for M. penn- 
sylvanicus, 53% were males (Myers and Krebs, 1971). 


relative not only to other species of Microtus but also to other rep- 
resentative rodents. 

The average rate of growth in the first 21 days obscures changes 
in the growth rate during development (Fig. 3). In some species 
(M. pennsylvanicus, for example), the growth rate remains rela- 
tively constant throughout the first 21 days of postnatal develop- 
ment. The mean growth rate is 0.38 g/day (SD = 0.07) (Innes and 
Millar, 1979). In other species, the growth curve appears to be 
biphasic; the growth rate in early development is higher than in 
later development. In M. californicus, for example, the average 
growth rate is 1.07 g/day (SD = 0.17) from parturition to day 7 
and 0.76 g/day (SD = 0.20) from day 8 to day 21 (Hatfield, 1935). 
By contrast, the pattern is reversed in at least two populations of 
M. ochrogaster (Kruckenberg et al., 1973; Lee and Horvath, 1969); 
that is, the growth rate in early development is lower than in later 
development. From parturition to day 10, for example, the mean 
growth rate is 0.58 g/day (SD = 0.9), whereas from day 11 to day 
14 the mean growth rate is 1.45 g/day (SD = 0.57) (Lee and Hor- 
vath, 1969). A similar pattern occurs in M. oregoni (Cowan and 
Arsenault, 1954) and in some populations of M. pennsylvanicus 
(Hamilton, 1941). The age at which the change in growth rate 
occurs also varies. The change occurs between days 12 and 13 in 
M. ochrogaster, between days 7 and 8 in M. californicus, and days 
10 and 11 in M. pennsylvanicus. The change invariably occurs, 
however, when pup weight is between 8 and 10 g. The significance 


272. Nadeau 


WEIGHT (g) 


. breweri 
. pennsylvanicus 


. ochrogoster 
_ californicus 


. gapperi 


2. 4¢ 6 8 10 l2 14 16 I8 20 
DAY OF POSTNATAL DEVELOPMENT 


Fic. 3. Patterns of postnatal growth in representative New World Microtus. The 
pattern for Clethrionomys gapperi is presented for comparison. Data are from the 
following sources: Microtus brewer: (P. H. Kohn, J. H. Nadeau, and R. H. Tamarin, 
pers. comm.); M. pennsylvanicus (Innes and Millar, 1979); M. californicus (Hatfield, 
1935); M. ochrogaster (Kruckenberg et al., 1973). 


Ontogeny 273 


of these patterns is not known. Because descriptions of the stages 
of development of these three species were not published, it is im- 
possible to determine whether the change in growth rate is related 
to the appearance of a particular developmental character or reflects 
an adaptation to particular demographic or environmental condi- 
tions. 


Postnatal Development 


Data on postnatal development in New World Microtus are sum- 
marized in Table 9. In addition, Pépin and Baron (1978) described 
the development of locomotor activity during postnatal development 
of M. pennsylvanicus. Three stages were recognized: 1) the nest 
stage (days 0 to 7), characterized by random movements; 2) a tran- 
sitional stage (days 8 to 10), in which crawling was first observed 
and pups first left the nest; and 3) third stage (days 11 to 21), in 
which coordination of movement was refined. 


Postnatal Mortality 


Postnatal mortality is usually calculated by comparing the num- 
ber of young at week ¢ and the number of lactating females at week 
t — 3. Death, emigration, or immigration of mothers or young, and 
unrecognized pregnancies can influence these calculations. In M. 
townsendii, approximately 7.5% of young are lost before recruitment 
(Anderson and Boonstra, 1979). The loss occurs primarily in litters 
of average size. Of the entire litters that are lost, 13.6% are lost 
during the first week of lactation and 9.1% are lost during each of 
the next two weeks. Mortality often depends upon season. In M. 
ochrogaster, for example, the ratio of juveniles to pregnant females 
ranges from 0.69 in spring to 2.85 in fall (Cole and Batzli, 1978). 
It should be noted that this ratio is subject to a number of other 
influences such as emigration (see section on sex ratios above). 


Molting 


New World Microtus have two molts, a juvenile molt and an 
adult molt. There is considerable variation in the timing of these 
molts. Ecke and Kinney (1956) studied the molting pattern during 
the development of M. californicus collected in the field. The first 
or juvenile molt occurred at 23-25 days after parturition when pups 


274 Nadeau 


TABLE 9 


POSTNATAL DEVELOPMENT IN NEW WoRLD Microtus 


Day of 
development 
character 
Character appears 
Gray or black 1 
dorsum and 
pink ventrum 
Brown fur Z 
3 
5 
Incisors 1-2 
emerge 
3-6 
5 
See) 
6-7 
Molars 7 
emerge 8 
115 
Crawl 3-4 
4-5 
6.5 
9 
Eyes open -6 
5-10 
8-11 
(7.1-8.9 g) 


<s 


M. 


SS S585 


S S SS SSS 5885 SSSSEES 


Species 


. breweri 
. californicus 
. ochrogaster 


. oregoni 


pennsylvanicus 


breweri 


. ochrogaster 


caltfornicus 
oregont 
pennsylvanicus 
montanus 


ochrogaster 


brewert 
montanus 
oregonti 
pennsylvanicus 


montanus 
pennsylvanicus 
oregon 


breweri 


. ochrogaster 


. oregont 


. pennsylvanicus 


. brewert 
. ochrogaster 


montanus 


References 


Rothstein (1976) 

Hatfield (1935) 

Richmond and Conaway 
(1969) 

Cowan and Arsenault (1954) 

J. H. Nadeau, P. H. Kohn, 
and R. H. Tamarin, 
(pers. comm.) 


Rothstein (1976) 

Fitch (1957) 

Hatfield (1935) 

Cowan and Arsenault (1954) 
Hamilton (1941) 

Bailey (1924) 


Fitch (1957); Kruckenberg 
et al. (1973) 

Rothstein (1976) 

Bailey (1924) 

Cowan and Arsenault (1954) 

Hamilton (1941) 


Bailey (1924) 
Hamilton (1941) 
Cowan and Arsenault (1954) 


Rothstein (1976) 

Fitch (1957); Richmond and 
Conaway (1969) 

Cowan and Arsenault 
(1954) 

J. H. Nadeau, P. H. Kohn, 
and R. H. Tamarin (pers. 
comm.) 

Rothstein (1976) 

Fitch (1957); Kruckenberg 
et al. (1973); Lee and 
Horvath (1969) 

Bailey (1924); Fitch (1957); 
Jannett (1978); Krucken- 
berg et al. (1973); Rich- 
mond and Conaway (1969) 


Character 


Ontogeny 21D 


References 


Pinnae unfold 


Eat solid food 


Weaning 


TABLE 9 
CONTINUED 
Day of 
development 
character 
appears Species 
8-9 M. pennsylvanicus 
(10.2 g) 
9-10 M. californicus 
(8.3-11.4 g) 
9 M. oeconomus 
(7.3 g) 
10-11 M. oregoni 
12 M. pinetorum 
(7.0 g) 
1 M. breweri 
2-3 M. ochrogaster 
M. pennsylvanicus 
2D) M. oregoni 
8 M. pennsylvanicus 
10-14 M. ochrogaster 
8-9 M. breweri 
11-14 M. pennsylvanicus 
(15 g) 
12-17 M. montanus 
(10.7-13.1 g) 
13 M. oregoni 
14 M. californicus 
(14 g) 
15-17 M. montanus 
(11.9-13.1 g) 
17 M. pinetorum 
(11 g) 


11.9-18.4 g M. ochrogaster 


Hamilton (1937, 1941); Innes 
and Millar (1979, 1981) 

Greenwald (1956); Hatfield 
(1935); Selle (1928) 

Morrison et al. (1954) 


Cowan and Arsenault (1954) 
Hamilton (1938) 


Rothstein (1976) 

Kruckenberg et al. (1973) 

J. H. Nadeau, P. H. Kohn, 
and R. H. Tamarin (pers. 
comm.) 

Cowan and Arsenault (1954) 


Hamilton (1941) 
Richmond and Conaway 
(1969) 


Rothstein (1976) 

Hamilton (1937, 1941); Innes 
and Millar (1979, 1981); 
Lee and Horvath (1969) 

Bailey (1924); Fitch (1957); 
Jannett (1978); Krucken- 
berg et al. (1973); Rich- 
mond and Conaway (1969) 

Cowan and Arsenault (1954) 

Greenwalt (1956); Hatfield 
(1935) 

Fitch (1957); Kruckenberg 
et al. (1973); Jannett (1978) 

Hamilton (1938) 


Cole and Batzli (1979) 


276 Nadeau 


were 110 to 120 mm long and was complete by day 45. The second 
or adult molt began by day 50 and was complete by day 60. The 
first molt in M. pinetorum begins by day 35 and the second at day 
50 (Hamilton, 1938). In M. ochrogaster, the first molt begins be- 
tween day 21 and day 28 and the second molt between day 40 and 
day 84 (Jameson, 1947; Richmond and Conaway, 1969). In M. 
californicus, the first molt begins by day 21 and the second by day 
56 (Hatfield, 1935). In M. breweri, the first molt occurs when mice 
are 136-150 mm long and the second when mice are 161-165 mm 
long (Rowsemitt et al., 1975). Many of these studies also described 
the pattern of molting. 


Sexual Maturation 


Spermatogenesis in New World Microtus has not been studied, 
but it was described in at least one species of Old World Microtus 
(Grocock, 1972). On day 1 after parturition, only gonocytes and 
supporting cells are found in the seminiferous tubules. On day 3 
spermatogonia are found, on day 12 primary spermatocytes, and 
on day 24 round spermatids. The first meiotic divisions begin on 
day 21 and mature spermatozoa are first found on day 37. 

The criterion usually used for determining sexual maturity in 
males is the presence of mature sperm in the epididymis. The weight, 
but not necessarily the age, at which male New World Microtus 
become sexually mature appears to be similar among species. Ma- 
turity is attained at 35-41 g in M. californicus (Greenwald, 1956; 
Hoffmann, 1958), at 35 g in M. montanus (Hoffmann, 1958), at 
25-35 g in M. pennsylvanicus (Hamilton, 1937; Lee and Horvath, 
1969), and at 30 g in M. townsendu (MacFarlane and ‘Taylor, 
1981). Males first mate at 42 days of age in M. californicus (Hat- 
field, 1935) and at 6-8 weeks in M. pinetorum (MacFarlane and 
Taylor, 1981). M. pinetorum first sire at 52 days of age, but the 
average age is 60 days (Schadler and Butterstein, 1979). 

In females, the presence corpora lutea, embryos, or lactation tis- 
sue is evidence for sexual maturity. On the average, females become 
sexually mature at 25-35 g in M. californicus (Greenwald, 1956; 
Hoffmann, 1958), at 33 g in M. montanus (Hoffmann, 1958), at 
25 g in M. pennsylvanicus (Hamilton, 1937), at 70-100 g in M. 
richardsoni (Anderson et al., 1976), and at 25-45 g in M. townsend 
(MacFarlane and Taylor, 1981). It should be noted that, because 


Ontogeny Dill, 


adult weight varies considerably between these species, comparisons 
of weights at sexual maturity may not be particularly informative. 
In M. ochrogaster females, the first mating occurs at 33-34 days of 
age but the first litter is not produced until females are 60 days old 
(Richmond and Conaway, 1969). Cole and Batzli (1979) found that 
female M. ochrogaster first reproduce at 81-100 days of age. Fitch 
(1957) reported M. ochrogaster females that were pregnant at 4 
weeks of age and Beer et al. (1957) found M. pennsylvanicus fe- 
males that bred at 25 days of age. Schadler and Butterstein (1979) 
found that, although female M. pinetorum first conceive at 77 days 
of age, the average age at first conception was 105 days. Sterile 
matings (usually the first mating) have been described in M. oecon- 
omus (Hoyte, 1955), M. californicus (Greenwald, 1956), M. pine- 
torum (Kirkpatrick and Valentine, 1970), and M. pennsylvanicus 
(Mallory and Clulow, 1977). 

In M. montanus, the age and weight at sexual maturity in females 
varies considerably between years (Negus et al., 1977). In some 
years, most females become sexually mature at 13-14 g, with the 
lowest weight at pregnancy of 18 g. In other years, females became 
sexually mature at 24-29 g, with the lowest weight at pregnancy 
of 30 g. The estimated age at sexual maturity was 2-3 weeks in 
some years and 7-8 weeks in others. 

The age at which females become sexually mature depends on 
a number of factors including nutrition and social conditions. 
Greenwald (1956) and Negus and Pinter (1966) showed that sexual 
maturation in M. montanus is significantly influenced by diet. Social 
factors are also important. In M. ochrogaster, the vagina opens ear- 
lier and the first litter is born sooner when females are paired with 
adult males than when paired with male littermates (Hasler and 
Nalbandov, 1974). 


Synthesis 


One of the more useful ways to evaluate these diverse ontogenetic 
attributes as part of a species’ “ecological strategy” involves r- and 
K-selection. According to the theory of r- and K-selection (Mac- 
Arthur and Wilson, 1967), attributes such as occurrence in uncer- 
tain climates and high productivity are typical of r-selected species, 
whereas occurrence in more certain climates and high efficiency are 


278 Nadeau 


typical of K-selected species (Pianka, 1970; Southwood et al., 1974). 
There are several reasons for applying the theory of r- and K-se- 
lection to ontogenetic data for New World Microtus. First, r- and 
K-selection is one of the few theories that combines ontogeny and 
reproduction into a single argument. Second, and perhaps more 
importantly, it has been argued that the strength of population 
cycles in microtine rodents depends in part on the location of a 
species’ overall ecological strategy on an r-K continuum (Tam- 
arin, 1978). Although there are difficulties in its application and 
evaluation, the theory was nevertheless applied to the ontogenetic 
data for New World Microtus to determine whether the ontogenetic 
attributes are consistent with the theory of r- and K-selection. 
Only those species and ontogenetic attributes were included that 
provided the most complete set of data for analysis. This set con- 
sisted of six species and four attributes. For each species, the char- 
acter of each attribute was identified as being that expected of an 
r-selected species, or alternatively, that of a K-selected species. 
r-Selected species were expected to have high rates of prenatal mor- 
tality, low neonatal weights, large litter sizes, and high rates of 
postnatal development; K-selected species were expected to have 
converse attributes (Pianka, 1970; Southwood et al., 1974). To de- 
termine whether a particular attribute in a given species was more 
r- or more K-selected relative to the same attribute in other species, 
the following procedure, which is illustrated with the data for neo- 
natal weight, was used. If more than one estimate of neonatal weight 
was available for a species, an average weight was calculated. An 
average for all species was then calculated. If less than the mean 
weight for all species, the weight for a given species was considered 
to be r-selected, whereas if the weight was greater than the mean 
weight for all species, the weight for a given species was considered 
to be K-selected. This procedure was also applied to data for litter 
size. For prenatal mortality and postnatal development, modifica- 
tions in this procedure were necessary. For estimating the rate of 
prenatal mortality, the sum of the rates of pre-implantation and of 
post-implantation mortality was calculated for each species. These 
sums were then used to calculate a mean rate for all species and to 
assign the r or K status for each species as described above. For the 
rate of postnatal development, each species was given a score cor- 
responding to the time of appearance of a given developmental 
feature, such as emergence of incisors; a low score corresponded to 


Ontogeny 279 


TABLE 10 
R-K PROFILE OF CERTAIN ONTOGENETIC ATTRIBUTES IN SELECTED SPECIES OF NEW 
WORLD Microtus 


Rate of 
Prenatal Neonatal Litter postnatal 
Species mortality weight size development 

Microtus brewert r K K r 
M. montanus K K r r 
M. ochrogaster K K K r 
M. oregoni — r K K 
M. pennsylvanicus r r r K 
M. pinetorum — r K K 


early appearance, a high score to later appearance, and a tie score 
to similar times of appearance. The developmental features includ- 
ed appearance of fur, emergence of incisors, emergence of molars, 
crawling, opening of eyelids, unfolding of pinnae, and weaning. For 
each species an average of these scores was calculated and these 
averages were used as described above to determine the r or K status 
for each species. 

Results of the analysis are presented in Table 10. If each attri- 
bute is assumed to contribute equally to a species ecological strategy, 
then none of the species included in the analysis were uni- 
formly r-selected or uniformly K-selected. Species such as M. brewer 
and M. pinetorum, which are thought to be among the more K-se- 
lected species of Microtus, were r-selected for certain attributes. By 
contrast, other species such as M. pennsylvanicus, which is thought 
to be relatively r-selected, was K-selected for certain attributes. 
There are at least two complementary explanations for the absence 
of uniformity. The first involves the assumption that each of these 
four attributes contributes equally to a species ecological strategy. 
It is more likely that some attributes are more important than oth- 
ers. Litter size, for example, is certainly more important than pre- 
natal mortality, because the rate of prenatal mortality is only one 
of several factors determining litter size; litter size is therefore a 
composite measure of several attributes. Indeed, litter size shows 
the expected pattern of r- and K-selection (Table 10). Likewise, 
neonatal weight is a composite attribute determined by both the 
rate of growth and length of gestation. Determining the relative 


280 Nadeau 


importance of each of these ontogenetic attributes to a species’ eco- 
logical strategy represents an important problem to be studied. 
The second explanation for the absence of uniformity involves 
differences in the response of attributes to selection. Schaffer and 
Tamarin (1973) have shown that when an organism encounters an 
ecological challenge, the attribute responding most rapidly to selec- 
tion will be used to meet the challenge. Among Muicrotus and many 
other species, litter size is thought to be one of the diagnostic fea- 
tures of a species’ location on the r-K continuum. According to 
Schaffer and Tamarin’s argument, litter size is one of the attributes 
responding most rapidly and perhaps most often to selection. 


Summary 


Despite the extensive literature on certain aspects of the ontogeny 
of New World Microtus, much remains to be learned. The list of 
undescribed processes and unanswered questions is very long: there 
is no published description of the prenatal development of any New 
World Microtus; the factors determining the rates of prenatal and 
postnatal growth, development, and mortality remain to be identi- 
fied; the significance of migratory giant cells and interspecific vari- 
ation of litter size are unknown. In summary, although we recog- 
nize the distinguishing characteristics of New World Microtus, we 
have very little knowledge about the ontogenetic processes by which 
these characteristics are produced. In other words, we can describe 
Microtus but we know little about how growth and development 
occur. Until some of these problems are solved, the relationship 
between ontogenetic variation and phylogenetic diversity in New 
World Microtus will remain obscure. 


Acknowledgment 


This work was supported by general funds of the Jackson Lab- 
oratory. 


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284 Nadeau 


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HABITATS 
LOWELL L. GETZ 


Abstract 


N North America members of the genus Microtus are generally 
I associated with habitats dominated by graminoid vegetation. 
Species that occur in forested areas are frequently restricted to grassy 
clearings or to sites in which there is an understory of grasses or 
sedges. M. xanthognathus, M. longicaudus, and M. richardsoni are 
found in coniferous forests, but are most abundant where there is 
at least some grassy vegetation present on the forest floor. Another 
forest species, M. oregoni, is most often found in forest clearings 
dominated by forbs; that is, in early successional stages in clearcut 
forest sites. 

Microtus pinetorum, M. oaxacensis, M. umbrosus, and M. guate- 
malensis commonly occur in forested habitats where there is little 
graminoid vegetation; but M. pinetorum is also abundant in or- 
chards where it may be associated with dense grassy cover. M. 
chrotorrhinus is characteristically found in rocky talus within decid- 
uous and coniferous forests, but occurs in grassy balds in the south- 
ern Appalachians. 

Most species of Microtus are associated with mesic or wet habi- 
tats; several species occur in marshes or other wet areas where the 
voles readily enter the water and swim. Only M. mexicanus is rou- 
tinely found in arid habitats. Other species, including M. montanus, 
M. longicaudus, M. californicus, and M. townsendi are found in 
well-drained and sometimes arid habitats as well as in wet places. 
Individuals that occur in arid habitats, well-drained mesic sites, or 
in salt marshes obtain their water from the green vegetation upon 
which they feed. 

Graminoid vegetation serves both as the primary cover and as 
the major food source for most species of Microtus. Whether the 
voles construct underground or surface nests, most Microtus traffic 
occurs on the soil surface; however, M. pinetorum and M. parvulus 
are subfossorial, constructing tunnels 2-3 cm below the surface. 
Where the vegetation growth is sufficiently dense, voles frequently 

286 


Habitats 287 


make well-formed surface runways through the green vegetation or 
dead surface litter. 

Most species of Microtus feed on green vegetation; seeds, roots, 
dead vegetation, and insects may be eaten when green vegetation is 
not available. Although some species (for example, M. ochrogaster) 
may require forbs in their diet, most species feed extensively on 
grasses and sedges. 

Few species of Microtus are associated with agricultural situa- 
tions in North America. The frequent disturbance of vegetative 
cover during tillage and harvesting activities renders agro-ecosys- 
tems unsuitable habitats for most species of Microtus. Some species 
may become abundant in unharvested forage crops (alfalfa, clover 
and timothy). Major vole (primarily M. montanus) “outbreaks” in 
agricultural systems in North America occurred in Nevada and 
California in 1906-1908 and throughout the western United States 
in 1957-1958. 


Introduction 


Descriptions of the habitats utilized by the various species of 
Microtus are scattered throughout the literature. Most such infor- 
mation is included as anecdotal or descriptive accounts in papers 
dealing with geographic distributions, regional species lists, or pop- 
ulation studies. Relatively few studies concentrate specifically on 
factors responsible for occurrence of a species in given habitat types. 
In addition, because of the focus of different studies on specific 
habitat types, there are often conflicting conclusions as to the re- 
sponses of a species to a particular habitat feature, such as vege- 
tation type, cover conditions, and moisture regime. Since many 
species of Microtus are capable of utilizing rather wide ranges of 
habitat conditions, availability of information from a limited array 
of sites located in different regions complicates generalizations con- 
cerning habitat requirements of a species. That most species of 
Microtus display frequent (“‘periodic’’) fluctuations in abundance 
further confuses recognition of their preferred habitats. At times of 
regionally high population densities, individuals of a species may 
be crowded out of preferred habitats and be found (albeit tempo- 
rarily) in relatively high numbers in otherwise marginal habitats. 
There is seldom information as to phase of the local population 
cycle at the time of a given study or observation. 


288 Getz 


The primary approach of this review is, therefore, to emphasize 
specific habitat features with which given species have been asso- 
ciated rather than to enumerate the various specific habitat types 
utilized by each species. The latter approach would require lengthy 
accounts of habitats in which a species has been found throughout 
its range. Table 1 lists the primary references used to categorize 
the habitats of each species. Although these references are not all- 
inclusive, they provide details of specific situations or general sum- 
maries of habitat utilization of given species. Other references are 
cited where appropriate within the text. 

I grouped the species of Microtus in regard to what appears to 
be their most generalized responses to specific habitat factors. Species 
with a wide range of responses appear in more than one category. 
Wherever possible I included the range of response of a species to 
given habitat factors. In addition, I rank-ordered responses of sym- 
patric species to habitat factors whenever comparative data were 
available. A section on competitive exclusion addresses in a more 
analytical manner comparative responses of sympatric species to 
given habitat factors. 


Habitat Factors 


The habitat factors that appear most important in influencing 
local distribution of Microtus are: vegetation type, moisture condi- 
tions, and amount of cover. 

Herbaceous vegetation has a dual role as a habitat factor: pro- 
vision of both food and cover. The diet of most species of Microtus 
comprises primarily green vegetation. New growth, inflorescences 
or seed heads are the preferred parts of plants. Where the vegetation 
is dense, voles normally must cut the stems into numerous short 
segments so as to get to the upper parts of the plants. Piles of 4 to 
6-cm long clippings of grass and other plant stems indicate the 
presence of voles. 

Species occupying habitats in which green vegetation is seasonally 
absent or reduced in quantity (for example, in winter or dry season) 
may feed on dead plant material, seeds, roots, or on insects and 
other small animals during the period when green vegetation is not 
available. A few species (for example, M. pinetorum, M. caltfornicus, 
M. pennsylvanicus, and M. ochrogaster) feed on the bark of young 
trees in forestry plantations or on the bark and roots of orchard 


TABLE 1 


SELECTED REFERENCES PROVIDING IINFORMATION ABOUT HABITATS OF SPECIES OF 


<5 S55 SSS55 


<5 


M 


= 5° = 5 


SS SSS8ES8 


Species 


. abbreviatus 

. breweri 

. californicus 

. canicaudus 

. chrotorrhinus 


. coronarius 
. guatemalensis 
. longicaudus 


. ludovicianust 
. mexicanus 


. miurus 
. montanus 


. nesophilust 
. oaxacensis 
. ochrogaster 
. oeconomus 
. oregon 


parvulus 


. pennsylvanicus 


. pinetorum 


. quasiater 
. richardsoni 


. townsendit 


. umbrosus 
. xanthognathus 


+ Extinct. 


Miucrotus 


References 


Rausch and Rausch (1968) 

Tamarin and Kunz (1974) 

Ingles (1965); Krebs (1966) 

See references for M. montanus 

Goodwin (1929); Hamilton and Whitaker (1979); Kirk- 
land (1977a, 19776); Kirkland and Knipe (1979); Martell 
and Radvanyi (1977); Timm et al. (1977) 

Swarth (1911) 

Smith and Jones (1967) 

Borell and Ellis (1934); Dalquest (1948); Findley (1951); 

Findley and Jones (1962); Hall (1946); Ingles (1954, 1965); 

Ivey (1957) 

Lowery (1974) 

Baker and Phillips (1965); Brown (1968); Da- 
vis (1944, 1960); Davis and Robertson (1944); Davis and 
Russell (1954); Findley and Jones (1962); Hall and 
Dalquest (1963); Koestner (1944) 

Osgood (1901); Peterson (1967); Quay (1951) 

Borell and Ellis (1934); Dalquest (1948); Findley (1951); 
Findley and Jones (1962); Hall (1946); Hoffmann et 
al. (1969); Ingles (1965) 

Miller (1899) 

Goodwin (1969); Jones and Genoways (1967) 

Hamilton and Whitaker (1979); Jackson (1961) 

Peterson (1967); Quay (1951) 

Dahlquest (1948); Gashwiler (1972); Ingles (1965); Sullivan 
(1981) 

Howell (1916); Neill and Boyles (1955) 

Dalquest (1948); Getz (1961, 1970); Hamilton and Whita- 
ker (1979); Harris (1953); Jackson (1961); Peter- 
son (1966); Woods et al. (1982) 

Barbour and Baker (1950); Benton (1955); Davis (1960); 
Fisher and Anthony (1980); Glass and Halloran (1961); 
Hamilton and Whitaker (1979); Hanson (1944); Jack- 
son (1961); Jameson (1949); Lowery (1974); Mil- 
ler (1964); Miller and Getz (1969); Peterson (1967) 

Davis (1944) 

Dalquest (1948); Findley (1951); Hooven (1973); In- 
gles (1965); Wright (1950) 

Cowan and Guiguet (1965); Dalquest (1940, 1948); In- 
gles (1965) 

Goodwin (1969) 

Lensink (1954); Wolff and Lidicker (1980) 


289 


290 Getz 


trees. In general, however, food in the form of herbaceous vegetation 
is a necessary habitat requirement for most species of Microtus. 
Food habits may be involved in the preference of some species (for 
example, M. ochrogaster) for habitats with forbs; graminoid vege- 
tation alone may not fulfill the dietary requirements of the species 
(Cole and Batzli, 1978). 

Except for the subfossorial Microtus pinetorum, M. parvulus and 
perhaps M. chrotorrhinus, voles are active on the surface. In habitats 
where the vegetation is dense, voles usually construct distinct sur- 
face runways through the base of the vegetation or in the detritus. 
The greater the vegetation and detritus cover, the more protected 
are the runways. In habitats with sparse or more open vegetation 
growth, voles may form “paths” on the surface, or may move more 
randomly through their home ranges (personal observations in marsh 
habitats in Michigan, Wisconsin, and Connecticut, and in tall grass 
prairie and alfalfa habitats in Illinois). 

The more dense the vegetation cover, the greater the protection 
of voles from predators, especially from avian predators (Birney 
et al., 1976). Vegetation cover also moderates the microclimate (hu- 
midity and temperature) of the site (Getz, 1965, 1970, 1971). The 
more dense the vegetation cover, the greater the moderation of the 
microclimate, thus reducing potential temperature and moisture 
stresses upon voles. Protection from predation appears more likely 
to contribute to higher numbers of voles in dense vegetation. Mi- 
croclimatic stresses have not been shown to be sufficient to account 
for differences in local distribution in those species for which data 
are available (Getz, 1971). 

Most species of Microtus occur in mesic or wet habitats. Although 
water balance of few species has been studied, kidney inefficiency 
appears to be a major reason for restriction to mesic or wet areas 
(Getz, 1963). Evaporative water losses at humidities encountered 
in even drier, more sparsely vegetated sites do not place a significant 
stress on the water balance of voles (Getz, 1970, 1971). 

In mesic areas where standing water is not available, voles get 
water (preformed water) when eating green vegetation. Succulent 
vegetation associated with moist habitats is a likely reason for the 
positive responses of Microtus to soil moisture conditions. M. penn- 
sylvanicus living in salt marshes obtain their water from the green 
sedges upon which they feed (Getz, 1966). 


Habitats 291 


Responses to Habitat Features 


In this section the various habitat types occupied by the genus 
Microtus are grouped according to those factors most important in 
determining local distributions. The species are placed in the hab- 
itat type with which they are most commonly associated; specific 
responses to the major features of each habitat type are discussed 
where appropriate. 

Some species have very limited geographic ranges, such as M- 
crotus brewert, M. umbrosus, M. coronarius, and M. abbreviatus. Mi- 
crotus nesophilus and M. ludovicianus were also localized in distri- 
bution; both are now extinct. In addition, little habitat information 
has been presented for M. quasiater, M. oaxacensis, M. guatemalen- 
sis, and M. canicaudus. M. canicaudus has been separated only re- 
cently from M. montanus (Hsu and Johnson, 1970); I assume hab- 
itat requirements of M. canicaudus to be similar to those of M. 
montanus (given the potential habitat types within its range). I 
included the above species in the appropriate categories wherever 
possible; in most cases, however, little elaboration can be made in 
regard to their habitat requirements. 


Vegetation Types 


Species of Microtus occur from the Lower Sonoran (M. montan- 
us) to the Arctic (M. oeconomus, M. coronarius, and M. miurus) life 
zones. Species associated with forested life zones (Hudsonian, Ca- 
nadian, and Transition) are restricted for the most part to herba- 
ceous forest clearings. 

Graminoid habitats.—Grasslands and sedge marshes constitute the 
predominant Microtus habitats (Table 2); graminoid habitats uti- 
lized by species of Microtus range from relatively sparse, arid grass- 
lands to densely vegetated salt and freshwater marshes. Tempera- 
ture regimes of the grasslands inhabited by Muicrotus range from 
hot southern grasslands to the cold tundra. 

Species associated with herbaceous vegetation consisting mainly 
of grasses or sedges include Microtus pennsylvanicus, M. nesophilus, 
M. abbreviatus, M. miurus, M. oeconomus, M. montanus, M. ludovi- 
cianus, M. mexicanus, and M. townsendiu. Other species (M. ochro- 
gaster, M. californicus, M. longicaudus, M. quasiater, and M. brewer) 
are abundant in grasslands which also may include considerable 


292 Getz 


TABLE 2 
VEGETATION TYPES WITH WHICH SPECIES OF Microtus ARE 
COMMONLY ASSOCIATED 


Graminoids 
M. abbreviatus M. muurus 
M. brewer M. montanus 
M. caltfornicus M. nesophilust 
M. canicaudus M. ochrogaster 
M. coronarius M. oeconomus 
M. longicaudus M. pennsylvanicus 
M. ludovicianust M. quasiater 
M. mexicanus M. townsendu 
Forbs 
M. chrotorrhinus M. oregoni 
M. longicaudus 
Wooded 
Scrub or shrubs 
M. canicaudus M. montanus 
M. longicaudus M. parvulus 
M. mexicanus 
Deciduous (broadleaf) forests 
M. oaxacensis M. quasiater 
M. pinetorum M. umbrosus 
Coniferous forests 
M. coronarius M. richardson 
M. guatemalensis M. xanthognathus 


M. longicaudus 


+ Extinct. 


quantities of forbs or short woody shrubs. Although commonly as- 
sociated with stream banks in forested areas, M. richardsoni is found 
most often in graminoid vegetation along streams or in grassy alpine 
meadows. M. pennsylvanicus appears to avoid habitats in which 
there are large numbers of woody plants in addition to graminoid 
vegetation. 

Grassland sites do not necessarily have to be extensive or contig- 
uous to be inhabited by some species of Microtus (see below). M. 
mexicanus, M. montanus, M. longicaudus, M. quasiater, M. richard- 
son, and M. pennsylvanicus are commonly found in small, dis- 
persed, grassy habitat patches or in small isolated alpine meadows 
within otherwise forested areas. 


Habitats 293 


Other herbaceous habitats.—Few species occur exclusively in non- 
graminoid herbaceous habitats. Microtus oregoni occurs in redwood, 
fir, spruce, and hemlock forests where there is herbaceous vegetation 
(for example, in small clearings). M. oregonz is especially abundant 
in early successional clearcut timber sites where bracken fern and 
fireweed, as well as grasses, predominate. The species drops out 4 
to 5 years after logging, when grasses and forbs are shaded out by 
woody sprouts of deciduous and coniferous trees (Sullivan, 1981). 
M. chrotorrhinus also is associated with clearcut forest areas in West 
Virginia (Kirkland, 1977a). 

In Kentucky, Microtus pinetorum has been found in abandoned 
fields in which the dominant vegetation is a mixture of Rubus and 
Andropogon. M. longicaudus is less dependent upon the presence of 
grasses than are most other species, but the species normally is 
associated with graminoid habitats. M. pennsylvanicus may occur 
in Sphagnum mats, even where grasses or sedges are relatively scarce. 
M. coronarius extends into forested areas where there is a thick 
mossy mat, and few, if any, grasses or sedges. 

Wooded habitats.—A few species inhabit grassy areas with an 
overstory of small trees and shrubs. In eastern Washington, Micro- 
tus longicaudus is abundant where C7vataegus spp. and other shrubs 
are the dominant plants (Beck and Anthony, 1971; Randall and 
Johnson, 1979); elsewhere the species has been observed in scrub 
oak, sage brush, and in willow, alder, and aspen thickets (Borell 
and Ellis, 1934; Hall, 1946; Ingles, 1965). M. montanus has been 
captured in open aspen where the ground cover was sparse. At high 
population densities, M. montanus may extend from its character- 
istic grassy habitats out into shrub-dominated habitats (sometimes 
replacing M. longicaudus where the two species are sympatric; see 
below). M. mexicanus has been recorded from pinon, juniper, and 
yellow-pine habitats (Findley and Jones, 1962; Koestner, 1944). 
M. parvulus has been found in the ecotone between shrubby areas 
and pine stands. M. quasiater also occurs in wooded habitats. 

The author trapped Microtus pennsylvanicus in isolated shrub- 
dominated deciduous forest clearings with a grass understory in 
New England. These appeared to represent remnants of popula- 
tions of M. pennsylvanicus occupying once more extensive grassy 
clearings that were undergoing succession back to a forest. 

Microtus pinetorum is characteristic of mature deciduous forests. 
Although it may occur in young pine plantations where grass is the 


294 Getz 


dominant vegetation (Sartz, 1970), the species is not an inhabitant 
of mature pine forests. Forest types occupied by M. pinetorum range 
from mesic beech forests with well-developed litter and humus lay- 
ers to scrub oaks where litter is scarce and the humus layer poorly 
developed (Jameson, 1949; Miller, 1964; Neill and Boyles, 1955). 
Other forests types commonly occupied by M. pinetorum include 
dry beech forests, spruce-yellow birch stands and red and white oak 
forests. 

Microtus quasiater has been recorded from oak forests, but such 
sites most likely represent marginal habitats for this species. M. 
oaxacensis and M. umbrosus occur in high elevation evergreen 
broadleaf rainforests. M. mexicanus has also been recorded from 
cool wet oak forests in southern Mexico. M. pennsylvanicus may 
invade both deciduous and coniferous forests during peak density 
years (Cameron, 1964; Grant, 1971). 

Microtus xanthognathus, M. coronarius, and M. richardsoni are 
characteristic of northern coniferous forests. However, all three are 
associated most often with sites where there is at least some grami- 
noid vegetation. M. xanthognathus is found in black-spruce, white- 
spruce, birch, and aspen stands with a thick Sphagnum mat, horse- 
tail (Equisetum), or clumps of sedges. Although usually associated 
with sites dominated by herbaceous vegetation, M. oregoni has been 
found in dry coniferous forests, as well as in damp mossy sites 
within such forests. M. richardsoni is found in marshy places along- 
side streams and in wet alpine and subalpine meadows within co- 
niferous forest regions (Dalquest, 1948; Rasmussen and Chamber- 
lain, 1959); infrequently it occurs in pure forest stands. 

Microtus longicaudus has been recorded from yellow pine, lodge- 
pole pine, hemlock, white fir, and spruce forests. M. mexicanus has 
been taken in pine forests, but usually where grasses are present in 
the understory. M. guatemalenis occurs in high-elevation pine cloud- 
forests where the understory is composed of low bushes, ferns, and 
bromeliads. M. chrotorrhinus is more abundant in rocky areas in 
coniferous forest than in similar rocky sites in deciduous forests 
(Kirkland, 19775). 


Rocky Habitats 


The rock vole, Microtus chrotorrhinus, is associated primarily with 
broken rock outcrops, talus slopes and similar rocky situations. This 


Habitats 295 


species also has been found in sites where moss-covered rocks and 
logs are common (Hamilton and Whitaker, 1979; Kirkland and 
Knipe, 1979). M. chrotorrhinus usually is abundant where grasses 
are present among rocks, but it is frequently most common where 
there are dense stands of ferns. 

Microtus oregoni and M. longicaudus also are found from time to 
time in rockslides. Both species are more abundant in herbaceous 
vegetation, however. M. pinetorum has been recorded from rocky 
areas in Oklahoma, but mainly where spaces between rocks were 
covered with dense herbaceous vegetation. 


Moisture Regimes 


Most species of Microtus are associated with mesic or wet places; 
none is found exclusively in arid habitats (Table 3). Those species 
commonly found in wet habitats include M. pennsylvanicus, M. 
coronarius, M. xanthognathus, M. oeconomus, M. miurus, M. brewert, 
M. oaxacensis, and M. guatemalensis. Microtus oeconomus is found 
in the wet swales throughout the vast flat tundra; where it occurs 
on mountain slopes, M. oeconomus is most abundant in wetter sites 
(Peterson, 1966). However, on Unalaska Island M. oeconomus was 
found to avoid very marshy sites. M. miurus also inhabits the wet 
tundra region, but avoids low swales; it is most abundant on peat 
mounds, terraces, raised polygons, and on stream and lake banks 
(Quay, 1951). 

Microtus oaxacensis, M. umbrosus, and M. guatemalensis occur in 
high-elevation forests where the soil is cool and damp. 

Although a number of species of Microtus occur in well-drained 
upland habitats, most also appear in wet marshes. M. ochrogaster 
appears to be relatively uncommon in sites with standing water; M. 
abbreviatus has not been taken in standing water. M. ludovicianus 
was recorded only from “‘damp” sites. Species commonly found in 
well-drained upland sites, but which also occur in wet marshy areas 
where standing water is present, include M. californicus, M. oregon, 
M. townsendu, M. longicaudus, and the now extinct M. nesophilus. 
M. xanthognathus and M. richardsoni occur in wet areas adjacent 
to streams in forested areas; M. longicaudus also is adjacent to streams 
in some forested areas. Species occurring in coastal areas (M. penn- 
sylvanicus, M. californicus, M. townsendi, M. oregoni, and M. brew- 
eri) commonly are found in salt marshes. 


296 Getz 


TABLE 3 
So1L MOIsTURE CONDITIONS WITH WHICH SPECIES OF Microtus ARE COMMONLY 
ASSOCIATED 
Semi-arid 
M. mexicanus M. pinetorum 
M. parvulus M. quasiater 
Mesic, well-drained 
M. abbreviatus M. montanus 
M. canicaudus M. ochrogaster 
M. chrotorrhinus M. pinetorum 
M. coronarius M. umbrosus 
M. ludovicianust 
Wet, marshes 
M. breweri M. oeconomus 
M. coronarius M. pennsylvanicus 
M. guatemalensis M. richardsoni 
M. miurus M. xanthognathus 
M. oaxacensis 
Wide range of conditions, arid to marshes 
M. californicus M. oregoni 
M. longicaudus M. townsendu 


M. nesophilust 


+ Extinct. 


Most species occupying wet areas readily enter water and swim; 
swimming behavior has been observed in Microtus richardson, M. 
longicaudus, M. pennsylvanicus, M. californicus, and M. xanthogna- 
thus (Blair, 1939; Dalquest, 1948; Ingles, 1965; Johnson, 1957; 
Lensink, 1954; Murie, 1960; Peterson, 1967). M. californicus and 
M. longicaudus dive and swim underwater. M. pennsylvanicus has 
been found in marshes where only clumps of vegetation extend 
above the water (Getz, 1961). Feeding platforms and nests are built 
above water in the sedges and cattails. Individuals living in such 
marshes resemble “small muskrats’”’ (Murie, 1960) in their behav- 
ior. 

Even though species occurring in wet areas appear to be strong 
swimmers, drowning may occur during extensive inundation of salt 
marshes, as during unusually high tides associated with storms. The 
combined effects of deeper water and strong wave action may cause 
mortality among “good” swimmers. Microtus californicus and M. 


Habitats 297 


pennsylvanicus occasionally drown at such times (Hadaway and 
Newman, 1971; Harris, 1953). 

In the southwestern regions of its range, Microtus pennsylvanicus 
is restricted mainly to the hydrosere, whereas in more northern 
areas of the west the species is an inhabitant of well-drained grass- 
lands associated with deciduous and coniferous forests (Findley, 
1954). When M. pennsylvanicus is found in well-drained upland 
habitats, it usually is restricted to sites with dense vegetation cover 
(Getz, 1971; Hodgson, 1972). However, such an association does 
not appear to be related to a more humid microclimate under vege- 
tation (see above). Other species (M. ochrogaster, M. calvfornicus, 
M. montanus, M. coronarius, and M. chrotorrhinus) occupying well- 
drained upland habitats are not so restricted to sites with dense 
vegetation cover. M. chrotorrhinus usually is found in crevices be- 
tween and under rocks and boulders; this microhabitat is relatively 
mesic, even though well drained. The importance of microclimate 
upon the occurrence of M. chrotorrhinus in rocky habitats is not 
known. 

Microtus mexicanus, M. pinetorum, and M. parvulus usually are 
associated with drier habitats than are other species of Mucrotus. 
M. mexicanus commonly is found in arid, sparsely vegetated habi- 
tats, including pinon, yellow pine, juniper, rabbit brush, and dry 
bunch grass. In other places, however, the species is abundant in 
mesic meadows within high-elevation coniferous forests. M. mexi- 
canus also is found from time to time in marshy areas in desert 
regions, where runways may lead into water. And, M. pinetorum 
frequently is associated with deciduous forests where the substrate 
contains considerable humus and is relatively moist (Lowery, 1974; 
Peterson, 1966); however, the species is not abundant in swamps 
(Miller and Getz, 1969). 

Species such as Microtus californicus, M. oregoni, M. townsend, 
and M. longicaudus, although usually found in wet or mesic areas, 
also inhabit seasonally arid sites. Reproduction and population den- 
sities in these sites may decline during dry periods. 

When they occur alone, some species frequently are found over 
a wide range of moisture conditions; but, when sympatric with other 
species of Microtus, there often is a segregation of species along the 
moisture gradient. Species with relatively wide moisture tolerances 
display more restricted distributions when sympatric with other 
species, as follows: 

Microtus pennsylvanicus—M. ochrogaster: M. pennsylvanicus is in 


298 Getz 


wetter areas, whereas M. ochrogaster occurs in well-drained sites 
(DeCoursey, 1957; Findley, 1954; Miller, 1969). 

Microtus pennsylvanicus-M. montanus: M. pennsylvanicus is in 
moist sites, whereas M. montanus is more abundant in drier habitats 
(Hodgson, 1972; Murie, 1971). 

Microtus mexicanus—M. longicaudus-M. montanus—M. pennsyl- 
vanicus: M. mexicanus is in the most arid places; M. longicaudus is 
in the next most arid sites; M. montanus often is restricted to mesic 
sites, M. pennsylvanicus is limited to grass-sedge meadows along 
streams (Findley and Jones, 1962). 

Microtus montanus—M. longicaudus: M. montanus is in drier sites 
than is M. longicaudus in Eastern Washington, but in Nevada and 
Wyoming the reverse relationship was observed (Beck and Antho- 
ny, 1971; Borrel and Ellis, 1934; Findley, 1951; Vaughan, 1974). 


Cover 


Most species of Microtus display a positive response to vegetation 
cover; population densities are usually higher in sites with greater 
cover (Birney et al., 1976; Eadie, 1953; Grant et al., 1977). 

Few species of Microtus occur in open habitats. Although usually 
more abundant in dense grasses, M. mexicanus may be found in 
relatively sparse grassy habitats. When sympatric with M. montan- 
us, M. mexicanus is in more open sites while M. montanus is in 
densely vegetated habitats (Anderson, 1959; Findley and Jones, 
1962). When sympatric with M. pennsylvanicus, however, M. mon- 
tanus occurs in less-dense grassy habitats (Anderson, 1959; Hodg- 
son, 1972). 

Microtus ochrogaster commonly occurs in sparse grass habitats, 
even though it also occurs in dense vegetation. When sympatric 
with M. pennsylvanicus, M. ochrogaster is restricted to more sparsely 
vegetated sites; M. pennsylvanicus is in denser grass (Getz et al., 
1978; Miller, 1969; Zimmerman, 1965). In central Illinois, M. 
ochrogaster is abundant in grassy sites that are mowed two to three 
times a year (for example, roadsides); M. pennsylvanicus is seldom 
found in such short grass habitats. 

Microtus xanthognathus is more or less restricted to forested sites 
with a dense Sphagnum ground cover. M. pinetorum is frequently 
most abundant in deciduous forests with a thick leaf-litter layer, 
but it is not necessarily restricted to such habitats; it also is found 


Habitats 299 


commonly in areas with a sparse litter layer on the surface (Miller, 
1964; Neill and Boyles, 1955). 


Competitive Exclusion and Habitat Utilization 


There is considerable evidence that competition between species 
of Microtus and with species of other genera influence both mam- 
malian community structure and the habitat utilization of several 
species of Microtus (Rose and Birney, this volume). I summarize 
only the influence of competition upon habitat utilization in areas 
where given species appear to interact. 

Where both Microtus pennsylvanicus and M. montanus are pres- 
ent (and when in approximately equal numbers), M. pennsylvanicus 
is restricted to wet or mesic areas, whereas M. montanus is prevalent 
in more arid sites (and occupies a wider range of habitat types than 
does M. pennsylvanicus). There are conflicting views as to why this 
occurs. Murie (1971) suggests M. pennsylvanicus is aggressively 
dominant over M. montanus, thus restricting M. montanus to the 
drier sites (wet areas are preferred habitat for M. pennsylvanicus). 
But, Stoecker (1972) indicates M. montanus is dominant over M. 
pennsylvanicus and that when M. montanus is removed from an 
area of possible competitive interaction, M. pennsylvanicus extends 
into more arid sites. This suggests M. montanus excludes M. penn- 
sylvanicus from arid habitats. 

When only one species is present, Microtus longicaudus and M. 
montanus may be found in shrub habitats and in grasslands. In 
areas where the two species are sympatric, however, M. montanus 
depresses M. longicaudus populations in shrub habitats, whereas 
M. longicaudus excludes M. montanus from grasslands (Randall and 
Johnson, 1979). 

When it occurs alone, Microtus ochrogaster occurs in dense grassy 
habitats as well as in sparsely vegetated areas; in addition, M. 
ochrogaster occurs in both wet and well-drained areas when M. 
pennsylvanicus is not present. In areas where both species occur, 
M. ochrogaster usually is restricted to drier sites and to more sparse- 
ly vegetated habitats. When sympatric with M. ochrogaster, M. 
pennsylvanicus is most prevalent in low wet areas or in dense grass- 
es. Krebs et al. (1969) indicated that both species cohabit the same 
study areas in central Indiana; however, there was evidence of higher 


300 Getz 


densities of M. ochrogaster when M. pennsylvanicus was absent. 
Klatt and Getz (unpubl. observ.) have evidence of M. pennsylvan- 
icus excluding M. ochrogaster from dense grassy habitats in central 
Illinois. The mechanism for such competitive exclusion is not known. 
Getz (1962) concluded that M. ochrogaster was aggressively domi- 
nant over M. pennsylvanicus, whereas Miller (1969) found the op- 
posite. 

Several studies have shown that Microtus pennsylvanicus is ex- 
cluded from shrub or wooded areas by Clethrionomys gapperi (Cam- 
eron, 1964; Clough, 1964; Grant, 1971; Morris, 1969). Experi- 
mental removal studies indicate competitive interactions to be 
responsible for the exclusion of M. pennsylvanicus from wooded 
areas by C. gapperi (Cameron, 1964; Clough, 1964). 

Sigmodon hispidus, a species which forms surface runways in 
dense grassy habitats, excludes Microtus pinetorum from such hab- 
itats, even though M. pinetorum is subfossorial (which reduces the 
potential for direct interaction) (Goertz, 1971). M. pennsylvanicus, 
a species which also uses surface runways and surface nests, and 
M. pinetorum commonly cohabit orchards with dense grass cover 
(Benton, 1955; Fisher and Anthony, 1980). 


Habitat Utilization on Islands 


Island populations of Microtus pennsylvanicus and M. coronarius 
have been found in wooded habitats as well as in grassland habitats, 
even though the apparent preferred habitat of these species is gram- 
inoid vegetation (Cameron, 1958; Grant, 1971). M. coronarius ap- 
pears to be restricted to wooded island sites with mossy carpets 
(Swarth, 1911); M. pennsylvanicus has been taken in open woods, 
however. 

In some instances occupancy of non-grassy habitats may involve 
“surplus” animals forced out of more favorable grassy habitats as 
a result of population pressure during peak periods of the popu- 
lation cycle. In other cases, absence of competitors (for example, 
Clethrionomys gappert) may allow Mucrotus pennsylvanicus to oc- 
cupy forested habitats on islands (Grant, 1971). When C. gapperi 
is present on islands, M. pennsylvanicus usually is restricted to grassy 
habitats (Cameron, 1958, 1964). 

There is no indication of Microtus townsendu occurring in for- 


Habitats 301 
TABLE 4 
PRESUMED HABITAT-PATCH CONFIGURATION OCCUPIED BY Microtus SPECIES PRIOR 


TO HUMAN DISTURBANCE 


Large, contiguous, relatively stable habitats 


M. californicus M. oeconomus 
M. muurus M. pinetorum 
M. ochrogaster M. townsendu 
Small, isolated, or ephemeral habitat patches 
M. canicaudus M. parvulus 
M. chrotorrhinus M. pennsylvanicus 
M. longicaudus M. quasiater 
M. mexicanus M. richardsoni 
M. montanus M. xanthognathus 
M. oregoni 
Entire species restricted to one or a very few small or localized areas 
M. abbreviatus M. ludovicanust 
M. breweri M. nesophilust 


M. coronarius 


+ Extinct. 


ested habitats when on islands. On islands, M. townsendii was re- 
corded from under driftwood on sandy beaches and in rockpiles and 
dry grasslands as well as in wet marshes and “lush” vegetation, but 
not in forests (Cowan and Guiguet, 1965; Dalquest, 1940). 


Habitat Configuration and Stability 


It appears that there may be a relationship between patchiness 
or stability of habitat in which some species of Microtus arose and 
social structure displayed by the species (Getz, 1978; Getz and 
Carter, 1980; Lidicker, 1980; Madison, 1980; Wolff, 1980). Thus, 
it is of interest to identify those species that appear to have evolved 
in large contiguous permanent habitats as contrasted to species whose 
original habitat comprised small isolated or ephemeral patches. Such 
information can be used in explaining the similarities and differ- 
ences in social organization and mating systems among different 
species. 

As suggested previously, a species may occupy a variety of hab- 
itats under given population density conditions; in many instances 


302 Getz 


populations are found in intervening marginal habitats at these 
times. This may give the impression of occupancy of larger contig- 
uous habitat patches than occurs under lower density conditions. 
Thus, it is difficult to ascertain with a high degree of accuracy from 
published accounts the “normal” habitat in terms of patchiness. A 
study may have concentrated only on specific sites (and at a partic- 
ular time), which biases the impression as to patch configuration of 
the habitat of the species. In addition, humans have disrupted the 
habitats of most species, thereby changing the original patch con- 
figuration; this further complicates determination of the configu- 
ration of the original species’ habitat. As nearly as can be surmised 
from published accounts, Table 4 summarizes the general catego- 
rizations of habitat patch configuration. Insufficient data are avail- 
able to estimate the habitat patch size and configuration of Microtus 
oaxacensis, M. guatemalensis and M. umbrosus. 


Effects of Human Activities on Microtus 
Habitats 


The original habitats of most species of Microtus have been al- 
tered greatly by a variety of human activities. Such changes include 
reduction in natural habitats and modification of patch size and 
dispersion. Those species whose habitats were altered by human 
activities include M. ochrogaster, M. pennsylvanicus, M. californicus, 
and M. townsendiv. 

Habitat reduction resulted primarily from conversion of grass- 
lands for farming and grazing. The original prairie grassland hab- 
itats of Microtus ochrogaster especially were reduced by agriculture. 
Almost all the once extensive grasslands are now cultivated or grazed. 
M. ochrogaster does not occupy most agricultural croplands; thus, 
populations of M. ochrogaster now are relatively isolated in the few 
remnants of prairie areas or they occupy new habitats created by 
humans (see below). The original habitat of M. californicus also 
was reduced greatly by grazing and agriculture. Populations of M. 
californicus remain in ungrazed or less-disturbed grasslands; many 
of these grasslands now include a large number of exotic species of 
plants. 

Species of Microtus occupying wet and marshy areas, including 


Habitats 303 


salt marshes (for example, M. pennsylvanicus, M. californicus, and 
M. townsendi) also experienced a reduction in available wetland 
habitats. Wet areas were drained for agriculture or filled in for 
industrial development (as in the case of salt marshes). Filling in 
of large areas of San Francisco Bay is a prime example of loss of 
salt-marsh habitats of Microtus. 

The habitat of Microtus nesophilus on Great Gull and Little Gull 
Islands was completely destroyed by the construction of a military 
fort. The species declined rapidly in numbers from relatively high 
abundance to extinction. There is no indication of habitat distur- 
bance being a factor in the extinction of M. ludovicianus; a relatively 
large area of apparently suitable habitat remains. 

New habitats suitable for occupancy by Microtus also were cre- 
ated by humans. “New” habitats were formed for M. pinetorum, 
M. ochrogaster, M. pennsylvanicus, M. californicus, M. montanus, and 
perhaps M. oregoni. Some agricultural crops (alfalfa, wheat and 
timothy) provide at least a temporary habitat for Microtus (for ex- 
ample, M. californicus, M. montanus, and M. ochrogaster). Establish- 
ment of bluegrass pastures that are allowed to remain idle or are 
abandoned provides habitat for species such as M. ochrogaster and 
M. pennsylvanicus. Grassy roadsides along county roads, state high- 
ways, interstates, and railroads provide extensive habitats for M:- 
crotus (for example, M. pennsylvanicus, M. ochrogaster; Getz et al., 
1978). Within the past decade financial constraints reduced mowing 
of many state and interstate roadsides creating considerable areas 
of dense grassy habitat. Such unmowed areas are especially impor- 
tant in providing grassy habitats otherwise scarce or absent in high- 
intensity agricultural and forested regions. There is evidence that 
such avenues of habitat were used by M. pennsylvanicus to effect a 
significant expansion of its range in the high intensity agricultural 
region of central Illinois. 

Orchards with dense grassy ground cover provide a different, but 
suitable, habitat for Microtus pinetorum, as well as for species that 
normally make use of grassy habitats (especially M. pennsylvanicus 
and M. ochrogaster). 

Clearcut forestry practices, and the resultant successional se- 
quences, increase the available habitat for Microtus oregoni. Al- 
though similar successional sequences follow natural forest fires, 
clearcut logging operations provide extensive areas of suitable hab- 
itat for M. oregoni and M. chrotorrhinus. 


304 Getz 


Agricultural Habitats 


Because of frequent disturbances (tillage, removal of vegetation 
at harvest, and grazing by livestock), Mzcrotus species are seldom 
associated with agriculture in North America. Few agriculture sys- 
tems provide adequate vegetation cover for a sufficient length of 
time to permit Microtus populations to become established in fields. 
Occasionally some species are found in crops, however; in a few 
instances there have been economically damaging vole outbreaks. 

Microtus is associated most commonly with forage crops such as 
alfalfa, clover and timothy (Jameson, 1958; Lantz, 1905, 1907; 
Linduska, 1950; Morrison, 1953; White, 1965). When crops are 
cut and hay removed, cover is sufficiently disturbed to cause voles 
to disappear or decline to low densities. Only infrequently are voles 
able to achieve high densities in fields harvested at normal intervals. 
If such forage crops are not harvested, of course, voles may achieve 
high densities, depending upon the phase of the local population 
cycle. 

Perhaps the most dramatic outbreak of Microtus in agricultural 
systems in the United States was that of the montane vole (M. 
montanus) in Nevada and California in 1906-1908 (Piper, 1909). 
In Humboldt County, Nevada, alone approximately 10,000 ha of 
alfalfa were completely destroyed; voles ate all parts of alfalfa plants, 
including roots. Estimated population densities were in excess of 
25,000 voles/ha in areas with the most severe outbreaks. In 1957- 
1958 there was a more extensive outbreak of M. montanus in crop- 
lands throughout much of the western United States, including 
California, Oregon, Washington, northern Nevada, Utah, Idaho, 
southwestern Montana, and western Wyoming. Population densi- 
ties of 5,000-7,500/ha were recorded locally; most densities were 
in the hundreds per ha, however (White, 1965). Predator increases, 
especially of owls, hawks, and gulls, were documented during this 
outbreak. Predator populations remained high following the decline 
of voles and served to drive vole densities to low levels (White, 
1965). 

Other species that have been recorded from forage crops include 
Microtus ochrogaster, M. pennsylvanicus, M. coronarius, and M. cal- 
ifornicus. Both M. ochrogaster and M. pennsylvanicus occur in wheat 
fields in central Illinois (Getz, pers. observ.). There are only an- 
ecdotal data as to densities achieved before wheat is harvested in 


Habitats 305 


late June. In most cases wheat is combined before voles can achieve 
high densities. At least one field sustained losses of wheat of 25% 
in central Illinois (D. E. Kuhlman, pers. comm.). 

During the growing season, corn does not provide suitable 
cover for Microtus. Formerly, both M. pennsylvanicus and M. och- 
rogaster were abundant in corn fields in winter when corn was 
placed in shocks rather than picked or combined in the field, as is 
now common practice in almost all regions (Getz, pers. observ.; 
Linduska, 1950). Voles undoubtedly moved from adjacent grassy 
habitats into shocks during winter; neither species was found in 
corn fields during summer. 

Other crops in which Microtus have been observed include field 
beans (M. pennsylvanicus; Jackson, 1961); asparagus (M. califor- 
nicus; Morrison, 1953); and potatoes (M. californicus and M. coron- 
arius; Swarth, 1911; White, 1965). 

Although they are not strictly agricultural habitats, orchards sup- 
port populations of several species of Microtus (Holm, et al., 1959; 
Horsefall, 1953). M. pinetorum, M. pennsylvanicus, and M. ochro- 
gaster commonly are found in apple, pear, and peach orchards; M. 
californicus has been recorded from citrus orchards (Morrison, 1953). 


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308 Getz 


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JOHNSTON, R. F. 1957. Adaptations of salt marsh mammals to high tides. J. 
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Habitats 309 


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COMMUNITY ECOLOGY 


ROBERT K. ROSE AND 
ELMER C. BIRNEY* 


Abstract 


OMMUNITIES with Microtus tend to be structurally simple, usu- 
C ally grasslands or tundra, and to have no more than two species 
of Microtus and rarely more than six species of small mammals. 
Microtus often dominates both numerically and in total small mam- 
mal biomass, especially at higher latitudes. The small mammal 
community is most influenced by Microtus through its fluctuations 
in density, and thus also in biomass, by its relatively high level of 
diurnal activity, and by its year-round activity. Other species of 
small mammals may be adversely affected because Microtus usually 
is larger and behaviorally dominant and also because the mere 
presence of Microtus may focus predators on the area, especially 
during periods of high density. As generalized herbivores, primarily 
on grasses and herbs, Microtus has the potential to alter plant com- 
munities, either by selectively harvesting some species or through 
stimulating growth by grazing. Scarcely anything is known about 
the role Microtus plays in plant and small mammal communities, 
so both descriptive and experimental studies can make significant 
contributions to an understanding of the role and impact Muicrotus 
has on its communities. 


Introduction 


Microtus always lives with other small mammal associates, 
whether in combination with one or more shrews, or cricetine, sci- 
urid, heteromyid, murid, or other microtine rodents. Because it 
occurs primarily in temperate grasslands and in tundra (Getz, this 
volume), we anticipate that Microtus will usually be a member of 


* Order of authorship determined by flip of a coin. 


310 


Community Ecology Sill 


structurally simple plant communities, regardless of latitude. In 
North America, grassland and tundra (and often Microtus) are found 
between 35 and 70°N, and also in isolated montane and plateau 
regions of southwestern U.S. and northern Mexico (Hoffmann and 
Koeppl, this volume). In these ecosystems, Microtus often contrib- 
utes as much as 90% of the biomass of small mammals at the 
location. Consequently, an understanding of the role of Microtus is 
essential to an understanding of the ecology and dynamics of the 
ecosystem. Microtus has been evaluated in the context of primary 
consumers in grasslands, as in the IBP studies reported by Birney 
et al. (1976), French et al. (1976), and Grant and Birney (1979). 

Microtus most frequently has been studied at the population level 
(Taitt and Krebs, this volume). Population studies have reported 
in great detail the patterns of density, population growth and sur- 
vival, reproduction, behavior, dispersal, and changes in gene fre- 
quency, among others. Such studies have included only one or at 
most two species of Microtus or perhaps another microtine rodent, 
under the assumption that the common patterns underlying cycles 
could be detected in all microtines. The population dynamics and 
interactions of syntopic non-microtines have largely been ignored 
in the intensive study of Microtus population biology. As a result, 
we know very little about the role of Microtus in the small mammal 
community; that is, how Muicrotus affects other small mammals and 
how other small mammals affect Microtus. Some investigators, no- 
tably Lidicker (1973, 1978), have suggested that microtines should 
be studied in the community context, but this admonition has not 
been universally accepted. Indeed, we found that the majority of 
papers on Microtus population biology do not even list the small 
mammal associates in the community. 

In sum, small mammal ecologists have looked at least coarsely at 
the role of Microtus in some grassland and tundra ecosystems, and 
in great detail at the population biology of Microtus. But there are 
no reported studies of the role of Microtus in the community of 
small mammals living at specific locations. 

In a sense, a chapter on the community ecology of a genus is 
almost without precedent, especially a genus with 23 species living 
in a wide variety of environments from Guatemala to northern 
Alaska. Our goal in writing this chapter is to evaluate the role of 
Microtus in a range of successional, latitudinal, and altitudinal en- 
vironments in the context of other small mammals living with them, 


312 Rose and Birney 


and to explain the patterns of Microtus distribution and association 
in the context of evolutionary and historic events. 


Communities of Small Mammals with 
Microtus 


Patterns of Geographic Distribution 


In general, mammals follow the biogeographic principle of hav- 
ing more species in the tropics and progressively fewer toward the 
poles (McCoy and Connor, 1980; Simpson, 1964; Wilson, 1974). 
Fleming’s (1973) evaluation of forest-dwelling mammals at two 
locations at 65°N (15 and 16 species), 45 and 42°N (35 species 
each), and two locations at 9°N (70 species each) nicely illustrates 
this gradient of mammalian species in the New World. However, 
except at the extremes of latitude, small mammal communities do 
not follow this trend, for temperate and tropical grasslands, tem- 
perate forest, and tundra communities alike usually have six or 
fewer species (French, 1978). Instead of a gradient of numbers 
across the North American continent, numbers of small mammal 
species vary as much according to habitat type within climatic zones 
as across broad latitudinal zones. An even greater exception is the 
pattern of latitudinal gradients for the numbers of microtine, and, 
more specifically, Microtus species from the tundra to subtropical 
latitudes. 

Numbers of species of Microtus, other microtines, and non-mi- 
crotines for two north-south transects in North America are given 
in Table 1. Microtine species contribute more than 50% to the total 
rodent fauna north of 60°N in the western transect and north of 
55°N in the eastern transect. South of 35°N, the number of Microtus 
species never exceeds one. Microtines other than Microtus are not 
found below 30°N along either transect. Thus, the trend of increas- 
ing numbers of species toward the tropics is strongly reversed for 
all microtine rodents, including Microtus. 

Reasons for this reverse pattern of species diversity are many and 
varied, but originate in the biogeographic history of this exclusively 
Northern Hemisphere genus (Hoffmann and Koeppl, this volume). 
Given their northern origin, Microtus species tend to be well adapt- 
ed physiologically, morphologically, and behaviorally to withstand- 
ing extreme cold and long winters, but are largely unable to with- 


Community Ecology 313 


TABLE 1 
NUMBER OF SPECIES OF Microtus COMPARED TO OTHER MICROTINES AND 
NON-MICROTINE RODENTS ALONG Two NORTH-SOUTH TRANSECTS IN NORTH 
AMERICA (DATA FROM HALL, 1981) 


End points of transects 


70°N, 14°W 70°N, 110°W 
15°N, 100°W 15°N, 90°W 
Other Non- Other Non- 
Degrees micro-  — microtine micro- —s microtine 
N latitude Muicrotus tines rodents Microtus tines rodents 
70 3 4 2 0 2 0 
65 4 4 6 1 3 1 
60 2 4 8 1 6 4 
55 1 4 8 1 4 5 
50 4 4 15 1 4 7 
45 4 4 18 2 3 14 
40 2 4 16 2 3 12 
35 4 3 Pad 2 2 14 
30 0 1 33 1 1 ial 
25 0 0 25 Gulf of Mexico 
20 1 0 25 0 0 16 
15 1 0 16 


stand hot, arid conditions. Consequently, summer heat more than 
winter cold seems to determine the locations at which Microtus can 
live. Only M. ochrogaster, M. californicus, and, at some localities, 
M. montanus are found in grasslands that are hot and dry. 

Although such folivores (leaf-eaters) as Szgmodon are an impor- 
tant part of tropical grassland communities, they contribute rela- 
tively much less to the total small mammal community there com- 
pared to the importance of microtine folivores farther north, where 
vegetative structure and diversity are much reduced and many fewer 
mammalian species are found. It is in the grasslands, tundra, and 
taiga habitats that one or a few microtine rodents dominate and 
may occur with a few species of insectivores (mostly shrews), car- 
nivores (mostly weasels), and omnivores (such as Peromyscus 
maniculatus). 

When the geographic ranges of all North American Microtus are 
superimposed on a single map (Fig. 1), it can be seen that at many 
localities only a single species of the genus occurs. In addition to 
certain islands, these general regions include much of northeastern 


314 Rose and Birney 


a 
0 200 400 600 800 mi 


Fic. 1. Sketch map of North America showing approximate distributions of all 
species of Microtus in North America (compiled from Hall, 1981). Open areas in- 
dicate presence of no Muicrotus species. Stippling identifies areas that contain one 
(light stippling) to five (black) species of Microtus. Although as many as five or six 
species may overlap broadly, it is unusual for as many as three to co-occur in a single 
community. 


Community Ecology 315 


Canada (M. pennsylvanicus being the only Microtus), southeastern 
U.S. (M. pinetorum), most of the range of the genus south of the 
U.S. (M. mexicanus and the relictual species M. guatemalensis; M. 
quasiater, M. oaxacensis, and M. umbrosus are sympatric and some- 
times even syntopic with M. mexicanus), coastal areas of California 
and northern Baja California (M. californicus), and north-central 
Mackenzie Territory and sections of coastal Alaska (M. oeconomus). 
Other significant but small areas with only one Microtus species are 
western Kansas and adjacent Oklahoma (M. ochrogaster) and sec- 
tions of New Mexico and Nevada (M. longicaudus). ‘Two sympatric 
Microtus occur in much of the grasslands of the northern Great 
Plains and western Canada, where M. pennsylvanicus coexists with 
M. ochrogaster, M. xanthognathus, or M. longicaudus. Three and 
four broadly sympatric species tend to be limited to areas of con- 
siderable altitudinal relief and ecological diversity, including the 
Cascades, northern and southern Rockies, and parts of the Appa- 
lachians. The possibility of five Microtus species exists (on the basis 
of overlapping distributions only) for limited areas of the northern 
Rockies (mostly in Yukon) and the Cascades. Ranges of six species 
appear to approach each other closely in both the northern Cascades 
(M. longicaudus, M. montanus, M. oregoni, M. pennsylvanicus, M. 
richardsoni, and M. townsendi1) and southern Cascades (M. califor- 
nicus replaces M. pennsylvanicus as a possible sixth species). We 
know of no reports of more than three species of Microtus occurring 
together in a single small mammal community (see Getz, this vol- 
ume). For example, even where Findley (1951, 1954) studied small 
mammal assemblages at Jackson Hole, Wyoming, no more than 
two of four species of Microtus were taken together in any of the 
10 habitat types. Of the five Microtus in Colorado, Armstrong (1972) 
listed no more than three species for any of 14 community types. 
Possible triads were in yellow-pine woodland (M. montanus, M. 
longicaudus, and M. mexicanus), or montane subalpine meadow, 
highland streambank, and aspen woodland (M. pennsylvanicus re- 
places M. mexicanus). Steve West (pers. comm.) found three M:- 
crotus species together on only one of 25 study sites in central Alas- 
ka; that site, a recently burned black-spruce forest, also had three 
other microtine species. A total of six syntopic microtines is high, 
but non-Microtus species (for example, Synaptomys sp., Clethrion- 
omys sp.) commonly occur with one or two species of Microtus. 
The increase in small mammal species diversity in areas char- 


316 Rose and Birney 


acterized by great altitudinal relief is well known, and the impor- 
tance of this pattern to studies of latitudinal species diversity was 
reiterated recently by McCoy and Connor (1980). Its importance 
specifically to Microtus species was demonstrated for M. longicau- 
dus, M. pennsylvanicus, M. montanus, and M. mexicanus in New 
Mexico by Findley (1954, 1969) and Findley and Jones (1962). 
Armstrong (1972:Fig. 121) illustrated the relationship between 
mammalian species density and mountainous regions in Colorado 
(see also Table 1). 

In sum, communities with Microtus tend to be grasslands or tun- 
dra, and rarely to have more than two species of Microtus or six 
species of small mammals overall. Thus, their habitats tend to be 
structurally simple and the number of co-occurring species few. 
Microtus often dominates numerically and in its contribution to total 
small mammal biomass. 


Environmental Parameters 


Despite the fact that one or another species of Microtus can be 
found over most of North America, voles sometimes are restricted 
locally, and thus are not a ubiquitous component of North Ameri- 
can grasslands and tundra. Many interrelated environmental pa- 
rameters undoubtedly contribute to their presence or absence in a 
given community, including weather and climate, vegetative struc- 
ture, food availability, competition, and predators. 

Weather and climate.—Mucrotus is poorly adapted to conserve 
water or to thermoregulate at high ambient temperatures (Wunder, 
this volume). No Microtus species is found strictly in deserts or even 
desert grasslands. In southwestern Kansas, where M. ochrogaster 
reaches its southwestern distributional margin in relatively arid 
shortgrass prairie, this vole utilizes apparently self-dug burrows 
and is almost exclusively nocturnal during summer, presumably to 
avoid the extreme daytime heat and desiccating wind (Birney, pers. 
observ.). The short tail and ears and dense fur of Microtus serve 
well to conserve heat, but not to dissipate it. 

In contrast, most or all species of Microtus are able to persist and 
even thrive in extremely cold climates. For example, M. oeconomus 
and M. miurus occur exclusively in the subarctic and tundra of 
northwestern Canada and Alaska. M. xanthognathus, M. pennsyl- 
vanicus, and M. longicaudus also extend their distributions inside 


Community Ecology 317 


the Arctic Circle. Although the air temperature may be as low as 
—70°C, the subnivean environment of the vole is close to 0°C. Win- 
ter survival of some species is enhanced in part by their habit of 
communal nesting. M. xanthognathus in central Alaska constructs 
large middens of stored food and insulation for winter survival of 
the five to 10 occupants (Wolff, 1980). Communal winter nesting 
is known for other species as well, including M. pennsylvanicus in 
New York (Madison, this volume) and M. ochrogaster in warmer 
eastern Kansas (Fitch, 1957). 

Local weather conditions probably rarely affect the occurrence 
of voles in most small mammal communities, except indirectly 
through an effect on the vegetation. Martin (1960) reported that in 
the mixed prairie of western Kansas, M. ochrogaster was at low 
density during one drought and high density during another, indi- 
cating that even prolonged aridity does not invariably reduce the 
abundance of the species. However, on Martin’s study area (a west- 
ern wheatgrass community) the highest density recorded in two 
years was only 18.4 voles/ha, a much lower density than the 160 
or more per ha reported for the same species in ungrazed tallgrass 
and in irrigated and fertilized shortgrass (Birney et al., 1976). Gaines 
and Rose (1976) reported densities of prairie voles of about 180/ 
ha from brome oldfields in eastern Kansas. Thus, although vole 
populations can survive and apparently even thrive during tempo- 
rary periods of drought, their role in the small mammal community 
of such areas may be relatively less than in areas of greater or more 
regular rainfall. 

Flooding.—Flooding is a potentially serious short-term environ- 
mental factor that could affect small mammal communities. Voles 
are not adapted to climbing emergent vegetation, as has been ob- 
served for such rodents as Peromyscus and Oryzomys during floods. 
Wolff (1980) concluded that the flooding of old winter nests did 
not adversely affect M. xanthognathus because they dispersed at the 
time of snow melt. Similarly, Bee and Hall (1956) described the 
periodic flooding of the burrows of M. miurus, but the voles appar- 
ently were not excluded from the community by the temporary 
flooding. M. pennsylvanicus has been reported to avoid saturated 
substrates (Getz, 1967), but Lyon (1936) reported this vole living 
in grass tussocks surrounded by water in Indiana swamps. In peat- 
land fens in northern Minnesota, Birney (pers. observ.) has studied 


318 Rose and Birney 


breeding populations of M. pennsylvanicus living on sphagnum 
hummocks surrounded by standing water. Harper (1956) judged 
that a few hours of flooding during spring “‘break-up” in Keewatin 
had little effect on a population of M. pennsylvanicus, but that 
flooding and subsequent freezing on the same meadow in November 
greatly reduced their chances for winter survival. 

Substrate.—Mucrotus species invariably use subterranean burrows 
to one degree or another. Soil richness and texture undoubtedly 
affect the local distribution and abundance of all species indirectly 
depending on their ability to burrow. Only for the fossorial species, 
M. pinetorum, has this been clearly demonstrated. Fisher and An- 
thony (1980), studying woodland voles in Pennsylvania orchards, 
failed to find them in one orchard with soils having relatively low 
percentages of gravel and sand and high percentages of fines and 
silts. They concluded that soil texture strongly influences the dis- 
tribution of M. pinetorum, which requires more than 35% gravel 
and 20% clay, and less than 65% fines and 40% silt together with 
between 25 and 48% sand. In less-disturbed woodland habitats, this 
vole may burrow primarily in the duff and upper humus layers, 
and thus may be less rigidly tied to soil texture than to the surface 
covering. 

Soil moisture may be of considerable importance, but how much 
of this is directly related to moisture and how much is indirect as 
moisture affects vegetation has not been determined. Murie (1969) 
showed that M. pennsylvanicus favored wet over dry substrates in 
the laboratory, but that MM. montanus from the same area showed 
no preference. Getz (1967), on the other hand, found that M. penn- 
sylvanicus avoided saturated substrates in the laboratory. 

Microtus ochrogaster occupies burrows dug in hard, dry loam over 
much of its range, but most burrowing activities take place follow- 
ing autumnal rains that increase the friability of the soil (Rose, 
pers. observ.). Wolff and Lidicker (1980) noted that the complex, 
branching burrow systems of M. xanthognathus penetrated 15-25 
cm, that is, to mineral soil or permafrost. Populations of M. penn- 
sylvanicus on the Anoka Sand Plain of Minnesota reach high den- 
sities in the tall marsh grasses that grow there, but we know of no 
places where dry sand serves as a suitable substrate for Microtus. 
In Keewatin, Harper (1956) found M. pennsylvanicus in riverside 
meadows, sedge bogs, and on grass-covered sand dunes but never 
on the open summits of the gravelly ridges in the Barrens. 


Community Ecology 319 


Rocky soils in mountainous areas serve as suitable substrates for 
voles of several species. For example, the usual habitat of M. chro- 
torrhinus seems to be the edges of boulder fields, although rock voles 
are sometimes found in unburned clearcuts (Kirkland, 1977), where 
limbs and brush piles may substitute for rocks. 

Vegetation.—We believe that vegetation, more than any other 
single environmental factor, determines the presence or absence, as 
well as the relative role and importance of Microtus, in small mam- 
mal communities. Two field experiments on M. ochrogaster show 
the dramatic effect of increasing vegetative cover on this species. 
Birney et al. (1976) excluded cattle from grazing a 1-ha plot of 
tallgrass prairie in northeastern Oklahoma and observed the vole 
population increase dramatically during a single summer from none 
in May to 24 individuals/ha in October, while standing crop vege- 
tation increased from 230 to 400 g dry weight/m?. Only an occa- 
sional vole (1.0/ha) was trapped in an adjacent grazed control in 
October. Grant et al. (1977) provided irrigation water and nitrogen 
to two 1-ha plots of shortgrass prairie in eastern Colorado and 
compared the small mammal communities to those on initially sim- 
ilar controls. Over 4 years, M. ochrogaster located and became es- 
tablished on the experimental grids, showing a pattern of increasing 
from relatively low densities each spring to successively higher and 
earlier peak densities (over 100/ha in the fourth year) each summer 
or autumn. By comparison, no voles were trapped on the control 
grids until the third year of the study, and permanent populations 
never became established there. Cover levels on the experimental 
plots fluctuated between 600 and 1,200 g of dry weight/m’, com- 
pared to 300-600 g/m? on the controls. Abramsky and Tracy (1979) 
speculated that shortgrass prairie is unsuitable for M. ochrogaster 
under conditions of normal rainfall and fertility; sparse vegetation 
and summer heat probably limit the distribution (Fig. 1) of these 
populations. 

Birney et al. (1976; also see Elton, 1939; Frank, 1957; Getz, 
1971) discussed several attributes of vegetative cover for Muicrotus. 
Of perhaps greatest importance is concealment and protection from 
predators. Getz (1970) concluded that heavy predation on a pop- 
ulation of M. pennsylvanicus following mowing and baling of the 
vegetation accounted for the loss of most individuals, although his 
trapping results suggest that a few may have moved into an adjacent 
unmowed field. 


320 Rose and Birney 


Food provided by the vegetation obviously is also of great im- 
portance. Bee and Hall (1956), who studied the community asso- 
ciation of five microtine species in northern Alaska, found that each 
species was associated with a particular vegetation type. Studies by 
Jung and Batzli (1981) demonstrated that secondary plant com- 
pounds differentially affected the growth rates of arctic microtines, 
and thus that the mere presence of green forage, even though it 
might provide adequate cover, is not synonymous with the presence 
of high-quality food for microtines. For most Microtus species, how- 
ever, especially those that occur in vegetatively diverse habitats, a 
wide range of food is eaten (Zimmerman, 1965), and thus the species 
composition of grassy habitats is often of less importance to Microtus 
than is the presence of adequate cover (except see Batzli, this vol- 
ume). 

The presence of vegetative cover also must affect behavioral in- 
teractions among conspecifics. For example, Warnock (1965) dem- 
onstrated that cover reduced both fighting and mortality of crowded 
captive M. pennsylvanicus. Furthermore, the protection provided by 
dense cover undoubtedly permits daylight activity, which could be 
especially important for species living at high latitudes where day- 
light periods are long or even continuous during summer. 

Hopkins (1954) measured the effects of a mulch layer in grass- 
land habitat, and demonstrated its effect on the microhabitat. Such 
factors as surface-level humidity, temperature, penetration of light, 
and soil moisture all are affected by cover. Additionally, heavy cover 
prevents dense packing of snow at ground level, thus making the 
subnivean space more hospitable to the small mammals that live 
there. 

Grant et al. (1982) demonstrated that cover levels on four grass- 
land study areas had a greater effect on herbivorous rodents than 
on omnivorous or granivorous ones. Removal of cover by grazing 
ungulates affected the three most important herbivorous small 
mammals (M. montanus, M. ochrogaster, and Sigmodon hispidus) 
more adversely than any of the other eight common rodents. These 
results were interpreted as strong support for the hypothesis (French 
et al., 1976; Grant and Birney, 1979) that the general composition 
of grassland small mammal communities is determined primarily 
by structurally simple attributes (including cover) of the habitat. 
This hypothesis appears to be especially applicable to communities 
with one or more species of Microtus. 


Community Ecology 321 


Not all species of Microtus are restricted to structurally simple 
grassland and tundra environments. Wolff and Lidicker (1980) 
pointed out that M. xanthognathus is restricted to the taiga. Within 
this broad habitat type, taiga voles appear to utilize a wide variety 
of forested and grassland areas from burned to unburned black- 
spruce forest to wet, grassy swamp. However, West (1979) found 
M. xanthognathus primarily in grass-sedge habitat associations with 
early successional stages, and considered M. oeconomus to have the 
widest habitat use pattern of Alaskan Microtus. Whitney (1976) 
also studied populations of M. oeconomus in vegetationally diverse 
taiga near Fairbanks, Alaska, but considered the species to have a 
narrower niche than sympatric Clethrionomys rutilus. Bee and Hall 
(1956) found M. miurus in a variety of wet and dry habitats, but 
usually associated with willows, on which it seemed to be partially 
dependent for winter food. M. pinetorum, commonly found in east- 
ern deciduous forest, seems to reach high population densities only 
in grassy orchards (Benton, 1955), sometimes in the presence of M. 
pennsylvanicus (Fisher and Anthony, 1980). Additional evidence 
that grasses can enhance habitat quality of woodland voles was 
provided by Gentry (1968), who studied a population of M. pine- 
torum within enclosures in a Lespedeza- Andropogon oldfield in South 
Carolina, where trees were absent. Findley (1951) found M. lon- 
gicaudus on forested rocky hillsides, in alder-willow swamps, and 
in grassy, open woods. Armstrong (1972) found long-tailed voles in 
a wide variety of habitats including sagebrush and pine woodland 
in Colorado. Other species that may be found in forested habitats 
include M. pennsylvanicus, especially in open woodlands with a 
grassy floor and on small islands (Cameron, 1958); M. montanus, 
but only if grass is available; M. richardsoni, in association with 
mountain streams and alpine marshes; M. oeconomus, present in all 
but the most mature black- and white-spruce forest in Alaska (West, 
1979); and M. oregoni, which lives in a variety of habitats including 
damp areas within redwood, fir, spruce, and hemlock forests (In- 
gles, 1965). 

Competition.— Despite the fact that there have been few studies 
of competition in Microtus (for example, Conley, 1976), we see 
competition as being very important in the shaping of communities 
with Microtus. There are many examples of Microtus numerically 
dominating other species, many of which have been given in this 
chapter. The most dramatic are those in which voles, such as M. 


322 Rose and Birney 


pennsylvanicus, outnumber all other small mammals combined, and 
may contribute more than 90% to total small mammal biomass 
(French, 1978; Pruitt, 1968). At some locations, two species share 
a prominent role in the community, such as in the central U.S. 
where M. ochrogaster and M. pennsylvanicus overlap in distribution 
(Krebs et al., 1969). At others, such as in eastern Kansas, M. och- 
rogaster shares the herbivore role with Synaptomys cooperi, another 
microtine rodent and a presumed ecological equivalent (Gaines et 
al., 1979) or with the larger cricetine, Sigmodon hispidus (Rose et 
al 197): 

It is clear that Microtus is a dominant herbivore of northern 
origin and affinities and that Sigmodon is a dominant herbivore in 
grasslands from Mexico northward into the central plains. S. Ais- 
pidus has moved progressively northward during historic times, and 
its movement across Kansas and into Nebraska has been docu- 
mented by Genoways and Schlitter (1966). In part, this colonization 
northward was due to the ability of S$zgmodon to use disturbed areas 
and perhaps cropland (Fleharty and Olson, 1969), but also to its 
ability to respond to semiarid conditions such as occurred during 
the 1930’s “‘dustbowl” era. Droughts have a strongly adverse effect 
on Microtus (Martin, 1960; French et al., 1976), and this climatic 
factor may have contributed to the replacement of M. ochrogaster 
by Sigmodon as the dominant folivore in the grasslands of Kansas 
and perhaps of neighboring states as well. Some investigators (for 
example, Glass and Slade, 1980; Terman, 1974) have attempted to 
study competition between Sigmodon and M. ochrogaster, using 
combinations of field and laboratory experiments. Sigmodon tends 
to win under the conditions used in these studies. A counterbalanc- 
ing force is high winter mortality in Szgmodon, which is poorly 
adapted to severe winters (Fleharty et al., 1972). There is good 
evidence that local populations of Szgmodon go extinct during severe 
winters (Slade, pers. comm.), at least in eastern Kansas. We imag- 
ine that such events would happen with greater frequency the far- 
ther north the populations. Thus, in this example of intergeneric 
competition of the dominant small herbivores in the central plains, 
it seems that Microtus contends better with the winters and Sig- 
modon with both summers and drought. Baker (1971) provided 
several examples of pairs of Si:gmodon species that coexist in the 
Mexican grasslands in much the same way that pairs of Microtus 
do north of 35°N. 


Community Ecology 325 


Competition has been proposed as the mechanism that tends to 
separate two or more coexisting Microtus. Findley (1951, 1954), in 
some of the earliest examples of possible biological competition in 
vertebrates, never found more than two of four Microtus species at 
the same location near Jackson Hole, Wyoming. The association 
between M. montanus and M. pennsylvanicus also has been studied 
by others, including Douglass (1976), Hodgson (1972), Koplin and 
Hoffmann (1968), and Murie (1969, 1971), using both laboratory 
and field experiments. Despite the numerous examples of possible 
competitive interactions of two Microtus, Krebs (1977) was unable 
to find any evidence that M. ochrogaster and M. pennsylvanicus had 
negative effects on one another. Nor could Gaines et al. (1979) find 
evidence that M. ochrogaster and Synaptomys coopert adversely af- 
fected one another. 

One of the most interesting examples of how competition may be 
important in shaping small mammal communities is found in the 
distributional patterns of M. pennsylvanicus and Clethrionomys gap- 
pert in the islands of the St. Lawrence River and off the east coast 
of mainland Canada. In parts of the Maritime Provinces, Cleth- 
rionomys is absent, probably due to events of the post-Pleistocene 
period. There M. pennsylvanicus occupies a much wider range of 
habitats than is considered typical of that species, including interior 
forest habitats far removed from patches of grasses (Cameron, 1964). 
On islands in the St. Lawrence River, some of which have become 
connected with the mainland during historic times, some have M:- 
crotus and others have Clethrionomys. The species present lives in 
a wider range of habitats than would be characteristic on the nearby 
mainland where the two occur together. Cameron’s explanation is 
that chance has played a role in determining which species colonized 
an island, but that once established the resident species was able to 
prevent successful colonizations by the other. Two later studies of 
this pair of microtines (Iverson and Turner, 1972; Turner et al., 
1975) reported their winter coexistence, first in grassland habitat 
and then in spruce forest. In each case, when aggression levels 
increased with the onset of the reproductive season, the species that 
seemed to be in the “wrong” habitat left to return to its typical 
habitat. During the second study, Turner et al. (1975) used behav- 
ioral studies in the laboratory to determine that, although it dom- 
inated behaviorally throughout the winter, Microtus still was ex- 
cluded by Clethrionomys from the forest habitat when breeding 


324 Rose and Birney 


resumed. They interpreted these studies as competitive habitat ex- 
clusion related to reproduction-associated aggression. In a 10-year 
study of these two microtine rodents and Peromyscus maniculatus 
on islands in Maine, Crowell (1973) implicated competition as the 
principal reason for Microtus dominating the other two in nature. 

Microtus pinetorum usually lives at low densities in disjunct pop- 
ulations in eastern deciduous forests. However, in orchards (Ben- 
ton, 1955; Byers, this volume) or in enclosures where competitors 
are absent (Gentry, 1968), it can reach much higher densities. It is 
unclear how M. pinetorum responds to competition by M. pennsyl- 
vanicus but such studies are now in progress in orchards. M. pi- 
netorum may be restricted mostly to forests because its poor com- 
petitive abilities prevent it from thriving elsewhere. If so, we would 
expect it to be displaced by M. pennsylvanicus in orchards. 

Determining the role of competition in structuring communities 
with Microtus will require a combination of approaches including 
field experiments in which pairs of Microtus species coexist in some 
plots and live as separate species in others. Grant (1972) has con- 
ducted such studies with pairs of different species, including M:- 
crotus, in Ontario. Studies such as Getz (1963), of the renal effi- 
ciencies of M. ochrogaster and M. pennsylvanicus, and Zimmerman 
(1965), of the food habits of the same species, will be particularly 
useful in evaluating why species may be living syntopically in some 
places and not at others. Radiotelemetry and radio-isotopic tech- 
niques undoubtedly will be very useful in evaluating the micro- 
distributions of individuals of the same and related species. We 
emphasize the need to have the non-Microtus rodents included as a 
part of these experiments because the evaluation of their role may 
be crucial to the proper interpretation of the results of all com- 
munity studies. 

Predation.—The importance of predation in population regula- 
tion and in determining the composition of small mammal com- 
munities has long been debated. Interactions between predators and 
Microtus species, considered in depth elsewhere (Pearson, this vol- 
ume), may be relatively important under some circumstances in 
determining the magnitude of the impact of Microtus in the total 
small mammal community. Both mammalian (Pearson, 1971) and 
avian (Korschgen and Stuart, 1972) predators feed regularly and 
heavily on Microtus when they are available. 

Pearson (1964:Fig. 2) clearly demonstrated the high percentage 


Community Ecology 329 


of a population of M. californicus that could be accounted for in 
predator scats as the vole population declined from August of one 
year until March of the next. Similarly, Maher (1967) observed 
evidence on Banks Island, Northwest Territories, that Mustela er- 
minea had killed all but a few lemmings (both Dicrostonyx and 
Lemmus) on the island during winter after the lemming populations 
had been at least moderately high the previous autumn. Pearson 
(1971) concluded that predators have a major impact on microtine 
populations, especially following a “‘crash,” when the presence of 
secondary prey species enables carnivores to exert heavy predation 
pressures on the remaining low population of voles. We concur with 
this conclusion, and suggest that such predator pressure may result 
in lower biomass and higher species diversity of the small mammal 
community than might otherwise exist. However, at moderate or 
high population densities, especially during periods of recruitment, 
we doubt that predators have much impact on the Microtus com- 
ponent of the community (see Golley, 1960). 


The Influence of Microtus on Communities 


Microtus influences its plant and animal communities because of 
frequently great density, relatively large size among small mam- 
mals, and indirectly because of high metabolic rates. In the extreme, 
these combine to produce denuded habitats during Microtus plagues, 
but more typically Microtus is a prominent, if not always dominant, 
member of the small mammal community. Its effects on plant com- 
munities are largely unmeasured but high differential consumption 
of some plant species may affect the relative success of plant species 
and thereby alter the habitat sufficiently to affect the animal com- 
ponent of the community. 

The small mammal community with Microtus is often more vari- 
able than, for example, desert rodent or forest mammal communi- 
ties, which typically lack Microtus. The latter communities have a 
high proportion of nocturnal species, and their numbers tend to 
fluctuate from season to season in a relatively predictable annual 
pattern. These communities may have some species that hibernate 
during the winter season, thereby affecting the seasonal dynamics 
of the community. Nevertheless, the year-to-year composition and 
biomass estimates of a desert or forest community of small mammals 


326 Rose and Birney 


are likely to be more predictably constant than a community with 
Microtus. 

By contrast, communities with Microtus: 1) often fluctuate greatly 
in numbers, not only from season to season but from year to year 
as well, mainly because of Microtus; 2) have proportionately more 
individuals active throughout the daylight hours as well as at night, 
which is largely due to the intermittent activity periods of Microtus 
(Madison, this volume; Shields, 1976); 3) have more predators fo- 
cusing on them, because Microtus are relatively large among small 
mammals, often numerous, and available to diurnal as well as noc- 
turnal predators; 4) have continuous activity because, although oth- 
er community members such as Zapus, Spermophilus, and more 
rarely Perognathus, may hibernate, Microtus is active year-round; 
and 5) have relatively constant harvesting of vegetation because 
Microtus, with few exceptions, does not store food in caches. Com- 
munities with Microtus, then, often have high densities of small 
mammals that are active throughout the day, night, and year. Fur- 
thermore, during much of the year these small mammals tend to be 
dispersed more or less uniformly in the available habitat, in part 
because of spacing behavior described by Madison (this volume). 
In M. xanthognathus (Wolff, 1980) and M. pennsyluvanicus (Mad- 
ison, this volume), winter aggregations of voles conserve heat by 
communal nesting behavior but may suffer to a greater extent from 
predation because of it. 


Effects of Density 


Certainly the greatest influence of Microtus on the community is 
due to its great numbers when populations are near or at peak 
densities (see Taitt and Krebs, this volume). Densities of 100-300/ 
ha are typical of peak periods in the multi-year cycle, and more 
than 1,000/ha have been reported. Only when the high densities 
persist for months or occur outside the growing season is there a 
significant depletion of the covering and edible vegetation. Rodent 
plagues can occur under these conditions, as reported for M. oregoni 
in 1957, when densities of 4,500—6,500/ha were estimated in ag- 
ricultural fields in Oregon (Fed. Coop. Ext. Serv., 1959). Even at 
moderately high densities, it seems likely that the community of 
small mammals must be adversely affected, probably in many ways. 
As densities increase, suboptimal habitat is colonized by Microtus. 
The consequences of such habitat expansion rarely have been mea- 
sured, except in the extreme case of house-mouse populations going 


Community Ecology 327 


to extinction as a result of successful colonization and subsequent 
population explosion of M. californicus on Brooks Island (Lidicker, 
1966). Nevertheless, at high Microtus densities, most other small 
mammal species in the community will be affected somehow, either 
directly through interference competition for space or perhaps even 
for food, or indirectly through a physical alteration of the habitat 
as a result of partial denuding of vegetation, extensive digging of 
soil surface, and almost certainly by focusing predators on the large 
biomass of prey available in that habitat. It seems unlikely that a 
high biomass of Microtus would have a positive or beneficial impact 
on any species of small mammal, unless, as some have speculated, 
Blarina is a predator of nestling and young voles (Eadie, 1952). 


Effects of Large Body Size 


Not only is Microtus often abundant, but it is usually the largest 
small mammal species in the community, especially grasslands. 
Large body size accentuates the effects of numerical dominance and 
may help to promote the dominating influence of Microtus in many 
communities. For example, large body size in small mammals often 
is associated with large litter size, thereby contributing to species 
density and biomass. Also promoting the ability to produce large 
litters is their high metabolic rate, higher than predicted by the 
Kleiber curve (Kleiber, 1961). The high metabolic rates that pro- 
mote rapid body growth, early maturity, and large litters, often in 
rapid succession, require the rapid conversion of grass into small 
mammal biomass. McNab (1980) speculated that because natural 
selection tends to favor as high a metabolic rate as the diet will 
permit, a species with a high metabolic rate potentially will be more 
successful than a competitor with a lower metabolic rate. In the 
community context, this may mean that Microtus has an edge over 
other species primarily because of its high metabolic rate. In sum, 
these factors combine to contribute to the influential position of 
Microtus in many small mammal communities. 


Effects on Community Succession 


Because high populations of Microtus often are associated with 
herbaceous vegetation of early stages of secondary plant succession, 
it might be expected that voles would influence the nature and rate 
of changes in plant communities. If that influence is real, then we 
would predict a concommitant secondary effect on succession of the 


328 Rose and Birney 


small mammal community. Unfortunately, there is almost no in- 
formation on the influence Microtus has on the dynamics of plant 
succession. Unless the climax vegetation is tundra or grassland, 
Microtus is a transitory species, present only in early to middle seral 
stages. For example, Wetzel (1958), who studied biological succes- 
sion on abandoned strip mines in IIlinois, found that M. ochrogaster 
was absent during the initial revegetation stages when annuals dom- 
inated the vegetation, but became the dominant element of the small 
mammal community after grasses and woody perennials achieved 
dominance of the plant community. Prairie voles were abundant 
only for about 20 years, and they disappeared from the area when 
the deciduous trees achieved approximately 65% of the plant cov- 
erage. 

When forests are cut, significant and rapid changes in the vege- 
tation composition occur. Herbaceous species tend to dominate for 
a few years, creating a habitat in which one or more species of 
Microtus often comes to dominate the small mammal community. 
Kirkland’s (1977) study in the northern Appalachian forests dem- 
onstrated the transitory nature of Muicrotus in the deciduous and 
coniferous forests there. M. pennsylvanicus and Synaptomys coopert 
were absent in both forest types that had not been cut for more 
than 25 years. After cutting, both microtines appeared, but they 
were absent after 5 years. M. chrotorrhinus was present at moderate 
densities in the 7- to 25-year-old forests, but increased significantly 
in both forest types after clearcutting and remained there for at 
least 15 years. Initial responses of the total small mammal com- 
munity included increases in density and in community diversity as 
well as shifts in relative abundance of individual species and trophic 
groups. Krefting and Ahlgren (1974) reported similar responses by 
the small mammal communities following forest fires in Minnesota. 

Gashwiler (1970) obtained similar results in a coniferous (mostly 
Douglas fir) forest in Oregon, where M. oregon: appeared in the 
clearcuts 1 year after cutting and increased to moderate densities 
by the fourth year, then decreased slightly but remained appreciably 
higher than populations in nearby virgin forest. M. richardsoni oc- 
casionally was taken on the clearcut but apparently did not establish 
a resident population there. 

The ability of Microtus to colonize productive habitat quickly 
was demonstrated clearly by Grant et al. (1977), where only a single 
M. ochrogaster was trapped during 15,000 trap-nights in a grazed 
pasture and none was present on the nearby experimental grids 
prior to the application of irrigation water and nitrogen. Yet, within 


Community Ecology 529 


a few weeks a rapidly growing population of prairie voles was 
present in the dense vegetation that resulted from the experimental 
treatment. Although Microtus species can recolonize quickly after 
such disturbances as mowing (Getz, 1970) or grazing (Birney et 
al., 1976), succession of a small mammal community following the 
plowing of a prairie and its subsequent abandonment has not been 
studied adequately. In wetter tallgrass prairie, grasses undoubtedly 
would reappear more quickly than in drier mixed or shortgrass 
prairies, which would have a longer period of domination by an- 
nuals. Here, omnivores such as Peromyscus maniculatus probably 
would dominate for several years before Microtus would invade and 
come to dominate as the climax grasses reappeared. Succession in 
this case would lead to Microtus as the long-term dominant rather 
than as the transitory species it is when forest is the climax vege- 
tation of the region. 

Because the experiments excluding Microtus from some plots but 
not others have not been conducted, it is unknown whether Microtus 
influences the progression of plant succession at a given location. 
Although these exclosure studies would be long-term studies of plant 
and animal community dynamics, we believe that the influence of 
Microtus on the process can only be evaluated through such exper- 
imentation. 


The Role of Microtus in Small 
Mammal Communities 


The major role of Microtus in the small mammal community is 
as principal herbivore in almost all plant communities where it 
lives. As grazers, primarily of stems and leaves, Microtus has the 
potential to alter plant communities and indirectly to help deter- 
mine the habitat structure and resources available to other syntopic 
small mammals. 

Microtus is usually the dominant primary consumer among the 
small mammals living in grassland and tundra communities. Species 
of Microtus that have been studied for their dietary selection eat 
mostly vegetative plant parts. Zimmerman (1965), studying Micro- 
tus food and habitat in western Indiana, reported that M. ochro- 
gaster ate proportionately more roots and seeds (18.8% of volume) 
than did M. pennsylvanicus (0.4% of volume). These two species 
ate insect material at the rate of 4.7 and 3.6%, respectively. Each 


330 Rose and Birney 


species consumed a small amount of Muicrotus flesh and subterra- 
nean fungi, but about 93% of the volume of food was vascular 
plants, mostly stems and leaves. Zimmerman (1965) noted that M. 
ochrogaster took the most common plants in greatest frequency (also 
reported by Fleharty and Olson, 1969, and Martin, 1956, in Kan- 
sas), but some plants, especially the somewhat aromatic Ambrosia, 
Aster, and Solidago, generally were avoided. Meadow voles in In- 
diana (Zimmerman, 1965) ate fewer kinds of plants but were sim- 
ilar to prairie voles in relying heavily on the common species. 
M°’Closkey and Fieldwick (1975), who evaluated the foods of co- 
existing Peromyscus leucopus and M. pennsylvanicus, found that the 
former ate 74% and the latter 8% insect material, the remainder 
being combinations of dicots, monocots, subterranean fungi and, for 
Microtus only, ferns (6%). 

Food selection by M. xanthognathus in black-spruce forest has 
been studied by Wolff and Lidicker (1980) and West (1979), both 
in interior Alaska, and by Douglass (1976, 1977) in Northwest 
Territories. In Alaska, more than 85% of the diet was grasses and 
berries; in Wolff and Lidicker’s (1980) study, a large proportion 
(37% of the volume) was Equisetum (horsetails). Douglass and 
Douglass (1977), who examined the summer foods of M. xantho- 
gnathus, reported the following composition of 629 piles of cuttings: 
89% Carex spp., 5% Rumex, 3% Calamogrostis, 2% Vaccinium, and 
1% Equisetum. Thus, despite their use of taiga as habitat, taiga 
voles ate little woody material but did rely heavily on the grasses 
and other herbs for food. This dietary selection possibly accounts 
for the fact that the densities of M. xanthognathus are much greater 
than have been reported for either M. pinetorum or M. chrotorrhinus 
in other forest environments. 

Stomach content analyses, coupled with a census of the available 
foods, are badly needed to learn more of the details of the role of 
Microtus as consumers. Studies of food habits during periods of 
gradual community change may be especially revealing in explain- 
ing why Microtus often is present only for a relatively brief period 
in early seral stages. During biological succession, if Mzcrotus per- 
sists in relying almost entirely on the ever-diminishing grasses and 
herbs, the replacement of Microtus by Peromyscus leucopus, P. 
maniculatus (woodland subspecies), or Clethrionomys spp. may be 
related more to diminishing food resources than to competition with 
these rodents. Although the water- and nitrogen-supplementation 


Community Ecology 331 


experiments of Grant et al. (1977) suggest a strong positive asso- 
ciation between primary production of grasses on the Colorado 
shortgrass prairie and secondary production of Microtus, additional 
experimental studies are needed, including those of forest-dwelling 
Microtus, to demonstrate a link between the biomass of herbaceous 
vegetation and that of Microtus. The abundance of M. pennsylvan- 
icus, M. oeconomus, and especially M. xanthognathus and vegetative 
cover values correlated positively in early successional stages of 
burned-over black-spruce forest in Alaska, but correlated negatively 
in advanced successional stages (West, 1979). 

Relatively few attempts have been made to examine the biomass 
of small mammal communities, and to measure the changing role 
of the member species from year to year. Pruitt (1966) was unable 
to find synchrony between sample plots of either species or number 
of individuals. However, when he considered biomass per sample 
plot (Pruitt, 1968), he did detect synchrony among the biomasses 
of small mammals. Pruitt’s studies, conducted over 8 years in dif- 
ferent regions of Alaska, evaluated the differential contributions of 
two species of Sorex, two of Microtus, and those of three other 
microtine rodents. Pruitt (1968) interpreted these results to mean 
that ecosystem productivity ‘““waxes and wanes in a regular pro- 
gression.” Chance, which he believed determined the “massive in- 
crease or decrease” of species, perhaps plays less of a role where 
the climatic extremes are not so severe. Martin (1956) looked at 
the relationship between plant production and the biomasses of M. 
ochrogaster and Sigmodon hispidus, but he only reported values for 
a single month; repeated values would have permitted an evaluation 
of the changing roles of the two herbivores to determine whether 
Microtus contributed relatively more during the cool months and 
Sigmodon more in the warm months. 

Grant et al. (1982) compared the effects of habitat perturbation 
(grazing) on the small mammal biomass in different grassland types, 
using treatment and control grids. The detrimental effects were 
substantially greater in the tallgrass prairie (where M. ochrogaster 
and Sigmodon hispidus shared the herbivore role) than at the bunch- 
grass or shortgrass sites. Grant et al. (1982) suggested that seasonal 
and year-to-year fluctuations in the biomass of small mammal species 
cause a high variability in the community biomass of a site, and 
they argued that biomass changes are characteristic of many types 
of North American grasslands (French et al., 1976; Grant and 


332 Rose and Birney 


Birney, 1979). These variations are similar to what Pruitt (1968) 
called “fortuitous” events that determine the changing contributions 
of individual species from year to year at the same location. At the 
tallgrass site, Grant et al. (1982) found that grazing resulted in an 
increased contribution of Spermophilus and Peromyscus maniculatus 
bairdit to small mammal biomass; the contribution of M. ochrogaster 
and Sigmodon to biomass dropped by 90% on the grazed plots. 

French et al. (1976) evaluated the energetics of small mammals 
of grassland ecosystems in the central U.S. Except for 1 year on a 
desert grassland, small mammals consumed less than 10% of the 
available herbage foods. By contrast, a high proportion of animal 
food was eaten at many sites in different years. These authors 
speculated that seed-eaters are more K-selected (they exhibit hi- 
bernation and torpor) and have social mechanisms and body-size 
differences to reduce competition. They argued that these adapta- 
tions contributed to their success relative to the grass-eaters in short- 
grass prairie, where Microtus is abundant only on experimental 
plots in which water and nitrogen stimulated growth of grasses 
(Grant et al., 1977). 

Golley (1960) measured energy flow in a grass-Microtus-Mustela 
system in Michigan. He estimated that M. pennsylvanicus consumed 
only 1.6% of the energy available to it, and that the weasel con- 
sumed 31% of energy available in the form of Microtus. 

The presence of Microtus in a community often results in a sig- 
nificant physical alteration of the environment because they con- 
struct runways and burrows and extensively clip herbaceous vege- 
tation. Pearson (1959), using photographs, showed that many other 
species of small mammals used runways built and maintained by 
Microtus. Digging activities of Microtus may create exposed soil 
substrates needed by seeds to germinate. Effects of grazing by M:- 
crotus are disputed and undoubtedly are variable; grazing may stim- 
ulate some plants to produce new vegetative growth but also may 
seriously or mortally wound other plants. Experiments to evaluate 
critically the role of Microtus in altering the habitat, using exclo- 
sures and measured densities of voles, have not been conducted at 
even a single location, to our knowledge. This is certainly an area 
of research where large contributions can be made in our under- 
standing of the role of Microtus in the small mammal community 
and in the ecosystem. 


Community Ecology 333 


Conclusions and Perspectives 


Microtus is found in most grassland and tundra communities, and 
to a lesser extent in forest communities north of 35°N. As many as 
four to six species of Microtus may be broadly sympatric in some 
regions, such as in the western U.S. Muicrotus often is both the 
largest and the most numerous small mammal, and the genus may 
contribute 90% or more of the small mammal biomass per unit 
area. Exceptions to this trend can be found in marginal habitats, 
in the usually brief periods of low density in population cycles, in 
certain successional stages, and in forests. Predators may focus on 
Microtus where it is abundant, and Microtus influences the small 
mammal community in other ways. Microtus eats plant parts almost 
exclusively and is usually the dominant primary consumer. 

Despite this prominent position in its community, Microtus rarely 
has been evaluated, and almost never studied, in the community 
context. Sometimes Microtus and one or two syntopic microtines are 
examined, either for evidence of competition or of synchrony of 
population cycles. In some instances, the composition and relative 
numbers of small mammals in the community are reported, per- 
mitting the reader to assess the potential effect of coexisting species 
on Microtus. Occasionally authors make it clear that non-microtines 
were or were not permanently removed from the study grids, but 
in many cases no statement is given about the occurrence of other 
species. Although it is understandable that microtine population 
ecologists may foresee little immediate benefit from the trapping, 
tagging, and handling during each trapping period of dozens of 
Peromyscus, Sigmodon, Reithrodontomys, or other species, an under- 
standing of the dynamics of these species may be crucial to explain- 
ing microtine cycles, especially if Lidicker (1973, 1978) is correct 
in his assertion that many factors are involved in population reg- 
ulation of Microtus. More importantly, neither the influence of M:- 
crotus on the small mammal community nor the role of Microtus in 
the ecosystem can be evaluated critically until all small mammals 
are examined together. 

One thing we have learned, more than any other, from writing 
this chapter, is that the study of Microtus in the community context 
is a potentially fertile area of research. Microtus typically is not 
present in community studies of small mammals in desert (Brown, 


334 Rose and Birney 


1973, et seq.) nor in eastern decidious forest (Dueser and Shugart, 
1978, 1979). Among those studying Microtus, only West (1979) has 
used Dueser and Shugart’s technique of measuring vegetation struc- 
ture and predicting which species will use which components of the 
physical habitats. Except for Grant’s (1969, et seq.) experimental 
studies of competition with field populations of M. pennsylvanicus 
and one other species, planned experiments have not been conducted 
to learn more details of the respective roles of the four to six small 
mammal species in grassland and tundra communities. The study 
of mammalian community ecology in these plant communities will 
not be easy, in part because the number of Microtus often is much 
greater than that of all others. On the other hand, when numbers 
of Microtus are low, poor trapping success may cause the investi- 
gator to question whether or not to continue the study. Perhaps the 
best descriptive studies could be conducted in plant communities 
that are in transition; for example, large grasslands that grade into 
shrubby ecotones and then into young and old forest could be ideal. 
Here it would be possible to see the changing role of grassland 
Microtus as the woody elements increase to dominance. Leaps of 
insight will be possible using perturbation experiments, especially 
large and well-replicated ones in which more than two species can 
be evaluated simultaneously. Finally, some investigators, such as 
West (1979), have the necessary detailed information from fairly 
long-term studies to meld what may have been designed as multiple 
population studies into reports of small mammal communities with 
Microtus. Such reports would be extremely valuable in providing 
direction for the descriptive and experimental studies that are nec- 
essary if we are to learn the true influence and role of Microtus in 
small mammal communities. 


Acknowledgments 


We thank our wives, Aleene Rose and Marcia Birney, for their 
indulgence during the 10 days we devoted to writing the first draft 
of this chapter. Prassede Calabi, Ray Dueser, Roger Everton, Norm 
French, Lowell Getz, Gerda Nordquist, John Porter, and an anon- 
ymous reviewer all provided useful suggestions on earlier drafts. 
Steve West assisted us immeasurably by reviewing the manuscript, 
making a copy of his dissertation available to us, and especially by 
verifying our interpretation of statements about Alaskan mammals. 


Community Ecology 335 


Neither of us has studied mammals in the tundra or taiga in North 
America and we thank Steve for contributing to the accuracy of 
several of our remarks. Full responsibility for all interpretations 
and conclusions, of course, rests with us. 


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Community Ecology 339 


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BEHAVIOR 
JERRY O. WOLFF 


Abstract 


EHAVIOR of Microtus may be categorized as either non-social or 
B social. Non-social behaviors such as locomotory, exploratory, 
body maintenance, swimming, and nest and runway construction 
are adapted to the two-dimensional grassland environment inhab- 
ited by these animals. The social organization of microtines is the 
result of behaviors associated with courtship and mating, parental 
care, social structure (spacing patterns), aggression, communication, 
and communal nesting. Mating systems of Microtus are commonly 
promiscuous (for example, M. pennsylvanicus and M. richardsont.), 
polygynous (for example, M. xanthognathus, M. californicus, and M. 
montanus), and rarely, but sometimes monogamous (for example, 
M. ochrogaster). Species-specific copulatory patterns are adapted to 
particular social organizations in specific habitats and may also be 
a reproductive isolating mechanism between similar sympatric 
species. Most social groupings consist of mother-young units and 
paternal care is minimal or non-existent. In some species territo- 
riality occurs only in males (for example, M. xanthognathus), in 
females (for example, M. pennsylvanicus and M. richardsont), or in 
both sexes (for example, M. montanus, M. ochrogaster, and M. cal- 
ifornicus). Patterns of aggression may vary between species, but 
within a species they follow a predictable pattern that is correlated 
with a particular type of social system. If females are aggressive, 
they usually fight for space, whereas males fight for space and/or 
females. Scent-marking by the deposition of sebum from sebaceous 
glands located in the hip or flank region is described for several 
species and functions in individual recognition, territorial marking, 
and mate attraction. Communal winter nesting and food storing 
occur in several northern species and are adaptations for survival 
in severe boreal climates. An attempt is made to integrate the social 
structure and socio-ecology of Mucrotus within the life history 
framework of this mammal group. 


340 


Behavior 341 


Introduction 


In North America, members of the genus Microtus are concen- 
trated in grassland habitats between 40° and 70°N latitude. This 
range is characterized by a fluctuating environment which favors 
life history strategies adapted to seasonality and a variety of extrin- 
sic variables. The adaptive zone of Microtus includes: 1) consump- 
tion of vegetation parts (primarily grasses); 2) r-selected reproduc- 
tive features; 3) ability to colonize new habitats; and 4) a complex 
repertoire of behaviors associated with each of these features. These 
behaviors may be non-social, such as locomotory, exploratory, and 
foraging and food gathering behaviors, nest and runway construc- 
tion, and body maintenance; or social, which include mating, pa- 
rental, communicatory, agonistic, and other behaviors involving in- 
teractions between individuals. Social behavior is extremely complex 
and variable, and more difficult to observe, document, and interpret 
than non-social behavior, but it is essential to understanding the 
evolutionary significance of life history traits. In this chapter, I 
summarize the available literature on Microtus behavior and em- 
phasize the evolutionary significance of social behavior and orga- 
nization. An attempt also is made to compare behavioral patterns 
across species to show parallel adaptations to similar ecological re- 
gimes. 


Non-social Behavior 


A description and classification of behavioral components of lo- 
comotion, grooming, general body maintenance, and comfort move- 
ments have been described for several species of Microtus (Dews- 
bury et al., 1980; Jannett, 1977; Sloane et al., 1978; Webster et al., 
1979; Wilson et al., 1976) (Table 1). Locomotor-exploratory be- 
havior is the most prevalent behavior for all species. All species 
exhibit wall-seeking behavior, rearing at wall, grooming head mov- 
ing, and freezing. Jumping is infrequent and climbing is not ob- 
served. Climbing does not appear to be an adaptive feature in Mi- 
crotus species that inhabit a two-dimensional grassland habitat. In 
addition, depth perception is not apparent in M. montanus and is 
only slightly developed in M. californicus and M. pennsylvanicus 
(Sloane et al., 1978). In comparative studies between different taxa, 


342 Wolff 


TABLE 1 
NON-SOCIAL BEHAVIORS FOR NEW WoRLD Microtus 


Locomotion, 


maintenance, Runway Nest 

and comfort Dig- Swim- construc- _ build- 

movements’ ging? ming? tion‘ ing? 
M. californicus xX xX x 
M. canicaudus x x 
M. montanus x x x xX x 
M. ochrogaster x x x x x 
M. pennsylvanicus Xx x x Xx xX 
M. richardson x x xX 
M. xanthognathus x x x 


' Dewsbury et al. (1980); Jannett (1977); Sloane et al. (1978); Webster et al. (1979); 
Wilson et al. (1976). 

>? Webster et al. (1981). 

> Evans et al. (1978); Getz (1967); Ludwig (1981); Wolff (pers. observ.). 

* Fitzgerald and Madison (1983); Ludwig (1981); Thomas and Birney (1979); 
Wolff (1980); Wolff and Lidicker (1981). 

* Ambrose (1973); Dalquest (1948); Hartung and Dewsbury (1979a); Jame- 
son (1947); Jannett (1978a, 1981a); Ludwig (1981); Martin (1956); Maser and 
Storm (1970); Salt (1978); Thomas and Birney (1979); Wolff and Lidicker (1981). 


field-dwelling species such as Microtus exhibit more boli deposition, 
freezing, and grooming compared to forest and desert dwelling gen- 
era (Wilson et al., 1976). 

Apparently all Microtus species are capable of digging as evi- 
denced by the extensive network of underground runways and tun- 
nels; however, this behavior has not been analyzed and described 
for all species. Digging behaviors of three Microtus species (M. 
montanus, M. ochrogaster, and M. pennsylvanicus) have been ob- 
served on peat and sand substrates in the laboratory (Webster et 
al., 1981). The most prevalent digging pattern involved simulta- 
neous use of the rear paws together with alternating use of the 
forepaws. The amount of digging for each species varied depending 
on substrate. 

Swimming behavior has been documented and quantified in the 
laboratory for M. pennsylvanicus, M. montanus, M. ochrogaster, and 
M. californicus (Evans at al., 1978) (Table 1). Based on their ten- 
dency to enter the water and the amount of time spent swimming, 
Evans et al. (1978) concluded that M. ochrogaster was the best 
swimmer and M. californicus and M. pennsylvanicus were the worst. 


Behavior 343 


Getz (1967) also found that M. ochrogaster avoided water more than 
M. pennsylvanicus and he correlated this with the dry grassland 
nature of M. ochrogaster in contrast to the more moist habitat char- 
acteristic of M. pennsylvanicus. Microtus richardson and M. xan- 
thognathus occur along streams and in mesic habitats and both swim 
regularly (Ludwig, 1981; J. Wolff, pers. observ.). 

Most Microtus species are active day and night (Madison, this 
volume) and use well-established runway systems. These systems 
consist of a complex network of above-ground runways and under- 
ground tunnels and burrows. Microtus montanus makes extensive 
use of tunnels, whereas M. pennsylvanicus is more active above 
ground. Microtus pinetorum is almost entirely fossorial, coming to 
the surface only occasionally to feed. About half of the runway 
systems of M. xanthognathus and M. richardsoni are above ground 
and the other half underground (Ludwig, 1981; Wolff and Lidick- 
er, 1980). In M. xanthognathus and M. richardson, runway systems 
are concentrated along streams and frequently incorporate water- 
ways into the runway system. Surface and subterranean runways 
of Microtus species in general are interconnected with numerous 
branches going to feeding areas, waterways, and dead ends which 
are apparently used for resting or temporary shelters. ‘The number 
of underground versus above-ground runways is apparently related 
to friability of soils and accessibility of food. Several species are 
known to maintain runways to keep them clear of debris that may 
hinder movements (for example, M. ochrogaster [Thomas and Bir- 
ney, 1979]; M. xanthognathus [Wolff, 1980]). 

Nests usually are constructed of dried grass and may be located 
above or below ground. Exclusive use of grasses for nests has been 
reported for M. canicaudus, M. montanus, and M. pennsylvanicus 
(Maser and Storm, 1970), and M. ochrogaster (Jameson, 1947; 
Martin, 1956). Microtus montanus has surface and subsurface nests, 
but brood nests are always located underground (Jannett, 1978a, 
1981a). Both male and female M. ochrogaster have been observed 
to construct nests in the laboratory, but males do most of the runway 
maintenance (Thomas and Birney, 1979). Ambrose (1973) found 
that most M. pennsylvanicus nests were located in slightly elevated 
dense tussocks of living grass. 

Dalquest (1948) and Salt (1978) reported that water voles used 
subterranean nests in summer and subnivean nests on the soil sur- 
face in winter. Ludwig (1981), however, found that water voles 


344 Wolff 


used subterranean nests year-round. Nests ranged in size from 
10 to 24 cm in diameter and were constructed of short segments of 
leaves and stems of grasses, sedges, and rushes (Agropyron, Cala- 
magrostis, Carex, and Juncus) (Ludwig, 1981). Nest chambers were 
located beneath logs, stumps, or at the herbaceous/soil interface. 
Both summer and winter nests of M. xanthognathus are subterra- 
nean (Wolff and Lidicker, 1980). Eight summer nests examined by 
Wolff and Lidicker averaged 15 cm in diameter and were made of 
dried grass (Calamagrostis). Some nests were cup-shaped and others 
were round with an inner chamber. Most nests were situated at the 
moss-soil interface, but some were located on top of abandoned 
winter nests. Winter nests were larger than summer nests and were 
located in underground chambers, but above permafrost. 

Hartung and Dewsbury (1979a) observed nest building behavior 
of M. ochrogaster, M. montanus, M. californicus, and M. pennsylvan- 
icus in the laboratory. Microtus ochrogaster built few nests while the 
other three species built mostly cup-shaped nests and equal num- 
bers of platform (pallet of cotton on floor but not shaped) and 
covered nests. Males and females built the same numbers of nests 
of each type. 


Social Behavior 


Mating Systems and Social Structure 


Because of the secretive nature of voles, microtine social behavior 
has been difficult to study. Much of the information on Microtus 
behavior has been anecdotal or collected inadvertently in studies on 
demography. Several recent studies, using a variety of field and 
laboratory techniques, have provided insight into the social biology 
of a few select species of Microtus. The results of these studies have 
been discussed in detail (see The Biologist, Vol. 62, No. 1, 1980, 
Special Symposium Volume, Social Organization of Microtine Ro- 
dents). 

Microtine behavioral systems are highly variable, but fall into 
four arrangements: 1) males occupy exclusive ranges and females 
mate polygynously or promiscuously within the range of a territo- 
rial male; 2) females occupy exclusive territories overlapped by 
home ranges of one or more males; 3) both males and females are 


Behavior 345 


territorial and intolerant of conspecific adults of the same sex, or of 
both sexes, except during courtship and mating; and 4) more than 
one male or female occupy exclusive communal territories. Various 
parameters of the social organization of several Microtus species are 
summarized in Table 2 and are discussed below. 

Meadow voles (Microtus pennsylvanicus).—'The social biology 
of meadow voles has been studied most extensively by Madison 
(1978, 1979, 1980a, 19806, 1980c, 1981, 1984), Madison et al. 
(1984), and Webster and Brooks (1981). With the aid of radiote- 
lemetry, these studies have provided the most conclusive data on 
social organization in any microtine species. Meadow voles have a 
promiscuous mating system and socially are organized into terri- 
torial maternal-young units during the breeding season (Madison, 
1980a) and communal mixed-sex and age groups during winter 
(Madison et al., 1984; Webster and Brooks, 1981; Table 2). 

During the breeding season, reproductively active females main- 
tain individual territories that are actively defended against other 
females. Madison (1980a) found that when overlap occurred be- 
tween females, one female was usually 10-25 g larger than the 
other and only she bore young. Madison proposed that these fe- 
males were mother-daughter units and the mother in some way 
inhibited the daughter from reproducing. Getz (1961) also found 
that subadults do not move from their home range before reaching 
sexual maturity. Other than these proposed mother-daughter units, 
territories remain exclusive with respect to other females during the 
breeding season. After reproductive shutdown in fall and winter, 
females will tolerate sons and other males in their nests (Madison, 
pers. comm.). 

Home ranges of males may overlap those of several other males 
as well as those of several females (Getz, 1961; Madison 1980c; 
Webster and Brooks, 1981). Male ranges are three times larger 
than those of females (244 and 74 m’, respectively; Madison, 19800; 
see also Ambrose, 1969; Getz, 1961; Hamilton, 1937; Webster and 
Brooks, 1981). Home-range and territory sizes are inversely cor- 
related with habitat quality and population density (Getz, 1961). 
Male home ranges are not well defined and may change daily; the 
greatest overlap occurs in the vicinity of estrous females (Getz, 
1961; Madison, 19805; Webster and Brooks, 1981). 

The mating system of meadow voles appears to be promiscuous 
with males competing for access to females (Madison, 1980a, 1980c). 


Wolff 


346 


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Behavior 347 


Based on spatial distribution and sequential use of live-traps, Reich 
and Tamarin (1980) found that female meadow voles avoided each 
other, and were indifferent towards males. Males, on the other 
hand, did not avoid each other, and were attracted to females. Web- 
ster and Brooks (1981) reported five male voles coming into the 
territory of an estrous female with four attempting to copulate with 
her. Using multiple-capture live-traps, Getz et al. (1981) caught 
male-female pairs in only 1.8% (128) out of 7,104 captures. No 
male-female pair was ever recaptured in the same trapping session 
or at other trap stations. Using radiotelemetry, Madison (1980a) 
located 100 voles over 14,000 times and had no instances of nest 
cohabitation or pair-bonding. Space use patterns of adults and lack 
of multiple captures of male-female pairs suggest a lack of external 
well-developed social grouping among adults during the summer 
breeding season. 

Females appear to exhibit some choice in mate selection. Madi- 
son (1980c) proposed two possible strategies for mate selection by 
female meadow voles. One, supported by the observation of Webster 
and Brooks (1981), is that vocalization by a female may attract a 
known resident male who chases off “low quality” suitors. ‘Thus, 
the female may assess male quality as a result of male-male com- 
petition. Secondly, Madison proposed that it may be advantageous 
for females to mate with all suitors to encourage their confidence 
of paternity. Males who are potentially sires of these offspring 
would be inhibited intrinsically from committing infanticide. 

Multiple inseminations may also be a strategy to increase genetic 
variation and adaptation in littermates as suggested for ground 
squirrels (Hanken and Sherman, 1981). The benefits of secondary 
matings accruing to males as a result of sperm competition must 
also be considered (Dewsbury and Baumgardner, 1981). 

Montane voles (Microtus montanus).—The social organization 
of montane voles has been studied extensively in the laboratory and 
in fields of northwestern Wyoming by Jannett (1978a, 19786, 1980, 
1981a, 1981b). The social structure of montane voles is based on 
male and female territoriality and a variable mating system ranging 
from polygyny to facultative monogamy (Jannett, op. cit.) (Table 
2). 

Using a variety of field techniques including live-trapping, track- 
ing animals implanted with irradiated tantalum ('*’TA) wires, and 
manipulating populations in an enclosure, Jannett found that dur- 


348 Wolff 


ing the breeding season parous female montane voles were intra- 
sexually territorial. Females maintained exclusive areas and drove 
away other females, but they did not drive away males or their own 
young. Adult males also maintained stable territories that were 
mutually exclusive of other territorial males, but that overlapped 
those of one or more females. Males shifted their activity within 
their territories to be in the vicinity of estrous females. Males and 
females are not known to co-nest (Jannett, 1982). 

The use of space and territorial maintenance by females varies 
with population density ( Jannett, 1980). In low-density areas where 
the chances of reestablishment are high, parous females abandon 
their young and maternal nest site and set up a new territory in a 
new area, while the young remain in the natal area. At high den- 
sities there is little vacant habitat available, and females continue 
to nest with juveniles from one or two litters; they do not desert 
their home site. Abandonment of the brood nest by the dam also 
may occur, as suggested by anecdotal observations, in M. pennsyl- 
vanicus (Getz, 1961; Hamilton, 1941; Madison, 1978; Myers and 
Krebs, 1971), M. ochrogaster (Myers and Krebs, 1971), M. oecon- 
omus (Tast, 1966), and in two Old World species, M. arvalis (Frank, 
1957) and M. agrestis (Myllymaki, 1977). 

Female montane voles apparently mate with only one familiar 
male, but do not form a monogamous pair bond. Paternal behavior, 
such as sitting on the pups, licking pups, and manipulating nesting 
material, has been observed in the laboratory, but this is not nec- 
essarily indicative of monogamy in the wild (Hartung and Dews- 
bury, 19795). Polygyny appears to be a common mating system in 
montane voles, although facultative monogamy obviously occurs at 
low densities. 

Prairie voles (Microtus ochrogaster) .—Although the mating sys- 
tem and social organization of prairie voles has not been docu- 
mented in the field, the circumstantial evidence obtained from lab- 
oratory studies on parental care and mating behavior presents a 
strong case for monogamy. (Getz and Carter, 1980; Gray and 
Dewsbury, 1973; Thomas and Birney, 1979). 

Thomas and Birney (1979) recorded monogamous mating in 26 
of 27 groups observed in the laboratory. In only one case did they 
observe a polygynous mating. In this case, the two females nursed 
communally and co-nested with litters of different ages. Gray and 
Dewsbury (1973) and Dewsbury (1981) found that prairie voles 


Behavior 349 


failed to demonstrate the Coolidge effect (when a satiated male 
does not copulate with a new estrous female). This suggests that 
male prairie voles are not promiscuous by nature, but rather pair- 
bond with one female at a time. 

In dyadic encounters in the laboratory, males and females from 
breeding pairs tended to show high levels of aggression toward 
unfamiliar animals of the opposite sex, but never toward each other 
(Getz et al., 1981). The male played the prominent role in attacking 
both male and female strangers (Getz and Carter, 1980). Introduc- 
tion of a new male to caged females caused abortion in pregnant 
females (Stehn and Richmond, 1975). Females will accept a strange 
male only if the stud male is killed or removed (Getz et al., 1981). 

Male and female prairie voles contribute equally to care of the 
young with the exception of lactation (Getz and Carter, 1980; Getz 
et al., 1981; Thomas and Birney, 1979). Paternal activities include 
nest and runway construction, food caching, and grooming, retriev- 
ing, and brooding the young. In eight out of 45 litters observed, 
males constructed a second nest and brooded part of the litter while 
the female brooded the remaining young in the primary nest 
(Thomas and Birney, 1979). In these cases, the litters that were 
separated into two nests were larger on average (3.5 pups/litter) 
than young kept in a single nest (2.5 pups/litter). 

In M. ochrogaster, older pups frequently stay in the nest and 
groom, retrieve, and brood neonates from a succeeding litter (Getz 
and Carter, 1980; Getz et al., 1981; Thomas and Birney, 1979). 
Maternal care of the second litter is significantly less than that 
devoted to the first litter. Baby-sitting by the older litter, therefore, 
allows the breeding female more time for feeding and other activities 
away from the nest (Getz and Carter, 1980). 

The only field study which examined the social structure of prai- 
rie voles was conducted by Getz et al. (1981). Using multiple- 
capture live-traps, Getz et al. captured male-female pairs together 
in 13.2% (1,664 out of 12,565) of their total captures. Multiple 
captures of males and females do not occur in a promiscuous species 
such as meadow voles. Getz and his colleagues found that these 
male-female associations persisted through the non-breeding season 
indicating a long-term pair bond. 

Taiga voles (Microtus xanthognathus) .—The only studies on the 
social system of taiga voles are those of Wolff (1980) and Wolff 
and Lidicker (1981). During the breeding season the social orga- 


350 Wolff 


nization of taiga voles is based on male territoriality and a polyg- 
ynous mating system (Table 2). The social system fits the model 
for resource-defense polygyny (Emlen and Oring, 1977). Based on 
a mark-recapture live-trapping study, Wolff (1980) found that 
males occupied well-defined territories. An average of two to four 
females had overlapping home ranges within the territory of each 
male. On two occasions, two pregnant females were caught together 
in the same trap. This does not occur in species in which females 
are territorial (for example, in M. pennsylvanicus; Getz et al., 1981). 

Little evidence is available on mating behavior and paternal care 
in taiga voles. I have observed males in the laboratory mate with 
as many as three females in one day, indicating that multiple mat- 
ings do occur. According to Dewsbury (1981), multiple matings are 
indicative of polygynous or promiscuous mating. I have observed 
males nesting with lactating females, but have not observed any 
paternal behaviors as described for prairie voles (Thomas and Bir- 
ney, 1979). I have observed females retrieving young and tucking 
them under the male, but the male played no active role in retriev- 
ing or grooming the young. 

Pine voles (Microtus pinetorum).—Anecdotal evidence by Paul 
(1970) and Boyette (1966) suggested that pine voles were “loosely 
colonial” or occurred in locally abundant aggregations (Benton, 
1955; Hamilton, 1938). The most conclusive data on spacing, move- 
ments, and social organization of pine voles has been provided by 
a radiotelemetry and live-trapping study (Fitzgerald and Madison, 
1981, 1983). Pine voles occur in apple orchards and their ecology 
and behavior are closely tied to the spacing of apple trees. Fitzgerald 
and Madison found that pine voles existed in discrete non-overlap- 
ping family units with an average of 4.2 individuals per unit (n = 
20). Each family had a discrete non-overlapping territory with 
neighboring family units. The average family unit consisted of 1.9 
adult scrotal males, 1.2 adult females, 0.7 subadult and juvenile 
males, and 0.4 subadult and juvenile females. Home ranges of fam- 
ily members overlapped extensively. All family members utilized 
one or two communal nests within the family territory and all of 
the members commonly used the same nest at the same time. 

Fitzgerald and Madison (1981, 1983) found that home ranges of 
pine voles were linear with an average width for both males and 
females of 3 m (conforming to the approximate drip-line of the 
trees within a row). The average family unit occupied a territory 


Behavior 351 


14.7 m long and 3.1 m wide. Home-range size averaged 44.7 m?’ 
for males and 41.7 m? for females. Fitzgerald and Madison (1981, 
1983) concluded that each family was a discrete unit with little 
movement between family ranges. They recorded movement be- 
tween territories in only 25 out of over 7,500 telemetry positions. 
Only six individuals moved permanently from one group to an 
adjacent group. 

The mating system of pine voles has not been studied directly in 
the laboratory or in the field, but it has been inferred from radio- 
telemetry and live-trap data (Fitzgerald and Madison, 1981, 1983). 
The mating system of pine voles appears to be flexible, covering 
monogamy, polygyny, and even polyandry. The genetic relation- 
ships between and among breeding males and females in a family 
unit have not been determined. However, based on extensive trap- 
ping and radiotelemetry, the constituents of the group appear to be 
the founding pair and their mature (and immature) offspring. 

Water voles (Microtus richardsoni) .—Several aspects of the so- 
cial organization of water voles have recently been elucidated in a 
live-trapping and radio-tracking study conducted by Ludwig (1981) 
in west-central Alberta, Canada. Water voles have linear home 
ranges along streams (see also Anderson et al., 1976; Pattie, 1967). 
Home ranges of adult females are about 94 m long and 10 m wide 
and exhibit minimal or no overlap with other females. Mean home- 
range size for males is 332 m by 10 m and home ranges overlap 
those of other males and from one to four females. Female ranges 
are overlapped by one to three males. Home ranges for females are 
fairly stable throughout the breeding season and apparently are 
territories. Ludwig recorded one instance of male-female cohabi- 
tation which lasted a short time, but most voles nest singly. Based 
on male and female spacing patterns in the field, it appears as 
though water voles exhibit a promiscuous or polygynous mating 
system. The social organization of M. richardsoni is apparently very 
similar to that of Arvicola terrestris (Stoddart, 1970). 

California vole (Microtus californicus).—The social biology of 
the California vole has been reviewed by Lidicker (1980), who 
made reference to his earlier works (Lidicker, 1973, 1976, 1979) 
and those of Stark (1963), Pearson (1960), and Kenney et al. (1979). 
Lidicker concluded that the California vole is a “‘social moderate, 
avoiding the mongamous rigidity of M. ochrogaster on the one hand 
(Getz and Carter, 1980; Thomas and Birney, 1979) and the ramp- 


352 Wolff 


ant polygyny or promiscuity of M. xanthognathus and M. pennsyl- 
vanicus on the other (Wolff, 1980; Madison, 1980c).” 

Territorial behavior seems well developed in both sexes. Adult 
males have larger home ranges than do females (Batzli and Pitelka, 
1971; Krebs, 1966; Lidicker, 1973), although both sexes have ap- 
proximately the same size core areas where they spend over 85% 
of their time (Ford and Krumme, 1979). Unbalanced sex ratios in 
free-ranging populations suggest that one male may be mating with 
more than one female. 

Lidicker (1976, 1979) introduced seven populations of California 
voles consisting of two or three pairs into 10 x 10-m enclosures. In 
five cases, fighting was intense; no reproduction occurred until a 
single pair remained. In one instance, one male and two females 
survived the initial fighting. Females divided up the enclosure, and 
both reproduced successfully while the male moved throughout. In 
the final case, two pairs persisted, dividing up the enclosure into 
two approximately equal territories. Six out of these seven cases 
resulted in monogamous matings. In a plastic runway system in the 
laboratory, adult males have been observed driving away and some- 
times killing females that are not their mates (Lidicker, 1980). 

Using automatic cameras placed in vole runways, Pearson (1960) 
found that: 1) individual runways were used by family groups rang- 
ing in number from 2 to 12 (X = 6); 2) family groups consisted of 
an adult male and one or more females and their young; and 3) 
there was very little interchange of individuals among runway sys- 
tems. This evidence further suggests that the mating system of Cal- 
ifornia voles is bordering on monogamy-polygyny. 

Only fragmentary information is available regarding paternal 
care of young. Brooding of young by fathers has been reported by 
Hatfield (1935) and Hartung and Dewsbury (19796). In captivity, 
males gather nesting material and retrieve and manipulate nest- 
lings; furthermore, lactating females are not antagonistic to their 
mates (Hartung and Dewsbury, 19796; Lidicker, 1980). Given the 
opportunity, however, adult males will cannibalize nestlings which 
are not their own offspring (Lidicker, 1980). 

Lidicker (1980) concluded that the basic social unit is the family 
group. Monogamy occurs at low densities and may be facultative 
as opposed to obligate (Kleiman, 1977). Polygyny occurs and may 
be the prevailing pattern at high densities. Weak pair-bonding oc- 
curs, but it is not the pair bond typical of monogamous species. 


Behavior 353 


Dewsbury (1981) has proposed a “monogamy scale” by which 
rodent mating systems can be predicted by measuring a series of 
correlates derived from a variety of sources. Characteristics that 
appear to be correlated with monogamy include: sexual monomor- 
phism (see also Dewsbury et al., 1980), latency to initiate copula- 
tion, allogrooming of female by the male, low number of ejacula- 
tions prior to satiety, lack of the Coolidge effect, lack of copulatory 
plugs, low reproductive potential, paternal behavior and pair-bond- 
ing, low rate of physical maturation, and delayed rate of sexual 
maturation. The converse of these characteristics are indicative of 
promiscuous or polygynous mating systems. 

Based on the monogamy scale, Dewsbury predicted that M. pi- 
netorum, M. ochrogaster, and M. californicus would be most likely 
to display monogamy and M. montanus and M. pennsylvanicus to 
be least likely. Microtus xanthognathus, M. canicaudus, M. oecono- 
mus, and M. montanus fall somewhere between these two extremes 
on the scale. Evidence gathered from field studies is largely sup- 
portive of this model. 


Copulatory Behavior 


Descriptions of copulatory behavior and discussions on the adap- 
tive significance of copulatory patterns in Microtus have been re- 
ported for M. californicus (Kenney et al., 1978), M. montanus 
(Dewsbury, 1973), M. ochrogaster (Gray and Dewsbury, 1973), M. 
pennsylvanicus (Gray and Dewsbury, 1975; Gray et al., 1977), M. 
pinetorum (Dewsbury, 1976), and M. canicaudus, M. oeconomus, 
and M. xanthognathus (Dewsbury, 1982). The basic motor pattern 
of copulation in all Microtus species includes the following. The 
male mounts the female from behind, grasping her flanks with his 
forepaws. Concommitantly, the female assumes a lordotic posture. 
On mounting, the male executes a series of short, rapid pelvic move- 
ments and vigorously palpates the females flanks. Extra-vaginal 
thrusting usually occurs before intromission, which is then followed 
by intra-vaginal thrusting. Ejaculation occurs at the terminal por- 
tion of certain intromissions, usually following several intra-vaginal 
thrusts. Non-copulatory behaviors such as running, sniffing part- 
ner, nuzzling, sparring, genital grooming, general grooming, and 
locomotory-exploratory behavior commonly occur between copula- 
tory bouts. 


354 Wolff 


The number of ejaculations, mounts, intromissions, thrusts per 
intromission, and time intervals between each behavior vary con- 
siderably between species. For instance, M. montanus and M. och- 
rogaster exhibit multiple intromissions followed by multiple ejacu- 
lations, whereas M. pennsylvanicus, M. californicus, and M. pinetorum 
exhibit a single intromission followed by multiple ejaculations. The 
mean number of ejaculations prior to satiety range from 2.0 in M. 
ochrogaster (Gray and Dewsbury, 1973) to 5.0 in M. montanus 
(Dewsbury, 1973) and 5.9 in M. pennsylvanicus (Gray and Dews- 
bury, 1975). The mean time interval between intromissions within 
a given ejaculatory series was 14.8 s in M. montanus (Dewsbury, 
1973) and 32.9 sin M. pennsylvanicus (Gray and Dewsbury, 1975). 
Microtus montanus and M. pennsylvanicus exhibit the Coolidge ef- 
fect, whereas M. ochrogaster does not (Dewsbury, 1981). 


Communal Winter Nesting and Food Storing 


Communal winter nesting and storing food in the vicinity of the 
nest occur in several species of Microtus (Table 2). These behaviors, 
which appear to be more common at northern than at southern 
latitudes, are apparent adaptations for overwintering in cold envi- 
ronments. The energetic gains from communal nesting have been 
well documented (Beck and Anthony, 1971; Gebczynska and Geb- 
czynski, 1971; Wiegert, 1961; Wrabetz, 1980). West and Dublin 
(1984) and Madison et al. (1984) provide reviews on communal 
nesting in small mammals. Communal nesting consists of group 
living in which 5-10 or more individuals co-nest during part of the 
year. Communal nesting does not normally occur during the repro- 
ductive season (except in pine voles; Fitzgerald and Madison, 1981, 
1983), but is rather common during the non-reproductive season, 
usually winter. Food storage consists of collecting and storing food 
in a food cache which is then eaten during the subsequent inclement 
period. 

Communal winter nesting of non-reproductive individuals of 
mixed sex and age groups has been reported in meadow voles 
(Madison et al., 1984; Webster and Brooks, 1981). Madison et al. 
(1984) found that winter communes of M. pennsylvanicus consisted 
of non-overlapping maternal families in early winter and shifted to 
mixed non-lineage groups during late winter. They found that win- 
ter communal nesting did not always occur, but was dependent on 


Behavior 355 


ambient temperature and snowfall. Communal nesting was not 
found during the summer breeding season, but females tolerate sons 
and fathers in their nests in late fall. 

Winter food caching by meadow voles (M. pennsylvanicus) has 
been reported on a number of occasions (Bailey, 1920; Gates and 
Gates, 1980; Hatt, 1930; Lantz, 1907; Riewe, 1973). Caches con- 
tained fruits of Falcata comosa, and tubers of Helianthus tuberosus 
(Bailey, 1920), roots of Convolvulus sepium (Lantz, 1907), and leaves 
and roots of Leontodon autumnalis and Trifolium spp. (Riewe, 1973). 
Gates and Gates (1980) described a meadow-vole food cache con- 
sisting of underground parts of Potentilla canadensis, Viola papilio- 
nacea, and Ranunculus bulbosa. Food hoarding and communal nest- 
ing in non-reproductive individuals is probably the typical behavior 
pattern of M. pennsylvanicus in winter, and no doubt occurs in 
many other species of Microtus as well. 

Communal winter nesting in groups of 5-10 individuals also 
occurs in taiga voles (Wolff, 1980; Wolff and Lidicker, 1981). An 
underground food cache that contains rhizomes of Fquisetum and 
Epilobium is located adjacent to the nest. The nest and food cache 
are frequently located about 30 cm under the ground, often under 
a tangled mass of branches, roots, or a fallen log. Nests have up to 
five entrances, whereas the food cache has a single access from the 
nest. Food is collected and stored from mid-August to mid-Septem- 
ber. Taiga voles remain active all winter, but over 90% of their 
food consists of rhizomes stored in the food cache and the remainder 
is obtained from foraging under snow (Wolff and Lidicker, 1980). 

Each communal group consists of an average of 7.1 individuals 
of mixed sex and age groups (Wolff and Lidicker, 1981). Com- 
munal groups may contain sisters but most group members do not 
appear to be siblings or parent-offspring groups. Wolff and Lid- 
icker (1981) concluded that communal winter nesting was a ther- 
moregulatory behavior adapted to survival in severe boreal climates. 
Communal nesting with non-relatives may be a mechanism to re- 
duce predation on family units or to reduce the chance of inbreeding 
(Wolff, 1980; Wolff and Lidicker, 1981). 

The singing vole (M. miurus) is also known to nest communally 
and store food (Murie, 1961). Singing voles build haypiles which 
consist of fireweed (Epilobium), horsetail (Equisetum), coltsfoot (Pe- 
tasites), willow leaves (Salix), mountain avens (Dryas), lupine (Lu- 
pinus), sage (Artemesia), pyrola (Pyrola), and grass (Calamagrostis). 


356 = Wolff 


These plant parts are clipped and layered over rocks or in lower 
branches of willow clumps to dry before being cached underground. 
The size of these haypiles may range from a handful to over a 
bushel (Murie, 1961). 

Communal groups of prairie voles are known to occur in field 
populations (Criddle, 1926; Fitch, 1957), but they have not been 
studied in detail. Prairie voles are known to store food in the field 
(Hamilton and Whitaker, 1979; Jameson, 1947) and in the labo- 
ratory (Lanier et al., 1974). Thomas and Birney (1979) observed 
reproductively active prairie voles of both sexes and all age groups 
caching food in the laboratory. Food was stored both before and 
after the birth of a litter. 

Food caches are not known for M. californicus (Stark, 1963), but 
food and nesting material are sometimes hoarded in captivity (Lid- 
icker, 1980). Pearson (1960) observed California voles carrying blades 
and stems of grass, herbs (Rumex), and wild oats (Avena) at all 
times of the year. Whitaker and Martin (1977) have some field and 
laboratory evidence for food storing in M. chrotorrhinus. Microtus 
oeconomus stores rhizomes of Equisetum (Wolff, 1984). Miucrotus 
brandti, an apparent colonial species from the Old World, also stores 
food (Naumov, 1972, zn Anderson, 1980). 


Olfactory Communication 


Many species of Microtus possess enlarged modified sebaceous 
glands on the posterolateral portion of the body which are used for 
scent-marking. In Microtus, these glands are present either on the 
flanks or hips, or do not occur at all (Quay, 1968; Table 3). Al- 
though scent glands do not normally occur in M. pennsylvanicus 
and M. longicaudus, Jannett (1975) was able to induce their devel- 
opment by administering testosterone to mature males. ‘Tamarin 
(1981) reported one incidence of gland development in a 73-g scro- 
tal male M. pennsylvanicus from an outdoor enclosure and Jannett 
(1975) caught one adult scrotal male M. longicaudus that had visible 
hip glands. However, Boonstra and Youson (1982) reported the 
regular occurrence of hip glands in M. pennsylvanicus in Ontario. 

In species that have them, scent glands are more prevalent in 
males than females. Glands begin to develop at the time of sexual 
maturity and regress during the non-breeding season (Howell, 1924; 
Maclsaac, 1977; Wolff and Lidicker, 1980). 

Scent-marking (the deposition of glandular secretions) has been 


Behavior 357 
TABLE 3 
SUMMARY OF SCENT-GLAND INFORMATION FOR NEW WoRLD Microtus SPECIES WHERE 


ADEQUATE DATA ARE AVAILABLE. GLAND LOCATION IS ACCORDING TO Quay (1968) 


Scent 


; mark- 
pel gneoctuen ing de- Reference for 
Hip Flank Sex scribed scent marking 
M. abbreviatus x M 
M. californicus xX M xX Lidicker (1980) 
M. chrotorrhinus xX M, ? 
M. muurus xX M, F xX Youngman (1975) 
M. montanus xX M x Jannett and Jannett 
(1974) 
M. oeconomus xX M,F 
M. richardsoni x M, F x Jannett and Jannett 
(1974, 1981) 
M. townsendit xX M,F xX Maclsaac (1977) 
M. xanthognathus x M, F x Wolff and Johnson (1979) 


described for a few select species. ‘Taiga voles scent-mark by scratch- 
ing the flank glands with their hindfeet, which stimulates the flow 
of sebum from the gland (Wolff and Johnson, 1979). The gland is 
then rubbed on the surface of objects in the environment. Males 
mark more frequently than do females and marking occurs more 
in strange environments than in home cages. Scent-marking in taiga 
voles is apparently used for individual recognition, to indicate re- 
productive condition, and for marking territorial boundaries (Wolff 
and Johnson, 1979). 

In M. richardsoni, glands begin to develop in young as small as 
19 g and reach a peak in July (males) or July-August (females) 
(Jannett and Jannett, 1974; Ludwig, 1981). Glands in males are 
2-3 times larger than in females and are positively correlated with 
body weight. When glands are functional, the hair covering the 
raised gland is greasy and matted down. At the end of the breeding 
season the gland regresses and becomes nonfunctional. 

Jannett and Jannett (1974, 1981) described two distinct marking 
patterns in which the flank gland secretions were deposited. Drum- 
marking involved raking the feet over the glands; flank-rubbing 
involved rubbing the flank gland against objects in the environment. 
Both behaviors are more common in males than in females and do 


358 Wolff 


not occur in juveniles. The behaviors and the context in which they 
are used are similar to those described for M. xanthognathus (Wolff 
and Johnson, 1979) and Arvicola terrestris (Stoddart, 1970). 

Flank glands, similar to those described for M. xanthognathus 
and M. richardsonz, also occur in singing voles, M. miurus (Young- 
man, 1975). Sexually excited males scratch these glands with their 
hindfeet when the gland becomes hypertrophied during the breed- 
ing season. Females apparently recognize males and assess their 
reproductive condition by smelling these glands (Youngman, 1975). 

Maclsaac (1977) also showed a correlation between hip-gland 
development and reproductive condition in male Townsend’s voles 
(M. townsendi). He found a positive correlation between testes 
weight and hip-gland size. Maclsaac also noted that a greater pro- 
portion of breeding females possessed hip glands than did non- 
breeding females. MaclIsaac described scent-marking behavior in 
Townsend’s voles: “marking action consists of three distinct figure- 
eight motions of the hips. In each instance, the hips touched the 
upper sides of the plexiglas tube,” presumably depositing sebum 
on the walls of the tube. A similar form of marking behavior has 
been recorded for montane voles, M. montanus (Jannett and Jan- 
nett, 1974). 

Hip glands are present in some male California voles (M. cali- 
fornicus) and their activity is correlated with reproduction (Lidicker, 
1980). Lidicker assumed hip glands had a social function though 
he was not able to discern its exact nature. California voles have 
been observed swaggering from side to side in plastic tunnels ap- 
parently rubbing their hips on the walls of the tube. Microtus mon- 
tanus has also been observed raising its hips in a tunnel (Jannett 
and Jannett, 1974). 

Jannett (198165) discussed the evolutionary significance of scent 
glands of M. montanus in a social context. He found that agonistic 
attacks between males were directed more at glands than other parts 
of the body. More wounding in glandular than non-glandular areas 
also has been reported in M. townsendi (Maclsaac, 1977), M. cal- 
ifornicus (Lidicker, 1980), and M. oeconomus (Quay, 1968). Jannett 
(19816) concluded that scent glands are indicative of a type of social 
organization and are used in territorial defense. Males of both M. 
xanthognathus (Wolff, 1980; Wolff and Johnson, 1979) and M. 
montanus have well-developed posterolateral scent glands and 
marking behaviors and both species are territorial and polygynous 


Behavior 359 


(Jannett, 19815). Neither M. ochrogaster nor M. pennsylvanicus 
appear to have well-developed posterolateral scent glands and their 
other glands are relatively small (Jannett, 1980; but see Boonstra 
and Youson, 1982); neither has stable polygynous relationships 
(Getz and Carter, 1980; Madison, 1980c). In non-territorial species, 
or during non-breeding seasons, glands may be a “behavioral load”’ 
(Jannett, 19815) and either have been selected against or regress as 
a mechanism to reduce aggression and promote sociality (Clarke 
and Frearson, 1972; Jannett, 19815; Wolff, 1980, 1984; Wolff and 
Lidicker, 1981). 

Scent-marking by dragging the anogenital region on the substrate 
has been reported for male taiga voles, M. xanthognathus (Wolff 
and Johnson, 1979) and montane voles, M. montanus (Jannett, 
198165). Reich and Tamarin (1980) found that male M. pennsyl- 
vanicus and M. breweri were attracted to the scent of females, but 
not the reverse. Deposition of droppings into scat piles or latrine 
sites also seems to have a communicatory significance. Wolff (1980) 
reported that taiga voles deposited scat piles at junctions of runways 
and along borders of territories. He also noted that in the labora- 
tory, dominant males had 2-3 scat piles in a 2 X 3-m enclosure. 
They also were used by pregnant or lactating females, but not by 
non-reproductive females or subordinate males. Jannett (19816) 
found that scat piles of adult male M. montanus were concentrated 
in the vicinities of brood nests of females in their territories. He 
also found that non-territorial adult males do not scent-mark during 
the non-breeding season. Scat piles or latrine sites also have been 
reported for M. richardson: (Ludwig, 1981), M. miurus (Murie, 
1961), Arvicola terrestris (Stoddart, 1970), M. chrotorrhinus (Mar- 
tin, 1971), M. pennsylvanicus, M. oeconomus, (Wolff, pers. observ.); 
they probably occur in most other Microtus species as well. 


Vocalization 


Several types of vocalizations have been reported for Microtus; 
they serve a variety of communicatory functions. D. Colvin (1973) 
recorded vocalizations by free-ranging M. montanus and M. longi- 
caudus that were engaged in an agonistic encounter. He also re- 
corded vocalizations of each species in both offensive and defensive 
behaviors during dyadic aggressive encounters in the laboratory. 
Caplis (1977, in Madison, 1980c) found that M. pennsylvanicus 


360 Wolff 


was more apt to vocalize in defensive than in offensive displays. 
Vocalizations during agonistic encounters also have been recorded 
for M. montanus (Jannett, 19816), M. californicus, M. ochrogaster 
(D. Colvin, 1973; Househecht, 1968), M. oeconomus, and M. xan- 
thognathus (pers. observ.). These vocalization patterns, which are 
qualitatively similar and occur under similar conditions, probably 
characterize most, if not all, Mzcrotus species. 

Wolff (1980) described a high-pitched vocalization by taiga voles 
(M. xanthognathus) which he has interpreted as an alarm call. The 
call is ventriloquial, making it hard to locate in the field. The calls 
are given by males and females of all age groups and are most 
common during the breeding season and again in fall, primarily 
around nesting areas. Similar calls have been reported for the sing- 
ing vole (M. miurus), and the context in which they are given ap- 
pears similar to M. xanthognathus (Youngman, 1975). 

M. Colvin (1973) discussed the structure and function of ultra- 
sound production in neonates of five Microtus species (M. pennsyl- 
vanicus, M. montanus, M. californicus, M. longicaudus, and M. och- 
rogaster). She concluded that stressed neonates used ultrasounds to 
elicit parental care. Neonates subjected to stress (for example, cold) 
produced ultrasounds that elicited a warming response by their 
mother. The intensity and frequency of calling were most pro- 
nounced during early development and decreased with age of neo- 
nates (DeGhett, 1976). 


Agonistic Behavior 


Agonistic behavior consists of a set of behavioral acts occurring 
in aggressive interactions which include all acts of aggression and 
submission (Wittenberger, 1981). Aggression, the most conspicuous 
and most studied component of agonistic behavior, includes a rep- 
ertoire of behaviors in which one individual displays a physical act 
of fighting or threat of fighting toward an opponent to obtain dom- 
inance or access to females, food, space, or some other resource. ‘The 
basic components of an encounter between two voles have been 
described by Banks and Fox (1968), Clarke (1956), D. Colvin 
(1973), Skirrow (1969), Tamura (1966), and Turner and Iverson 
(11973): 

Clarke (1956) described and illustrated agonistic behavior in the 
Old World short-tailed vole (M. agrestis), which is probably similar 
for most if not all vole species. The basic dominant display involves 


Behavior 361 


raising the body off the ground, tail extended straight and parallel 
to the ground, and ears cocked forward. This position is often ac- 
companied by a raising of one or both forefeet and gnashing of the 
teeth. The typical submissive posture consists of lowering the body, 
sometimes rolling over in a supine position, ears flattened against 
the body or flopped downward, and tail raised slightly or sometimes 
in a sigmoid shape when the animal is in a defensive or retaliatory 
position. Jannett (1977) described a subordinate behavior of a M. 
montanus in which the animal remains quiet, with head held low, 
eyes partly closed, and ears somewhat flat. Clarke (1956) also de- 
scribed several other behaviors associated with aggressive encoun- 
ters. These include: digging, simulated digging or tunneling activity 
in the sawdust or substrate; marking time, movement of legs while 
the body remains in place; fidgeting, general body movements; 
waltzing, rotating in place up to 360° while marking time; and 
dancing, rapid movements of feet with a sudden change in direction 
of the body. Autogrooming and toilet behaviors were also commonly 
observed during agonistic encounters, especially by subordinate an- 
imals. 

D. Colvin (1973) classified the basic components of an encounter 
into nine functional categories: approach, offense, attack, chase, de- 
fense, retreat, vocalization, box, and wrestle. This classification is 
similar to that described for collared lemmings, Dicrostonyx tor- 
quatus (Allin and Banks, 1968). Turner and Iverson (1973) added 
several behavioral components to this list, some of which were not 
aggressive behaviors: time together, naso-anal, grooming self, fol- 
lowing, mutual upright, threat, fighting, and submissive. Rothstein 
(1976) and Skirrow (1969) presented more detailed descriptions of 
microtine behaviors. 

These behaviors have been observed in the laboratory, but are 
quite stereotyped and are likely to occur in a similar pattern in a 
natural setting. Aggressive encounters have been observed in the 
field on several occasions. D. Colvin (1973) recorded five of these 
behaviors in an agonistic encounter that he observed in the field 
between an adult male M. montanus and an adult male M. longi- 
caudus. These behaviors included vocalization, chase, retreat, attack, 
and wrestle. Madison (1980c) documented 35 behavioral interac- 
tions between adult M. pennsylvanicus in natural populations. Nine 
of these interactions were between females, one between males, and 
seven involved females rejecting the advances of males. Madison 


362 Wolff 


concluded that behavioral interactions involving defense of space 
were most common among females, whereas aggression involving 
males was usually associated with competition for mates. Similar 
results have been found by Webster (1979). 

Caplis (1977, zn Madison, 1980c) studied aggressive behavior of 
reproductively active male and female meadow voles in dyadic en- 
counters in the laboratory. She found that males and females ex- 
hibited the same level of aggressive activity, but males exhibited 
more open conflict than females, and females exhibited more non- 
contact threat displays than males. Both males and females exhib- 
ited less aggression when paired with neighbors than when paired 
with strangers. Neighbor recognition implies a form of “social or- 
der” or “kin recognition” among free-ranging voles (Madison, 
1980c). 

Wounding patterns have been used on various occasions as an 
indirect measure of aggression (Christian, 1971; Getz, 1972; Rose, 
1979; Rose and Gaines, 1976; Turner and Iverson, 1973). Madison 
(1980c) summarized the results of several studies on M. pennsyl- 
vanicus as follows. Christian (1971) found that wounding in mead- 
ow voles is 1) frequent among males and almost non-existent among 
females, 2) linked to sexual activity among males (immature males 
were rarely attacked), and 3) dependent on density among sexually 
mature males. Rose (1979), on the other hand, found 1) consider- 
able wounding among females as well as males, 2) wounding during 
breeding and non-breeding seasons, and 3) no density dependence 
in wounding among males or females. Turner and Iverson (1973) 
found that 1) aggressive acts (primarily threats, vocalizations, mu- 
tual uprights, and tail wounding) increased in frequency as males 
became reproductively active and decreased in frequency as the 
breeding season ended, 2) submissive behaviors were most common 
early in the reproductive period, 3) allogrooming was most common 
when juveniles were in the population, 4) adult males were more 
aggressive than young of the year, and 5) residents were more ag- 
gressive than nonresidents. Getz (1972) found 1) no indication of 
greater antagonism between adult males than between adult females 
or between males and females, 2) no significant antagonism between 
adult and immature males, and 3) no indication of lasting male- 
female pair formation. Miller (1969) found that males were more 
aggressive than females. 

In M. ochrogaster, wounding is more frequent in males (32.6%) 


Behavior 363 


than in females (18.3%) and is the most intense during the repro- 
ductive period (Rose and Gaines, 1976). Wounding was more com- 
mon in medium-sized males and large females than in small non- 
reproductive males or females. In M. richardson, adult males also 
show more signs of wounding than females (64% versus 20%, re- 
spectively) (Ludwig, 1981). In M. montanus, fighting is most in- 
tense in adult males following snowmelt just prior to the breeding 
season and establishment of territories (Jannett, 1981a). 

Rose and Hueston (1978) documented some of the problems in 
using wounding as a measure of aggression. They found that 90% 
of wounds heal by 2—4 weeks and are undetectable, and by 8 weeks, 
all wounds are totally healed. Field measurements are therefore 
conservative and may vary seasonally; there is little wounding dur- 
ing the non-breeding season in winter when population densities 
are usually lower. Aggression also may vary with density, phase of 
population cycles, and between residents and dispersers (Krebs, 
1970; Reich et al., 1982; Turner and Iverson, 1973). Although there 
are conflicting results in data on wounding and aggression, the 
points about which all studies agree is that wounding is more com- 
mon among males than females and that this wounding reflects 
physical conflict associated with breeding activity (Madison, 1980c). 

Patterns of aggression may vary between species, but within a 
species they follow a predictable pattern that is correlated with a 
particular type of social system. The social system, in turn, is based 
on several factors such as defensibility of resources (Emlen and 
Oring, 1977), polygyny-threshold models (Orians, 1969), and pa- 
rental investment (Trivers, 1972). Within a species, if females are 
aggressive, they usually fight for space, whereas males may fight 
for space or females. In M. pennsylvanicus, a promiscuous species, 
females are territorial and males have large overlapping home ranges 
(Madison, 1980c). Females are aggressive toward other females in 
defense of territories and males are aggressive toward other males 
in the presence of estrous females. Estrous females are also aggres- 
sive toward males and may reject certain “low quality” males 
(Madison, 1980c). Aggression is reduced during winter when the 
animals are communally nesting (Webster, 1979). In a polygynous 
species such as M. xanthognathus, males are extremely aggressive 
and fight for territories (Wolff, 1980). Females, on the other hand, 
are aggressive toward strange males and strange females, but are 
amicable with other familiar females in the male’s territory. During 


364 Wolff 


the non-breeding season, all animals are less aggressive and nest 
communally (Wolff and Lidicker, 1981). 

The social system of California voles (M. californicus) ranges 
from monogamy to polygyny; both sexes are territorial (Lidicker, 
1980). During the breeding season, adult male California voles are 
antagonistic toward each other, and females are amiable unless an 
adult male is present, in which case they fight (Lidicker, 1980). 
Adult males are sometimes aggressive toward (and may even kill) 
females that are not their mates. In M. montanus, patterns of aggres- 
sion are apparently similar to those of California voles (Jannett, 
1980, 19815; Randall, 1978), and both species have a similar social 
system. In M. ochrogaster, which is monogamous and territorial, 
paired males and females are aggressive toward strangers of either 
sex (Getz, 1962; Getz et al., 1981; Miller, 1969; Thomas and Bir- 
ney, 1979). Aggression in other species of voles has not been eval- 
uated with regard to the species social system, but it is likely that 
predictable patterns will emerge that fit these models. 


Summary of Social Organization 


The social organization of microtines is the result of behaviors 
associated with courtship and mating, parental care, social structure 
(spacing patterns), aggression, and communication. Mating systems 
are commonly promiscuous (for example, M. pennsylvanicus and 
M. richardsoni), polygynous (for example, M. xanthognathus, M. 
californicus, and M. montanus), and rarely, but sometimes monog- 
amous (M. ochrogaster). Mating systems may be facultative (M. 
californicus and M. montanus) or obligate (M. ochrogaster); some 
species exhibit one, two, or all three mating patterns, depending on 
the social environment. Species-specific copulatory patterns are ap- 
parently adaptive to particular social organization in specific hab- 
itats and also may be a reproductive isolating mechanism between 
similar sympatric species (Kenney et al., 1978). Paternal care may 
be an important component of monogamous species, but in most 
microtines it is minimal or non-existent. Most social groupings are 
mother-young units, but some species have extended families that 
include two or more generations in one nest (for example, M. mon- 
tanus, M. ochrogaster, and M. pinetorum). 

In some species only males are territorial (for example, M. xan- 
thognathus and M. agrestis), only females (for example, M. penn- 


Behavior 365 


sylvanicus and M. richardsont) or both sexes are territorial (for ex- 
ample, M. montanus, M. ochrogaster, and M. californicus). Microtus 
xanthognathus and M. richardsoni live in patchy riparian habitats 
but exhibit different behavioral systems. The relationship between 
habitat and social structure of M. montanus, M. californicus, and M. 
pennsylvanicus is not clear, but see Jannett (1980), Lidicker (1980), 
and Madison (1980c) for interpretations. Microtus ochrogaster lives 
in a stable, relatively uniform habitat in which food is a limiting 
resource. ‘These ecological conditions apparently select for monog- 
amy, a strong pair bond, paternal care, and dispersal of young to 
reduce competition (Getz and Carter, 1980). 

These behavioral systems are maintained by agonistic behavior. 
Aggression may be for defense of territories or for access to estrous 
females. Aggression and territoriality may also regulate population 
numbers (Getz, 1978; Jannett, 19816; Madison, 1980a). Webster 
and Brooks (1981) suggest that social behavior and demography 
are closely integrated and it is essential to know the social-behavior 
characteristics of the species to understand its population dynamics. 
They concluded that “population dynamics of microtine rodents 
may be better understood by combining sociobiological investigation 
with the traditional demographic manipulation of ‘black box’ pop- 
ulations of voles.” 

Dispersal is another important aspect of microtine social biology 
(Lidicker, this volume). Dispersal following weaning may include 
all offspring, just male or just female offspring, or in some cases 
the dam may abandon her nest and leave it for her offspring. Com- 
munication, which is an essential component of maintaining social 
organization, may include scent-marking and production of pher- 
omones associated with reproduction (Seabloom, this volume), es- 
tablishment of dominance relations, or individual recognition. 
Vocalizations are used by neonates to elicit maternal care, as a 
threat or defensive behavior in agonistic encounters, or as an alarm 
signal to warn conspecifics. 

In seasonal environments, overwintering behavioral strategies, 
such as communal nesting and food storing, are adaptations for 
survival in severe boreal climates. Communal nesting requires a 
different suite of behaviors than those used during the reproductive 
season, or by a social or territorial species. Although mammal social 
behavior is extremely labile (Wilson, 1975) and is subject to dif- 
ferential expression resulting from learning, developmental pro- 


366 Wolff 


cesses, and the social environment, predictable patterns do emerge 
in microtine socio-ecology. Because of these influences, social sys- 
tems may vary between populations within a species, or between 
years within the same population. Relationships between social 
structure and ecological parameters have been postulated for several 
groups of mammals (Bradbury, 1980; Clutton-Brock and Harvey, 
1977; Crook et al., 1976) and undoubtedly are relevant to microtine 
social organization (Anderson, 1980; Getz, 1978; Webster and 
Brooks, 1981). An understanding of microtine behavior is in its 
infancy, but is recognized as an essential and integral component 
of the life-history strategies of this mammal group. 


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ACTIVITY RHYTHMS AND SPACING 
DALE M. MADISON 


Abstract 


ICROTINE rodents have different behavioral and physiological 
M rhythms, but the 2-6 h ultradian rhythm of activity is a 
dominant feature in the day-to-day existence of these species. Vari- 
ability in the timing of this rhythm with maintenance activities, 
growth, reproduction, and a complex of other social and environ- 
mental stimuli frequently make the characterization of these rhythms 
difficult, but no less significant, under field conditions. The ultra- 
dian rhythm is essentially a feeding rhythm, and the periodicity is 
linked closely to food quality and energy needs. Circadian rhythms 
occur in microtines, but infradian rhythms need further study. Re- 
cent technical advances combined with adjustments or controls for 
the shortcomings of traditional laboratory studies give promise of 
significant advances in the understanding of the mechanisms and 
adaptive significance of microtine activity rhythms. This review 
identifies six generalities or hypotheses for future study. 

Studies of spacing in microtines have been concerned primarily 
with home-range size, but despite rather sophisticated analytical 
approaches in these studies, little insight has been gained beyond 
that expressed by Burt over 40 years ago. In this review, the home- 
range concept of Burt (1943) is applied to microtine rodents, and 
a 24-h home-range model, based on radiotelemetry data from M:- 
crotus pennsylvanicus, is developed. Home ranges are classified into 
stable, variable, and shifting types. General categories of movement 
are also defined: local, distant reconnaissance, and dispersal. These 
types of home range and movement vary in their frequency of oc- 
currence in the order presented above, the most frequent listed first. 
Variability in space use is discussed with respect to energetics, diet, 
gender differences, reproductive condition, social factors, interspe- 
cific interactions, and weather and seasonal factors. Six generalities 
or hypotheses relative to space use are presented for future study 
and testing. ° 


374 Madison 


Introduction 


Concern for patterns of movement in microtine rodents in time 
and space is fundamental to a consideration of a host of behavioral 
and ecological issues. Emphasis in this chapter is placed on descrip- 
tions of movement patterns in time and space and on questions of 
adaptive significance. The meadow vole, Microtus pennsylvanicus, 
receives the most emphasis, because it is the most thoroughly studied 
and widely distributed species of the genus Microtus in North 
America. I also include information on some Old World species for 
comparison. Finally, the chapter is not so much a review as it is 1) 
an appeal for greater awareness among investigators of the natural 
patterns of movement of microtine rodents, and 2) a statement of 
the flexibility that at least certain microtine rodents have in adjust- 
ing to their environment. 


Activity Rhythms 


Rhythms of behavior among voles include those less than 24 h 
(ultradian rhythms), those of approximately 24 h (circadian 
rhythms), and possibly those greater than 24 h (infradian rhythms) 
(Aschoff, 1981). Terms such as nocturnal, diurnal, and crepuscular 
refer to circadian rhythms in which the active phase of the organism 
occurs at night, during the day, or at dawn and dusk, respectively. 
Where activity is distributed randomly throughout the diel (24-h) 
period, the organism is said to be arrhythmic (Daan, 1981). A strict 
ultradian pattern has no nocturnal, diurnal, or crepuscular empha- 
sis, but ultradian rhythms in Microtus commonly have these em- 
phases because of the concurrent presence of circadian rhythms. 
Thus, for example, a nocturnal-ultradian rhythm is one in which 
the regular, short term pulses of activity occur at night, either ex- 
clusively or with greater amplitude or duration (that is, the active 
phase of the ultradian period is elongated but the period remains 
the same). The information on rhythms to follow complements the 
more physiological discussions of endogenicity and cueing in Mam- 
mal Review (1972, Vol. 1, nos. 7-8), Aschoff (1981), Aschoff et al. 
(1982), Pinter and Negus (1965), Rowsemitt (1981), and Seabloom 
(this volume). Most of the rhythms referred to in this review have 
not been rigorously quantified and verified, such as by time-series 


Actiity Rhythms and Spacing BID 


analyses (Broom, 1979; Rowsemitt et al., 1982; Sollberger, 1965), 
and thus most of the conclusions reached should be interpreted as 
first approximations for the genus Microtus. 


Methods 


A large array of techniques have been used to record the activity 
rhythms of voles (Table 1). Generally, different methods show dif- 
ferent types of activity (for example, nesting, feeding, reconnais- 
sance and exploration, nursing, defecation, and reingestion), and the 
activities often show different temporal patterning. For example, 
activity wheels typically measure movements that are naturally ex- 
pressed during the night, but omit foraging and nesting activity that 
commonly occur in the same organisms in the same cage throughout 
the diel cycle (Calhoun, 1945; Daan and Slopsema, 1978; Dews- 
bury, 1980; Lehmann, 1976; Lehmann and Sommersberg, 1980; 
Mather, 1981). Wheel-running itself may vary with cage size, for 
Lehmann (1976) observed Old World M. agrestis to change from 
a nocturnal-ultradian pattern, to a strict nocturnal pattern, and then 
to a strict ultradian pattern in successively smaller cages. Nest mon- 
itors in the field do not discriminate between foraging, social or 
other activities (Barbour, 1963; Madison, 1981). Multiple monitors 
in the same cage were used by Daan and Slopsema (1978) to dis- 
tinguish between ultradian feeding (photocell and food hopper), 
nesting (treadle), and nocturnal wheel-running, but whether these 
devices reveal natural patterns is subject to criticism. For example, 
Graham (1968) showed that free-ranging meadow voles, Microtus 
pennsylvanicus, were diurnal, but caged individuals in the field were 
crepuscular, and caged voles in the laboratory were nocturnal. Also, 
Kavanau (1962) showed that photoperiods with abrupt light-on, 
light-off transitions in the laboratory affect rodents differently than 
the same photoperiod with gradual intensity transitions (for ex- 
ample, dawn and dusk). 

Although studies relying on mechanical devices in the laboratory 
can be criticized for their lack of natural relevance, studies of free- 
ranging voles relying on radiotelemetry or radioisotopes can also be 
criticized. Hamley and Falls (1975) demonstrated that radiotrans- 
mitter collars with 10-cm whip antennas affect activity levels in 
caged meadow voles, and Webster and Brooks (1980) showed that 
meadow voles in winter typically lose 2-3 g after being tagged with 
transmitters. Isotopes, instead of imposing a weight burden on the 


Madison 


376 


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Activity Rhythms and Spacing 381 


free-ranging vole, expose the organism to very high gamma emis- 
sion that could easily have detrimental effects (Mihok, pers. comm.). 

Despite the wide variety of potential biases inherent in the dif- 
ferent methods, a little common sense and ‘natural-mindedness”’ 
during interpretation reduces much of the apparent contradiction 
and allows laboratory data to be used, at least as a first reading of 
natural rhythms of behavior. 


Ultradian Rhythms 


The short-term activity rhythm, typically varying from 2 to 4 h, 
is common for vole species when study methods allow it to be mea- 
sured (Table 1). The more common findings are that: 1) the period 
varies within and between individuals; 2) the activity pulses are 
more prominent at certain times of the 24-h cycle; 3) the ultradian 
peaks shift with season; and 4) the peaks appear to synchronize 
with dawn or dusk, but gradually drift out of phase because of 
individual variation until resynchronization 24 h later. Figure 1 
shows one example for M. pennsylvanicus of a natural winter ul- 
tradian rhythm with a 4-h period. ‘The vole was carrying a 50 uCi 
Ta-182 collar, and the vole’s movement was monitored every 15 
min for 24 h with a portable scintillation meter and probe. During 
tracking the vole was in a meadow under 1 m of snow. The data 
suggest that there is a free-running rhythm under snow, as observed 
for beavers (Potvin and Bovet, 1975). Figure 2 shows the shifting 
of this rhythm to a nocturnal-ultradian pattern under the same 
photoperiod but with no snow cover and at moderate temperatures 
in a greenhouse. The records give a clear indication of the vari- 
ability, and the periodicity, typical of ultradian rhythms. 


Circadian Rhythms 


The available literature on rhythms in microtines leaves little 
doubt that most, if not all, microtines are flexible in their activity 
scheduling through the diel period, and that circadian rhythms ex- 
ist, as evidenced by free-running rhythms slightly shorter or longer 
than 24 h in voles held under constant light or darkness (Calhoun, 
1945; Daan and Slopsema, 1978; Lehmann, 1976; Mossing, 1975; 
Seed and Khalili, 1971; Swade and Pittendrigh, 1967). Under lab- 
oratory conditions, voles are active at night, yet under natural con- 


382 Madison 


0000 SUNRISE 1200 SUNSET 2400 


Fic. 1. Activity rhythm of a 30-g female meadow vole (M. pennsylvanicus) wear- 
ing a Ta-182 collar in a field covered with 1 m of snow in Quebec, Canada, 1975. 
The vertical axis is movement (m) between 15-min detection points. The smallest 
vertical unit indicates any movement up to 1 m, or the stationary position of a vole 
away from the nest. The spacing between the 3 days for which data were obtained 
reflects the time elapsed between these days. Dashed lines represent ultradian periods 
of about 4 h that have an underlying, free-running circadian periodicity of 23.85 
h/day. The dotted line represents time of sunrise and sunset. 


ditions voles are commonly found to be more diurnal or crepuscular 
(Calhoun, 1945; Graham, 1968; Heidt, 1971; Seed and Khalili, 
1971). There is also a seasonal shift, to be discussed later, from a 
nocturnal or crepuscular pattern during summer to a diurnal em- 
phasis during winter (for example, see Baumler, 1975; Carley et 
al., 1970; Erkinaro, 1961; Lehmann, 1976). But whatever the em- 
phasis is in activity (nocturnal or diurnal), some activity outside the 
nest usually occurs in nature during the “inactive” phase, unlike 
the condition for strictly nocturnal or diurnal rodents (for example, 
Peromyscus and Tamias). 

The patterns above are generalizations and therefore should not 
be considered rules, for some circadian periods can vary consider- 
ably. For example, Erkinaro (1970) noticed during one January 
that M. oeconomus was conspicuously nocturnal, but observed dur- 
ing the following January an obvious diurnal pattern. Pearson 
(1960) observed distinct diurnal and nocturnal patterns among M. 
californicus in the same population at the same time in comparable 
habitats only 9.5 m apart. 


Infradian Rhythms 


Behavioral rhythms in Microtus with period lengths greater than 
24 h are not clearly described. Behavioral estrus with a period 


Actiity Rhythms and Spacing 383 


0000 SUNRISE 1200 SUNSET 2400 


Fic. 2. Activity rhythm of a solitary, 45-g female meadow vole (M. pennsylvan- 
icus) for 27 days in a 3 X 3-m grass enclosure wired with passage counters inside a 
greenhouse in Montreal, Quebec, 1975. The number of passages used each 15 min 
is shown. The vertical axis is in units of 0-4, 5-9, 10-14, 15-19, and 20+ passages 
(the shortest vertical bar indicates 0-4 passages; the tallest, 20+ passages). Dotted 
lines give sunrise and sunset. 


384 Madison 


length of several days occurs (Hutchinson, 1972), but female voles 
have not been observed in isolation for behavioral changes during 
these cycles. No clear behavioral “circarhythms” (sensu Aschoff, 
1981) greater than 24 h are known for Microtus; ground squirrels 
(Spermophilus lateralis) are the closest relatives with demonstrated 
circannual behavioral rhythms (Pengelley and Fisher, 1957). 


Factors Correlated with Activity Rhythms 


Genetic factors—The only study of Microtus showing a genetic 
basis for intraspecific differences in rhythmic behavior is by Ras- 
muson et al. (1977). M. agrestis from northern populations of Swe- 
den showed 4-h ultradian rhythms, whereas southern populations 
showed very low levels of activity and no ultradian periodicity. 
Hybrids showed intermediate activity levels but ultradian rhythms 
similar to the northern populations. Both sexes gave the same result. 

Energetics, diet, and food.—Energetic considerations involving 
weight, metabolic rate, and diet have been linked with the existence 
and period of ultradian rhythms. In eutherian mammals, ultradian 
periods are common among species feeding on high bulk diets (Ash- 
by, 1972), and the short-term rhythms are specifically associated 
with foraging and food intake (Daan and Aschoff, 1981, 1982). 
The herbivorous diet of Microtus, consisting of large amounts of 
low-quality food, necessitates frequent feeding through the 24-h 
cycle with brief rest periods for efficient digestive processing (Daan 
and Aschoff, 1981). Granivorus rodents, such as Peromyscus, do not 
exhibit comparable ultradian rhythms, nor are they active through- 
out the diel cycle as are the herbivorus microtines (Hansson, 1971). 
Since bulk feeding also entails frequent defecation, the necessity of 
leaving the nest intermittently to avoid fouling the nest has been 
suggested as another reason for the ultradian rhythm (Lehmann, 
1976). The habit of fecal reingestion during the inactive phase of 
the ultradian cycle is consistent with the fouling-avoidance expla- 
nation (Ouellette and Heisinger, 1980). The period length of the 
ultradian rhythm has been shown to be directly proportional to 
body weight, and inversely proportional to metabolic rate (Daan 
and Aschoff, 1981, 1982; Daan and Slopsema, 1978; Lehmann, 
1976). Hence, the smaller the vole, the greater will be the energy 
needs per gram body weight, and the shorter will be the length of 
the ultradian period. 


Activity Rhythms and Spacing 385 


Gender and reproduction.—An examination of the literature for 
gender and reproductive differences in behavioral rhythms reveals 
several correlations. Evans (1970) and Madison (pers. observ.) show 
female meadow voles to be more diurnal than males, but other 
workers report no gender differences for M. pennsylvanicus (Gra- 
ham, 1968; Stebbins, pers. comm.), M. californicus (Pearson, 1960), 
or M. agrestis (Rasmuson et al., 1977). Webster and Brooks (1981a) 
showed that reproductively active female meadow voles are about 
180 degrees out of phase with the rest of the population in the dawn 
ultradian period of activity. This difference might be linked with 
the greater energy demands of these females. For example, Madison 
(1981) found that the period of the ultradian rhythm decreases 
during lactation from 6.5 to 4.0 h, and Kaczmarski (1966) and 
Migula (1969) showed that the energy needs of lactating voles in- 
crease rapidly during lactation to their highest levels near weaning. 
This inverse relationship between period length and energy needs 
in lactating voles correlates with the findings discussed in the pre- 
vious section. The relationship even occurs for communally nursing 
females with different size young in the same nest (McShea and 
Madison, 1984). Finally, Rowsemitt (1981) showed that castrated 
male M. montanus are diurnal and that intact and sham-castrated 
males are nocturnal, suggesting that non-reproductives in nature 
may be more diurnal. 

Social factors.—The influence of social behavior on rhythmic ac- 
tivity is demonstrated by the synchronization of the ultradian 
rhythms of some voles (Daan and Slopsema, 1978; Graham, 1968; 
Lehmann and Sommersberg, 1980; Madison, 1984; Madison et al., 
1984; Rasmuson et al., 1977; Rijnsdorp et al., 1981; Webster and 
Brooks, 1981a), but not others (McShea and Madison, 1984). Ev- 
ans (1970) showed that a male M. pennsylvanicus in the presence 
of a female is more active, especially during the day, than when 
alone. Since an isolated male is equally active both day and night, 
and since an isolated female is more active during the day, the 
results indicate the effect of the female on the male. Juvenile voles 
have rhythms that differ from those of adults. They are more noc- 
turnal in M. agrestis (Baumler, 1975) and M. pennsylvanicus (Web- 
ster, 1979). In M. arvalis, the juveniles do not synchronize with the 
adults until at least a week after emergence from the natal nest 
(Lehmann and Sommersberg, 1980). The small size of juvenile 
voles relegates them to subordinate social status in the population 


386 Madison 


(Turner and Iverson, 1973), and direct competition between adults 
and young would be reduced substantially if these animals were 
active at times different from the adults. The absence of apparent 
differences in activity rhythms of adult and juvenile M. californicus 
(Pearson, 1960) and M. pinetorum (FitzGerald, pers. comm.) sug- 
gests that these species may live in cohesive family groups where 
competition and the need for temporal isolation is reduced. Such 
social organization is known for M. pinetorum (FitzGerald and 
Madison, 1983). Since both social status and energy requirements 
vary with body size, any final statement regarding the reason for 
rhythm differences in voles of various sizes must await further study. 

Interspecific interactions.—Three different kinds of interspecific 
interactions, specifically predation, parasitism, and competition, ap- 
pear to be correlated with behavioral rhythms in voles. Predation 
was implicated as a causal agent in the diurnal synchrony of ultra- 
dian rhythms in Old World M. arvalis (Daan and Slopsema, 1978; 
Rijnsdorp et al., 1981). In this case, kestrels preyed intensively on 
voles, and any vole that was out of phase with the activity of other 
voles in the population stood a much greater chance of being taken 
by a kestrel. Lehmann and Sommersberg (1980) questioned this 
“‘safety-in-numbers” hypothesis for M. arvalis and suggested instead 
that the synchronous ultradian rhythmicity is for the purposes of 
social signalling and territorial defense, the advantage of strong 
defense being the inheritance of the family territory by kin. How- 
ever, in revealing that the daytime activity is within grass runways, 
and that the night activity is outside these tunnels on the surface, 
Lehmann and Sommersberg gave further evidence of apparent pre- 
dation pressure during the day. Voles may also avoid the active 
periods of predators. Hamilton (1937) indicated that the activity 
peak of M. pennsylvanicus just before dusk corresponds to, and 
results from, a lull in activity of a wide range of predators, and the 
same is true during the secondary peak at dawn. Fulk (1972) sug- 
gested that M. pennsylvanicus decreases the chances of shrew pre- 
dation by becoming more diurnal in areas of overlap with this 
predator. 

Parasitism is also a type of interspecific interaction, and one case 
has been reported in which a trypanosome parasite actually induced 
a change in the rhythmic behavior of M. montanus (Seed and Khal- 
ili, 1971). In this case, the change was the result of neurological 
damage caused by the parasite. 


Activity Rhythms and Spacing 387 


Temporal avoidance of interspecific competition is suggested for 
prairie voles. M. ochrogaster has non-overlapping activity peaks with 
sympatric Peromyscus maniculatus and Reithrodontomys megalotis 
(Carley et al., 1970) and with Sigmodon hispidus (Glass and Slade, 
1980). 

Weather and seasonal factors.—The effects of weather variables 
and seasonal changes on the activity rhythms of voles have been 
studied by many investigators. Temperature extremes emerge as a 
potentially important factor in several ways. In the summer, high 
daytime temperatures depress daytime activity in M. pennsylvanicus 
(Getz, 1961) and M. californicus (Pearson, 1960), and this may 
account for the depression of summer daytime activity observed in 
M. ochrogaster (Martin, 1956), M. agrestis (Davis, 1933; Erkinaro, 
1961; Lehmann, 1976), M. californicus (Shields, 1976), M. xan- 
thognathus (Wolff and Lidicker, 1980), and M. arvalis (Erkinaro, 
1970; Ostermann, 1956; Rijnsdorp et al., 1981). Cold temperatures 
during winter, especially at night, correlate with the more diurnal 
activity of overwintering M. ochrogaster (Barbour, 1963; Carley et 
al., 1970; Martin, 1956), M. agrestis (Baumler, 1975; Erkinaro, 
1961), and M. arvalis (Erkinaro, 1970; Lehmann and Sommers- 
berg, 1980). With a temperature increase but no change in photo- 
period during winter, meadow voles (M. pennsylvanicus) shift from 
an ultradian to a nocturnal-ultradian pattern of movement (Fig. 1). 
The link between temperature extremes and altered behavioral or 
seasonal rhythms in M. pennsylvanicus (and probably other species) 
may be confounded by other factors, because several studies on this 
species show no major seasonal or temperature effects on activity 
rhythms (Madison, pers. observ.; Osterberg, 1962; Stebbins, pers. 
comm.; Webster and Brooks, 1981a), and one study shows longer 
ultradian periods of activity at high temperatures (20 to 35°C) than 
at low temperatures (0°C) (Hatfield, 1940). The appearance of 
synchronous communal nesting and huddling during winter in M. 
pennsylvanicus and other species (Madison, 1984); Webster and 
Brooks, 1981a; Wolff, 1980; Wolff and Lidicker, 1981), and the 
increased movement during winter on warm days or on days fol- 
lowing heavy snow strongly suggests that low temperature stimu- 
lates synchronous nest use and inhibits activity during the winter 
(Madison et al., 1984). 

No clear effects of precipitation on activity rhythms are reported 
in the literature, although Pearson (1960) felt that the summer 


388 Madison 


activity pattern of M. californicus is determined by the availability 
of dew early in the morning. Activity levels were reported to in- 
crease during rainfall and overcast conditions for M. pennsylvanicus 
(Bider, 1968), M. californicus (Pearson, 1960), and M. agrestis 
(Baumler, 1975). Other investigators found the opposite to be true 
for M. pennsylvanicus. Madison (1980a) observed increased activity 
on warm, dry days with high barometric pressure and low relative 
humidity, especially following days of wet weather. Graham (1968) 
noticed positive correlations with light and temperature, and neg- 
ative correlations with humidity. Lehmann and Sommersberg (1980) 
showed that when precipitation was combined with cold tempera- 
tures during late autumn, the combination markedly reduced activ- 
ity in M. agrestis. 

Lighting conditions may affect behavioral rhythms as a result of 
changes in both photoperiod and intensity of illumination. The 
seasonal shift from an emphasis on nocturnal-crepuscular behavior 
during summer to diurnal behavior during winter, as reported ear- 
lier for several species, may depend on seasonal changes in photo- 
period rather than on temperature changes. Rowsemitt (1981) 
showed that male M. montanus under constant temperature condi- 
tions shift from a nocturnal pattern under 16L:8D to diurnal pat- 
tern under 8L:16D. The fact that five Microtus species show free- 
running rhythms under constant light or dark is firm evidence of 
photoperiodic events acting as zeitgebers (Calhoun, 1945; Daan and 
Slopsema, 1978; Lehmann, 1976; Mossing, 1975; Seed and Khalili, 
1971; Swade and Pittendrigh, 1967). In Fig. 1, the ultradian rhythm 
of a meadow vole under 1 m of snow suggests the possibility of a 
free-running system under constant darkness. The ultradian pulse 
at dawn, which often synchronizes with dawn (see Fig. 2), loses 
about 8 min/day over the 29 days of Ta-182 tracking. A partial 
day of tracking 1 week later (not included in Fig. 1) agrees with 
the explanation of a free-running rhythm. Light penetration through 
the snow is essentially extinguished at a 50-cm snow depth (Evern- 
den and Fuller, 1972). Light intensity effects are demonstrated: 1) 
by the preference of M. californicus and M. agrestis for low intensity 
light (Erkinaro, 1973; Kavanau and Havenhill, 1976); 2) by the 
disappearance of wheel-running activity for M. agrestis during the 
subjective night under high-intensity light, but not low-intensity 
light (Lehmann, 1976); 3) by the depressed activity of M. pennsyl- 


Activity Rhythms and Spacing 389 


vanicus on bright moon-lit nights (Doucet and Bider, 1969); and 4) 
by the increased activity of M. californicus on moonless nights 
(Pearson, 1960). The rate of change of light intensity, sudden in 
the laboratory but gradual in the field, also appears to have an 
effect (Kavanau, 1962). 


Spacing 


Few other subjects have been given as much attention among 
microtine rodents as has spacing, which subsumes home range, den- 
sity, territoriality, and dispersal, to mention a few. And few other 
subjects in this volume overlap as broadly with the others as does 
spacing. Space use is the product of movement through time, and 
any understanding of why this movement takes place must include 
a consideration of factors relating to competition (intraspecific and 
interspecific), resource needs (food, habitat), reproduction, and so 
forth. Obviously, the treatment here must be limited; and as with 
activity rhythms, the emphasis is mainly on description and on 
direct correlations between area use or use intensity and ecological 
and social variables. The concepts of home range, territory, and 
dispersion are reviewed, but the emphasis is on an examination of 
extensive and intensive radiotelemetry data for free-ranging M. 
pennsylvanicus not yet published. 


Methods 


A wide variety of techniques have been used to record home range 
and movement in microtines, and many analytical methods have 
been employed (Table 2). Both the techniques and analytical meth- 
ods have received ample review (Brown, 1966; Ford and Krumme, 
1979; Hayne, 1950; Koeppl et al., 1975; Meserve, 1971; Sanderson, 
1966; Schoener, 1981; Van Vleck, 1969; Van Winkle, 1975), so no 
further review is attempted here. Basically, as was mentioned by 
Sanderson (1966), no single analytical method gives measures of 
space use suitable for all potential uses. And it is apparent that 
techniques of analysis have in most cases gone far beyond the prac- 
tical or meaningful limits of the data set. Too little is known about 
where voles go, why they go there, and what happens there, and 
too much time is spent analyzing data on capture points that are at 


Madison 


390 


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best a small and abstract sampling of vole movement and behavior 
(see Hayne, 1950). But few alternatives exist, and the reward for 
meaningful explanations concerning vole space and resource utili- 
zation, no matter how tentative, is considerable. And so the attempts 
continue. 

More recent technology permits the collection of many positions 
on free-ranging voles per unit time, and this is at least an advance 
in the right direction. When monitoring the minute-to-minute or 
hour-to-hour movements of many voles over many days, certain 
patterns of area use and movement emerge that can be defined and 
used as a framework for further, especially comparative, studies. A 
classification of types of home range and movement in Mucrotus 
pennsylvanicus accompanies the different facets of space use re- 
viewed below. 


Home Range 


A home range according to Burt (1943) is “that area traversed 
by the individual in its normal activities of food gathering, mating, 
and caring for young.” The subsequent discussion by Burt (1943) 
implies a short-term range, one whose value would change with 
age, season, reproductive condition, density, and so on. Burt clearly 
did not imply that there is a typical home-range value for a species 
that encompasses a single area within which all these activities 
occur, yet many investigators apparently seek and publish such 
values. Burt’s home range would include all the routine travels 
occurring over just a few days, and the value would require recal- 
culation with each major change in environmental or individual 
condition. Since voles have small home ranges relative to their mo- 
bility (that is, a vole can move across its entire range with a few 
seconds, certainly in less than 1 min), and since voles typically have 
four to six activity periods every 24 h (see section on Activity 
Rhythms), I use the one-day-range as a home-range unit for voles, 
and classify types of ranges based on how these daily values vary 
through time. Each daily range is composed of 24 positions, one 
per h, or of 144 positions, one per 10 min. A convex polygon (formed 
by a line connecting the positions around the perimeter) is used to 
represent the daily range (Fig. 3). 

The convex-polygon or minimum-area method (Dalke, 1942) is 
used in the present study because it is the easiest way of identifying 


Activity Rhythms and Spacing 399 


and enclosing the actual positions recorded for an animal that 1s 
active in essentially two dimensions. Until more is known about the 
motivation and manifestation of space use in nature, any model is 
quite arbitrary, and so the simplest was chosen. The frequency of 
peripheral and multiple areas of high-use intensity and the occur- 
rence of both sharp and gradual border segments for the same 
individual must eventually be recognized. The study of these fine- 
grained patterns may answer basic questions regarding the deter- 
minants of space use. Exact location information, especially for 
locations visited less frequently, is essentially lost when probability 
models are used. 

The important features of the daily range estimates in this study 
are the short duration (24 h) of the estimates and the fixed time 
interval between positions. As such, the estimates are sensitive to, 
and representative of, day-to-day changes in vole movement. No 
matter how sophisticated the mathematical manipulations applied 
to position information (for example, to capture data), as the time 
span over which the data are collected increases, the estimates of 
range use and overlap (and therefore estimates of social interac- 
tions) become exaggerated. This bias would occur for M. pennsyl- 
vanicus because: 1) the daily ranges of males expand or shift with 
the occurrence of estrus in neighboring females; 2) the daily ranges 
of females contract at parturition and expand during weaning 
(Madison, 1978); 3) the cumulative area, but not the daily range, 
continues to expand over long periods of study, especially for males; 
and 4) fluctuating densities and high mortality rates for microtines 
(Madison, 1979; Pearson, 1971) create chronic instability in space 
ownership, such that range values pooled for several days or more 
would likely indicate overlap between two individuals whose actual 
periods of residence did not overlap. The daily range values mini- 
mize the above problems. 

Based on long sequences of daily ranges for over 100 meadow 
voles to date, three general types of home ranges emerge. The stable 
home range is one where the center of activity varies little from one 
day to the next, and where the convex polygons of the successive 
daily ranges overlap considerably (Fig. 3A). The variable home range 
may be either disjunctive or floating. ‘The disjunctive range is one 
in which two or more areas of intense utilization are separated by 
areas used only in transit. The center of activity is stable, although 
it rarely marks an area of intense utilization (Fig. 3B). The floating 


400 Madison 


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20m = Q +O 
Fic. 3. Types of home range and movement for meadow voles (M. pennsylvan- 
icus). All home ranges are composed of 24 radiotelemetry positions, one each h for 
24 consecutive h. Dashed lines enclose areas that are 40% or more of the home-range 
size but contain no telemetry positions (other than the one or two peripheral positions 
indicated. A, stable: female, 40 g, New York, 1978; B, variable disjunctive: male, 52 
g, Virginia, 1975; C, variable floating: female, 35 g, New York, 1978; D, variable 


Activity Rhythms and Spacing 401 


range is one in which the center of activity may shift noticeably on 
a daily basis, but does not change much over the long term. The 
successive polygons of the floating range may at times fail to overlap 
(Fig. 3C, D). The third home-range type is the shifting home range. 
Unlike the stable and variable home ranges, the shifting range shows 
a significant net change in center of activity. The shifting range 
may be conjunctive or disjunctive. The conjunctive shift in home 
range is a gradual, unidirectional displacement of the successive 
daily ranges, with each subsequent range overlapping the previous 
range (Fig. 3E). A disjunctive shift in home range occurs when a 
vole passes back and forth between two separate areas but even- 
tually shifts all of its activity from one area to the other (Fig. 3F, 
G). The shifting home range is a transient state of area use, and 
perhaps shouldn’t be classified as a home-range type; but because 
the organism still remains in the same general region, the shifting 
home range is still considered a form of local area utilization, hence 
a type of home range. Burt (1943) also included the shifting range 
as a home-range type. 

The stable and variable home-range types are much more com- 
mon than the shifting type. They are shown by 69% of adult male 
and 89% of adult female meadow voles under summer breeding 
conditions in good habitat (Madison, 1980a), but the percentages 
are bound to vary under a wide variety of environmental and social 
conditions. Tanaka (1972) reported stable home ranges in about 
56% of the M. montebelli studied. Shifting home ranges occur in 
about 31% of male and 11% of female M. pennsylvanicus (Madison, 
1980a), and these values agree with those of 12 to 19% reported by 
Getz (1961). 


Territory 


Another type of space-use pattern frequently mentioned in the 
literature for voles is territoriality. The territory may include the 
entire home range (all-purpose territory), or a smaller space unit 


—_— 

floating: male, 63 g, New York, 1978; E, conjunctive shifting: male, 37 g, Quebec, 
1974; F, disjunctive shifting: female, 40 g, Virginia, 1975; G, disjunctive shifting: 
male, 40 g, Virginia, 1975; H, dispersal: male, 37 g, Virginia, 1975. 


402 Madison 


within the home range (feeding territory, nesting territory; Nice, 
1937). Definitions vary but a common definition is the sole occu- 
pation of an area (at least with respect to others of the same sex 
during breeding activity) in a region where the density conditions 
lead to expectations of overlap. Such a situation exists for repro- 
ductive female meadow voles, but not for males (Madison, 19806, 
1980c). 

Territoriality among Microtus varies from individual territories 
for males (M. xanthognathus; Wolff, 1980) or females (M. penn- 
sylvanicus; Madison, 19805) or both (M. montanus; Jannett, 1980), 
to pair territories (M. ochrogaster; Getz and Carter, 1980; M. cal- 
ifornicus; Lidicker, 1980), and finally to communal territories (M. 
pinetorum; FitzGerald and Madison, 1983). These territorial pat- 
terns may vary with reproductive activity, density, and season. For 
example, M. ochrogaster shifts from pair territories to loose polyg- 
ynous or promiscuous groups with an increase in population density 
(Getz and Carter, 1980), and M. pennsylvanicus shifts from female 
territories during the summer breeding period to communal groups 
during the winter (Madison, 1984; Madison et al., 1984). 

Figure 4 shows the maintenance of exclusivity by female meadow 
voles during breeding in October, and the existence of communal 
groups in December. The communal groups had non-overlapping 
membership in November and December, but by January meadow 
voles moved freely between the groups. In October, the one female 
with the largest home range that “overlapped” the ranges of the 
others did not normally occupy the area of overlap, and was only 
located in the overlap area twice during one “‘distant reconnais- 
sance” trip (see next section). 


Movement Types 


A close examination of the sequence of positions of free-ranging 
M. pennsylvanicus, coupled with notes on what the voles are doing 
at each check, allows an evaluation of movement and space use in 
connection with home range. The first category of movement is local 
movement. These movements are either maintenance or reconnais- 
sance. Maintenance movements are often localized around the nest, 
and the vole is frequently seen chewing on grass blades or in the 
act of grooming. Usually no more than 0-3 m of movement occurs 
between successive 10-min or 60-min position checks (Fig. 5, po- 
sitions 1-4, 10-14). The local reconnaissance is characterized by 


Activity Rhythms and Spacing 403 


UNITS OF DISPERSION 


INDIVIDUAL KIN GROUP 


optimum area 


SS SS SS SS SS a eS ES oe 


suboptimum area 


(ie ae a) 


5m 


Fic. 4. Individual and group units of dispersion in meadow voles (M. pennsyl- 
vanicus) radiotracked in field enclosures in New York. Each vole is represented by 
a polygon enclosing 10 positions collected hourly from 0700 h to 1600 h. The sub- 
optimum area was created by repeated mowing and the collection of cuttings during 
the summer. Only six males and five females, all of adult size, were present on 4 
October; four adults of each sex plus 17 offspring from the original five females 
made up the kin groups on 12 December. 


loops of movement during which the vole is usually seen in alert 
postures or moving. Although some nibbling on grass may be seen 
occasionally, no sustained grazing is observed (Fig. 5, positions 5- 
9). The distinction between maintenance and local reconnaissance 
is more clear at night. During the night, the sleeping location is 
well defined. Maintenance activities occur near the nest, and local 
reconnaissance occurs away from the night nest about once every 
bout of activity (Figs. 5, 6). The local reconnaissance loops are 
thought to involve scent-marking or be surveys for other voles, since 
little feeding or shelter seeking is apparent during these runs. 

The second category of movement is the distant reconnaissance. 
This type is also called “wandering,” “‘sallies,” or “excursions” in 
the literature (Ambrose, 1969; Burt, 1943; Jannett, 1978; Lidicker, 
this volume; Madison, 1978, 1980a; Martin, 1956; Myllymaki, 1977; 
Stickel and Warbach, 1960). This movement is quite similar to 


404 Madison 


Caf CNEST 


Fic. 5. Local movements for a 52 g male meadow vole (M. pennsylvanicus) from 
2150 h to 0200 h on 17 and 18 August 1975 in Virginia (see Fig. 6, male 2). 
Positions (@) were recorded using radiotelemetry every 10 min; 14 such positions are 
represented between nest (@) departure at 2150 and nest return at 0200 h (position 
1 is first dot after leaving nest, position 2 is second dot, etc.). Approximate course is 
indicated by straight lines. Distance between reference markers (+) is 15 m. 


local reconnaissance in that the vole is typically ‘on the move.” It 
differs in occurring at least one range length beyond the normal 
daily range. Such trips may last up to 12 h, but 2 to 5-h journeys 
are most common. Considerable distances are sometimes reached, 
not atypically of 50 m or more. The trips begin and end suddenly; 
there is no change in behavior either before or after the trip that 


Actiity Rhythms and Spacing 405 


might suggest the occurrence of this behavior (Fig. 3A [8/8], G [7/ 
24, 7/31]). Distant reconnaissance has many potential reproductive 
advantages to both sexes (Madison, 1978, 19805, 1980c), but it also 
may be a means of assessing food and shelter resources in adjacent 
areas at times when these are declining in the immediate home 
area. That distant reconnaissance in males is about twice as fre- 
quent as that for females in both meadow voles (Madison, 1980a) 
and prairie voles (Martin, 1956) suggests that males use these trips 
at least in part to maximize paternity. 

The third general category of movement is dispersal. It is similar 
to wandering in its suddenness and long distance nature, but the 
vole in this case does not return to its former home range (Fig. 3H 
[7/17]). The incidence and significance of dispersal is discussed by 
Lidicker (this volume). 

Of all these types of movement during the reproductive season, 
the local-maintenance and reconnaissance types are the most com- 
mon, occurring essentially during each of the 4-6 activity periods 
each day. Distant reconnaissance occurs at least once every 20 days 
for females, and at least once every 12 days for males. Dispersal is 
relatively rare for M. pennsylvanicus under the conditions studied, 
having occurred in three out of the 56 voles tracked for 3 or more 
weeks (Madison, 1980a, 1980c). 


Dispersion 


An understanding of factors influencing space use must include 
a clear definition of the unit of dispersion (Brown and Orians, 
1970). Specifically, do individuals move about more or less inde- 
pendently of other individuals, or do pairs or larger assemblages 
move about together, occupy the same range and nest, and use the 
same basic resource base? Individual and social units of dispersion 
demand different sets of analytical precautions during studies of 
resource preference and space use. 

For M. pennsylvanicus, the unit of dispersion changes seasonally, 
although the dispersion pattern (uniform vs. random vs. clumped) 
does not. From spring to mid-fall, individual units of dispersion 
appear (Fig. 4). The females involved in breeding have uniform 
(territorial) distributions; the males are more variable and range 
from random to clumped (for example, around estrous females) 
(Madison, 1980a, 1980c). From mid-fall to early winter, the unit 
of dispersion changes to communal (kin) groups; these groups show 


406 Madison 


little overlap, suggesting territorial female families (Madison, 1984; 
Madison et al., 1984). Figure 4 shows the territories of five females 
in December that had terminated breeding for the year. Each of 
these females shared their nest and home range with a group com- 
posed of the female’s offspring and from 0 to 2 adult males. This 
kin group gradually gives way to mixed lineage groups for the rest 
of winter. Mixed lineage groups arise when, as a result of winter 
mortality among many kin groups, the voles redistribute themselves 
in space in order to stay above the minimum “huddle” density 
necessary for overwinter survival (Madison et al., 1984). Home- 
range size and overlap is similar within the kin and mixed lineage 
groups, but the latter group is more permeable to changing mem- 
bership, and hence is not territorial. In addition, since the total 
population density gradually decreases with winter, and since group 
size necessarily remains about the same, the mixed groups become 
more separated as the winter progresses. The transition from group 
to solitary living with the onset of breeding in spring includes some 
communal nesting and even communal nursing among females, but 
these groups disappear by May (McShea and Madison, 1984). 

Besides meadow voles, M. arvalis also changes from a female 
territorial system in summer to a group unit in winter (Chelkowska, 
1978; Mackin-Rogalska, 1979). M. xanthognathus shifts from a 
male territorial organization to non-kin communal groups from 
summer to winter (Wolff, 1980). There are no known microtine 
species that exhibit individual units of dispersion throughout the 
year; however, several microtines, such as M. pinetorum, live in 
cohesive social units year-round (FitzGerald and Madison, 1981, 
1983; Madison, 1984). The unit of dispersion varies with density 
from more or less stable pairs to largely individual units associated 
with polygyny and promiscuity in M. ochrogaster (Getz and Carter, 
1980) and M. californicus (Lidicker, 1980). 


Factors Correlated with Space Use 


Energetics, diet, and food.—Despite the large amount of general 
literature concerning the effect of food on density and movement, 
not much is known concerning voles in the genus Microtus (Table 
2). McNab’s (1963) prediction that home-range size should in- 
crease with decreased food resources is supported by Taitt and 
Krebs (1981) and Taitt et al. (1981) for M. townsendi1, and by 


Activity Rhythms and Spacing 407 


Myllymaki (1977) for M. agrestis. However, no such relation was 
found between home-range length and biomass of preferred food 
for M. ochrogaster (Abramsky and Tracy, 1980), and a positive 
relation between food availability and movement was noted for M. 
californicus (Krebs, 1966). Since density was not controlled in the 
above studies, and since density typically increases with extra food, 
the changes in movement and home-range size above may result 
from social factors and not be due to the changes in available food. 
Thus, the issue remains to be resolved. 

Gender and reproduction.—Considerable information shows that 
at least for certain species the size of the home range is larger for 
males than females, and that the degree of difference is a function 
of reproductive activity (Table 2). Recent radiotelemetric studies 
have confirmed the above relations for M. pennsylvanicus (Gaulin 
and FitzGerald, in press; Madison, 19805; Webster and Brooks, 
19815). In this species, the range of the female decreases during 
early lactation, but returns to normal values with weaning (Mad- 
ison, 1978). If many females are breeding in a population, the 
average short-term home range for the females is smaller because 
of the home-range reduction during lactation. However, the reduc- 
tion may be offset under natural conditions by the tendency of 
females of some species to shift home ranges (Myers and Krebs, 
1971; Tast, 1966) or show distant reconnaissance (Madison, 1978) 
just before parturition. The range of breeding male meadow voles 
(M. pennsylvanicus) is typically much larger during the reproduc- 
tive season, but once the communal groups form during mid- to late 
fall (see section on Dispersion), the range size of males decreases 
to about the size of female home ranges, which change little from 
summer to winter. The large size of the male range during the 
breeding period is primarily the result of distant reconnaissance 
movements and floating and shifting home ranges, all likely the 
result of mating activity (Madison, 1980a, 19806, 1980c; see section 
on Home Range). 

The above pattern for meadow voles is probably also character- 
istic of most other microtines. Exceptions arise in those species that 
live in social groups year-round. In M. pinetorum, the male and 
female home ranges of each exclusive social group essentially co- 
incide during all seasons (FitzGerald and Madison, 1981, 1983). 
Similar isometry is predicted during the breeding season in situa- 
tions in which monogamy often occurs, such as in M. ochrogaster 
(Getz and Carter, 1980) and M. californicus (Lidicker, 1980). Isom- 


408 Madison 


etry is predicted to be the basic condition for all microtines outside 
the breeding season, and it may even prevail among adult non- 
reproductives during the breeding period (Webster and Brooks, 
19816). 

Social factors—The influence of social factors on space use is 
suggested by non-random patterns of spacing in homogeneous hab- 
itat, by differences in the space use of voles of different social status, 
and by differences in spacing and movements of voles at different 
population densities. The overdispersion of breeding female mead- 
ow voles strongly suggests mutual antagonism and female avoidance 
(Madison, 19806, 1980c). That these exclusive areas between fe- 
males are not strictly necessary for, nor determined by, individual 
food needs is suggested by the cohabitation of these same areas by 
extended family units of up to seven subadult and adult voles during 
the late fall and winter (Madison, 1984; Madison et al., 1984). 
Other species of voles also exhibit territoriality (see Wolff, this 
volume; Madison, 1980). The only study to date to determine the 
effects of social status on space use in Microtus concerns meadow 
voles (Ambrose, 1973). Dominant M. pennsylvanicus, as determined 
in dyadic encounters, were much less likely to change home ranges 
in the field than were subordinate voles. The effect of social vari- 
ables on spacing also should be apparent under conditions of dif- 
ferent population density. This relation assumes that as density 
increases, so should competition for spatially distributed resources. 
The cost of utilization or defense of widely dispersed resources 
should increase, and so it is expected that home-range size should 
decrease with increased density, at least to some minimal level nec- 
essary for survival. The general pattern among voles is a negative 
relationship between density and home range (see Table 2). For 
M. oeconomus, this relationship is parabolic and is expressed as: 


3.55 
= 0.11 + (— 


where Sis the home range size in ha and d is the density in voles/ 
ha (Okulova et al., 1971). Ambrose (1973) found that meadow voles 
(M. pennsylvanicus) didn’t change home-range size with increased 
density, but rather increased the intensity of utilization within the 
home range. In this study, the home ranges already may have been 
at the minimum levels tolerated. Van Vleck (1969) observed a neg- 
ative relationship only for males, but his measure of space use (the 


Actiity Rhythms and Spacing 409 


number of different traps visited) was not very refined, especially 
for female voles with small home ranges relative to the trap spacing 
(14 m). Other aspects of spacing relating to social behavior are 
discussed by Wolff (this volume). 

Interspecific interactions.—Very little is known regarding the ef- 
fects of predation, parasitism, or interspecific competition on space 
use in Microtus. In some circumstances shrews are known to kill 
voles, but Barbehenn (1958) found no negative effect of the presence 
of Blarina or Sorex on meadow-vole distribution. However, Fulk 
(1972) showed that M. pennsylvanicus tended to avoid areas occu- 
pied by Blarina brevicauda. Recently, Madison et al. (1984) showed 
that predation by foxes and weasels on overwintering meadow voles 
appeared to stimulate spatial avoidance and smaller nesting groups 
in the voles. Interspecific competition as measured by spatial avoid- 
ance has been demonstrated for M. ochrogaster, which avoids co- 
habitation with Sigmodon (Glass and Slade, 1980), and M. mon- 
tanus appears to exclude M. pennsylvanicus from certain habitats 
(Stoecker, 1972). ‘That such relationships may be complex is sug- 
gested by Douglass (1976), who found the opposite relationship 
between M. montanus and M. pennsylvanicus. 

Weather and seasonal factors.—The time required for the collec- 
tion of information in most studies of space use precludes the mea- 
surement of day-night shifts in home-range use as well as responses 
to daily weather variations. Radiotelemetry permits the measure- 
ment of these local changes in spacing, and most information of this 
kind is available only for M. pennsylvanicus. During summer, 
meadow voles appear to vary their movements between day and 
night. Figure 6 shows four voles whose positions were determined 
every 10 min for 24 h, thus giving 24 positions every 4 h (the same 
number of positions that constitute all the daily ranges in Fig. 3). 
The 4-h ranges show that the nest used during the night is different 
from the nest or refuges used during most of the day for all four 
voles. The space use at night is reduced for females, but not for 
males, and this agrees with the lower activity of females at night 
(Evans, 1970; Fig. 6). The space-use patterns of these voles, which 
were selected for study because of their close proximity, vary from 
no overlap between the females and between the males during the 
0400-0750 period, to generally higher levels of overlap or proximity 
during the day. Why there appears to be a nighttime reduction in 
space use for females is not known, but the fact that lactating fe- 


410 Madison 


4-HOUR HOME AREAS 
1200-1550 1600-1950 2000-2350 0000-0350 0400-0750 0800-1150 


MALE | Pe 


MALE 2 


FEMALE | 


Fic. 6. Space use for four free-ranging meadow voles (M. pennsylvanicus) during 
a 24-h period on 17 and 18 August 1975 in Virginia. Positions were recorded by 
radiotelemetry every 10 min for all four voles. The space use for each vole is shown 
for each 4-h period, first separately, then combined. Reference markers (*+, '+) are 
the same for all voles and are 15 m apart. Note that the scale was changed for 
combined plots. Males 1 and 2 were 50 g each; female 1 was 41 g; female 2 was 43 g. 


Activity Rhythms and Spacing 411 


males show this reduction throughout the 24-h period suggests that 
energetic demands peculiar to females may be a factor (Madison, 
1978). 

Day-to-day changes in space use in response to weather condi- 
tions have been recorded only for M. pennsylvanicus (Madison, 
1980a; Madison et al., 1984). The home ranges of both males and 
females significantly increase with environmental temperature. Male 
home ranges also significantly increase with time since precipitation 
and with higher barometric pressures. Blair’s (1940) finding that 
meadow voles have larger home ranges in dry habitats than in wet 
habitats generally agrees with the above observation. Why meadow 
voles, and males in particular, show larger home ranges under 
“good” weather conditions is not known. Madison (1980a) specu- 
lated that reduced ability to detect inhibitory pheromonal signals 
on dry days may be an important factor. 

Seasonal changes in space use are relatively well known for mi- 
crotines. IT'wo patterns appear to be common. The first is a reduc- 
tion in home-range size of males during the non-breeding season 
(see section on Gender and Reproduction). The second is a shift in 
home range during periods of habitat flooding in fall and spring 
(Hansson, 1977; Ludwig, 1981; Tast, 1966; Webster, 1979). Two 
other patterns that are hypothesized to be common are: 1) local 
shifts in home range during winter as a result of vole efforts to 
locate larger huddling groups for thermal benefit or to escape pre- 
dation (Madison, 1984; Madison et al., 1984); and 2) shifts in home 
range during spring from overwintering groups to dispersed, indi- 
vidual ranges for purposes of maximizing reproductive success. 


Generalities and Predictions for 
Future Testing 


Day-night patterns of activity and home-range size in microtine 
rodents have been studied for many years, but generalizations con- 
cerning activity and spacing have been slow in coming. Insights 
from recent radiotelemetric studies of rhythms and space use com- 
bined with information from laboratory and mark-recapture studies 
permit certain tentative generalizations that can be used to form 
hypotheses for future experimental studies, as follows. 


412 


Madison 


Activity Rhythms 


1) 


2) 


3) 


4) 


5) 


6) 


A recurring ultradian rhythm with a 2- to 6-h period, each 
entailing 1-3 h of rest and 1-3 h of activity, is typical for 
microtine rodents. 

The period of the ultradian rhythm is inversely related to 
energy demand; thus, reproductively active males, late gestat- 
ing or lactating females, and small-sized voles should show 
shorter periods. 

The period of the ultradian rhythm can be modified by con- 
serving energy; thus, if social synchrony is critical to survival, 
small-sized voles may “huddle” more and breeding voles may 
temporarily forego reproduction to maintain synchrony. 
Rhythm synchrony between voles is most conspicuous in the 
morning, and sunrise appears to be the timing event for cir- 
cadian periodicities. 

Some voles in a population may adjust the phasing of their 
ultradian rhythm to reduce social confrontation or competi- 
tion for resources. 

Microtines tend to be more day-active in winter and more 
night-active in summer. 


Spacing 


1) 


2) 


3) 


4) 


5) 


Most microtine species exhibit individual units of dispersion 
during most of the breeding season, especially those members 
of each species that are reproductively active. 

Most microtine species are promiscuous or polygynous and, 
during the breeding season, males of these species have larger 
home ranges than females. 

Microtine species that live throughout the year in cohesive 
social groups tend toward monogamy, and the home-range 
size for males and females of these species approach isometry. 
Whether voles live alone or in social groups during the breed- 
ing season, group living and home-range isometry between 
the sexes appears to be the general rule during the non-breed- 
ing or winter season. 

Absolute home-range size for adult male voles during the non- 
breeding season or winter period is equivalent to, or only 
slightly smaller than, that of females of the same species in 
comparable habitat during the summer. 


Activity Rhythms and Spacing 413 


6) Non-breeding, winter groups are composed of kin early in the 
winter, but by late winter usually are composed of voles of 
mixed lineage. 


Acknowledgments 


I thank Brad Davis, Melissa Ditton, Randy FitzGerald, Bill 
McShea, Bruce Webster, and many other field assistants who helped 
collect the data presented and discussed here. The chapter consid- 
erably benefited from discussions with, or the editorial criticisms 
and general help of, Pat DeCoursey, Bill Lidicker, Norm Negus, 
Carol Rowsemitt, Frank Sulzman, Bob Tamarin, Jerry Wolff, and 
Irv Zucker. ‘The research was supported by the National Research 
Council of Canada, McGill University, the Research Foundation 
of the State University of New York, the National Science Foun- 
dation (DEB-22821), and the U.S. Fish and Wildlife Service (Con- 
tract No. 14-16-0009-79-066). 


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DISPERSAL 
WILLIAM Z. LIDICKER, JR. 


Abstract 


ISPERSAL is a major factor in the life history of voles. Moreover, 
D it is a heterogeneous phenomenon encompassing a variety of 
timings, motivations, and consequences. The study of dispersal will, 
therefore, be more effective if this variety of movement patterns is 
acknowledged. A preliminary and heuristic classification of dis- 
persal for the genus Microtus is proposed. Among 10 North Amer- 
ican species, only the pine vole fails to show definite evidence of 
pre-saturation types of dispersal. 

Attempts to characterize dispersers are hampered by the inherent 
heterogeneity of the behavior. With respect to sex, age, and repro- 
ductive status, the following generalizations can be made: 1) males 
predominate slightly overall, but saturation dispersers are unbiased 
sexually or even female dominated; 2) subadults dispersing during 
the breeding season typically are coming rapidly into breeding con- 
dition and often reach sexual maturity at a younger age than resi- 
dents; 3) adult males moving at the beginning of the breeding season 
are reproductively active; and 4) pregnant females have been found 
dispersing in at least four species. Behaviorally, dispersers tend to 
be less aggressive than residents. A phenotypic-plasticity model is 
proposed to explain this relationship. The possibility that dispersers 
as a class may be genetically distinct from residents is explored. 
The evidence fails to support such a conclusion, although in some 
cases dispersers are not a genetically random subset of residents and 
heterozygous genotypes are sometimes in excess among dispersers. 

Dispersal is increasingly viewed as having significant demo- 
graphic causes and consequences. These impacts stem from the 
quantity of dispersal, the differential nature of dispersers, the suc- 
cess rate of dispersers in reestablishing themselves, and the spatial 
structuring of populations. These effects are reviewed, and it is 
concluded that pre-saturation dispersal is a key element in many of 
the observed processes. Of particular interest is the question of the 


420 


Dispersal 421 


role of dispersal in population regulation, and especially in our 
understanding of the enigmatic multi-annual cycles often exhibited 
by voles. The best evidence that vole populations can be regulated 
by dispersal comes from the “fence effect.” This has been demon- 
strated for at least six species of Microtus. This evidence and the 
widespread occurrence of pre-saturation dispersal combine to sug- 
gest a model of regulation in which dispersal prevents or slows 
population growth as long as a dispersal sink is available. With the 
filling of the sink, populations grow to peak densities. Conditions 
suitable for multi-annual cycling occur when habitat patchiness 
provides a limited availability of survival habitat relative to colo- 
nizing habitat during the poorest time of the annual cycle. The 
recently proposed hypothesis that immigration is required for multi- 
annual cycles is found to be unnecessary and without significant 
support. 

Lastly, dispersal is discussed in terms of the evolutionary issues 
upon which it impinges. Voles offer considerable potential for con- 
tributing to general theory in this area. For species exhibiting multi- 
annual cycles, selection should favor the evolution of pre-saturation 
dispersal from low-density populations. This pattern should be more 
characteristic of species inhabiting patchy rather than more contin- 
uous habitat. Other areas of inquiry include life-history correlates 
of dispersal types, heritabilities of dispersal, dispersal polymor- 
phisms, demic differentiation and species cohesion, and the possible 
role of group selection. 


Introduction 


Movements of voles away from their home ranges have profound 
and pervasive influences on many aspects of vole biology. There are 
consequences for individual fitness, social structure, demography, 
and evolution. Moreover, such dispersal movements are extremely 
common, impinging regularly on the lives of nearly every individual 
vole. Not only may individual voles themselves become dispersers 
one or more times during their relatively brief lives, but they also 
are very likely to have to contend with other dispersing voles in- 
truding upon their home ranges. 

It would be a serious mistake, however, to assume that the phe- 
nomenon of dispersal is homogenous throughout the genus Micro- 


422 Lidicker 


tus, or even within a single species. Just as there is a multitude of 
causes and consequences of mortality within the genus, so too we 
should anticipate that dispersal will have a variety of motivations, 
timings, and consequences. It is surely a heterogeneous phenomenon 
with many explanations. 

In this discussion dispersal is defined as any movement in which 
an individual leaves its home range without returning. If such 
movements result in individuals entering or leaving the demograph- 
ic unit (population) under study, they become immigration and 
emigration, respectively (Lidicker, 1975; Lidicker and Caldwell, 
1982; Tamarin, 1980). Other related phenomena are excursions, 
in which individuals leave their home ranges but return after a 
brief exploratory episode, and nomadism, in which there is no es- 
tablished home range. The study of dispersal is a relatively new 
aspect of Microtus biology and has received detailed attention only 
in recent years. Data are therefore few and unevenly distributed 
among North American species. I organized this chapter around 
the techniques used, the kinds of dispersal found in Microtus, the 
characterization of dispersers, the demographic causes and conse- 
quences, and the evolutionary implications of dispersal. 


Review of Techniques 


A major problem in the study of dispersal among small, cryptic, 
and short-lived members of the genus Microtus is the technique 
used to identify dispersing individuals. The problem is exacerbated 
by the near certainty that dispersal is heterogeneous with respect 
to its causal factors, average distance moved, and quality of voles 
involved. Hence, a particular technique likely will be biased toward 
identifying only a particular subset of dispersers. For example, traps 
set to intercept dispersers at a considerable distance from a source 
population will underestimate dispersal if most movements are short, 
if dispersers suffer high mortality, or if dispersers are relatively 
untrappable. 

Traditionally, dispersal was an indistinguishable component of 
“gross mortality.” It did not really matter if an individual dispersed 
or fell prey to a predator. The demographic, social, and genetic 
consequences were assumed to be the same. Recently, some authors 
caught up in the enthusiasm for the importance of dispersal, have 
gone to the other extreme and assumed that all losses were due to 


Dispersal 423 


dispersal unless proven otherwise (for example, Hilborn, 1975; Hil- 
born and Krebs, 1976). 

Attempts to measure dispersal in voles directly have met with 
varied success. A widely used technique is to trap out an area and 
then assume that individuals caught subsequently are dispersers 
(Baird and Birney, 1982; Gaines et al., 1979; Hilborn and Krebs, 
1976; Keith and Tamarin, 1981; Krebs et al., 1976; Myers and 
Krebs, 1971; Staples and Terman, 1977; Tamarin, 1977). This 
poses several sources of error. Because Microtus tend to have rela- 
tively low trappabilities (Boonstra and Krebs, 1978; Hilborn et al., 
1976; Stoddart, 1982), it is extremely difficult to trap out an area. 
Thus some residents will almost surely remain, possibly to be caught 
later as “dispersers.”” Additionally, residents on the edge of such 
low-density areas will be very likely to expand their home ranges 
into it. Thirdly, low-density areas may induce some individuals to 
colonize, such as those on an excursion, who otherwise might not 
become dispersers. Finally, the subsequent history of colonizers to 
a trapped-out area may be significantly different from those that 
disperse into undisturbed areas. 

Some workers (Beacham, 1979a, 1980, 1981; Hestbeck, 1982; 
Tamarin, 1980) have attempted to minimize these biases by pro- 
viding barriers or poor habitat strips around their trapped-out areas 
(“‘sinks’’; see Lidicker, 1975). This was intended to discourage near- 
by residents and others not highly motivated to move from reaching 
the low-density patches. Hestbeck’s (1982) experiments included 
social as well as physical barriers. A variant of this was Tamarin 
et al.’s (1984) use of partial enclosures, opening only into non- 
habitat (forest in this case). To minimize the magnetic effect of low- 
density patches, Krebs et al. (1978) tried “pulsed removals.” By 
regular but infrequent trapping episodes, more normal densities 
were maintained on experimental plots. However, this complicated 
further the problem of distinguishing residents from immigrants. 
Dueser et al. (1981) tried a single trapping-out of residents followed 
by no further manipulations. They then assumed that all individ- 
uals first caught above a certain body weight were immigrants while 
those caught first at a lower weight were born on the plot. This is 
a credible way to circumvent some of the difficulties mentioned 
above, but fails to avoid the serious problem of incomplete trapping. 
Almost surely, some individuals born on the area will escape cap- 
ture until they are above the arbitrary weight level and will be 


424 Lidicker 


classified as dispersers. Likewise, some individuals may disperse 
before they reach that critical weight, and be classed incorrectly as 
resident recruits. The magnitude of these errors is unknown. 

Another approach is to use leaky enclosures. If the exits are 
difficult to transgress, then it can be assumed that successful voles 
are highly motivated to disperse. If the escape routes are then mon- 
itored, dispersing individuals can be identified. For example, Riggs 
(1979) used long exit tubes leading from the corners of large en- 
closures. ‘These tubes were guarded by an earth barrier, a bare 
area, and sometimes a pool of water. Gaines et al. (1979) employed 
exit traps placed at 15.2-m intervals around three 0.8-ha enclosures. 
Entrance to the traps was via a pipe opening into the center of a 
1-m buffer strip of suboptimal habitat maintained around the edges 
of the enclosures. Verner (1979) also used dispersal exits in his 
study. This approach does not absolutely exclude residents from 
exploring the exit paths and also carries the artificial conditions 
associated with enclosed populations. 

Garsd and Howard (1981, 1982) reported on a long-term study 
in which drift fences equipped with drop-bottles filled with alcohol 
were used. This requires a minimum of effort, but unless the drift 
fences are placed beyond a substantial strip of non-habitat, it is very 
difficult to distinguish residents from dispersers. 

Finally, there is the long-standing technique of trapping at var- 
ious distances from a marked source population (Stoddart, 1970; 
Wolff and Lidicker, 1980). This can be done with assessment lines 
extending from the source population or by sampling at various 
distances away. This technique gives reliable data when a marked 
animal is caught and can even distinguish excursions if live-traps 
are used. However, because of the geometry of area-distance effects 
this approach is extremely inefficient and unlikely to provide quan- 
tifiable results. 

Radioactive isotopes have been used occasionally to relocate adult 
voles. Godfrey (1954) used “Co on leg rings to determine home- 
range size in 23 M. agrestis. Hilborn and Krebs (1976) glued '**T'a 
wires to the ear tags of 219 M. townsendii, and assessed dispersal 
rates by whether or not the radioactive tags remained on their grids. 
They found that tags could be detected as much as two feet under- 
ground, permitting the location of dead voles. The method, however, 
fails to distinguish between losses from predation and dispersal. 
Wolff and Holleman (1978) marked three pregnant females (M. 
xanthognathus) with “Zn and then were able to follow movements 


Dispersal 425 


of the radioactively tagged juveniles. This approach was expanded 
by Tamarin et al. (1983) who used eight different radionuclides, 
sometimes in combinations, to greatly increase the number of preg- 
nant females in a single population that could be marked simulta- 
neously. The use of radioactive materials clearly has some potential 
in dispersal studies. However, there are severe limitations on the 
number of animals that can be marked in this way, on the distances 
over which movements can be detected, and on the appropriateness 
of using this approach in populated areas. 

The use of radio transmitters to track vole movements is in its 
infancy, and promises to be a much more widely used technique in 
the future. Madison (1978, 1980a, 19806, 1981) pioneered this 
approach on voles, greatly increasing our understanding of spacing 
behavior and social dynamics in M. pennsylvanicus. 

As always, each technique offers certain advantages and liabilities. 
With increased knowledge, we should be able to design techniques 
that improve resolution. In part this will be abetted by focussing 
our attention on specific types of dispersal rather than by trying to 
measure a general class of behavior that may defy simplistic eval- 
uations. 


A Classification of Dispersal 


Within the genus Microtus it is already clear that dispersal be- 
havior is generally not independent of season, density, and life-his- 
tory events. Moreover, a variety of proximal motivating circum- 
stances can be invoked. This variety tempts one to erect different 
categories of dispersal behavior that will be helpful in organizing 
our thinking about dispersal and in designing research programs 
for its further elucidation. I therefore propose the following tenta- 
tive classification of dispersal for members of the genus Microtus. 

A) Saturation 

B) Pre-saturation 

1) Seasonal 

2) Ontogenetic 
3) Colonizing 
4) Interference 


I do not imply that all categories will apply to all species in the 
genus, but only that evidence exists for these five types of dispersal 


426 Lidicker 


in at least one species. These categories also are not discrete nor 
mutually exclusive. Ambiguous cases and combinations of types are 
to be anticipated. The value of such a classification is intended to 
be heuristic, not operational. 

Saturation dispersal refers to the classic situation in which es- 
sential resources (food, water, shelter) are limiting numbers; that 
is, the population is at its carrying capacity, and individuals leave 
because to stay would result in their prompt demise. For a more 
complete discussion of this phenomenon, see Lidicker (1975). This 
is the kind of dispersal most logically incorporated into “‘gross mor- 
tality.” By contrast, pre-saturation dispersal occurs when individ- 
uals leave home before carrying capacity is reached. In some cases 
these movements are correlated with regularly recurring seasonal 
events (B-1) such as reproduction or preparation for over-winter- 
ing. They may also occur (B-2) at a certain life stage (many species), 
or when empty habitat becomes available (B-3), such as following 
a population crash. Caution is required in identifying individual 
cases, because some instances of saturation dispersal may also occur 
regularly at particular seasons or perhaps result in colonization. 

I know of only one case of interference dispersal, which is char- 
acterized by movements motivated by predators, parasites, or su- 
perior competitors. Fulk (1972) reported that movements of M. 
pennyslvanicus were responsive to the presence of the predatory 
shrew, Blarina brevicauda. 

Table 1 summarizes available information on dispersal organized 
into the four common categories. Saturation dispersal is surely not 
as rare as implied by the table. It must occur in all unconfined 
populations at least occasionally (when densities reach carrying ca- 
pacity). The European species M. agrestis and M. arvalis also have 
been shown to exhibit all four types of dispersal (Hansson [1977], 
Myllymaki [1977], and Pokki [1981] for M. agrestis; and Frank 
[1954], Mackin-Rogalska [1979], and Pelikan [1959] for M. ar- 
valis). 

One type of movement not included in Table 1, but that could 
be considered a form of ontogenetic dispersal because it involves a 
particular sex and age group, is that which occurs when a repro- 
ductive female abandons her nest to her weaned young. Sometimes 
this merely involves changing nests within the same home range 
and in other cases the home range is shifted as well. Only in the 
latter case should this phenomenon be considered dispersal. Appar- 


Dispersal 427 


ently, this interesting and important behavior is widespread in M:- 
crotus, occurring in at least five species (data summarized in Jan- 
nett, 1980). 

There have been at least two other attempts to classify movements 
among voles. Madison (1980qa) distinguished ‘“‘shifters” and “wan- 
derers” from “‘dispersers” based on patterns revealed by telemetry. 
Shifters seem closest to residents in that they progressively oc- 
cupied different sections of a composite home range, or gradually 
moved their home range in some direction. Wanderers, on the other 
hand, either returned to a previous home range, and hence were on 
an excursion, or did not establish home ranges and were the same 
as nomads. Baird and Birney (1982) differentiated moving voles 
into true dispersers, which colonize trapped-out areas, and ‘“‘mov- 
ers,” which travel long distances within a trapping grid. The latter 
category was dominated by adult males, and may have been com- 
posed largely of individuals on excursions. In neither of these papers 
was dispersal as defined here explictly viewed as a heterogeneous 
phenomenon. 


Characterization of Dispersers 


The attributes of dispersers can only be documented when dis- 
persers can be reliably distinguished from other individuals. Some 
of the difficulties encountered in such identifications were pointed 
out above. A second difficulty stems from the presumed heteroge- 
neity of dispersal behavior among voles. If dispersal varies in its 
causes, timing, and consequences, we should anticipate that dispers- 
ers will be a correspondingly heterogeneous assemblage. Hopeful- 
ly, in the future we will be able to characterize dispersers in relation 
to specific sorts of dispersal behavior. Only a beginning toward a 
realization of this goal can be made at present. 

Following the review by Gaines and McClenaghan (1980), I will 
discuss the characteristics of dispersers in three categories: demo- 
graphic, behavioral, and genetic. 


Demographic Features 


It is a common feature among mammals that males tend to be 
the more dispersive sex (Greenwood, 1980). Among species of M:- 
crotus this tendency is true mainly for subadults, and then not to a 


Lidicker 


428 


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(8961) Auquasy ¢ -joIpaid) (¢¢6]) uolusg wnLojaurd “Ay 


suIzIUojOTD 91u9801UQ, yeuoseas uoneinyes satsadg 


satiosaje0 [essadsiq 


GaNNILLNOD 
1 ATAVL 


430 Lidicker 


marked degree. For example, only 58% of dispersers in M. penn- 
sylvanicus are males (Dueser et al., 1981). In some cases a slight 
plurality of males among dispersers is correlated with an excess of 
males in the source population as well (Krebs et al., 1976; Riggs, 
1979; Tamarin, 1977). Adult males may predominate among dis- 
persers moving at the beginning of the breeding season (Beacham, 
1981; Lidicker, 1973; Pearson, 1960; Wolff and Lidicker, 1980), 
which is caused by a social reorganization that typically occurs at 
this time. Dispersal that occurs during summer lulls in reproduction 
or at unfavorable times of the year (probably saturation dispersal) 
tends to involve random samples of the population with respect to 
sex and age. In two such cases (Tamarin [1977] for M. pennsyl- 
vanicus, and Riggs [1979] for M. californicus), adult females were 
found to disperse in excess of the their proportions in the popula- 
tion. Generally, when numbers are summed over all seasons, many 
of these interesting details are obscured, and little sex or age bias 
in dispersals emerges. For example, in M. agrestis the overall sex 
ratio among dispersers is 54% males to 46% females (Pokki, 1981). 
Gaines et al. (1979) found that M. ochrogaster dispersing into re- 
moval grids were male-biased, but those colonizing burned areas or 
leaving enclosures were not. This result cautions against lumping 
results from different conditions of dispersal as well as over seasons. 

One interesting behavioral attribute that tends to equalize dis- 
persal between sexes among subadults is the tendency of litter mates 
to disperse as a group. Evidence was provided by Hilborn (1975) 
for four species of Microtus, and his conclusions were supported 
independently by Beacham (19796) for M. townsendut. 

The reproductive status of dispersers is a complex and contro- 
versial matter. Clearly, adults that disperse at the start of breeding 
(mainly males) are reproductively active. Saturation dispersers gen- 
erally are non-reproductive as are subadults moving after the end 
of the breeding season (for example, M. xanthognathus, Wolff and 
Lidicker, 1980). Subadults dispersing during the breeding season 
are typically coming rapidly into breeding condition so that they 
can breed without delay upon establishing a new home range. Thus, 
such dispersers intercepted while leaving tend to be pre-reproduc- 
tive and those caught upon arrival, for example in a trapped-out 
area, are reproductively active. Probably consistent with this, ‘Tam- 
arin (1977) reported that on the average dispersers in both M. 
breweri and M. pennsylvanicus were in reproductive condition to a 


Dispersal 431 


greater extent than residents. Baird and Birney (1982) reported the 
same finding in M. pennsylvanicus. Probably the act of dispersal 
serves to release subadults, especially females, from reproductive 
inhibition perpetrated by their home social environment (Lidicker, 
1975). Thus, sexual maturity may be reached sooner in dispersers 
than in residents. Evidence for this is available for M. pennsylvan- 
icus (Myers and Krebs, 1971; but see Baird and Birney, 1982), M. 
ochrogaster (Gaines et al., 1979; Myers and Krebs, 1971; Richmond 
and Conaway, 1969), and M. townsendi (Beacham, 1981; Krebs et 
al. 1976). In M. townsendii1, however, Beacham (1981) found that 
at least some subadults became reproductively mature before they 
dispersed. 

Dueser et al. (1981) made the interesting claim that dispersers 
(M. pennsylvanicus), once reestablished, continue to have a greater 
reproductive potential than non-dispersers. Lifespans were com- 
parable between the two groups. Pregnant females were found dis- 
persing in M. oeconomus (Tast, 1966), M. xanthognathus (Wolff 
and Lidicker, 1980), M. montanus (Jannett, 1980), and M. penn- 
sylvanicus (Dueser et al. 1981). Additional examples of this prob- 
ably will be found in those species in which adult females sometimes 
leave their home range to their weaned young (Jannett, 1980). An 
explanation for this curious finding may lie in the observation by 
Madison (1978) that female M. pennsylvanicus have a tendency to 
make excursions (distance reconnaissance) just before parturition. 
Myers and Krebs (1971) reported considerable dispersal among 
lactating females of M. pennsylvanicus and M. ochrogaster. Lastly, 
Myllymaki (1977) suggested that breeding female M. agrestis are 
the most efficient colonizers, as Mackin-Rogalska (1979) suggested 
for M. arvalis. Collectively this evidence adds to a surprisingly large 
role for reproductively active females in dispersal, a group tradi- 
tionally thought to be least likely to leave home. 

Correlations between dispersal and body weight are of limited 
value unless controlled for age and season. Further confusion is 
sometimes built into studies where the operational definition of 
disperser involves body weight. Generally, body weight is assumed 
to measure age. Therefore, the results usually are concordant with 
the age correlations given above. It would clearly be of great im- 
portance to know if dispersers as a group were in better or worse 
condition than residents. But I know of no study that examines this 
question by controlling for age effects on body weight. On average, 


432 Lidicker 


pre-saturation dispersers should be in better condition than those 
fleeing saturated conditions (Lidicker, 1975). 


Behavioral Features 


Considerable attention has been directed to the possibility that 
dispersers are behaviorally divergent from residents in ways other 
than the dispersal act itself. In particular, aggressive behavior has 
been examined because of its connection to the Chitty-Krebs hy- 
pothesis of density regulation in multi-annual cycles (Krebs, 1978a). 
At first a genetic polymorphism in aggressive behavior was hypoth- 
esized to be the key element in determing this cycle. Later, aggres- 
sion was coupled with dispersal. The hypothesis predicts that dur- 
ing population increases, aggressive morphs will tend to make 
dispersers out of non-aggressive individuals, thus slowing local pop- 
ulation growth and increasing the population of aggressive types in 
the source population. Under unfavorable conditions such dense and 
highly aggressive populations will decline rapidly with almost all 
losses being due to mortality. During the subsequent low-density 
period, the non-aggressive, dispersal morph is favored. This model 
predicts that dispersers are largely of the pre-saturation type and 
relatively non-aggressive. It further predicts that in populations that 
do not show multi-annual cycles, aggression will be independent of 
dispersal and undifferentiated between residents and dispersers. This 
last prediction is strongly supported by data for M. brewer: on 
Muskeget Island, Masschusetts (Reich et al., 1982). 

Krebs (1970) found changes in aggressiveness (males) associated 
with different phases of the density cycle in M. ochrogaster and M. 
pennsylvanicus. He did not, at that time, correlate these differences 
with dispersal, but did suggest that emigration might be the mech- 
anism selecting for increased aggression in growing populations. In 
1971, Myers and Krebs reported that dispersing males of both M. 
ochrogaster and M. pennsylvanicus showed less exploratory behavior 
in a maze than did males from control populations. On the other 
hand, male M. pennsylvanicus from removal grids (dispersers) were 
more aggressive than control males, at least during periods of high 
density. Male M. ochrogaster from removal grids, however, tended 
to be behaviorally subordinate. Turner and Iverson (1973) reported 
that resident M. pennsylvanicus were more aggressive than non- 
residents, and they did not find any consistent relation between 


Dispersal 433 


aggression and density. In the case of M. breweri, which does not 
show multi-annual cycles, Reich and Tamarin (1980) concluded 
that dispersers had higher levels of avoidance behavior as compared 
to residents. Thus, dispersers were likely to be subordinates as was 
the case for M. ochrogaster. Krebs et al. (1978) compared the be- 
havior of dispersers and residents in M. townsendi. Generally dis- 
persers showed less wounding, were more submissive in staged diadic 
encounters, and vocalized more. For most species tested, therefore, 
dispersers seemed to be less aggressive than residents. This finding 
is concordant with the Chitty-Krebs model. 

Christian (1970) and Anderson (1980) also predicted that dis- 
persers will be social subordinates, but for different reasons. Rather 
than suggesting that a behavioral polymorphism is involved, they 
argued that young are subordinate to parents and it is in the par- 
ents’ best interest to have the young disperse. Dispersal is thus 
involuntary. Anderson (1980) further predicted that fathers will 
drive off their sons, mothers will expel offspring only when re- 
sources become scarce, and sex ratio of dispersers will be strongly 
biased toward males early in the breeding season and tend toward 
equality later, and males will move farther than females. ‘This mod- 
el fails to account for the high proportion of adults that disperse in 
Microtus and for the relatively high proportion of females among 
dispersing subadults. It also tends to negate selection for dispersal 
through individual advantage to the dispersers. Anderson’s (1980) 
model, however, could apply to ontogenetic dispersal; its predictions 
should be tested. 

The tendency for dispersers to be relatively non-aggressive can 
support still other explanations of dispersal behavior. It is my sus- 
picion that dispersers are non-aggressive because they are not res- 
idents. That is, they are deficient in the well-known “territorial 
imperative” of property owners. This model predicts that if and 
when dispersers reestablish home ranges, they will become more 
aggressive. Aggressive behavior should in this case also have low 
heritability (in contrast to the Chitty-Krebs model). It is therefore 
of interest that Anderson (1975) reported zero heritability for ag- 
onistic behavior in M. townsendi. Socially mediated proximate mo- 
tivations are not ruled out by the model, but are presumed to in- 
teract with age, reproductive condition, and local density. In fact, 
this phenotypic-plasticity model also explains the reproductive 
stunting that occurs in high density populations (Batzli et al., 1977; 


434 Lidicker 


Lidicker, 1979, 1980). If reproductive maturation is an invitation 
for aggression, as seems likely, it should be advantageous for sub- 
adults to delay maturity under high-density situations if the chances 
of finding a suitable place for reestablishment are greatly reduced. 
As peak numbers are approached, average aggressiveness should 
fall rather than reach a maximum; mature adults, however, should 
remain aggressive and in fact some could be induced thereby to 
become dispersers. This possibility could explain the high level of 
aggression among male dispersers found in peak populations of M. 
pennsylvanicus by Myers and Krebs (1971). ‘The phenotypic-plas- 
ticity model shares some features with Anderson’s (1980) model but 
is more comprehensive in its incorporation of 1) adult dispersal, 2) 
greater emphasis on female movements, and 3) non-forced dispers- 
al. It applies particularly to pre-saturation dispersal because there 
probably is no controversy about saturation dispersers being behav- 
iorally subordinate for economic and social reasons. 

Bekoff suggested (Bekoff, 1977; Gaines and McClenaghan, 1980) 
that social interactions occurring prior to dispersal are most critical 
in determining who is going to disperse and when; the predominant 
social behavior around the time of dispersal is avoidance. Bekoff’s 
(1977) idea is compatible with either phenotypic-variation or be- 
havioral-polymorphism models, and would seem to apply most spe- 
cifically to ontogenetic dispersal. Data to test his model are not 
available for Microtus. A final behavioral trait of dispersers is the 
apparent tendency for littermates to disperse or not disperse as a 
unit (Beacham, 19795; Hilborn, 1975). This trait supports either 
the Chitty-Krebs polymorphism model or my phenotypic-plasticity 
model, but is inconsistent with the Christian-Anderson social-sub- 
ordination model. 


Genetic Features 


The possibility that dispersers may be genetically distinct from 
residents has been the subject of widespread speculation and inves- 
tigation. The idea of a dispersal morph is central to recent versions 
of the Chitty-Krebs hypothesis of population regulation. Evolution- 
ary and behavioral ecologists also have been fascinated by the pos- 
sibility of a genetic polymorphism for dispersal behavior. As early 
as 1949 Burt suggested that some individuals were programmed 
genetically for dispersal while others were not. The idea was de- 


Dispersal 435 


veloped more rigorously by Howard (1960), Johnston (1961), Lid- 
icker (1962), and others (see Lidicker and Caldwell, 1982: Part I, 
for review). 

With the widespread availability of electrophoretic techniques, a 
search was made for biochemical markers that might be associated 
in some way with dispersal behavior. The available data are sum- 
marized in Table 2. The two loci most frequently investigated are 
transferrin and leucine aminopeptidase (both from plasma). In ad- 
dition, Pickering et al. (1974) found differences in allele frequency 
at an esterase locus in a very small sample of M. pennsylvanicus. 
The results reported from Baird and Birney (1982) are summaries 
of a complex data set involving comparisions among sex and age 
groups, summer and autumn cohorts, and “movers” as well as dis- 
persers and residents. 

My conclusions from these data are that no consistent pattern 
has emerged, and that this approach has failed to support the hy- 
pothesis of a genetic polymorphism for dispersal. Interpretation of 
the LAP data is especially difficult since allelic frequencies at this 
locus are known to show shifts with season and density. Of course, 
the Chitty-Krebs model is not refuted by the biochemical data be- 
cause no functional connection between these biochemical traits and 
dispersal has been suggested, and indeed it would be surprising if 
they were found to be correlated in some way. LeDuc and Krebs 
(1975) experimentally manipulated LAP genotypes in populations 
of M. townsendu but could not produce any alteration of overall 
demography. This result thus fails to support a possible connection 
between LAP genotypes and dispersal in this species (Krebs et al., 
1976). The most that can be extracted from the biochemical data 
at this time is that dispersers are sometimes non-random samples 
of source populations. 

An intriguing finding was reported by Tamarin (1977) for M. 
brewert. He reported that the frequency of a white blaze on the 
forehead occurs more frequently among dispersers. Perhaps it is 
worth mentioning that Garten (1977) found an association between 
exploratory activity and overall heterozygosity at a series of bio- 
chemical loci in Peromyscus polionotus. Contrary conclusions were 
drawn by Blackwell and Ramsey (1972), although their study was 
limited to three loci. Some possible support for Garten’s notion 
could be gleaned from Table 2; heterozygote genotypes are some- 
times found in excess among dispersers. This is an area that would 
warrant further careful work in the future. 


436 Lidicker 


TABLE 2 
BIOCHEMICAL TRAITS FOUND TO BE PRESENT IN GREATER FREQUENCY IN DISPERSERS 
AS COMPARED TO RESIDENTS 


Species Sex LAP Tf References 
M. breweri 3 = Tfe/TEET Keith and 
Tamarin (1981) 
M. californicus 3,2 — Not poly- Riggs (1979) 
morphic 
M. ochrogaster 3,2 Te / Ee Meyers and 


Krebs (1971) 
— Gaines et al. 


(1979) 
M. pennsyl- 3} SS* RE /AE* Myers and 
vanicus g SS* fo / AEs * Krebs (1971) 
6,2 Tfe/Tfc*** Verner (1979) 
6 (subadult, F 
summer) 
6,2 (summer) FS! Baird and Birney 
(1982) 
M. townsend: 3, 2 F and Stt Krebs et al. 
(1976) 
Q FStt — 


Abbreviations: F, fast moving allele; LAP, leucine aminopeptidase; S, slow moving 
allele; TF, transferrin; —, no difference between colonizers and residents. 
* During late population peak and decline. 
** Periods of population increase. 
*** Significant for only one month; and among males for subadults only. 
+ Two month period only; adults. 
tt} Different alleles predominant among colonizers in different areas; FS in excess 
in one summer only. 
‘Only two alleles were distinguished in this study. 


Demographic Causes and Consequences 


With the recognition that dispersal is more than a safety valve 
for saturated habitats and that it can be high, investigators have 
inquired increasingly into its relationship to other demographic pro- 
cesses, including the regulation of numbers. This last relationship 
is particularly significant for Microtus in view of the enigmatic 
multi-annual cycles of abundance often seen in this group. The 
demographic role of dispersal was reviewed by Lidicker (1975) and 


Dispersal 437 


Gaines and McClenaghan (1980) for small mammals in general 
and (with respect to density regulation) by TTamarin (1980) for 
rodents, and by Tamarin (1978) and Taitt and Krebs (this volume) 
for Microtus. 

A corollary of this increasing focus on the demographic aspects 
of dispersal has been the growing realization of the importance of 
spatial structuring in understanding microtine population dynam- 
ics. Dispersal is studied most meaningfully in the context of the 
spatial and temporal discontinuities in numbers; empirical docu- 
mentation of such patterns of distribution is being accumulated at 
an accelerating rate. This area of investigation is reviewed for Mi- 
crotus by Lidicker (in press). 

The demographic implications of dispersal have to do both with 
the quantity of dispersal and with the probability that dispersers 
are qualitatively non-random subsets of source populations. ‘They 
further concern the success rate of dispersers both in travelling 
through unfamiliar and often hostile terrain and in establishing new 
home sites. 

Evidence already summarized on the nature of dispersers strong- 
ly suggests that in Microtus dispersers are generally a non-random 
subset of source populations. We can therefore anticipate that dis- 
persal will have an impact on age structure, natality and mortality 
rates, and sex ratios through the differential loss or gain of disper- 
sers. The particular effect of course will depend on the kind of 
biases that characterize dispersal in any given instance. Myllymaki 
(1977), for example, claims that in M. agrestis the female-biased sex 
ratios he observed during the breeding season, and especially at 
peak densities, were caused by differential dispersal. Dueser et al. 
(1981) found that in populations of M. pennsylvanicus that were 
dominated by dispersers, reproductive rates were higher than in 
other populations. Differences in age structure between populations 
dominated by residents on the one hand, or by immigrants on the 
other, can also be anticipated, but they have not been documented 
for Microtus. 

Quantitative information on the success rate of dispersers is not 
available for species of Microtus. It generally is assumed that dis- 
persers suffer higher mortality rates than residents. They often must 
cross regions of marginal or unsuitable habitat and confront phys- 
ical barriers of various kinds. Encounter rates with predators, par- 


438 Lidicker 


asites, and competitors may be greatly enhanced. Ambrose (1972) 
reported higher predation rates for M. pennsylvanicus unfamiliar 
with an artificial environment than for voles given 4 days to famil- 
iarize themselves with the experimental habitat. And, finally, dis- 
persers can expect to traverse socially hostile neighborhoods as well. 
In all of this potential adversity, dispersers that begin their journeys 
in good physical condition are surely more likely to succeed. We 
can therefore predict that the success rate of pre-saturation dispers- 
ers generally will be much greater than for saturation dispersers 
(Lidicker, 1975). It is satisfying to note that pre-saturation dispersal 
has been found to characterize unequivocally all species of Microtus 
for which dispersal data are available (see Table 1), with the ex- 
ception of M. pinetorum. Population density and the availability of 
empty habitat also will be critically important in affecting success 
rates. For populations exhibiting multi-annual cycles of abundance, 
we can therefore anticipate that average success will vary tremen- 
dously with stage of the density cycle. 

The final step in successful dispersal is the establishment of a 
new home range. If empty habitat is available, this should pose 
minimal risks associated with establishing a system of burrows and 
runways and finding a mate. On the other hand, if the disperser 
attempts to immigrate into an existing population, social antago- 
nisms may have to be overcome and possibly complex problems of 
mate choice confronted. This is an important but virtually unex- 
plored area of microtine research. 

The aspect of dispersal and demography which has received the 
greatest attention is that relating to the quantity rather than the 
quality of dispersers. Gaines and McClenaghan (1980) reviewed 
the data relating dispersal and population density, much of which 
is on Microtus. They concluded that: 1) the number of dispersers is 
correlated positively with population density; 2) a less consistent 
positive relationship can be found between density and rates of 
population increase; and 3) more dispersal consistently occurs dur- 
ing periods of increasing density than during phases of decline. This 
last point emphasizes the prevalence of pre-saturation dispersal in 
voles, and sets the stage for an examination of dispersal and pop- 
ulation growth rates. 

A potentially important relationship between dispersal and pop- 
ulation growth rates is predicted from the basic growth equation in 
which additions are derived from reproduction and immigration 


Dispersal 439 


while losses are composed of deaths plus emigration (for general 
treatment, see Lidicker and Caldwell, 1982). If there is a positive 
net emigration rate and densities are below carrying capacity, a 
suppressing effect of dispersal on growth rates will occur. The best 
documented case in Microtus for suppressed growth rates because 
of dispersal is that for M. californicus (Lidicker, 1975, 1980). Some 
evidence is also available for M. pennsylvanicus and M. ochrogaster 
(Krebs et al., 1969). 

Just as emigration can suppress population growth rate, immi- 
gration can enhance it. Clearly, where refugial populations are 
expanding into uninhabited or low-density areas, the densities in 
such non-refugial habitats will be determined largely by immigra- 
tion. Tast (1966) described how M. oeconomus seasonally re-invades 
flooded areas. Dueser et al. (1981), in their studies of M. pennsyl- 
vanicus, described grid populations that were more than 75% dis- 
persers, and claimed further that for some populations dispersal 
may continue to be a greater source of recruits than reproduction. 
Similarly, Ostfeld and Klosterman (pers. comm.) studied M. cali- 
fornicus in patchy habitats and reported that some habitats are 
chronically inhabited largely by immigrants. 

The intriguing and important question of the potential role of 
dispersal in population regulation was reviewed by Lidicker (1975), 
Tamarin (1978, 1980), Krebs (1978a, 19786), and Taitt and Krebs 
(this volume). Certainly dispersal could serve as a regulating factor 
if net losses to emigration increased proportionally as density in- 
creased (Lidicker, 1978; Nakano, 1981). Gaines and McClenaghan 
(1980), however, claimed that there is no evidence of such a pro- 
portional increase in dispersal with density. This statement was 
based on an analysis of “‘recovery ratios” (number of colonizers in 
removal areas divided by population size on control areas) in six 
species of rodents (including four species of Muicrotus). They also 
failed to find any proportional increase in dispersal with density in 
Sigmodon hispidus (McClenaghan and Gaines, 1976). What would 
be critical, however, is an analysis of how dispersal proportion 
changes as the population approaches zero growth rate (from pos- 
itive or negative directions). A regulating influence by dispersal is 
not incompatible with the possibility that at times the population 
may be regulated by other factors or even sometimes behave as if 
non-regulated. 

The best evidence that Microtus populations are in fact sometimes 


440 Lidicker 


regulated by dispersal is the “fence effect” phenomenon. When 
dispersal is prevented in growing populations by enclosing them in 
a fence or on a small island, densities characteristically increase 
dramatically. This has been demonstrated for at least six species of 
Microtus (Boonstra and Krebs, 1977; Clarke, 1955; Gentry, 1968; 
Hatt, 1930; Houlihan, 1963; Krebs, 1979; Krebs et al., 1969, 1973; 
Lidicker, 1979; Lousch, 1956; ‘Tamarin and Krebs, 1969; van 
Wijngaarden, 1960; Wiegert, 1972). This impressive evidence, and 
that for extensive and widespread pre-saturation dispersal (men- 
tioned above) suggests that numbers in unenclosed populations are 
ordinarily regulated by dispersal, but that when dispersal is pre- 
vented by the filling of the dispersal sink, peak densities result 
(Lidicker, 1973, 1975). Hestbeck (1982) modified this model slight- 
ly by suggesting that what is proximally important is not the filling 
of usable habitat but the erection of social barriers to dispersal. 

The above view of dispersal in vole populations implies that 
dispersal plays a density regulating role in two classes of circum- 
stances: 1) when a population is surrounded by a permanent dis- 
persal sink; and 2) when a population exhibiting multi-annual cycles 
undergoes the long growth phase. An example of the former was 
described by Abramsky and Tracy (1979). They studied popula- 
tions of M. ochrogaster living in artificially fertilized and watered 
plots surrounded by shortgrass prairie, which is very poor habitat 
for this species. In multi-annual cycles, dispersal should act in a 
regulating fashion during most of the low phase. This should be 
followed by a rapid increase in numbers when dispersal fails to 
keep up with reproduction because of a nearly filled dispersal sink 
and the longer breeding seasons and reduced mortality rates often 
associated with “pre-high” situations. Under peak and initially de- 
clining conditions, saturation dispersal should occur followed by a 
period of little or no dispersal. 

Recently, the curious idea was advanced that not only is emigra- 
tion important in determining population numbers, but immigra- 
tion is critical for generating multi-annual cycles (Abramsky and 
Tracy, 1979; Dueser et al., 1981; Gaines et al., 1979; Rosenzweig 
and Abramsky, 1980). Such a role for immigration has been attrib- 
uted to: 1) disruption of stability by influx of inappropriate geno- 
types to a habitat patch (Abramsky and Tracy, 1979; Rosenzweig 
and Abramsky, 1980); 2) prevention of local extinction (Gaines et 
al., 1979); and 3) a source of vigorous recruits to the populations 


Dispersal 441 


(Dueser et al., 1981). In addition, Smith et al. (1975) implied that 
high densities are encouraged by immigration through outbreeding, 
which leads to increased heterozygosity levels with consequent im- 
provements in vigor and reproductive performance. Only the first 
of these would seem to relate directly to multi-annual cycles. More- 
over, such genetic perturbations seem unnecessarily complex, and 
may require an inappropriate time scale. 

The factual basis for this immigration hypothesis seems to be the 
findings of Abramsky and Tracy (1979) and Gaines et al. (1979), 
who showed that enclosed populations of M. ochrogaster in which 
emigration is permitted do not develop multi-annual cycles. They 
came to the unnecessary conclusion that what is critically lacking 
in these cases is immigration. In my view, their results are more 
easily interpreted as instances of unfilled dispersal sinks preventing 
density buildup. Moreover, Tamarin et al. (1984) found that 
normal cycles occurred in M. pennsylvanicus housed in enclosures 
in which emigration but not immigration was permitted. According 
to my model, these results are expected because the emigration filter 
(forest in this case) was sufficient to extend the period of population 
growth but was inadequate to prevent peak densities from devel- 
oping eventually. What is therefore lacking in the non-cyclic ex- 
amples is not immigration but sufficient frustrated dispersal to gen- 
erate a peak density and subsequent crash. 

In recent years considerable attention has been directed toward 
connecting an explanation of multi-annual cycles in microtines to mi- 
cro-spatial structuring of populations (Abramsky and Van Dyne, 
1980; Anderson, 1980; Bowen, 1982; Charnov and Finerty, 1980; 
Cockburn and Lidicker, 1983; Hansson, 1977; Hestbeck, 1982; 
Mackin-Rogalska, 1979; Rosenzweig and Abramsky, 1980; Sten- 
seth, 1977; Stenseth et al., 1977). This approach is clearly a cor- 
relate of the potential importance of dispersal in microtine popu- 
lation dynamics. Discontinuities in distribution (structuring) become 
interesting when they are variously connected and modified by dis- 
persal. The role of population structuring in understanding multi- 
annual cycles was reviewed by Lidicker (in press). 

Up to this point my model of the role of dispersal in multi-annual 
cycles has two components. First, pre-saturation dispersal must oc- 
cur so that population growth can be suppressed for long periods, 
even at low densities. In addition to evidence already cited, a general 
relationship between pre-saturation dispersal and multi-annual cy- 


442 Lidicker 


clicity is supported by Gliwicz (1980), Krebs and Myers (1974), 
Rasmuson et al. (1977), Stenseth (1978), and Tamarin (1978). 
Possibly correlated with this evidence is the contention by Gaines 
and McClenaghan (1980) that males predominate among dispersers 
in cycling species but not in non-cyclers. Second, large dispersal 
sinks must exist which become periodically filled, causing frustra- 
tion of dispersal. In my recent review (Lidicker, in press) a third 
component is added. It seems characteristic of cycling populations 
that there is a limited availability of good survival habitats during 
the most stressful times of the year. Survival habitat (sensu Ander- 
son, 1980) is strongly limited relative to “‘colonizing habitat.” This 
feature is important in that densities are caused to periodically 
decline to levels several orders of magnitude below carrying capac- 
ities characteristic of favorable times. If severe declines don’t occur, 
recovery of densities from seasonal lows is rapid enough for annual 
peaks to be produced. Charnov and Finerty (1980) also predicted 
that patchy habitats are required for multi-annual cycles to occur. 
If any one of these components is missing, multi-annual cycles will 
not result. Of course, variations in the size of annually occurring 
peaks is to be expected, and occasional irruptions also may occur 
in non-cycling species because of some unusually favorable circum- 
stance. These latter variations should not be construed as multi- 
annual cycles in the sense intended here. 


Evolutionary Issues 


The evolution of dispersal behavior and the influence of dispersal 
on evolutionary processes constitute two enormous areas of inquiry. 
For brief overviews, see Gaines and McClenaghan (1980:186-189) 
and Lidicker and Caldwell (1982: Part V). With respect to Micro- 
tus, these subjects mostly raise questions for future investigation. 

In my view, however, research on microtine rodents will likely 
make a significant contribution to our understanding of these evo- 
lutionary issues. This is not only because microtines are relatively 
well known, but also because they exhibit a rich variety of dispersal 
behaviors, temporal density patterns, habitat relationships, social 
habits, and spatial structuring configurations. Moreover, these vari- 
ations can be studied in the same population (temporally), intra- 


Dispersal 443 


specifically, interspecifically, and intergenerically. Thus, the evolu- 
tionary biologist should find a substrate for answering a variety of 
questions relating to dispersal. 

Studies on species of Microtus have been, or should be in the 
future, addressed to the following general questions relating to dis- 
persal and evolution. 

1) How does environmental heterogeneity in space and time con- 
tribute to the evolution of various kinds of dispersal ? 

2) Are there particular life history features or social systems that 
are conducive to, or inhibiting to, the evolution of dispersal ? 

3) What is the nature of the genetic substrate for dispersal be- 
havior, and how does this vary across different kinds of dispersal ? 

4) Are there circumstances in which polymorphisms for dispersal 
occur? 

5) What are the consequences of dispersal for demic differentia- 
tion and species cohesion? 

6) Is group selection involved in the evolution of dispersal? 

Environmental heterogeneity as a factor in the evolution of dis- 
persal has been treated extensively in the theoretical literature. There 
seems no doubt that a positive relationship exists. On the other 
hand, Hamilton and May (1977) argued that dispersal can evolve 
even in stable habitats. Applications of this body of theory directly 
to Microtus have been limited (but see Hansson, 1977; Stenseth, 
1980; Tamarin, 1978). The nearly ubiquitous occurrences of pre- 
saturation types of dispersal in this genus strongly argues for some 
sort of selective advantage for it. We can predict that pre-saturation 
dispersal of some kind will be more prevalent in species inhabiting 
small patches of non-permanent habitat, such as M. xanthognathus, 
than in those occurring (at least historically) in more continuous 
habitat, such as M. ochrogaster. 

Although at least some kinds of dispersal seem to be important 
components of the life history of all species of Microtus, much re- 
mains to be learned regarding correlations between particular kinds 
of dispersal and life-history details (including social behavior). A 
few authors have concluded that dispersal is quantitatively low 
(Madison, 1980c; Tamarin et al., 1984; Verner, 1979), but these 
views are atypical among Microtus biologists. Recent attention has 
been directed at elucidating the possible role of dispersal in multi- 
annual cycles exhibited by many populations (see review by Lid- 
icker, in press). In the model outlined, a prominent but not exclusive 


444 Lidicker 


role for dispersal is proposed to explain this interesting pattern of 
density fluctuation. 

Little progress has been made in illuminating the genetic basis 
for dispersal in Microtus. As pointed out above, such behaviors are 
almost certainly heterogeneous, greatly complicating such an anal- 
ysis. Moreover, the inheritance of even one type of dispersal is likely 
to be complex. Ontogenetic and seasonal types of dispersal imply a 
strong genetic basis. Colonizing dispersal may not be rooted firmly 
in the genotype, and saturation dispersal should be least influenced 
by genetic constitution. The only attempt to measure heritability 
has been by Anderson (1975; see also Krebs, 1979), who reported 
that M. townsendi exhibited moderate heritability on the basis of 
comparisions between residency length within and between groups 
of siblings. Although a higher correlation in length of residency 
among sibs suggests a strong genetic basis for dispersal, this result 
is confounded by non-genetic factors that may affect littermates 
collectively, such as maternal influences. To a large extent these 
non-genetic influences were factored out by Anderson’s findings that 
the correlation with residency was significantly higher on unfenced 
grids (where dispersal was possible) than on fenced grids. Concor- 
dant with this result is the evidence that sibling groups either dis- 
perse or don’t disperse as units (Beacham, 19796; Hilborn, 1975). 

High heritabilities and genetic polymorphisms for dispersal be- 
havior are predicted by the Chitty-Krebs model of population reg- 
ulation in multi-annually cycling microtines (Krebs, 1978a). As 
pointed out above, the evidence so far fails to support the prediction 
of dispersal polymorphisms. However, the subject is sufficiently 
difficult and important that it warrants further investigation. 

The role of dispersal in demic differentiation is a major area of 
inquiry in population genetics (see also Gaines, this volume, for 
related discussion). The availability of electrophoretic techniques 
has permitted an empirical approach to this issue on a fine temporal 
and spatial scale. In M. californicus, Bowen (1982) and Lidicker 
(unpubl. observ.) demonstrated that genetic heterogeneity among 
small demes persisting at low densities is high relative to a more 
general panmixia prevailing at high densities. Moreover, stochastic 
processes are critical in determining the genetic composition of re- 
fugial demes. The approach needs to be expanded to larger geo- 
graphical arenas and to other species. Voles should contribute sub- 
stantially to future advances in this area. 

Finally, and perhaps most intriguing of all, investigations on 


Dispersal 445 


dispersal in voles has the potential for contributing to one of the 
current major philosophical issues now raging in evolutionary bi- 
ology. I refer to the general issue of levels of natural selection, and 
in particular to whether or not group selection has played a signif- 
icant role in evolution. Van Valen (1971) gave us a general model 
that suggested (under a rather robust set of conditions) that group 
selection can indeed lead to the evolution of dispersal (including 
polymorphisms). Charnov and Finerty (1980) have suggested that 
kin selection and dispersal may interact to explain low levels of 
aggression at low densities (when voles mostly interact with rela- 
tives) and rapidly increasing aggression in growing populations 
(when dispersal brings non-relatives into frequent contact). 

Of course, it is difficult to make critical observations or do ex- 
periments on such relatively long-lived animals as voles to directly 
test a particular evolutionary hypothesis. We can, however, discover 
whether or not the appropriate substrate for a given selection model 
exists in nature. This at least allows us to support the claim that a 
particular model can or cannot be operating, even if it is extremely 
difficult to establish that it actually does. By analogy with individ- 
ual-level selection, we observe differential reproduction and survival 
among individuals, and feel comfortable about natural selection oc- 
curring at this level even though we may not be able to show a 
direct connection between observed fitness differences and some ac- 
tual change in genetic composition of a population. In this regard, 
Wilson’s (1975, 1977) trait-group model of group selection seems 
particularly relevant to voles. In at least two species of Muicrotus, 
populations alternate, seasonally or multi-annually, through phases 
characterized by small isolated trait groups and large panmictic 
assemblages (Bowen, 1982; Lidicker, in press; Wolff and Lidicker, 
1981). In my view, this is an area that warrants additional atten- 
tion. 


Summary and Conclusions 


Dispersal is a major factor in the lives of voles. It also is definitely 
not a homogenous phenomenon, varying importantly in its timing, 
proximal motivations, demographic consequences, and in the nature 
of the dispersers themselves. This heterogeneity adds complexity to 
the inherent difficulty of studying dispersal in such small, cryptic, 
short-lived, and secretive animals. Techniques of study should be 


446 Lidicker 


designed specifically for a particular kind of dispersal in order to 
maximize effectiveness. Useful, if not always satisfying, results have 
been obtained with trapped-out grids, with and without barriers of 
poor habitat, and with and without “pulsed removals.” Another 
approach has been to use leaky enclosures. This gives more secure 
identification of dispersers, but also incorporates the artifacts of 
confinement. Assessment trap-lines provide accuracy but low res- 
olution. Radioactive isotopes have been used with some success, and 
radio transmitters have considerable potential for making important 
contributions. 

A classification for dispersal as found in the genus Microtus is 
proposed. This includes saturation dispersal and four categories of 
pre-saturation dispersal: seasonal, ontogenetic, colonizing, and in- 
terference. With the interesting exception of the pine vole (M. pi- 
netorum), at least some type of pre-saturation dispersal is found in 
all species for which data are available (nine North American and 
two European species). Undoubtedly saturation dispersal is ubiq- 
uitous as well, but it has not been so widely documented. 

The characterization of dispersers has been confused by the gen- 
eral failure to distinguish among the different kinds of dispersal. 
Some tentative generalizations are possible, however, based on 
available data. Males predominate only slightly among dispersers. 
The strongest male biases are present during seasonal dispersal that 
occurs in association with the beginning of the breeding season, and 
among juvenile emigrants. Saturation dispersal tends to be unbiased 
for sex or is female dominated. Subadults dispersing during the 
breeding season are typically coming rapidly into breeding condition 
and on average seem to reach sexual maturity at a younger age 
than residents. Adult males moving at the beginning of the breeding 
season are reproductively active; adult females may be the most 
adept colonizers. In at least three species, pregnant females have 
been found dispersing. Saturation dispersers are generally non-re- 
productive. Little is known about the general physiological condi- 
tion of dispersers. 

Dispersers tend to be less aggressive than residents. ‘This gener- 
alization fits the Chitty-Krebs model of population regulation, the 
Christian-Anderson social-subordination model, and a new phe- 
notypic-plasticity model proposed here. Testable predictions differ- 
entiate the three models relating dispersal and aggressive behavior. 


Dispersal 447 


The data available so far on Microtus best support the third model, 
which incorporates adult as well as subadult movements, low her- 
itabilities for dispersal, voluntary as well as forced movements, and 
a greater emphasis on female dispersal. 

The possibility that dispersers as a class may be genetically dis- 
tinct from residents has been explored extensively. The strongest 
support for this proposition comes from evidence (four species) that 
litters tend to disperse, or not disperse, as units. Biochemical genetic 
data suggest that at least in some cases, dispersers are not a random 
subset of residents. However, no consistent association of dispersal 
with particular genotypes has been found, and there is no evidence 
at all for a genetic polymorphism for dispersal. In some cases het- 
erozygote genotypes have been found in excess among dispersers. 

The demographic causes and consequences of dispersal have re- 
ceived increasing attention. There is a growing realization of the 
importance of spatial structuring in understanding vole population 
dynamics. Demographic implications of dispersal stem from: 1) the 
nature of dispersers relative to residents; 2) the success rate of dis- 
persers in reestablishing home ranges; and 3) the quantity of em- 
igration versus immigration. Because dispersers are generally a non- 
random subset of residents (at least for pre-saturation dispersal), 
they should have (and some evidence exists for) impacts on age 
structure, natality and mortality rates, and sex ratios. Little infor- 
mation is available on survival rates of dispersers and on reestab- 
lishment effectiveness. I assume that pre-saturation dispersers are 
more successful than saturation dispersers, and that colonization of 
empty habitat is less risky than immigration. If true, selection should 
strongly favor pre-saturation dispersal from low density populations 
during favorable seasons of the year. Quantitative data on these 
processes are needed badly. The quantative component of dispersal 
has received the greatest attention. Clear impacts on population 
growth rates, both by emigration and immigration, have been dem- 
onstrated for a few species. 

Research on Microtus has pioneered investigations into the role 
of dispersal in density regulation. Although it is theoretically fea- 
sible that dispersal can perform such a role, good evidence is difficult 
to obtain. The “fence effect” phenomenon, known for six species of 
Microtus, is the best evidence that densities reach supra-normal 
levels when dispersal is prevented. This evidence, in addition to the 


448 Lidicker 


existence of pre-saturation dispersal, has led to a model in which 
dispersal plays an important role in regulating numbers when den- 
sities are low. With the filling of the dispersal sink and the frus- 
tration of dispersal that follows, densities rise to peak levels. A 
second circumstance in which dispersal plays such a critical regu- 
lating role is when a population of voles is surrounded by a per- 
manent dispersal sink. ‘These early models have now been expanded 
to describe the role of dispersal in the multi-annual cycle. In ad- 
dition to pre-saturation dispersal and a large dispersal sink being 
consistent features of multi-annual cycles, a third feature has been 
added, namely the condition that survival habitat is strongly limited 
periodically compared to colonizing habitat. This last condition as- 
sures that populations will go regularly through bottlenecks of very 
low densities. This three-part model, of course, does not purport to 
explain multi-annual cycles, but emphasizes that dispersal is an 
important component of this demographic pattern. 

Finally, dispersal in Microtus is discussed in terms of the evolu- 
tionary issues with which it impinges. Because of the importance 
of dispersal to evolutionary processes and because of the complex 
spatial and temporal structuring exhibited by at least some species, 
dispersal inevitably will be central to any discussion of evolution in 
this group. Six general questions relating dispersal and evolution 
in voles are proposed, and the status of research in each of these 
areas is reviewed. Areas of inquiry include the role of environmental 
heterogeneity, life-history correlates of dispersal types, heritabilities 
of kinds of dispersal, dispersal polymorphisms, demic differentia- 
tion and species cohesion, and the possible role of group selection. 
I predict that, on these general topics, research with voles will make 
substantial contributions to our understanding of evolutionary pro- 
cesses. 


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Riccs, L. A. 1979. Experimental studies of dispersal in the California vole, 
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ROSENZWEIG, M. L., AND Z. ABRAMSKY. 1980. Microtine cycles: the role of habitat 
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454 Lidicker 


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PARASITES 
ROBERT M. TIMM 


Abstract 


HE objective of this review is to bring together and summarize 
T the diverse literature on parasites of New World Microtus, to 
summarize life cycles of the ectoparasitic fauna, and to put the 
different groups of parasites into a biological perspective. ‘The lit- 
erature on parasites of Microtus contains over 485 primary refer- 
ences covering the 91-year period from 1894 to 1984. However, of 
the 26 species of New World Microtus now recognized, parasite 
data exist for only 16 species. Most of the data available are for six 
of the most widely distributed species, Mzcrotus californicus, M. lon- 
gicaudus, M. montanus, M. ochrogaster, M. pennsylvanicus, and M. 
pinetorum. 

The ectoparasites on Microtus belong to the orders Acari (mites 
and ticks), Anoplura (suckling lice), Coleoptera (beetles), Diptera 
(flies), and Siphonaptera (fleas). 'welve families of mites are known 
from Microtus. These range in size from minute demodicids that 
live within hair follicles and sebaceous glands to the large, active 
laelapids. Very little work has been done on any of the mites with 
the exception of chiggers (family Trombiculidae). Most groups are 
in need of taxonomic revision. Chiggers have been intensively stud- 
ied, both taxonomically and biologically, as they are of direct med- 
ical importance to man. Eighteen species of ticks have been reported 
from Microtus. Several species of ticks carried by Microtus are re- 
sponsible for diseases that affect man, and the systematics and ecol- 
ogy of these vectors have received much attention. Only two species 
of sucking lice are true parasites of Microtus, although a few other 
species have been reported in the literature as being found on M:- 
crotus. The systematic relationships of the lice are well understood; 
however, little work has been done on their biology. Lice have been 
reported on only 12 species of Muicrotus; the absence of lice on 
several species (for example, M. chrotorrhinus) has not been ex- 
plained. Parasitic beetles belonging to two families have been found 
only occasionally on Microtus. It is likely that they are regularly 


455 


456 Timm 


associated with Microtus, living primarily within the nest and hence 
seldom encountered. Two families of parasitic flies are known from 
Microtus. Both bot flies and flesh flies are uncommon parasites of 
Microtus, and if found in high numbers may have an adverse affect 
upon the host. Seventeen genera of fleas regularly parasitize Mi- 
crotus in North America, and 26 other genera are reported as of 
accidental occurrence. A tremendous body of literature exists on the 
systematics and ecology of fleas, especially with respect to bubonic 
plague. However, little work has been undertaken on the effects of 
fleas or the diseases they transmit on Muicrotus. Most species of 
Microtus have several species of fleas; more than one species may 
be present on an individual host with additional species being re- 
stricted to the nest. 

Endoparasites belong to the Acanthocephala, Cestoda, Nemato- 
da, and Trematoda. Only two species of acanthocephalan have been 
found parasitizing Microtus. Several species of cestodes, nematodes, 
and trematodes have been reported from Microtus, and it is certain 
that this list will increase with additional study. A briefly annotated 
list of the endoparasites on New World Microtus is appended. 


Introduction 


Voles of the genus Microtus constitute one of the most widespread 
and intensively studied groups of mammals. However, of the species 
of Microtus now recognized from North America, parasites have 
been reported from only 16 species. This is not due to an absence 
of parasites, but rather reflects lack of study. Undoubtedly a diverse 
parasite fauna will be found on the remaining species of voles. Of 
the 16 species for which some parasite data exist, the vast majority 
of records are from six species, M. californicus, M. longicaudus, M. 
montanus, M. ochrogaster, M. pennsylvanicus, and M. pinetorum. 
The number of species of parasites recorded from a given vole 
species is a direct reflection of how well studied the host is. ‘The 
extent of the host’s geographic range can also affect the total number 
of parasite species as different parasites will occur in various hab- 
itats. Thus, widely distributed species like M. pennsylvanicus can 
be expected to have more species of parasites than a more restricted 
species. It is also possible that a single individual vole of a widely 
distributed species may harbor more species of parasites than an 
individual from a geographically restricted species. However, this 


Parasites 457 


remains to be tested. In spite of the volume of literature available 
on Microtus, we actually know very little about the biology of the 
parasites, and even less of the effects on their hosts. 

The objective of this chapter is to bring together the literature 
on ectoparasites of New World Microtus, and to put the various 
groups of parasites into a biological perspective, rather than just 
provide a list of names. A list of endoparasite records is presented 
in Appendix A. Because more is known about the distribution and 
systematics of North American ticks, lice, and fleas parasitizing 
Microtus, each genus and species is discussed briefly. Since the sys- 
tematics and ecology of the mites are less well known and there are 
so many more of them, mites are discussed by family. The discus- 
sions of each group of parasites vary considerably in content, re- 
flecting the current state of knowledge of that particular parasite 
on Microtus. Brief, informative summaries of all the ectoparasites 
reported from Microtus are presented, with an emphasis on what 
is known about the biology of those species on Microtus. ‘This chap- 
ter should also guide the reader to the primary literature and 
point out interesting and fruitful areas for future research. 

References included are those to the primary literature; second- 
ary listings of parasites from the various species of Microtus are 
generally not mentioned. No human-created experimental infec- 
tions are included. Current scientific names for all species of par- 
asites are used throughout. Synonymies are included within species 
lists for ticks, lice, and fleas. For synonymies of mites see the review 
paper of North American mites parasitizing mammals by Whitaker 
and Wilson (1974). Whitaker’s (1968) review of parasites on Pero- 
myscus provides an excellent summary on collecting and preserving 
parasites, and his (Whitaker, 1982) ‘“‘Ectoparasites of mammals of 
Indiana” provides keys to many of the species dealt with here. 


Mites 


The largest group of ectoparasites of Microtus are the mites and 
ticks of the order Acari. At least 12 families of mites and dozens of 
species are known to parasitize New World Microtus and undoubt- 
edly more will be found. The life cycle of a typical parasitic mite 
includes the following stages: egg, larva (a relatively inactive stage 
that often does not feed), protonymph (usually an active feeding 
stage), deutonymph (an active feeding stage), and adult. Some mites 


458 Timm 


are ovoviviparous so that the egg stage and perhaps the larval stage 
are bypassed. Considerable morphological diversity is found within 
parasitic mites, ranging from the large active laelapids (about 1 mm 
in length) to the minute follicle-inhabiting mites with reduced or 
highly modified legs. There are numerous reports of mites on M:- 
crotus, but surprisingly little work has been done on the effects of 
these mites on their hosts. An excellent list, including synonymies, 
of North American mites found on mammals was published by 
Whitaker and Wilson (1974). Because of the diversity and com- 
plexity of parasitic mites, a brief summary is presented of the fam- 
ilies known to be parasitic on Microtus. 

Cheyletidae.—Cheyletids are a diverse group of mites including 
both parasitic species living in fur of the host and free-living pred- 
atory species. Parasitic forms feed on tissue fluids and usually occur 
in low numbers. They seldom cause much damage to the host al- 
though they can cause dermatitis. The group is in need of revision. 

Demodicidae.—Demodicid mites are minute (0.1 to 0.4 mm in 
length), vermiform, and live within hair follicles, lymph nodes, and 
sebaceous glands. They are thought to be rigidly host specific. Dem- 
odex is often found within the meibomian glands of the eyelids. 
Severe infestations of Demodex cause the eyelids to be sealed shut 
in mice, a disease known as pseudoblepharitis simplex (lid sealing). 

Ereynetidae.—Nasal mites are widely distributed in birds, but 
few species are known from mammals. Within the genus Speleo- 
rodens there is no active nymphal stage; the larva gives rise directly 
to the adult. They reside within the nasal mucosa and apparently 
ingest whole blood. The only transfer between hosts apparently 
occurs between parents and offspring. Three adult females and a 
single larva of S. michigensis were taken by Ford (1962) from a 
single Microtus pennsylvanicus in Michigan. A review of what little 
is known about the biology of these nasal mites is found in OConnor 
(1978). It is likely that nasal mites will be found on other species 
and populations of Microtus. 

Glycyphagidae.—Adult glycyphagids are free-living inhabitants 
within nests of mammals where they probably feed on fungi. ‘The 
deutonymphs are usually found only on the mammalian host, either 
as a parasite in hair follicles or externally phoretic. Spicka and 
OConnor (1980:474) reported 500-1,000 Glycyphagus microti on 
Microtus pinetorum, and stated that the deutonymphs “‘may serve 
two purposes: 1) to disperse the species by transferral from host to 


Parasites 459 


host and nest to nest, and 2) to relieve pressures of overpopulation 
in the nest.” 

Laelapidae.—Laelapids are a large group of both parasitic and 
free-living mites. Most of the large, active mites commonly observed 
on small mammals belong to this family, with both Androlaelaps 
and Laelaps being especially abundant on Microtus. Timm (1972a) 
reported 61 Laelaps kochi from an apparently healthy adult M. 
pennsylvanicus in Nebraska, which is an unusually high parasite 
load. Not all laelapids found on mammals are obligate parasites; 
many of the free-living forms are found as predators of other mites 
in mammal nests. Haemogamasus ambulans, a common parasitic 
mite on Microtus, is known to feed on a variety of substances in 
addition to blood. Some of the nominal species actually represent 
species complexes that have yet to be investigated adequately (i.e. 
Androlaelaps fahrenholzi and Eulaelaps stabularis). Several species 
of laelapids are known to transmit tularemia. 

Listrophoridae.—Fur mites feed in hair follicles, and are often 
abundant on rodents. They cause loss of hair, dermatitis, and skin 
inflammation from scratching. 

Macronyssidae.—Mesostigmatic mites of the genus Ornithonyssus 
are large obligatory blood feeders. In laboratory colonies they cause 
severe exsanguination in sucklings; however, they apparently cause 
little damage to healthy adult animals when found in moderate 
numbers. Ornithonyssus bacoti has been shown to transmit murine 
typhus. O. bursa is commonly known as the tropical fowl mite; the 
single report from Muicrotus may be accidental. 

Myobidae.—Fur mites live in the pelage of their hosts, feeding 
on interstitial fluids, and may be found in high numbers, but they 
apparently cause little damage. Adults, larval stages, and eggs are 
found attached to the base of hairs; the entire life cycle is spent on 
the host. 

Myocoptidae.—Myocoptid fur mites feed on the surface of the 
skin by attaching to the proximal portion of the hair shaft, and may 
be very abundant. Damage to the host includes dermatitis, pruritus, 
and hair loss. 

Psorergatidae.—Psorergatic mange mites are cutaneous and sub- 
cutaneous parasites on a wide variety of mammals. Psorergates can- 
adensis was found on Microtus pennsylvanicus by Kok et al. (1971: 
1243) “within the epidermis of the ear concha, causing hypercer- 
atosis. In the hosts observed they seem to be a low-grade pathogen.” 


460 Timm 


Psorergates simplex is known to cause subcutaneous cysts and ul- 
cerous nodules in its hosts, and is an important parasite in labo- 
ratory colonies of mice. 

Sarcoptidae.—Sarcoptic itch mites or scabies mites live in the skin 
and burrow in the upper layers. Sarcoptids usually do not cause 
pathologies. In a severe infestation in Muicrotus californicus, No- 
toedres muris was found to “invade the ears, eyelids, and nose as 
well as the feet, tail, and anal region” (Lavoipierre, 1964:10); Lid- 
icker (1973) reported that the highest incidence on Brooks Island 
(California) occurred during the winter months. 

Trombiculidae.—Larval trombiculid mites are known as chiggers, 
and are parasites on mammals, birds, reptiles, and amphibians. 
They are parasitic only in the larval stage; all post-larval stages are 
free-living. Chiggers show a broad range of host specificity, with 
many occurring on a large number of hosts, whereas others are 
restricted to very few hosts. They are often associated with partic- 
ular soil or habitat types rather than specific hosts. The larvae inject 
saliva into the host and feed on partly digested fluids; nymphs and 
adults are predaceous on small arthropods or arthropod eggs. 
Trombiculid mites have a complex life cycle that includes four ma- 
jor stages: the egg, larva, nymph, and adult; there are three inter- 
vening inactive stages (see Table 1). Population levels of chiggers 
on rodents vary considerably, but there is seldom much damage to 
the host. The site of attachment is often clustered, especially on the 
ears and genitalia. Attached larvae are generally orange or red in 
color, and usually feed on a host for just a few days. Within the 
north temperate zone most species have one generation per year 
and a distinct seasonal pattern of abundance, with late summer and 
fall peaks being typical. Eutrombicula alfreddugesi, a common chig- 
ger on both man and Microtus, is known to have a single generation 
per year in the northern part of its range, and several generations 
per year in the south. Chiggers are responsible for the transmission 
of several rickettsial diseases, including scrub typhus. Additionally, 
dermatitis may be produced as a result of the salivary secretions of 
the feeding mite. A tremendous body of literature exists on the 
ecology and systematics of chiggers since they are of direct medical 
importance to humans. Keys and synopses to the various groups of 
North American chiggers were provided by Brennan and Goff 
(1977), Brennan and Jones (1959), Gould (1956), Jenkins (1949), 
Kardos (1954), Loomis (1956), and Wharton and Fuller (1952). 


TABLE 1 


Parasites 461 


LIFE CYCLE OF Eutrombicula alfreddugesi (AFTER WOLFENBARGER, 1952) 


Major Intervening 
stages stages 
Egg 

Deutovum 
Larva 

Prenympha 
Nymph 

Preadult 
Adult 


Characteristic features 


Spherical, laid singly 

Quiescent, within broken egg 
shell, unsegmented append- 
ages 


Active, six segmented legs 


Quiescent, within dead larval 
integument 


Active with eight legs, two 
pairs of genital suckers 

Quiescent, within nymphal in- 
tegument 


Active, with eight legs, three 
pairs of genital suckers 


Duration (days) 
15=20 


(minimum 13) 


Up to 24 before 
feeding (over 30) 


1-4 on host (1-48) 


1-8 after leaving 
host (average 2) 


9-10 (about 6) 


12-32 (minimum 
7) 


5-10 (minimum 7) 


Up to 52 (over 20 
months) 


Eggs laid within 
14 (12) 


Ecological studies of chiggers in the midwest were conducted by 
Kardos (1954) and Loomis (1956). 
The records of mites parasitizing Microtus are as follows: 


Microtus abbreviatus 
Laelapidae 


Haemogamasus ambulans (Thorell, 1872) (Rausch and Rausch, 1968 [reported 
as H. alaskensis Ewing]) 

Laelaps clethrionomydis Lange, 1955 (Rausch and Rausch, 1968) 

Laelaps kochi Oudemans, 1836 (Rausch and Rausch, 1968) 


Microtus brewert 


Laelapidae 


Androlaelaps fahrenholzi (Berlese, 1911) (Strandtmann, 1949) 
Laelaps kochi Oudemans, 1836 (Winchell, 1977) 


Microtus californicus 
Laelapidae 


Androlaelaps fahrenholzi (Berlese, 1911) (Holdenried et al., 1951; Jameson, 
1947; Strandtmann, 1949) 


462 


Timm 


Haemogamasus ambulans (Thorell, 1872) (Furman, 1959a, 19596; Holdenried 
et al., 1951; Keegan, 1951) 

Haemogamasus liponyssoides Ewing, 1925 (Furman, 1959a; Holdenried et al., 
1951; Radovsky, 1960a, 19606) 

Haemogamasus reidi Ewing, 1925 (Keegan, 1951; Redington, 1971) 

Laelaps kochi Oudemans, 1836 (Evans and Till, 1966; Ewing, 1933; Grant, 
1947; Holdenried et al., 1951; Jameson, 1947) 

Sarcoptidae 
Notoedres muris Mégnin, 1877 (Lavoipierre, 1964; Lidicker, 1973) 
Trombiculidae 

Acomatacarus hirsutus (Ewing, 1931) (Brennan and Jones, 1954) 

Euschoengastia ambocalis Wrenn and Loomis, 1973 (original description) 

Euschoengastia criceticola Brennan, 1948 (Brennan and Jones, 1954; Gould, 
1956) 

Euschoengastia oregonensis (Ewing, 1929) (Gould, 1956) 

Euschoengastia peromysci (Ewing, 1929) (Gould, 1956) 

Euschoengastia pomerantzi Brennan and Jones, 1954 (original description) 

Euschoengastia radford: Brennan and Jones, 1954 (original description) 

Neotrombicula californica (Ewing, 1942) (Brennan and Jones, 1954; Ewing, 
1942; Gould, 1956; Holdenried et al., 1951) 

Neotrombicula cavicola (Ewing, 1931) (Gould, 1956) 

Neotrombicula dinehartae (Brennan and Wharton, 1950) (Brennan and Jones, 
1954) 

Neotrombicula jewetti (Brennan and Wharton, 1950) (Brennan and Jones, 
1954) 

Odontacarus hirsutus (Ewing, 1931) (Brennan and Jones, 1954) 

Walchia americana (Ewing, 1942) (Brennan and Jones, 1954) 


Microtus chrotorrhinus 


Glycyphagidae 
Glycyphagus hypudaei (Koch, 1841) (Whitaker and French, 1982) 
Glycyphagus sp. (hypudaei group) (Kirkland and Jannett, 1982) 
Orycteroxenus canadensis Fain, Kok, Lukoschus, and Clulow, 1971 (Whitaker 
and French, 1982) 
Orycteroxenus soricis (Oudemans, 1915) (Whitaker and French, 1982) 
Laelapidae 
Androlaelaps fahrenholzi (Berlese, 1911) (Timm, pers. observ.; Whitaker and 
French, 1982) 
Echinonyssus isabellinus (Oudemans, 1913) (Whitaker and French, 1982) 
Eulaelaps stabularis (Koch, 1836) (Whitaker and French, 1982) 
Haemogamasus ambulans (Thorell, 1872) (Martin, 1972; Timm et al., 1977; 
Whitaker and French, 1982) 
Haemogamasus liponyssoides Ewing, 1925 (Whitaker and French, 1982) 
Laelaps alaskensis Grant, 1947 (Kirkland and Jannett, 1982; Martin, 1972; 
Timm, 1974, 1975; Tipton, 1960; Whitaker and French, 1982) 
Laelaps kochi Oudemans, 1836 (Kirkland and Jannett, 1982; Komarek and 
Komarek, 1938; Linzey and Linzey, 1973; Timm, 1974, 1975; Timm et 
al., 1977; Tipton, 1960; Whitaker and French, 1982) 
Listrophoridae 
Listrophorus mexicanus Fain and Hyland, 1972 (Whitaker and French, 1982) 
Listrophorus squamiferus Fain and Hyland, 1972 (Kirkland and Jannett, 1982) 


Parasites 463 


Myobiidae 
Radfordia hylandi Fain and Lukoschus, 1977 (Whitaker and French, 1982) 
Radfordia sp. (Kirkland and Jannett, 1982; Whitaker and French, 1982) 
Myocoptidae 

Myocoptes canadensis Radford, 1955 (Kirkland and Jannett, 1982) 

Myocoptes japonensis Radford, 1955 (Whitaker and French, 1982) 

Myocoptes squamosus Fain, Munting, and Lukoschus, 1969 (Whitaker and 
French, 1982) 

Trichoecius tenax (Michael, 1889) (Whitaker and French, 1982) 

Trichoecius sp. (Kirkland and Jannett, 1982; Whitaker and French, 1982) 

Trombiculidae 

Euschoengastia blarinae (Ewing, 1931) (Whitaker and French, 1982) 

Euschoengastia peromysci (Ewing, 1929) (Farrell, 1956; Komarek and Ko- 
marek, 1938) 

Euschoengastia setosa (Ewing, 1937) (Whitaker and French, 1982) 

Mtyatrombicula esoensis (Sasa and Ogata, 1953) (Whitaker and French, 1982) 

Neotromibucla harperi (Ewing, 1928) (Kirkland and Jannett, 1982; Martin, 
1972?; Timm et al., 1977; Whitaker and French, 1982) 

Neotrombicula microti (Ewing, 1928) (Buech et al., 1977; Timm et al., 1977) 

Microtus longicaudus 
Laelapidae 

Androlaelaps fahrenholzi (Berlese, 1911) (Allred and Beck, 1966; Augustson, 
1941b; Hansen, 1964; Whitaker and Maser, 1984) 

Echinonyssus incomptis (Eads and Hightower, 1952) (Allred and Beck, 1966) 

Echinonyssus isabellinus (OQudemans, 1913) (Allred and Beck, 1966; Hansen, 
1964; Herrin, 1970; Jameson and Brennan, 1957; Kinsella and Pattie, 
1967) 

Eubrachylaelaps debilis Jameson, 1950 (Allred and Beck, 1966; Furman, 1955) 

Eulaelaps stabularis (Koch, 1836) (Whitaker and Maser, 1984) 

Haemogamasus ambulans (Thorell, 1872) (Allred and Beck, 1966; Hansen, 
1964; Jameson and Brennan, 1957) 

Haemogamasus liponyssoides Ewing, 1925 (Allred and Beck, 1966; Augustson, 
1941b; Hansen, 1964; Jameson and Brennan, 1957) 

Haemogamasus longitarsus (Banks, 1910) (Allred and Beck, 1966) 

Haemogamasus occidentalis (Keegan, 1951) (Allred and Beck, 1966; Whitaker 
and Maser, 1984) 

Haemogamasus reid: Ewing, 1925 (Allred and Beck, 1966; Hansen, 1964; 
Jameson and Brennan, 1957; Redington, 1971; Whitaker and Maser, 
1984) 

Laelaps alaskensis Grant, 1947 (Jameson and Brennan, 1957) 

Laelaps incilis Allred and Beck, 1966 (original description) 

Laelaps kochi Oudemans, 1836 (Allred and Beck, 1966; Augustson, 1941); 
Hansen, 1964; Jameson and Brennan, 1957; Whitaker and Maser, 1984) 

Trombiculidae 

Chatia ochotona (Radford, 1942) (Gould, 1956; Traub and Nadchatram, 1966) 

Euschoengastia oregonensis (Ewing, 1929) (Allred and Beck, 1966) 

Euschoengastia peromysci (Ewing, 1929) (Jameson and Brennan, 1957) 


464 


Timm 


Euschoengastia radfordi Brennan and Jones, 1954 (Jameson and Brennan, 
1957) 

Leptotrombidium potosina Hoffmann, 1950 (Brennan and Beck, 1955) 

Neotrombicula browni (Brennan and Wharton, 1950) (Brennan and Wharton, 
1950 [original description]; Kardos, 1954; Radford, 1954; Wharton and 
Fuller, 1952) 

Neotrombicula californica (Ewing, 1942) (Brennan and Beck, 1955) 

Neotrombicula harper: (Ewing, 1928) (Allred and Beck, 1966; Brennan and 
Beck, 1955; Brennan and Wharton, 1950; Kardos, 1954; Wharton and 
Fuller, 1952) 

Neotrombicula jewetti (Brennan and Wharton, 1950) (Brennan and Wharton, 
1950 [original description]; Jameson and Brennan, 1957; Radford, 1954; 
Wharton and Fuller, 1952) 

Neotrombicula microti (Ewing, 1928) (Brennan and Beck, 1955; Kardos, 1954) 


Microtus mexicanus 


Laelapidae 


Androlaelaps fahrenholzi (Berlese, 1911) (Allred and Beck, 1966; Bassols, 1981) 
Echinonyssus breviseta Strandtmann and Morlan, 1953 (Bassols, 1981) 
Echinonyssus utahensis Allred and Beck, 1966 (Hoffman et al., 1972) 
Haemogamasus ambulans (Thorell, 1872) (Bassols, 1981) 

Haemogamasus reid: Ewing, 1925 (Redington, 1971) 

Laelaps kochi Oudemans, 1836 (Bassols, 1981) 


Listrophoridae 


Listrophorus mexicanus Fain, 1970 (Fain and Hyland, 1974) 


Myobiidae 


Radfordia hylandi Fain and Lukoschus, 1977 (original description) 


Trombiculidae 


Neotrombicula microti (Ewing, 1928) (Brennan and Wharton, 1950; Wharton 
and Fuller, 1952) 


Muicrotus montanus 


Glycyphagidae 


Glycyphagus hypudaei (Koch, 1841) (Whitaker and Maser, 1984) 


Laelapidae 


Androlaelaps fahrenholzi (Berlese, 1911) (Allred, 1970; Allred and Beck, 1966; 
Augustson, 19416; Hansen, 1964; Kartman et al., 19585; Strandtmann, 
1949; Whitaker and Maser, 1984) 

Brevisterna utahensis (Ewing, 1933) (Kartman et al., 1958) 

Echinonyssus isabellinus (Oudemans, 1913) (Allred, 1970; Allred and Beck, 
1966; Hansen, 1964; Herrin, 1970; Kinsella and Pattie, 1967; Whitaker 
and Maser, 1984) 

Echinonyssus occidentalis (Ewing, 1923) (Augustson, 19416) 

Eubrachylaelaps croweri Jameson, 1947 (Hansen, 1964) 

Eubrachylaelaps debilis Jameson, 1950 (Whitaker and Maser, 1984) 

Eulaelaps stabularis (Koch, 1836) (Hansen, 1964; Whitaker and Maser, 1984) 

Haemogamasus ambulans (Thorell, 1872) (Allred and Beck, 1966; Hansen, 
1964; Keegan, 1951) 

Haemogamasus liponyssoides Ewing, 1925 (Augustson, 19416; Hansen, 1964) 

Haemogamasus occidentalis (Keegan, 1951) (Whitaker and Maser, 1984) 


Parasites 465 


Haemogamasus reidi Ewing, 1925 (Augustson, 19416; Whitaker and Maser, 
1984) 

Ischyropoda armatus Keegan, 1951 (Allred, 1970) 

Laelaps alaskensis Grant, 1947 (Hansen, 1964; Kartman et al., 19586; Kinsella 
and Pattie, 1967; Whitaker and Maser, 1984) 

Laelaps incilis Allred and Beck, 1966 (original description) 

Laelaps kochi Oudemans, 1836 (Allred and Beck, 1966; Augustson, 19416; 
Hansen, 1964; Kartman et al., 19585; Kinsella and Pattie, 1967; Tipton, 
1960; Whitaker and Maser, 1984) 

Listrophoridae 
Listrophorus mexicanus Fain, 1970 (Whitaker and Maser, 1984) 
Psorergatidae 

Psorergates townsendi Giesen, Lukoschus, Whitaker, and Gettinger, 1983 

(original description and type-host) 
Trombiculidae 

Comatacarus americanus Ewing, 1942 (Easton, 1975) 

Neotrombicula californica (Ewing, 1942) (Gould, 1956) 

Neotrombicula cavicola (Ewing, 1931) (Easton, 1975) 

Neotrombicula harperi (Ewing, 1928) (Allred and Beck, 1966; Easton, 1975; 
Kardos, 1954) 

Neotrombicula microti (Ewing, 1928) (Kardos, 1954; Kinsella and Pattie, 1967) 

Microtus ochrogaster 
Glycyphagidae 

Glycyphagus hypudaei (Koch, 1841) (Basolo and Funk, 1974; Buckner and 
Gleason, 1974; Fain and Whitaker, 1973; McDaniel, 1979; Mumford 
and Whitaker, 1982; Rupes and Whitaker, 1968; Turner, 1974; Whit- 
aker and Wilson, 1968) 

Orycteroxenus soricis (Oudemans, 1915) (Mumford and Whitaker, 1982) 

Laelapidae 

Androlaelaps fahrenholz (Berlese, 1911) (Amin, 1973, 19766; Basolo and Funk, 
1974; Batson, 1965; Buckner and Gleason, 1974; Jameson, 1947; Mum- 
ford and Whitaker, 1982; Rapp, 1962; Strandtmann, 1949; Timm, 19726; 
Turner, 1974; Whitaker and Wilson, 1968) 

Echinonyssus utahensis Allred and Beck, 1966 (Timm, 19726) 

Eulaelaps stabularis (Koch, 1836) (Batson, 1965; Jameson, 1947; Mumford 
and Whitaker, 1982; Whitaker and Wilson, 1968) 

Haemogamasus ambulans (Thorell, 1872) (Turner, 1974) 

Haemogamasus liponyssoides Ewing, 1925 (Keegan, 1951; Mumford and Whit- 
aker, 1982; Whitaker and Wilson, 1968; Wilson, 1957 [reported as H. 
barber: Ewing]) 

Laelaps alaskensis Grant, 1947 (Mumford and Whitaker, 1982; Whitaker and 
Wilson, 1968) 

Laelaps kochi Oudemans, 1836 (Basolo and Funk, 1974; Buckner and Gleason, 
1974; Jameson, 1947; Mumford and Whitaker, 1982; Rapp, 1962; Timm, 
19726; Tipton, 1960; Turner, 1974; Whitaker and Wilson, 1968; Wilson, 
1957) 

Listrophoridae 

Listrophorus mexicanus Fain, 1970 (Basolo and Funk, 1974; Buckner and 
Gleason, 1974 [reported as L. leuckarti]; Mumford and Whitaker, 1982) 

Listrophorus sp. (Jameson, 1947) 


466 


Timm 


Macronyssidae 

Ornithonyssus bacoti (Hirst, 1913) (Buckner and Gleason, 1974; Mumford and 

Whitaker, 1982; Turner, 1974) 
Myobiidae 

Radfordia ensifera (Poppe, 1896) (Manischewitz, 1966) 

Radfordia hylandi Fain and Lukoschus, 1977 (Mumford and Whitaker, 1982) 

Radfordia lemnina (Koch, 1841) (Basolo and Funk, 1974; Buckner and Glea- 
son, 1974; Whitaker and Wilson, 1968) 

Myocoptidae 

Myocoptes japonensis Radford, 1955 (Basolo and Funk, 1974) 

Myocoptes musculinus (Koch, 1844) (Basolo and Funk, 1974; McDaniel, 1979; 
Mumford and Whitaker, 1982; Turner, 1974; Whitaker and Wilson, 
1968) 

Myocoptes sp. (Basolo and Funk, 1974; Buckner and Gleason, 1974; Jameson, 
1947) 

Trichoecius tenax (Michael, 1889) (Mumford and Whitaker, 1982) 

Trombiculidae 

Euschoengastia diversa Farrell, 1956 (Farrell, 1956 [original description]; 
Loomis, 1956) 

Euschoengastia peromysci (Ewing, 1929) (Basolo and Funk, 1974; Jameson, 
1947 [reported as Ascoschongastia breviceps]; Loomis, 1956) 

Euschoengastia setosa (Ewing, 1937) (Lampe et al., 1974; Mumford and Whit- 
aker, 1982; Turner, 1974; Whitaker and Loomis, 1979) 

Euschoengastia trigenuala Farrell, 1956 (Loomis, 1956) 

Eutrombicula alfreddugesi (Oudemans, 1910) (Loomis, 1956; Mumford and 
Whitaker, 1982; Turner, 1974; Whitaker and Loomis, 1979; Wolfen- 
barger, 1952) 

Eutrombicula lipovskyana Wolfenbarger, 1952 (Loomis, 1956; Wolfenbarger, 
1952 [original description]) 

Eutrombicula lipovskyi (Brennan and Wharton, 1950) (Kardos, 1954; Loomis, 
1956) 

Neotrombicula autumnalis (Shaw, 1790) (Kardos, 1954; Loomis, 1956) 

Neotrombicula sylvilagi (Brennan and Wharton, 1950) (Kardos, 1954; Loomis, 
1956) 

Neotrombicula whartoni (Ewing, 1929) (Basolo and Funk, 1974; Kardos, 1954; 
Loomis, 1956; Mumford and Whitaker, 1982; Whitaker and Loomis, 
1979) 

Pseudoschongastia hungerford: Lipovsky, 1951 (Loomis, 1956) 


Microtus oeconomus 


Laelapidae 
Androlaelaps fahrenholzi (Berlese, 1911) (Strandtmann and Wharton, 1958) 
Echinonyssus tsabellinus (Oudemans, 1913) (Strandtmann and Wharton, 1958) 
Eulaelaps stabularis (Koch, 1836) (Strandtmann and Wharton, 1958) 
Haemogamasus reidi Ewing, 1925 (Keegan, 1951) 
Laelaps kochi Oudemans, 1836 (Strandtmann and Wharton, 1958) 
Myobiidae 
Radfordia lemnina (Koch, 1841) (Fain and Lukoschus, 1977) 


Parasites 467 


Microtus oregont 
Glycyphagidae 
Dermacarus ondatrae Rupes and Whitaker, 1968 (Whitaker and Maser, 1984) 
Glycyphagus hypudaei (Koch, 1841) (Whitaker and Maser, 1984) 
Laelapidae 
Androlaelaps fahrenholzi (Berlese, 1911) (Strandtmann, 1949; Whitaker and 
Maser, 1984) 
Eulaelaps stabularis (Koch, 1836) (Whitaker and Maser, 1984) 
Haemogamasus ambulans (Thorell, 1872) (Keegan, 1951) 
Haemogamasus occidentalis (Keegan, 1951) (Whitaker and Maser, 1984) 
Laelaps kochi Oudemans, 1836 (Whitaker and Maser, 1984) 
Listrophoridae 
Listrophorus mexicanus Fain, 1970 (Whitaker and Maser, 1984) 
Myobiidae 
Radfordia hylandi Fain and Lukoschus, 1977 (Whitaker and Maser, 1984) 
Trombiculidae 
Euschoengastia oregonensis (Ewing, 1929) (Easton, 1975) 
Neotrombicula cavicola (Ewing, 1931) (Brennan and Wharton, 1950; Easton, 
1975; Wharton and Fuller, 1952) 
Neotrombicula harperi (Ewing, 1928) (Easton, 1975) 
Microtus pennsylvanicus 
Demodicidae 
Demodex sp. (Nutting and Desch, 1979) 
Dermanyssidae 
Dermanyssus sp. (Drummond, 1957) 
Ereynetidae 
Speleorodens michigensis Ford, 1962 (original description and type-host) 
Glycyphagidae 
Dermacarus newyorkensis Fain, 1969 (Fain, 1969a [original description and 
type-host], 19695; Rupes and Whitaker, 1968) 
Glycyphagus hypudaei (Koch, 1841) (Fain, 19696; Mumford and Whitaker, 
1982; Rupes and Whitaker, 1968; Whitaker and French, 1982; Whitaker 
and Wilson, 1968) 
Glycyphagus microti Spicka and OConnor, 1980 (original description) 
Orycteroxenus soricis (Oudemans, 1915) (Fain, 19696) 
Laelapidae 
Androlaelaps fahrenholzi (Berlese, 1911) (Allred and Beck, 1966; Amin, 1973, 
1976b; Baker, 1946; Drummond, 1957; Florschutz and Darsie, 1960; 
Genoways and Jones, 1972; Harper, 1961; Jameson, 1947; Judd, 1950, 
1953; Lawrence et al., 1965; MacCreary, 1945a; Mellott and Connell, 
1965; Mumford and Whitaker, 1982; Strandtmann, 1949; Timm, 1972a, 
19726, 1975; Turner, 1974; Whitaker and French, 1982; Whitaker and 
Wilson, 1968; Wilson, 1967) 
Androlaelaps sp. (Wright, 1979) 
Echinonyssus carnifex Koch, 1839 (Lawrence et al., 1965) 
Echinonyssus isabellinus (Oudemans, 1913) (Allred and Beck, 1966; Harper, 
1961; Herrin, 1970; Timm, 1972a, 19726, 1975; Whitaker and French, 
1982) 


468 


Timm 


Echinonyssus sp. (Amin, 19766; Genoways and Jones, 1972; Scholten et al., 
1962; Wright, 1979) 

Eulaelaps stabularis (Koch, 1836) (Drummond, 1957; Genoways and Jones, 
1972; Lawrence et al., 1965; Timm, 1975; Wilson, 1967; Wright, 1979) 

Haemogamasus ambulans (Thorell, 1872) (Drummond, 1957; Harper, 1956, 
1961; Keegan, 1951; Lawrence et al., 1965; Timm, 1975; Whitaker and 
French, 1982) 

Haemogamasus liponyssoides Ewing, 1925 (Drummond, 1957; Keegan, 1951; 
Lawrence et al., 1965; MacCreary, 1945a; Mellott and Connell, 1965; 
Mumford and Whitaker, 1982; Timm, 1975) 

Haemogamasus longitarsus (Banks, 1910) (Ewing, 1925 [described as H. mi- 
croti]; Keegan, 1951) 

Laelaps alaskensis Grant, 1947 (Amin, 1973, 19766; Drummond, 1957; Flor- 
schutz and Darsie, 1960; Harper, 1956, 1961; Lawrence et al., 1965; 
Mellott and Connell, 1965; Mumford and Whitaker, 1982; Timm, 1975; 
Whitaker and French, 1982; Whitaker and Wilson, 1968; Wilson, 1967) 

Laelaps kochi Oudemans, 1836 (Allred and Beck, 1966; Amin, 1973, 19768; 
Baker, 1946; Drummond, 1957; Florschutz and Darsie, 1960; Genoways 
and Jones, 1972; Harper, 1956, 1961; Jameson, 1947; Judd, 1950, 1953, 
1954; Lampe et al., 1974; Lawrence et al., 1965; MacCreary, 1945a; 
Mellott and Connell, 1965; Mumford and Whitaker, 1982; Scholten et 
al., 1962; Shoemaker and Joy, 1967; Timm, 1972a, 19726, 1975; Tipton, 
1960; Turner, 1974; Whitaker and French, 1982; Whitaker and Wilson, 
1968) 

Laelaps multispinosa (Banks, 1910) (Lawrence et al., 1965) 

Laelaps muris (Ljungh, 1799) (Judd, 1950, 1953, 1954) 


Listrophoridae 


Listrophorus mexicanus Fain, 1970 (McDaniel et al., 1967; Mumford and 
Whitaker, 1982; Whitaker and French, 1982; Whitaker and Wilson, 
1968 [reported as L. leuckarti]) 

Listrophorus pitymys Fain and Hyland, 1972 (Fain and Hyland, 1974) 

Listrophorus squamiferus Fain and Hyland, 1972 (Fain and Hyland, 1974; 
McDaniel et al., 1967 [reported as L. leuckarti]) 

Listrophorus sp. (Drummond, 1957) 


Macronyssidae 


Ornithonyssus bacoti (Hirst, 1913) (Drummond, 1957; Mumford and Whita- 
ker, 1982) 
Ornithonyssus bursa (Berlese, 1888) (Drummond, 1957) 


Myobiidae 


Protomyobia brevisetosa Jameson, 1948 (Whitaker and French, 1982) 

Protomyobia claparedei (Poppe, 1896) (Manischewitz, 1966) 

Radfordia ensifera (Poppe, 1896) (Manischewitz, 1966) 

Radfordia hylandi Fain and Lukoschus, 1977 (Fain and Lukoschus, 1977 [orig- 
inal description]; Mumford and Whitaker, 1982; Whitaker and French, 
1982) 

Radfordia lemnina (Koch, 1841) (Drummond, 1957; Ewing, 1938; Manis- 
chewitz, 1966) 


Parasites 469 


Myocoptidae 

Myocoptes japonensis Radford, 1955 (Fain and Hyland, 1970; Fain et al., 
1970; Mumford and Whitaker, 1982; Radford, 1955 [originally described 
as M. jamesoni]; Whitaker and French, 1982) 

Myocoptes musculinus (Koch, 1844) (Harper, 1956; McDaniel, 1979) 

Myocoptes squamosus Fain, Munting, and Lukoschus, 1969 (Fain and Hyland, 
1970; Whitaker and French, 1982) 

Myocoptes sp. (Drummond, 1957) 

Trichoecius tenax (Michael, 1889) (Fain and Hyland, 1970; Fain et al., 1970; 
Whitaker and French, 1982) 

Psorergatidae 

Psorergates canadensis Kok, Lukoschus, and Clulow, 1971 (original description 
and type-host) 

Psorergates simplex Tyrrell, 1883 (Lee and Horvath, 1969) 

Trombiculidae 

Euschoengastia diversa Farrell, 1956 (original description) 

Euschoengastia peromysci (Ewing, 1929) (Farrell, 1956; MacCreary, 1945a 
[reported as Neoschongastia breviceps]; Manischewitz, 1966; Mumford and 
Whitaker, 1982; Whitaker and Loomis, 1979) 

Euschoengastia setosa (Ewing, 1937) (Turner, 1974) 

Euschoengastia sp. (Drummond, 1957; Wilson, 1967) 

Eutrombicula alfreddugesi (Oudemans, 1910) (Ewing, 1944; Jenkins, 1949; 
MacCreary, 1945a [reported as E. tropical; Mumford and Whitaker, 1982; 
Wharton and Fuller, 1952; Whitaker and Loomis, 1979) 

Eutrombicula splendens (Ewing, 1913) (Wharton and Fuller, 1952) 

Eutrombicula sp. (Wright, 1979) 

Mtyatrombicula esoensis (Sasa and Ogata, 1953) (Whitaker and French, 1982) 

Neotrombicula autumnalis (Shaw, 1790) (Kardos, 1954; Loomis, 1956) 

Neotrombicula bisignata (Ewing, 1929) (Brennan and Wharton, 1950; Ewing, 
1929a [original description and type-host]; Radford, 1954; Wharton and 
Fuller, 1952) 

Neotrombicula goodpasteri (Brennan and Wharton, 1950) (Brennan and Whar- 
ton, 1950 [original description]; Radford, 1954; Wharton and Fuller, 
1952) 

Neotrombicula harper: (Ewing, 1928) (Brennan and Wharton, 1950; Harper, 
1929; Lawrence et al., 1965; Manville, 1949; Timm, pers. observ.; Whar- 
ton and Fuller, 1952; Whitaker and French, 1982) 

Neotrombicula lipousky: (Brennan and Wharton, 1950) (Mumford and Whit- 
aker, 1982; Whitaker and Loomis, 1979) 

Neotrombicula microti (Ewing, 1928) (Baker, 1946; Brennan and Wharton, 
1950; Ewing, 1928; Lawrence et al., 1965; Timm, pers. observ.; Wharton 
and Fuller, 1952) 

Neotrombicula richmond: (Brennan and Wharton, 1950) (Brennan and Whar- 
ton, 1950 [original description]; Radford, 1954; Wharton and Fuller, 
1952) 

Neotrombicula subsignata (Brennan and Wharton, 1950) (Brennan and Whar- 
ton, 1950 [original description and type-host]; Genoways and Jones, 1972; 
Kardos, 1954; Radford, 1954; Wharton and Fuller, 1952) 


470 Timm 


Neotrombicula whartoni (Ewing, 1929) (Brennan and Wharton, 1950; Drum- 
mond, 1957; Farrell, 1956; Kardos, 1954; MacCreary, 1945a; Manis- 
chewitz, 1966; Mumford and Whitaker, 1982; Wharton and Fuller, 1952; 
Whitaker and Loomis, 1979) 

Neotrombicula sp. (Manville, 1949) 

Microtus pinetorum 
Cheyletidae 
Eucheyletia bishoppi Baker, 1949 (original description) 
Glycyphagidae 

Dermacarus sp. (Benton, 1955a) 

Glycyphagus hypudaei (Koch, 1841) (Fain, 19696; Fain and Whitaker, 1973; 
Mumford and Whitaker, 1982) 

Glycyphagus microti Spicka and OConnor, 1980 (original description and type- 
host) 

Orycteroxenus soricis (Oudemans, 1915) (Fain and Whitaker, 1973) 

Laelapidae 

Androlaelaps fahrenholzi (Berlese, 1911) (Benton, 1955a; Drummond, 1957; 
Ellis, 1955; Hays and Guyton, 1958; Jameson, 1947; Judd, 1950; 
MacCreary, 1945a; Mellott and Connell, 1965; Morlan, 1952; Mumford 
and Whitaker, 1982; Strandtmann, 1949; Whitaker and Wilson, 1968) 

Eulaelaps stabularis (Koch, 1836) (Jameson, 1947; Mumford and Whitaker, 
1982; Whitaker and Wilson, 1968) 

Haemogamasus ambulans (Thorell, 1872) (Keegan, 1951; Whitaker and Wil- 
son, 1968) 

Haemogamasus liponyssoides Ewing, 1925 (Drummond, 1957; Keegan, 1951; 
Morlan, 1952) 

Haemogamasus longitarsus (Banks, 1910) (Drummond, 1957; Keegan, 1951; 
MacCreary, 1945a; Mellott and Connell, 1965; Mumford and Whitaker, 
1982; Whitaker and Wilson, 1968; Wilson, 1957) 

Laelaps alaskensis Grant, 1947 (Benton, 1955a; Mumford and Whitaker, 1982; 
Whitaker and Wilson, 1968) 

Laelaps kochi Oudemans, 1836 (Drummond, 1957; Hamilton, 1938; Hays 
and Guyton, 1958; Mumford and Whitaker, 1982; Whitaker and Wilson, 
1968) 

Listrophoridae 

Listrophorus pitymys Fain and Hyland, 1972 (Fain and Hyland, 1972 [original 
description], 1974) 

Listrophorus sp. (Drummond, 1957) 

Macronyssidae 
Ornithonyssus bacoti (Hirst, 1913) (Mumford and Whitaker, 1982) 
Myobiidae 

Radfordia ensifera (Poppe, 1896) (Manischewitz, 1966) 

Radfordia hylandi Fain and Lukoschus, 1977 (Fain and Lukoschus, 1977 [orig- 
inal description]; Mumford and Whitaker, 1982) 

Radfordia lemnina (Koch, 1841) (Drummond, 1957; Manischewitz, 1966) 

Myocoptidae 

Myocoptes canadensis Radford, 1955 (Mumford and Whitaker, 1982) 

Myocoptes musculinus (Koch, 1844) (Mumford and Whitaker, 1982) 

Myocoptes sp. (Benton, 1955a; Drummond, 1957) 


Parasites 471 


Psorergatidae 
Psorergates pinetorum Giesen, Lukoschus, Whitaker, and Gettinger, 1983 
(original description and type-host) 
Trombiculidae 
Euschoengastia carolinensis Farrell, 1956 (original description) 
Euschoengastia diversa Farrell, 1956 (Loomis, 1956) 
Euschoengastia ohwensis Farrell, 1956 (Farrell, 1956 [original description]; 
Mumford and Whitaker, 1982; Whitaker and Loomis, 1979) 
Euschoengastia peromysci (Ewing, 1929) (Farrell, 1956; Manischewitz, 1966; 
Mumford and Whitaker, 1982; Whitaker and Loomis, 1979) 
Eutrombicula alfreddugesi (Oudemans, 1910) (Wolfenbarger, 1952) 
Leptotrombidium myotis (Ewing, 1929) (Loomis, 1956; Manischewitz, 1966) 
Neotrombicula goodpasteri (Brennan and Wharton, 1950) (Brennan and Whar- 
ton, 1950 [original description]; Radford, 1954; Wharton and Fuller, 
1952) 
Neotrombicula lipovsky: (Brennan and Wharton, 1950) (Kardos, 1954; Loomis, 
1956; Mumford and Whitaker, 1982; Whitaker and Loomis, 1979) 
Neotrombicula microti (Ewing, 1928) (Kardos, 1954) 
Neotrombicula whartoni (Ewing, 1929) (MacCreary, 1945a; Manischewitz, 
1966) 
Microtus richardson 
Glycyphagidae 
Glycyphagus hypudaei (Koch, 1841) (Whitaker and Maser, 1984) 
Laelapidae 
Androlaelaps fahrenholzi (Berlese, 1911) (Whitaker and Maser, 1984) 
Echinonyssus isabellinus (OQudemans, 1913) (Kinsella and Pattie, 1967; Lud- 
wig, 1984; Whitaker and Maser, 1984) 
Haemogamasus ambulans (Thorell, 1872) (Kinsella and Pattie, 1967) 
Haemogamasus liponyssoides Ewing, 1925 (Kinsella and Pattie, 1967) 
Haemogamasus occidentalis (Keegan, 1951) (Whitaker and Maser, 1984) 
Haemogamasus reidi Ewing, 1925 (Whitaker and Maser, 1984) 
Laelaps alaskensis Grant, 1947 (Kinsella and Pattie, 1967; Ludwig, 1984; 
Whitaker and Maser, 1984) 
Laelaps kochi Oudemans, 1836 (Kinsella and Pattie, 1967) 
Listrophoridae 
Listrophorus mexicanus Fain, 1970 (Whitaker and Maser, 1984) 
Myocoptidae 
Myocoptes japonensis Radford, 1955 (Whitaker and Maser, 1984) 
Trombiculidae 
Neotrombicula microti (Ewing, 1928) (Brennan and Wharton, 1950; Ewing, 
1928 [original description and type-host]; Radford, 1954; Wharton and 
Fuller, 1952) 
Microtus townsend 
Glycyphagidae 
Glycyphagus hypudaei (Koch, 1841) (Whitaker and Maser, 1984) 
Laelapidae 
Androlaelaps fahrenholzi (Berlese, 1911) (Whitaker and Maser, 1984) 
Echinonyssus tsabellinus (Oudemans, 1913) (Whitaker and Maser, 1984) 
Echinonyssus obsoletus Jameson, 1950 (Whitaker and Maser, 1984) 


472 Timm 


Eubrachylaelaps debilis Jameson, 1950 (Whitaker and Maser, 1984) 
Eulaelaps stabularis (Koch, 1836) (Whitaker and Maser, 1984) 
Haemogamasus occidentalis (Keegan, 1951) (Keegan, 1951 [original description 
and type-host]; Whitaker and Maser, 1984) 
Haemogamasus reidi Ewing, 1925 (Whitaker and Maser, 1984) 
Laelaps kochi Oudemans, 1836 (Whitaker and Maser, 1984) 
Listrophoridae 
Listrophorus mexicanus Fain, 1970 (Whitaker and Maser, 1984) 
Psorergatidae 
Psorergates townsend: Giesen, Lukoschus, Whitaker, and Gettinger, 1983 
(original description and type-host) 
Trombiculidae 
Neotrombicula jewetti (Brennan and Wharton, 1950) (Brennan and Wharton, 
1950 [original description]; Radford, 1954; Wharton and Fuller, 1952) 
Microtus sp. (Mexico) 
Laelapidae 
Eulaelaps stabularis (Koch, 1836) (de Barrera, 1979) 
Echinonyssus breviseta Strandtmann and Morlan, 1953 (de Barrera, 1979) 
Echinonyssus utahensis Allred and Beck, 1966 (de Barrera, 1979) 
Haemogamasus ambulans (Thorell, 1872) (de Barrera, 1979) 
Laelaps kochi Oudemans, 1836 (de Barrera, 1979) 


Ticks 


All ticks known from Microtus belong to the family Ixodidae 
(hard ticks). The life cycle of a typical ixodid tick includes four 
stages: egg, nymph, larva, and adult. For the most part, ticks are 
not strongly host specific, although nymphs and larvae generally 
feed on small mammals, birds, or reptiles, and adults feed on larger 
mammals. Larvae, nymphs, and adults all require blood meals for 
metamorphosis. The entire life cycle may require 1-3 years. ‘The 
life cycle and natural history of Dermacentor variabilis, the Ameri- 
can dog tick, is perhaps the best known of all ticks, and is sum- 
marized as follows. Eggs hatch in 30-35 days. Newly hatched lar- 
vae, called seed ticks, feed on small mammals for 5-12 days, drop 
from the host, and metamorphose into the nymphal stage. Nymphs 
feed 6-10 days and drop off to metamorphose into adults. Copu- 
lation takes place on the host. Males may copulate with several 
different females. Females die soon after egglaying. Nymphs and 
adults can withstand long periods (hundreds of days) without feed- 
ing. Unfed adults and larvae are the main overwintering stage. In 


Parasites 473 


Novia Scotia, larvae are active from April through September, 
nymphs are active from May through August, and adult activity 
extends from April to mid-August. Also, Garvie et al. (1978:28) 
found that “The voles Microtus pennsylvanicus and Clethrionomys 
gapperi sustained almost 80% of all larvae [Dermacentor variabilis] 
and over 85% of all nymphs collected from mammal hosts.” 

Ticks are responsible for the transmission of numerous diseases 
including babesiosis (Babesia), Colorado tick-fever virus, relapsing 
fever, several Rickettsia diseases (for example, Q fever and Rocky 
Mountain spotted fever), tick paralysis, and tularemia. Addition- 
ally, exsanguination by a heavy load of ticks may be significant to 
a mouse. A recent review of tickborne disease is found in Hoogstraal 
(1981). 

Keys for the identification of North American ticks were provided 
by Clifford et al. (1961), Cooley and Kohls (1945), Gregson (1956), 
Keirans and Clifford (1978), and Sonenshine (1979). An excellent 
and comprehensive bibliography to the ticks was provided by Hoog- 
straal (see Bibliography of ticks and tickborne diseases from Homer 
(about 800 B.C.) to 31 December 1981, NAMRU-3, Cairo; seven 
volumes have been published as of 1983). 

Amblyomma maculatum, the Gulf Coast tick, ranges from south- 
eastern U.S. through Central and South America. The larvae and 
nymphs are found on small mammals and ground-dwelling birds. 
The adults generally are found on larger mammals, especially live- 
stock. 

Dermacentor andersoni is known as the Rocky Mountain spotted 
fever tick because it is one of the primary vectors of the Rickettsia 
causing the disease; it is also a vector of tick paralysis, Colorado 
tick fever, tularemia, and American Q fever. It is one of the most 
abundant ticks found in the western half of the U.S. and Canada. 
Small mammals, especially chipmunks, are the primary hosts; lar- 
vae, nymphs, and adults are most common on hosts in spring and 
summer. 

Dermacentor occidentalis, the Pacific Coast tick, is common in 
western California and Oregon. Small mammals are typical hosts 
for larvae and nymphs, whereas adults are common on deer, cattle, 
and horses. It is present on hosts during all seasons of the year, but 
adults generally are most abundant during the rainy season. 

Dermacentor variabilis, the American dog tick, is the most abun- 
dant tick in the eastern two-thirds of North America, east of the 


474 Timm 


Rocky Mountains. Larvae and nymphs have been recovered from 
most species of small mammals, but are especially abundant on 
cricetines; adults generally feed on dogs, foxes, and other medium- 
sized carnivores. It is the eastern U.S. counterpart of D. andersont. 
In southern U.S. it breeds throughout the year; in northern states 
a distinct seasonality is found. It is the main vector of Rocky Moun- 
tain spotted fever in the eastern U.S. Ecological studies on D. var- 
tabilis were provided by Campbell (1979), Garvie et al. (1978), and 
Sonenshine (1979). See references in those papers. 

Haemaphysalis leporispalustris, the rabbit tick, is found through- 
out North, Central, and South America. Lagomorphs (both Lepus 
and Sylvilagus) are preferred hosts; however, larvae and nymphs 
are often found on other small mammals and ground-feeding birds. 
This species is an important vector of Rocky Mountain spotted fever 
and tularemia. 

Ixodes angustus is found throughout North America, and is one 
of the most common ticks on small mammals. In the Pacific North- 
west, Bishopp and Trembley (1945) reported finding adult ticks on 
small mammals throughout the year, but immatures not later than 
the end of October. In northeastern Minnesota, Timm (1975) found 
larvae and nymphs of J. angustus on all species of shrews, moles, 
and cricetines. 

Ixodes auritulus is an uncommon species that has been collected 
primarily from birds along the coast of northwestern North Amer- 
ica. 

Ixodes californicus is a poorly known and rarely collected species 
from the far western U.S. It has been taken from both birds and 
small mammals. 

Ixodes cookei is a widely distributed species, although it appears 
to be most abundant in the east. It has been found on a variety of 
small mammals and birds. Sonenshine (1979:30) reported that “‘lar- 
vae and nymphs are most abundant on hosts during winter months,” 
and that medium-sized carnivores, especially skunks, raccoons, and 
foxes, appeared to be preferred hosts. 


Ixodes dammini is a widely distributed tick in the eastern U.S. 
that was described only recently (see Spielman et al., 1979). Adults 
appear most frequently on white-tailed deer and larvae and nymphs 
on a wide variety of small mammals. This species was confused for 


Parasites 475 


decades with J. scapularis and many of the older records of scapularis 
actually refer to dammini. I. dammini is the major vector of human 
babesia, a parasitic protozoan, in the northeastern U.S. Main et al. 
(1982) reported that both larvae and nymphs were abundant on 
small mammals in Connecticut from April through October, with 
peaks of abundance in early and late summer. 

Ixodes dentatus is found in the northcentral and eastern U.S., 
with cottontail rabbits of the genus Syluilagus being the most com- 
mon hosts. Larvae and nymphs are occasionally found on birds and 
rodents. Larvae appear to be most abundant on hosts in fall whereas 
adults are most abundant in spring. This species is a known vector 
of Rocky Mountain spotted fever. 

Ixodes eastoni is a recently recognized species from the Black Hills 
area of South Dakota and adjacent Wyoming. It has been reported 
on several species of small mammals, including the genera Cleth- 
rionomys, Eutamias, Microtus, Neotoma, Peromyscus, and Zapus. 
Adults of J. eastoni were confused previously with J. ochotonae and 
immature stages with /. angustus (Keirans and Clifford, 1983). 

Ixodes kingi is called the rotund tick, and is found in the western 
U.S. and northern Mexico on a variety of mammals. Carnivores 
seem to be preferred hosts. 

Ixodes muris is called the mouse tick, and is restricted to north- 
eastern U.S.; it is generally found on cricetine rodents, although it 
is found occasionally on shrews. Smith (1944:231) reported that 
Microtus is the most important host and that “adults of the mouse 
tick do not mate on the host, but on the ground before the females 
have attached.” 

Ixodes ochotonae is aptly named the pika tick; most of the records 
are from Ochotona. It is found in the far western U.S. and British 
Columbia. 

Ixodes pacificus is restricted to the Pacific coastal regions of Cal- 
ifornia, Oregon, and Washington. Adults feed primarily on mam- 
mals and are most active from fall to spring; larvae and nymphs 
feed primarily on lizards. Adults are considered a serious pest on 
dogs, livestock, and man. 

Ixodes sculptus is called the black-legged tick and is common in 
the midwest and western North America. Ground squirrels are the 
primary hosts, although it has been collected from a wide variety 
of small mammals and may be a pest on cattle. 


476 Timm 


Ixodes spinipalpis is an uncommon tick found in northwestern 
U.S. and adjacent Canada. Lagomorphs seem to be preferred hosts, 
although it has been collected on other mammals. 

The records of ticks parasitizing Microtus are as follows: 


Mucrotus brewer 
Dermacentor variabilis (Say, 1821) (Spielman and Piesman, 1979) 
Ixodes dammini Spielman, Clifford, Piesman, and Cerwin, 1979 (original de- 
scription) 
Ixodes muris Bishopp and Smith (Spielman et al., 1979; Winchell, 1977) 
Microtus californicus 
Dermacentor occidentalis Marx, 1892 (Furman and Loomis, 1984; Holdenried 
et al., 1951; Mohr et al., 1964) 
Dermacentor variabilis (Say, 1821) (Coultrip et al., 1973; Furman and Loomis, 
1984) 
Ixodes angustus Neumann, 1899 (Cooley and Kohls, 1945; Furman and Loomis, 
1984; Holdenried et al., 1951; Mohr et al., 1964) 
Ixodes pacificus Cooley and Kohls, 1943 (Arthur and Snow, 1968; Furman and 
Loomis, 1984; Mohr et al., 1964) 
Ixodes spinipalpis Hadwen and Nuttall, 1916 (Furman and Loomis, 1984; Mohr 
et al., 1964) 
Ixodes sp. (Holdenried et al., 1951) 
Microtus canicaudus 
Ixodes angustus Neumann, 1899 (Easton and Goulding, 1974) 
Muicrotus chrotorrhinus 
Ixodes angustus Neumann, 1899 (Kirkland and Jannett, 1982; Timm, 1974, 
1975; Timm et al., 1977; Whitaker and French, 1982) 
Ixodes sp. (Komarek and Komarek, 1938) 
Microtus longicaudus 
Dermacentor andersoni Stiles, 1908 (Augustson, 19415; Bacon, 1953; Beck, 1955; 
Chamberlin, 1937; Clark et al., 1970; Hansen, 1964; Johnson, 1966; 
Stout, 1979) 
Dermacentor variabilis (Say, 1821) (Stout, 1979; Stout et al., 1971) 
Dermacentor sp. (Beck, 1955) 
Ixodes angustus Neumann, 1899 (Chamberlin, 1937; Cooley and Kohls, 1945; 
Easton and Goulding, 1974; Furman and Loomis, 1984; Stout, 1979) 
Ixodes californicus Banks, 1904 (Chamberlin, 1937) 
Ixodes eastoni Keirans and Clifford, 1983 (original description) 
Ixodes sculptus Neumann, 1904 (Allred et al., 1960) 
Ixodes spinipalpis Hadwen and Nuttall, 1916 (Stout, 1979) 
Ixodes sp. (Allred et al., 1960) 
Microtus miurus 
Ixodes angustus Neumann, 1899 (Rausch, 1964) 
Muicrotus montanus 
Dermacentor andersoni Stiles, 1908 (Allred, 19685; Bacon, 1953; Bacon et al., 
1959; Bishopp and Trembley, 1945; Hansen, 1964; Harkema, 1936; 
Hooker et al., 1912 [reported as D. venustus]) 
Dermacentor sp. (Beck, 1955) 
Ixodes angustus Neumann, 1899 (Allred et al., 1960; Furman and Loomis, 1984; 
Seidel and Booth, 1960) 


Parasites 477 


Ixodes kingi Bishopp, 1911 (Allred, 19685) 

Ixodes muris Bishopp and Smith, 1937 (Johnson, 1966) 

Ixodes sculptus Neumann, 1904 (Allred et al., 1960) 

Ixodes sp. (Allred, 19686) 

Microtus ochrogaster 

Dermacentor andersoni Stiles, 1908 (Cooley, 1938; Parker and Wells, 1917 [re- 
ported as D. venustus]) 

Dermacentor variabilis (Say, 1821) (Basolo and Funk, 1974; Buckner and Glea- 
son, 1974; Cooney and Burgdorfer, 1974; Jameson, 1947; Mumford and 
Whitaker, 1982) 

Ixodes sculptus Neumann, 1904 (Jameson, 1947) 

Ixodes spinipalpis Hadwen and Nuttall, 1916 (Turner, 1974) 

Microtus oeconomus 

Ixodes angustus Neumann, 1899 (Fay and Rausch, 1969; Schiller and Rausch, 

1956) 
Microtus pennsylvanicus 

Dermacentor andersoni Stiles, 1908 (Cooley, 1938; Gregson, 1956; Harkema, 
1936; Hooker et al., 1912 [reported as venustus]; Hunter and Bishopp, 
1911 [reported as D. venustus]; Turner, 1974) 

Dermacentor variabilis (Say, 1821) (Anastos, 1947; Anderson and Magnarelli, 
1980; Bequaert, 1945; Bishopp and Smith, 1938; Campbell, 1979; Carey 
et al., 1980; Clifford et al., 1961; Coher and Shaw, 1951; Cooley, 1938; 
Dodds et al., 1969; Drummond, 1957; Eddy and Joyce, 1944; Garvie et 
al., 1978; Gould and Miesse, 1954; Hertig and Smiley, 1937; Knipping 
et al., 1950a; Larrouse et al., 1928; Lawrence et al., 1965; MacCreary, 
19455; Magnarelli et al., 1983; McEnroe, 1983; Mellott and Connell, 
1965; Mumford and Whitaker, 1982; Parker et al., 1933; Smith et al., 
1946; Sonenshine, 1972, 1979; Sonenshine and Atwood, 1967; Sonenshine 
and Levy, 1972; Sonenshine and Stout, 1968; Sonenshine et al., 1965, 
1966; Spielman and Piesman, 1979; Timm, 19726; Wilkinson, 1979; 
Wilson, 1943; Wilson and Baker, 1972; Wright, 1979) 

Haemaphysalis leporispalustris (Packard, 1869) (Lawrence et al., 1965; Martell 
et al., 1969; Wright, 1979) 

Ixodes angustus Neumann, 1899 (Burroughs et al., 1945; Gregson, 1956; Martell 
et al., 1969; Timm, 1975; Wright, 1979) 

Ixodes cooke: Packard, 1869 (Clifford et al., 1961) 

Ixodes dammini Spielman, Clifford, Piesman, and Corwin, 1979 (Anderson and 
Magnarelli, 1980; Carey et al., 1980; Main et al., 1982; Spielman and 
Piesman, 1979; Spielman et al., 1979 [original description]; White and 
White, 1981) 

Ixodes dentatus Marx, 1899 (Bequaert, 1945; MacCreary, 19455; Sonenshine et 
al., 1965, 1966) 

Ixodes eastoni Keirans and Clifford, 1983 (original description) 

Ixodes muris Bishopp and Smith, 1937 (Anastos, 1947; Bequaert, 1945; Bishopp 
and Smith, 1937 [original description and type-host]; Bishopp and Trem- 
bley, 1945; Clifford et al., 1961; Cooley and Kohls, 1945; Easton, 19830; 
Jones and Thomas, 1980; Martell et al., 1969; Smith, 1944; Spielman et 
al., 1979; Timm, 1975; Wright, 1979) 


478 Timm 


Ixodes scapularis Say, 1821 (Bequaert, 1945; Cooley and Kohls, 1945) 
Ixodes spinipalpis Hadwen and Nuttall, 1916 (Turner, 1974) 
Microtus pinetorum 
Amblyomma maculatum Koch, 1844 (Bishopp and Hixson, 1936) 
Dermacentor variabilis (Say, 1821) (Bequaert, 1945; Bishopp and Smith, 1938; 
Bishopp and Trembley, 1945; Carey et al., 1980; Clifford et al., 1961; 
Cooley, 1938; MacCreary, 1940, 19455; Mellott and Connell, 1965; 
Mumford and Whitaker, 1982; Smith et al., 1946; Sonenshine, 1972, 
1979; Sonenshine and Levy, 1972; Sonenshine et al., 1965, 1966; Tugwell 
and Lancaster, 1962; Wilson and Baker, 1972) 
Ixodes dammini Spielman, Clifford, Piesman, and Corwin, 1979 (Carey et al. 
1980; Main et al., 1982) 
Microtus townsendii 
Ixodes angustus Neumann, 1899 (Bishopp and Trembley, 1945; Cooley and 
Kohls, 1945; Easton and Goulding, 1974) 
Microtus sp. 
Ixodes auritulus Neumann, 1904 (Gregson, 1956) 
Ixodes ochotonae Gregson, 1941 (Gregson, 1956) 


> 


Lice 


Lice (Anoplura: Hoplopleuridae) of three genera (Hoplopleura, 
Neohaematopinus, and Polyplax) are known from North American 
Microtus. American workers commonly recognize two orders of lice, 
the Anoplura or sucking lice, and the Mallophaga or chewing lice; 
Europeans generally recognize a single order, Phthiraptera. The 
Mallophaga are found primarily on birds, although a few genera 
parasitize mammals; the Anoplura are exclusively parasites of 
mammals. Anoplurans feed exclusively on blood and have complex, 
highly specialized mouthparts modified to pierce the skin of the 
host. 

The entire life cycle of lice is spent on the host, and transmission 
occurs only when hosts are in direct contact, for the lice cannot live 
independently of the host. Each individual egg, called a nit, is glued 
to a single hair. There are three nymphal instars and the duration 
of the life cycle is about a month. The number of lice on an indi- 
vidual host varies greatly; Cook and Beer (1958) reported a range 
of 1-748 Hoplopleura acanthopus per host on Microtus pennsyl- 
vanicus, with a mean infestation rate for male voles of 25.1 and for 
females 10.1 lice per infested host. They (1958:651) found a “‘pos- 
itive correlation between age and rate of infestation in male meadow 
voles with the older animals having higher rates than the younger”; 


Parasites 479 


no corresponding correlation was found in female voles. Also (p. 
649), “over the whole year ... 72.6% of the male meadow voles 
harbored lice as opposed to only 60.9% of the females.’’ Rates of 
infestation varied with the year and season, with peak rates found 
in December and April. Female lice are more numerous than males 
on M. pennsylvanicus, which Cook and Beer attributed to a shorter 
life span of males. The main factor controlling louse populations 
may be the efficiency of the host at mutual and self grooming; 
molting of hair on the host may be significant in egg loss. Cook 
and Beer (1958:419) also stated that ‘“.... in general higher infes- 
tations were found on host populations which were stable or de- 
clining, and the lower rates were on hosts which were increasing.” 
On M. arvalis in the U.S.S.R., Vysotskaia (1950) reported that H. 
acanthopus occurred all over the host’s body in spring and summer, 
but in fall was concentrated anteriorly, especially in the region of 
the neck and chest up to the ears. In winter, lice were concentrated 
in the region of the neck. These changes in position on the host’s 
body were attributed to changes in nest temperature. In cold pe- 
riods, the lice congregated on the warmest parts of the body. Cook 
and Beer (1955, 1958) provided detailed studies of population dy- 
namics of Hoplopleura acanthopus on Microtus pennsylvanicus in 
Minnesota. 

It seems probable that reproduction in these lice may be cued to 
the reproductive cycle of their hosts, as has been demonstrated in 
the rabbit flea, Cediopsylla simplex (Rothschild and Ford, 1964, 
1966, 1969). The reproductive steroids of the host presumably trig- 
ger the reproductive steroids of the parasite. This remains to be 
tested in lice, but may prove to be a fruitful area of research. An- 
oplurans may prove to be important in the transmission of tulare- 
mia (Francisella tularensis). 

Hoplopleura is a worldwide genus of some 117 species that par- 
asitizes rodents. H. acanthopus is a true parasite of microtine ro- 
dents; it is found on Clethrionomys, Lemmus, Microtus, and Syn- 
aptomys. ‘The species as now defined is Holarctic; however, in reality 
the microtine Hoplopleura is most likely a complex of several closely 
related species. H. hesperomydis is a true parasite of Peromyscus, 
the few records from Microtus being either natural transfers or 
contamination. 

Neohaematopinus is a worldwide genus of about 41 species that 


480 Timm 


parasitizes rodents and insectivores. N. sciurinus is a true parasite 
of tree squirrels of the genus Sciurus; the single report from M. 
longicaudus is probably a contaminate. 

Polyplax is a worldwide genus of about 76 species, most of which 
parasitize murid rodents. P. alaskensis is a Holarctic species on 
microtine rodents, especially Clethrionomys and Microtus. P. serrata 
and P. spinulosa are worldwide species whose normal hosts are 
murid rodents, Mus and Rattus, respectively. 

The records of lice parasitizing Microtus are as follows: 


Microtus brewert 
Polyplax alaskensis Ewing, 1927 (Scanlon and Johnson, 1957; Winchell, 1977) 
Microtus californicus 
Hoplopleura acanthopus (Burmeister, 1838) (Ferris, 1921; Holdenried et al., 
1951; Jameson, 1947; Jellison et al., 1958; Kellogg and Ferris, 1915; 
Mohr and Stumpf, 1964; Ryckman and Lee, 1958) 
Polyplax alaskensis Ewing, 1927 (Ferris, 1916, 1923 [reported as P. abscisa and 
P. spinulosa]; Holdenried et al., 1951 [reported as P. abscisa]; Mohr and 
Stumpf, 1964 [reported as P. abscisa]; Ryckman and Lee, 1958 [reported 
as P. abscisa]; Scanlon and Johnson, 1957) 
Microtus longicaudus 
Hoplopleura acanthopus (Burmeister, 1838) (Augustson, 19415; Emerson et al., 
1984; Hansen, 1964; Ignoffo, 1956; Morlan and Hoff, 1957; Spencer, 
1966) 
Hoplopleura hesperomydis (Osborn, 1891) (Morlan and Hoff, 1957) 
Neohaematopinus sciurinus (Mjoberg, 1910) (Augustson, 19416) 
Polyplax alaskensis Ewing, 1927 (Ignoffo, 1956 [reported as P. abscisa]; Kellogg 
and Ferris, 1915 [reported as P. spinulosa]) 
Microtus mexicanus 
Hoplopleura acanthopus (Burmeister, 1838) (Emerson, 1971) 
Polyplax alaskensis Ewing, 1927 (Emerson, 1971) 
Muicrotus miurus 
Polyplax alaskensis Ewing, 1927 (Quay, 1951) 
Microtus montanus 
Hoplopleura acanthopus (Burmeister, 1838) (Allred, 1970; Augustson, 19416; 
Emerson et al., 1984; Hansen, 1964; Jellison et al., 1958, 1959; Kartman 
et al., 19585; Seidel and Booth, 1960; Spencer, 1966; Stanford, 1934) 
Polyplax alaskensis Ewing, 1927 (Allred, 1970 [reported as P. spinulosa]; Hansen, 
1964 [reported as P. spinulosa]; Scanlon and Johnson, 1957) 
Polyplax serrata (Burmeister, 1839) (Augustson, 19416) 
Polyplax spinulosa (Burmeister, 1839) (Hansen, 1964) 
Microtus ochrogaster 
Hoplopleura acanthopus (Burmeister, 1838) (Basolo and Funk, 1974; Batson, 
1965; Buckner and Gleason, 1974; Ferris, 1951; Jameson, 1947; Mum- 
ford and Whitaker, 1982; Turner, 1974) 
Hoplopleura hesperomydis (Osborn, 1891) (Buckner and Gleason, 1974) 
Microtus oeconomus 
Polyplax alaskensis Ewing, 1927 (Quay, 1949, 1951; Scanlon and Johnson, 1957) 


Parasites 481 


Microtus oregont 
Hoplopleura acanthopus (Burmeister, 1838) (Emerson et al., 1984; Spencer, 1966) 
Polyplax spinulosa (Burmeister, 1839) (Spencer, 1966) 
Microtus pennsylvanicus 
Hoplopleura acanthopus (Burmeister, 1838) (Amin, 19766; Cook and Beer, 1955, 
1958, 1959; Florschutz and Darsie, 1960; Genoways and Jones, 1972; 
Harper, 1956, 1961; Ignoffo, 1959; Jameson, 1947; Judd, 1953, 1954; 
Lampe et al., 1974; Lawrence et al., 1965; MacCreary, 1945a; Mathew- 
son and Hyland, 1962; Mumford and Whitaker, 1982; Race, 1956; Schol- 
ten et al., 1962; Spencer, 1966; Timm, 19726, 1975; Wilson, 1967) 
Hoplopleura erraticus (Osborn, 1896) (original description; probably a misiden- 
tification) 
Hoplopleura hesperomydis (Osborn, 1891) (Cook and Beer, 1958; Race, 1956) 
Neohaematopinus sciurinus (Mjoberg, 1910) (Gyorkos and Hilton, 1982a, 19825) 
Polyplax alaskensis Ewing, 1927 (Baker, 1946; Ferris, 1942 [reported as P. ab- 
scisa]; Florschutz and Darsie, 1960; Ignoffo, 1959 [reported as P. abscisa]; 
Mathewson and Hyland, 1962; Race, 1956 [reported as P. abscisa]; Scan- 
lon and Johnson, 1957; Whitaker and French, 1982; Wilson, 1943 [re- 
ported as P. spinulosa}) 
Polyplax serrata (Burmeister, 1839) (Race, 1956) 
Microtus pinetorum 
Hoplopleura acanthopus (Burmeister, 1838) (Benton, 1955a; Ferris, 1921, 1951; 
Hamilton, 1938; Mumford and Whitaker, 1982; Race, 1956) 
Hoplopleura hesperomydis (Osborn, 1891) (Race, 1956) 
Polyplax alaskensis Ewing, 1927 (Morlan, 1952 [reported as P. spinulosa]}; Race, 
1956 [reported as P. abscisa}) 
Microtus townsend 
Hoplopleura acanthopus (Burmeister, 1838) (Spencer, 1966) 


Beetles 


Leptinidae.—Beetles of the genus Leptinus represent one of the 
few groups of parasitic Coleoptera. Leptinus is a Holarctic genus, 
with three species in the Nearctic and six species in the Palearctic. 
They are small beetles, usually only 2-3 mm in length, and have 
greatly reduced or no eyes, and hindwings reduced or absent. All 
members of the family Leptinidae are parasitic on mammals. In 
North America two genera are found in addition to Leptinus: Lep- 
tinillus with one species on beaver (Castor canadensis) and one on 
mountain beaver (Aplodontia rufa), and Platypsyllus with one species 
on beaver. 

Adults of Leptinus are found either on the mammalian host or 
in the host’s nest. Small mammals, especially cricetines, shrews, 
and moles are typical hosts. Both adults and larvae probably feed 
on “dead organic matter, such as skin debris, hair fragments, skin- 


482 Timm 


gland secretions, and excreta” rather than live tissue (Peck, 1982: 
1518). Eggs, larvae, and pupae are found in the nest. Adults are 
more abundant on mammals during winter months. There may be 
up to three generations per year; adult and larval stages overlap. 
Little is known about the biology of the North American species 
and the effect of beetles on their hosts. The absence of Leptinus on 
ground squirrels, pocket gophers, pocket mice, and woodrats is of 
interest considering its wide distribution on shrews, moles, voles, 
and deer mice. 

A recent revision, including an excellent key, of the Leptinus of 
North America was provided by Peck (1982), who concluded that 
there are three species in North America: Leptinus americanus, re- 
stricted to the central United States; Leptinus occidentamericanus, 
found in western North America from California to Alaska; and 
Leptinus orientamericanus, widespread east of the Mississippi River. 

The records of Leptinus parasitizing Microtus are as follows: 

Microtus oregoni 

Leptinus occidentamericanus Peck, 1982 (Maser and Hooven, 1971 [reported as 
L. testaceus; Peck, 1982 [original description]; Spencer, 1956 [reported as 
L. testaceus]) 
Microtus pennsylvanicus 
Leptinus americanus LeConte, 1866 (Peck, 1982) 
Leptinus orientamericanus Peck, 1982 (original description) 
Microtus pinetorum 
Leptinus orientamericanus Peck, 1982 (original description) 
Microtus townsendi 
Leptinus occidentamericanus Peck, 1982 (original description) 


Cryptophagidae.—A single species of cryptophagid or silken fun- 
gus beetle, Cryptophagus bolivari, has been collected on Muicrotus 
mexicanus and Peromyscus melanotis in México (Barrera and Mar- 
tinez, 1968). Although little is known of the diet of these beetles, 
the genus Cryptophagus has been found associated with mammals 
on several occasions; it is likely that they feed on dead skin and 
scrapings from the hair which might include grains of pollen and 
smaller soft-bodied arthropods. Nothing is known of the effects of 
these beetles on their hosts. 


Flies 


The dipteran family Cuterebridae (bot flies or warbles) is found 
only in the New World; larvae in all species are subcutaneous, 
obligate parasites of mammals. The genus Cuterebra includes ap- 


Parasites 483 


proximately 36 species, and is distributed widely throughout North 
America. The primary hosts are sciuromorph and myomorph ro- 
dents and lagomorphs. Adults are short-lived and apparently do not 
feed; they are typical winged flies that resemble bumblebees. 

Cuterebrids are not common on Muicrotus, even in areas where 
they heavily infest Peromyscus and sciurids. The highest incidence 
of Cuterebra infestation reported in Microtus was on M. chrotor- 
rhinus in the Great Smokey Mountains, with 65% of the animals 
captured carrying one or more bots (Komarek and Komarek, 1938); 
more typical infestation rates range from 6 to 45% (Maurer and 
Skaley, 1968). The following discussion of a generalized life cycle 
for Cuterebra is based on other hosts because little has been done 
to date on Microtus parasitized by bots. 

Although rarely observed in the field, adult bots emerge, mate, 
and oviposit during mid-summer. Females probably oviposit along 
runways and burrows of the hosts, with no direct contact between 
the gravid female bot fly and the host. Egg-hatching is triggered by 
a sudden rise in environmental temperature as would occur near a 
potential host. After hatching, the first-instar larvae assume a 
“questing position,” standing on their caudal! ends. ‘They then at- 
tach to any object coming in contact with them. It is believed that 
the larvae crawl over the body of the host and are only able to en- 
ter through a natural body orifice. For 7-10 days after entering 
through the nose or mouth, the larvae migrate dorsally and medially 
between the skin and muscle layers until the breathing hole is cut, 
marking the site of warble formation. Larvae are typically located 
in the posterior third of the abdomen, although they are occasionally 
found on the neck, back, flank, and between the forelegs. Com- 
monly, one to three larvae are found per host, with similar infes- 
tation rates for male and female hosts. Peak infestations occur from 
mid-August through mid-September. Larval development is com- 
pleted in 3% weeks, when the third-instar larvae emerge through 
the breathing hole, burrow into the soil and pupate, overwintering 
in the puparium. 

The effect of bot flies on their hosts has been a matter of debate 
for some time. The popular notion in the literature is that bot flies 
live in the testis and castrate their hosts. In recent reviews of the 
subject, Timm and Lee (1981, 1982) demonstrated that bot flies 
are found exclusively in the subcutaneous region between the skin 
and underlying muscle. They do not consume muscle or reproduc- 
tive tissue, but rather feed on the tissue debris and exudate pro- 


484 Timm 


duced. The site of larval development is usually in the posterior 
third of the host’s body, but is unrelated to the gonads. Upon emer- 
gence of the mature third-instar larvae, the wound heals rapidly, 
with few apparent aftereffects. Bot-fly larvae can have a physiolog- 
ical effect upon their hosts. In Peromyscus, significantly lower eryth- 
rocyte counts, hematocrit percentages, albumin-globulin ratios, and 
hemoglobin concentrations have been found, whereas the leucocyte 
number, spleen size, and thymus size were significantly larger 
(Clough, 1965; see Timm and Cook, 1979, for a review). Timm 
and Cook (1979) found no significant reduction in reproduction in 
adult Peromyscus leucopus parasitized by Cuterebra fontinella. In 
adult females there was no significant decrease in the number of 
embryos, corpora lutea, or placental scars; in adult male mice the 
presence of one or two larvae had no effect on the size of the 
reproductive organs. 

An excellent and recent review of cuterebrid biology was provided 
by Catts (1982). 

The records of bot flies parasitizing Microtus are as follows: 


Microtus chrotorrhinus 
Cuterebra sp. (Komarek and Komarek, 1938; Martin, 1972) 
Microtus oregont 
Cuterebra sp. (Hunter et al., 1972) 
Microtus pennsylvanicus 
Cuterebra fontinella Clark, 1827 (Getz, 1970 [listed as C. angustifrons]; Timm, 
pers. observ.) 
Cuterebra grisea Coquillett, 1904 (Buckner, 1958) 
Cuterebra sp. (Amin, 1973; Clough, 1965; Hensley, 1976; Iverson and Turner, 
1968; Jacobsen, 1966; Lawrence et al., 1965; Manville, 1961; Maurer 
and Skaley, 1968; Seton, 1909; White and White, 1981) 
Microtus pinetorum 
Cuterebra sp. (Hamilton, 1930) 
Microtus townsendi 
Cuterebra grisea Coquillett, 1904 (Beacham and Krebs, 1980; Boonstra, 1977; 
Boonstra and Krebs, 1978; Boonstra et al., 1980) 
Wohlfahrtia vigil (Walker, 1849) (Boonstra, 1977; Boonstra and Krebs, 1978) 
Microtus sp. 
Cuterebra grisea Coquillett, 1904 (Buckner, 1958) 


Fleas 


Fleas (Siphonaptera) are obligate parasites that are found on 
most species of mammals and on a few species of birds. Adults are 


Parasites 485 


active and may be found either on the host or in the nest or burrow. 
Eggs are generally laid in the nest. ‘The larvae are active and mag- 
got-like, but are not parasitic. They feed on a variety of organic 
materials, often including the feces of the adults. After two larval 
molts, the mature larva pupates in a cocoon spun from secretions 
from the salivary glands. Adult fleas may live for several hundred 
days and move between various hosts; they feed only on blood. An 
excellent series on the systematics and distribution of Siphonaptera 
worldwide was provided by Lewis (1975 and references therein). 

Amphipsylla is a genus of approximately 27 species centered 
mainly in the Siberian subregion of the Palaearctic; most parasitize 
rodents, especially microtines. Two species are found on microtines 
in the northern Nearctic. A. marikouski is a Holarctic species with 
New World populations recognized as a separate subspecies (A. m. 
ewingi); it is marginally separable from the Siberian populations 
and is known only from Alaska off Microtus oeconomus. A. sibirica 
also is a Holarctic species with several recognized subspecies, two 
of which occur in North America. A. s. pollionis is known from 
Alaska and northern Canada and is a parasite of microtines, es- 
pecially M. pennsylvanicus. 

Atyphloceras is a Holarctic genus containing six species; of these, 
four are found in the Nearctic. Microtine and cricetine rodents are 
the primary hosts. A. bishopi is found in the eastern U.S. and ad- 
jacent Canada, with Microtus and Clethrionomys being the primary 
hosts. A. echis is found in the western U.S. and is a true parasite 
of Neotoma; the few records from Microtus californicus can be con- 
sidered accidental. A. multidentatus is a common winter nest flea 
found in the western U.S. and British Columbia; the genera M:- 
crotus and Peromyscus are probably the primary hosts, although this 
species has been taken from Clethrionomys, Lagurus, Mus, Neotoma, 
Reithrodontomys, Rattus, and Tamuasciurus. A. tancitari is known 
only from a few higher elevation localities in southcentral Mexico; 
it has been recorded from Microtus mexicanus, Peromyscus, and 
Reithrodontomys. 

Catallagia is a genus of 15 species occurring mainly in the Nearc- 
tic, but a few representatives occur in the eastern Palaearctic. Mi- 
crotine rodents appear to be the normal hosts, but accidental hosts 
often include carnivores and insectivores. C. borealis is a winter flea 
found in the northeastern U.S. and adjacent Canada; Clethrionomys 
gapperi is the normal host, although records from M. chrotorrhinus 


486 Timm 


and M. pennsylvanicus are not uncommon. C. charlottensis is a com- 
mon nest flea of Microtus and Peromyscus found in the late winter 
and spring in the Pacific Northwest. C. dacenkoi is a Holarctic 
species; the Nearctic populations represent a subspecies (C. d. ful- 
leri) distinct from Siberian populations. It has been found only in 
Alaska, Northwest Territories, and the Yukon, on both Clethrion- 
omys and Microtus. C. decipiens is a widespread and common flea 
in western North America and is known from a variety of small 
mammals, including Clethrionomys, Microtus, Neotoma, Peromyscus, 
Reithrodontomys, and sciurids. C. jellisoni is known only from Al- 
berta and British Columbia from Clethrionomys gappert, Microtus 
pennsylvanicus, and Neotoma cinerea. C. mathesoni is known only 
from the west coast of the U.S.; most records are from Peromyscus. 
C. sculleni occurs in coastal British Columbia, California, Oregon, 
and Washington on a variety of small mammals, including Cleth- 
rionomys, Microtus, Neotoma, and Peromyscus. 

Ctenophthalmus is a genus of approximately 116 species found 
in all zoogeographic regions, although it is most abundant in the 
Palaearctic and Ethiopian regions; it includes about 10% of all 
known fleas. Most are parasites of rodents, although a few are 
found exclusively on Insectivora. C. caballeroi was described from 
the nest of Microtus mexicanus mexicanus and is only known from 
a few specimens collected in southcentral Mexico. C. haagi is known 
only from a few specimens collected in south-central Mexico; most 
records are from M. mexicanus. C. pseudagyrtes is an abundant flea 
that occurs throughout the year in eastern North America; it has 
been collected on numerous species of small mammals including 
most rodents, insectivores, and smaller carnivores. 

Delotelis is a northern and western Nearctic genus of two species; 
their apparent rarity is due to their occurrence in nests. D. holland: 
is known only from northern California, Oregon, and British Co- 
lumbia; Microtus and Peromyscus are the most common hosts. D. 
telegoni appears to be widespread in northwestern North America; 
Clethrionomys and Microtus appear to be the most common hosts. 

Epitedia is an exclusively Nearctic genus of seven species which 
primarily parasitize cricetids and insectivores. E. scapani is found 
in the Pacific coastal lowlands of northern California, Oregon, 
Washington, and adjacent British Columbia; Microtus and Pero- 
myscus appear to be the most common hosts. E. stanford: is a winter 
flea found in the Rocky Mountain region of the U.S.; various species 


Parasites 487 


of Peromyscus appear to be the primary hosts, although it has been 
collected on a variety of small mammals. E. stewart: is known only 
from northern California and Oregon; it has been collected on M:- 
crotus californicus, Peromyscus maniculatus, and Sorex trowbridget. E. 
wenmanni, a common, transcontinental species throughout North 
America to northern Mexico, has two recognizable subspecies that 
intergrade over a broad area of the U.S. (Benton, 19556). Pero- 
myscus is the most common host, although it is likely that this 
species can complete its life cycle on a wide variety of small mam- 
mals, including Microtus. 

Hystrichopsylla is a Holarctic genus of 15 species; six species are 
found in the Nearctic; most appear to be weakly host specific. H. 
dippiei is a widely distributed and common flea in the midwestern 
and western Nearctic with four distinctive subspecies; it usually is 
not abundant on the host itself, suggesting that it is a nest flea. 
Adults are most commonly collected during fall, winter, and spring. 
H. occidentalis is restricted to far-western North America, from 
Alaska south to Arizona and California. Campos and Stark (1979) 
recognized three distinctive subspecies; Microtus and Peromyscus are 
the most common hosts. H. orophila is known only from southcentral 
Mexico; the type host is Microtus mexicanus; it also has been col- 
lected on Peromyscus maniculatus. H. tahavuana is restricted to east- 
ern North America; the true hosts are Condylura cristata, Parasca- 
lops breweri, and Blarina brevicauda. 

Jellisonia is a poorly known genus of nine species distributed from 
southwestern U.S. through Mexico and Central America. Most 
records are from Peromyscus. J. hayesi is known only from a few 
specimens from central Mexico, although Traub (1950) recognized 
two distinct subspecies. /. h. breviloba was described from M. mex- 
icanus. 

Malaraeus is a Holarctic genus of roughly 12 species; most are 
parasites of cricetine and microtine rodents. M. bitterrootensis is a 
rare flea found in northwestern U.S. and adjacent Canada; Ocho- 
tona appears to be the primary host. M. dobbs: is known by several 
specimens, all from only one locality in Oregon off Microtus oregoni; 
repeated attempts to obtain additional specimens of this species have 
failed. M. euphorbi is a poorly known flea found in northwestern 
U.S. and southwestern Canada; most records are from early spring 
off Peromyscus. M. penicilliger is a widespread and abundant Hol- 
arctic species with several described subspecies, two of which occur 


488 Timm 


in northwestern North America. Microtines are the primary hosts. 
This species is generally the most abundant flea on the far-northern 
Microtus, M. abbreviatus and M. oeconomus (Haas et al., 1978). M. 
penicilliger is often placed in a separate genus, Amalaraeus, by Eur- 
asian workers. M. telchinus is a widespread and common flea in 
western North America. Peromyscus appears to be the most common 
host, although it has been collected from numerous mammal species; 
adults can be collected during all seasons of the year. 

Megabothris is a Holarctic genus of 18 species, most of which 
parasitize microtines. M. abantis ranges in western North America 
from New Mexico north to Alaska; it is found on most species of 
western and northern microtines. M. acerbus is a chipmunk flea 
found in the northeastern U.S. and adjacent Canada; Tamuas striatus 
is the primary host, and the single record from M. pennsylvanicus 
must be considered an accidental occurrence. Two subspecies of M. 
asio are recognized in northern North America, and a single inter- 
grade has been described from southeastern Wisconsin (Amin, 
1976a). M. asio asio is widespread and common in the east and is 
a true parasite of Microtus; it is usually more abundant in the nest 
than on the host. M. a. megacolpus is a western flea parasitizing 
Microtus primarily. M. calcarifer is a Holarctic species; Alaskan 
populations are recognized as a distinct subspecies, M. c. gregsont. 
Microtus and Clethrionomys are the primary hosts. ‘Three subspecies 
of M. clantoni are found in a restricted area of western U.S., and 
are true parasites of Lagurus. M. groenlandicus is a transcontinental 
Nearctic species occurring only in northern Alaska and Canada; 
lemmings (both Dicrostonyx and Lemmus) and Mucrotus are the 
primary hosts. M. lucifer is a rarely collected parasite of Microtus 
from the Rocky Mountain region of Alberta, British Columbia, and 
western U.S. M. quirini is a transcontinental vole flea found 
throughout the northern tier of states in the U.S. and in adjacent 
Canada; Microtus is the primary host, although M. quirini fre- 
quently is collected on Clethrionomys and Zapus. 

Monopsyllus is a Holarctic genus of 22 species, 13 of which occur 
in North America; most species parasitize squirrels, but two species 
are known only from Ochotona, and a few are found on a variety 
of hosts. Johnson (1961) provided the most recent revision of this 
group, although now that additional specimens are available, the 
specific and generic status of several members should be reexam- 
ined. M. ciliatus has four recognizable subspecies, and occurs 


Parasites 489 


throughout western North America west of the 100th meridian, 
from Alaska south to Arizona. It is primarily a squirrel flea, with 
the majority of records coming from Eutamias, Sciurus, Spermoph- 
lus, and Tamuiasciurus; the one record from Mucrotus longicaudus 
can be considered an accidental occurrence. M. eumolpi is a true 
parasite of Eutamias with two subspecies found throughout the range 
of Eutamias in the northern midwest and western portions of North 
America; it has been collected also from a wide variety of small 
mammals. M. vison is a common, northern sciurid flea, but has 
been collected on a variety of hosts. M. wagner: is found from the 
upper midwest to the west coast of the U.S. and Canada; Peromys- 
cus appears to be the primary host although it is taken occasionally 
from microtines. 

Orchopeas is a Nearctic genus of nine species in need of revision. 
Most of the species are parasites of squirrels; however, a few infest 
cricetids, especially Peromyscus and Neotoma. O. caedens is a north- 
ern squirrel flea, especially abundant on Jamuasciurus; the single 
record from Microtus oeconomus can be considered accidental. O. 
howardu is a true parasite of tree squirrels (Glaucomys, Sciurus, and 
Tamuasciurus), and is found from southern Canada south to Vene- 
zuela, with three recognized subspecies. It is an abundant flea; 
adults are present during all months of the year, and are found 
occasionally on a variety of small mammals. O. leucopus is one of 
the most abundant species of fleas found in North America; it is 
perhaps a true parasite of Peromyscus, although it frequently is 
found on many other species of mammals, suggesting that it is not 
an obligate parasite of Peromyscus. O. sexdentatus is a true parasite 
of woodrats and is found throughout North America wherever Ne- 
otoma occurs; the few records from Microtus can be considered ac- 
cidental. 

Peromyscopsylla is a Holarctic genus of 17 species; most are par- 
asites of microtines and murids. Johnson and Traub (1954) pro- 
vided an excellent revision of the genus. P. catatina is found in the 
northeastern U.S. and adjacent Canada; Microtus and Clethriono- 
mys are the primary hosts, although it has been recovered from 
numerous other species during all seasons of the year. P. ebrightz is 
a poorly known species from southern California. P. hamifer, a 
Holarctic species, is widely distributed throughout the northern half 
of this continent, and is generally most abundant in fall and winter. 
North American populations are all referred to P. h. hamifer. P. 


490 Timm 


hesperomys is an abundant flea throughout the U.S. and Canada, 
and extends south to central Mexico; adults occur throughout the 
year and cricetines, especially Peromyscus and Neotoma, are the 
primary hosts. P. oststbirica is a Holarctic species in which both 
Siberian populations and those in Alaska and adjacent Canada are 
little differentiated; Microtus is the primary host of this summer 
flea. P. scott: is a poorly collected flea from the eastern U.S.; it is 
apparently a fall and winter flea with Peromyscus as the primary 
host. P. selenis is a fall and winter flea parasitizing microtines in 
the western U.S. and adjacent Canada. 

Pleochaetis is a New World genus of 16 species restricted to 
southwestern U.S., Central America, and northern South America. 
Most are parasites of cricetid rodents although much remains to be 
learned about the systematics and host relationships of this group. 
P. asetus is known from the Mogollon Mountains of New Mexico 
and Cerro Potosi, Nuevo Leon; Microtus mexicanus is probably the 
true host, although this flea also has been collected on Peromyscus 
and Neotoma. P. sibynus has a wide distribution in Mexico with 
two recognized subspecies; specimens are known from Microtus 
mexicanus, Neotoma, Peromyscus, and Reithrodontomys. P. aztecus, 
P. mathesoni, P. mundus, P. paramundus, and P. parus are all poorly 
known species that have been collected on only a few occasions in 
central Mexico, primarily from Microtus and Peromyscus. 

Rhadinopsylla is a Holarctic complex genus of some 55 species; 
ten species are known from the Nearctic. Most are found as adults 
exclusively during winter months, and are nest fleas; they seldom 
occur on the host per se, but seem to be associated with a wide 
variety of rodents. Prior to Smit’s (1957) revision, all eastern North 
American specimens of the genus were included within R. fraterna. 
Smit recognized several species within that complex; thus, all older 
records of R. fraterna must now be considered in doubt. R. fraterna 
(sensu stricto) is found in the Rocky Mountain region of the U.S. 
and adjacent Canada, and is generally considered a true parasite of 
Cynomys and Spermophilus. R. mexicana is known only from Mex- 
ico and has been collected primarily on Neotoma and Peromyscus. 
R. orama is known only from the eastern U.S., and is probably a 
true parasite of microtines, especially Microtus. R. sectilis is a widely 
distributed flea in western North America, and has been associated 
with a wide variety of rodents. 

Stenoponia is a Holarctic genus of 14 species of which only two 
are found in North America. The vast majority of taxa are Pa- 


Parasites 491 


laearctic; they occur primarily on murid rodents, usually are nest 
fleas, and occur as adults mainly in winter months. S. americana is 
a widely distributed and common flea in eastern North America; it 
has been collected on a wide variety of small mammals, including 
both rodents and insectivores, and lacks host specificity. S. ponera 
is known only from Mexico and, in addition to Microtus mexicanus, 
has been collected on Peromyscus and Eutamias; most records are 
from fall and from elevations of 3,050—3,350 m. 

Strepsylla is a poorly known Nearctic genus of eight recognized 
species ranging from Guatemala north to central Mexico. Most 
records are from Peromyscus, but very little is known of the biology 
of this group. S. mina was described from Microtus mexicanus phaeus; 
it is known only from a few higher-elevation localities in southcen- 
tral Mexico; it also has been taken on Neotomodon alstoni and Pero- 
myscus melanotis. 

Many other species of fleas have been taken from Microtus, which 
in our present state of knowledge are assumed to be accidental. 
These include: Anomiopsyllus falsicalifornicus, A. nudatus-princei 
(complex), Callistopsyllus deuterus, Carteretta carteri, Cediopsylla in- 
aequalis, Ceratophyllus niger, Corrodopsylla curvata, Corypsylla kohl- 
st, C. ornata, Dactylopsylla bluei, D. rara, Dasypsullus gallinulae, Dia- 
manus montanus, Doratopsylla blarinae, Echidnophaga gallinacea, 
Foxella ignota, Hoplopsylla anomalus, Leptopsylla segnis, Megar- 
throglossus bisetis, M. divisus, Meringis cumming, M. hubbard, M. 
parkeri, M. shannoni, Nearctopsylla hyrtaci, Neopsylla inopina, Noso- 
psyllus fasciatus, Opisocrostis bruneri, Opisodasys keeni, O. pseudarc- 
tomys, Oropsylla arctomys, O. idahoensis, Pulex irritans, P. simulans, 
Thrassis spenceri, T. bacchi, and Xenopsylla cheopis. 

The records of fleas parasitizing Microtus are as follows: 


Microtus abbreviatus 
Malaraeus penicilliger (Grube, 1851) (Holland, 1963; Rausch and Rausch, 1968) 
Megabothris groenlandicus (Wahlgren, 1903) (Rausch and Rausch, 1968) 
Maicrotus breweri 
Epitedia wenmanni (Rothschild, 1904) (Fox, 1940a; Main, 1970; Winchell, 1977) 
Microtus californicus 
Anomiopsyllus falsicalifornicus C. Fox, 1929 (Barnes et al., 1977; Linsdale and 
Davis, 1956 [reported as A. congruens]) 
Atyphloceras echis Jordan and Rothschild, 1915 (Jellison and Senger, 1976; 
Linsdale and Davis, 1956 [reported as A. longipalpus]) 
Atyphloceras multidentatus (C. Fox, 19096) (Augustson, 1943 [reported as A. 
artius|; Augustson and Wood, 1953; Burroughs, 1944; Coultrip et al., 
1973; Fox, 19096 [original description]; Hopkins and Rothschild, 1962; 
Hubbard, 1947 [reported as A. felix]; Jellison and Senger, 1976; Kartman, 


492 


Timm 


1958, 1960; Kartman and Prince, 1956; Kartman et al., 1958a, 1958d; 
Linsdale and Davis, 1956; Macchiavello, 1954; Miles et al., 1957; Mitz- 
main, 1909; Murray, 1957; Stark and Miles, 1962; Stewart, 1940 [re- 
ported as A. felix]) 

Carteretta cartert Fox, 1927 (Augustson, 1943; Macchiavello, 1954) 

Catallagia charlottensis (Baker, 1898) (Fox, 1909a; Macchiavello, 1954) 

Catallagia sculleni Hubbard, 1940 (Burroughs, 1944 [reported as C. vonbloekert]) 

Catallagia wymani (Fox, 1909) (Fox, 1909c [original description and type-host]; 
Kartman, 1958, 1960; Kartman et al., 1958a, 1958d; Macchiavello, 1954; 
Miles et al., 1957; Murray, 1957; Stark and Miles, 1962) 

Cediopsylla inaequalis (Baker, 1895) (Linsdale and Davis, 1956) 

Ceratophyllus niger C. Fox, 1908 (Murray, 1957) 

Corrodopsylla curvata (Rothschild, 1915) (Miles et al., 1957) 

Corypsylla ornata C. Fox, 1908 (Murray, 1957) 

Dactylopsylla blue: C. Fox, 1909 (Hubbard, 1947; Macchiavello, 1954) 

Diamanus montanus (Baker, 1895) (Kartman et al., 1958d; Linsdale and Davis, 
1956; Miles et al., 1957) 

Echidnophaga gallinacea (Westwood, 1875) (Augustson, 1943; Linsdale and Da- 
vis, 1956) 

Epitedia stewarti Hubbard, 1940 (Hopkins and Rothschild, 1962) 

Foxella ignota (Baker, 1895) (Murray, 1957) 

Hoplopsyllus anomalus (Baker, 1904) (Holdenried et al., 1951; Linsdale and 
Davis, 1956; Rutledge et al., 1979) 

Hystrichopsylla dippier (Rothschild, 1902) (Burroughs, 1944; Macchiavello, 1954; 
Mitzmain, 1909) 

Hystrichopsylla gigas (Kirby, 1837) (Holdenried et al., 1951) (questionable iden- 
tification) 

Hystrichopsylla occidentalis Holland, 1949 (Campos and Stark, 1979; Coultrip 
et al., 1973; Holland, 1957; Hopkins and Rothschild, 1962; Kartman et 
al., 1958a, 1958c, 1958d, 1960; Miles et al., 1957; Quan et al., 1960a, 
19606; Schwan, 1975; Stark and Kinney, 1962; Stark and Miles, 1962) 

Leptopsylla segnis (Schonherr, 1811) (Fox, 1909a [reported as Ctenopsyllus mus- 
cult (Duges)]; Hardy et al., 1974; Kartman et al., 1958d; Macchiavello, 
1954; Miles et al., 1957; Mitzmain, 1909 [reported as C. musculi]; Mur- 
ray, 1957; Schwan, 1975) 

Malareus telchinus (Rothschild, 1905) (Augustson, 1943; Augustson and Wood, 
1953; Burroughs, 1944; Burroughs et al., 1945; Coultrip et al., 1973; 
Fox, 1909a; Jellison and Senger, 1976; Kartman et al., 1958a, 1958d, 
1960; Lidicker, 1973; Linsdale and Davis, 1956; Macchiavello, 1954; 
Miles et al., 1957; Mitzmain, 1909; Murray, 1957; Quan et al., 1960a; 
Rutledge et al., 1979; Schwan, 1975; Stark and Kinney, 1962; Stark and 
Miles, 1962; Wagner, 19366) 

Meringis cummingi (C. Fox, 1926) (Holdenried et al., 1951) 

Monopsyllus wagneri (Baker, 1904) (Kartman et al., 1958d; Linsdale and Davis, 
1956; Miles et al., 1957; Rutledge et al., 1979) 

Nosopsyllus fasciatus (Bosc, 1801) (Adams et al., 1970; Doane, 1908; Kartman 
et al., 1958a, 1958d; Lidicker, 1973; Macchiavello, 1954; Miles et al., 
1957; Stark and Miles, 1962) 

Opisodasys keeni (Baker, 1896) (Augustson, 1955; Holdenried et al., 1951 [re- 


Parasites 493 


ported as O. nesiotus]; Kartman et al., 1958a, 1958d; Miles et al., 1957; 
Murray, 1957; Quan et al., 1960a; Stark and Miles, 1962) 

Orchopeas sexdentatus (Baker, 1904) (Holdenried et al., 1951; Linsdale and Da- 
vis, 1956; Macchiavello, 1954) 

Peromyscopsylla ebrighti (C. Fox, 1926) (Burroughs, 1944) 

Peromyscopsylla hesperomys (Baker, 1904) (Linsdale and Davis, 1956; Macchia- 
vello, 1954; Stewart, 1940) 

Peromyscopsylla selenis (Rothschild, 1906) (Hubbard, 1947; Jellison and Senger, 
1976; Johnson and Traub, 1954) 

Xenopsylla cheopis (Rothschild, 1903) (Kartman et al., 1958d; Miles et al., 1957) 

Microtus canicaudus 

Atyphloceras multidentatus (C. Fox, 1909) (Easton, 1983a; Faulkenberry and 
Robbins, 1980; Hubbard, 1941a, 1947; Robbins, 1983; Robbins and 
Faulkenberry, 1982) 

Catallagia charlottensis (Baker, 1898) (Faulkenberry and Robbins, 1980; Hub- 
bard, 1941a, 1947; Robbins, 1983; Robbins and Faulkenberry, 1982) 

Catallagia sculleni Hubbard, 1940 (Easton, 1983a; Hubbard, 1941a, 1947 [re- 
ported as C. chamberlini}) 

Corrodopsylla curvata (Rothschild, 1915) (Faulkenberry and Robbins, 1980; 
Robbins, 1983) 

Epitedia scapani (Wagner, 1936) (Hubbard, 1941a, 1947 [reported as E. jor- 
dan1]) 

Hystrichopsylla dippier Rothschild, 1902 (Hubbard, 1941a, 1947) 

Hystrichopsylla occidentalis Holland, 1949 (Faulkenberry and Robbins, 1980; 
Robbins, 1983) 

Megabothris abantis (Rothschild, 1905) (Hubbard, 1947) 

Monopsyllus wagner: (Baker, 1904) (Faulkenberry and Robbins, 1980; Robbins, 
1983) 

Nosopsyllus fasciatus (Bosc, 1801) (Faulkenberry and Robbins, 1980; Robbins, 
1983) 

Opisodasys keent (Baker, 1896) (Hubbard, 19412) 

Peromyscopsylla selenis (Rothschild, 1906) (Faulkenberry and Robbins, 1980; 
Hubbard, 1941a, 1947; Robbins, 1983) 

Rhadinopsylla sectilis (Jordan and Rothschild, 1923) (Hubbard, 1941a, 19416, 
1947 [reported as Micropsylla goodt]) 

Microtus chrotorrhinus 

Atyphloceras bishopi Jordan, 1933 (Benton and Kelly, 1975; Benton and Smiley, 
1963; Martin, 1972) 

Catallagia borealis Ewing, 1929 (Benton and Kelly, 1975; Benton and Smiley, 
1963; Martin, 1972; Whitaker and French, 1982) 

Ctenophthalmus pseudagyrtes Baker, 1904 (Benton and Cerwonka, 1964; Benton 
and Kelly, 1975; Benton et al., 1969; Brown, 1968; Geary, 1959; Jame- 
son, 1943a; Linzey and Linzey, 1973; Lovejoy and Gaughan, 1975; Mar- 
tin, 1972; Whitaker and French, 1982) 

Epitedia wenmanni (Rothschild, 1904) (Benton and Kelly, 1975; Martin, 1972; 
Whitaker and French, 1982) 

Megabothris asio (Baker, 1904) (Benton, 1980; Benton and Cerwonka, 1964; 
Benton and Kelly, 1975; Benton et al., 1969; Martin, 1972) 

Megabothris quirini (Rothschild, 1905) (Benton, 1980; Benton and Cerwonka, 


494 Timm 


1964; Benton and Kelly, 1975; Benton and Timm, 1980; Benton et al., 
1969; Brown, 1968; Main, 1970; Martin, 1972; Osgood, 1964; Timm, 
1974, 1975; Whitaker and French, 1982) 

Orchopeas leucopus (Baker, 1904) (Martin, 1972) 

Peromyscopsylla catatina (Jordan, 1928) (Benton, 1980; Benton and Cerwonka, 
1964; Benton and Kelly, 1975; Benton and Smiley, 1963; Benton and 
Timm, 1980; Benton et al., 1969; Brown, 1968; Johnson and Traub, 
1954; Martin, 1972; Timm, 1974, 1975; Whitaker and French, 1982) 

Peromyscopsylla hesperomys (Baker, 1904) (Benton and Kelly, 1975) 

Microtus longicaudus 

Anomiopsyllus nudatus-A. prince: complex (Haas et al., 1973) 

Atyphloceras multidentatus (C. Fox, 1909) (Hopkins and Rothschild, 1962; Hub- 
bard, 19412) 

Callistopsyllus deuterus Jordan, 1937 (Augustson, 19416) 

Catallagia charlottensis (Baker, 1898) (Holland, 19496; Hubbard, 1947 [reported 
as C. motez]) 

Catallagia decipiens Rothschild, 1915 (Beck, 1955; Egoscue, 1966, 1976; Haas 
et al., 1973; Hansen, 1964; Holland, 19495; Hopkins and Rothschild, 
1962; Hubbard, 1947; Morlan, 1955) 

Catallagia scullent Hubbard, 1940 (Jameson and Brennan, 1957) 

Corrodopsylla curvata (Rothschild, 1915) (Hopkins and Rothschild, 1966) 

Delotelis holland: Smit, 1952 (Jameson and Brennan, 1957; Smit, 1952) 

Delotelis telegoni (Rothschild, 1905) (Holland, 19496; Jellison and Senger, 1973; 
Morlan, 1955; Stark, 1959) 

Epitedia scapani (Wagner, 1936) (Hopkins and Rothschild, 1962; Hubbard, 
1941a, 1947 [reported as E. jordanz]) 

Epitedia stanford: Traub, 1944 (Egoscue, 1966, 1976) 

Epitedia wenmanni (Rothschild, 1904) (Easton, 1982; Jameson and Brennan, 
1957) 

Hystrichopsylla dipper Rothschild, 1902 (Egoscue, 1966; Haas et al., 1973; Han- 
sen, 1964; Holland, 1949a, 19496, 1957; Hopkins and Rothschild, 1962; 
Hubbard, 1947; Morlan, 1955) 

Hystrichopsylla occidentalis Holland, 1949 (Campos and Stark, 1979; Holland, 
1957) 

Malaraeus telchinus (Rothschild, 1905) (Dunn and Parker, 1923; Egoscue 1966, 
1976; Haas, 1973; Hansen, 1964; Holland, 19495; Hubbard, 1947; 
Jameson and Brennan, 1957; Morlan, 1955; Wagner, 1936a) 

Megabothris abantis (Rothschild, 1905) (Allred, 1952; Augustson, 1941); Beck, 
1955; Burroughs, 1947, 1953; Egoscue, 1966, 1976; Haas et al., 1973; 
Hansen, 1964; Holland, 19495, 1958; Hubbard, 1941a, 1947; Jellison 
and Senger, 1973; Morlan, 1955; Tipton, 1950) 

Megabothris asio (Baker, 1904) (Hubbard, 1940a, 1947) 

Megabothris quirini (Rothschild, 1905) (Hubbard, 1947; Wiseman, 1955) 

Megarthroglossus bisetis Jordan and Rothschild, 1915 (Haas et al., 1973) 

Megarthroglossus divisus (Baker, 1895) (Holland, 19496) 

Meringis hubbardi Kohls, 1938 (Egoscue, 1966) 

Meringis parkert Jordan, 1937 (Stark, 1959) 

Monopsyllus ciliatus Baker, 1904 (Hubbard, 1941a, 1947) 


Parasites 495 


Monopsyllus eumolpi (Rothschild, 1905) (Egoscue, 1966; Morlan, 1955) 

Monopsyllus wagneri (Baker, 1904) (Augustson, 19416; Beck, 1955; Egoscue, 
1966, 1976; Haas et al., 1973; Hansen, 1964; Holland, 194945; Hubbard, 
1947; Jameson and Brennan, 1957; Morlan, 1955) 

Neopsylla inopina Rothschild, 1915 (Hansen, 1964; Svihla, 1941) 

Opisodasys keeni (Baker, 1896) (Egoscue, 1976; Hubbard, 1947) 

Orchopeas leucopus (Baker, 1904) (Egoscue, 1976) 

Oropsylla idahoensis (Baker, 1904) (Haas et al., 1973; Hubbard, 1947) 

Peromyscopsylla hamifer (Rothschild, 1906) (Egoscue, 1976; Haas, 1973; Haas 
et al., 1973; Holdenried and Morlan, 1956; Hopkins and Rothschild, 
1971; Morlan, 1955) 

Peromyscopsylla hesperomys (Baker, 1904) (Haas et al., 1973; Hubbard, 1947) 

Peromyscopsylla selenis (Rothschild, 1906) (Augustson, 19416; Egoscue, 1966, 
1976; Haas, 1973; Haas et al., 1973; Hansen, 1964; Holland, 19496; 
Hopkins and Rothschild, 1971; Jameson and Brennan, 1957; Jellison 
and Senger, 1973; Johnson and Traub, 1954; Morlan, 1955; Tipton, 
1950) 

Rhadinopsylla sectilis Jordan and Rothschild, 1923 (Hubbard, 1947) 

Muicrotus mexicanus 

Atyphloceras tancitari Traub and Johnson, 1952 (Traub and Johnson, 1952) 

Catallagia sp. (Barrera, 1968) 

Ctenophthalmus caballeroi Barrera and Machado, 1960 (Barrera, 1968; Barrera 
and Machado, 1960 [original description]) 

Ctenophthalmus haagi Traub, 1950 (Hopkins and Rothschild, 1966; Traub, 1950 
[original description; from M. mexicanus phaeus}) 

Ctenophthalmus pseudagyrtes Baker, 1904 (Barrera, 1968; Tipton and Mendez, 
1968) 

Epitedia wenmanni (Rothschild, 1904) (Tipton and Mendez, 1968) 

Hystrichopsylla orophila Barrera, 1952 (Barrera, 1952 [original description], 1968) 

Jellisonia hayest Traub, 1950 (Barrera, 1968; Traub, 1950 [original description]) 

Pleochaetis asetus Traub, 1950 (Barrera, 1968; Tipton and Machado-Allison, 
1972; Tipton and Mendez, 1968; Traub, 1950 [original description]) 

Pleochaetis aztecus Barrera, 1954 (Barrera, 1968) 

Pleochaetis mathesoni Traub, 1950 (Barrera, 1968) 

Pleochaetis mundus (Jordan and Rothschild, 1922) (Barrera, 1968) 

Pleochaetis paramundus Traub, 1950 (Barrera, 1968) 

Pleochaetis parus Traub, 1950 (Barrera, 1968) 

Pleochaetis stbynus Jordan, 1925 (Barrera, 1968; Fox, 19396; Tipton and Men- 
dez, 1968; Traub, 1950) 

Pulex simulans Baker, 1895 (Tipton and Mendez, 1968) 

Rhadinopsylla mexicana (Barrera, 1952) (Barrera, 1968; Tipton and Mendez, 
1968) 

Stenoponia ponera Traub and Johnson, 1952 (Tipton and Mendez, 1968) 

Strepsylla mina Traub, 1950 (Hopkins and Rothschild, 1962; Traub, 1950 [orig- 
inal description; from M. mexicanus phaeus)) 

Muicrotus miurus 
Corrodopsylla curvata (Rothschild, 1915) (Hopla, 1965d) 
Malaraeus penicilliger (Grube, 1851) (Hopla, 19655; Rausch, 1964) 


496 


Timm 


Megabothris calcarifer (Wagner, 1913) (Hopla, 19655; Hubbard, 1960; Rausch, 
1964) 

Megabothris groenlandicus (Wahlgren, 1903) (Hopla, 19655; Hubbard, 1960; 
Jellison and Senger, 1976; Rausch, 1964) 

Megabothris quirini (Rothschild, 1905) (Hopla, 19656) 

Peromyscopsylla ostsibirica (Scalon, 1936) (Rausch, 1964) 


Microtus montanus 


Amphipsylla sibirica (Wagner, 1898) (Allred, 1968a; Eads et al., 1979) 

Callistopsyllus deuterus Jordan, 1937 (Augustson, 19415) 

Catallagia decipiens Rothschild, 1915 (Allred, 1952; Beck, 1955; Haas et al., 
1973; Hansen, 1964; Holland, 19495; Hopkins and Rothschild, 1962; 
Stark, 1959) 

Catallagia mathesoni Jameson, 1950 (original description) 

Catallagia sculleni Hubbard, 1940 (Augustson, 1941a [described as C. rutherford: 
from M. montanus dutcheri]; Stark and Kinney, 1969) 

Corrodopsylla curvata (Rothschild, 1915) (Haas et al., 1973; Hansen, 1964) 

Dactylopsylla rara 1. Fox, 1940 (Haas et al., 1973) 

Delotelis holland: Smit, 1952 (original description) 

Epitedia stanford: Traub, 1944 (Stark, 1959) 

Epitedia wenmanni (Rothschild, 1904) (Allred, 1952; Beck, 1955; Stark, 1959; 
Tipton, 1950) 

Hoplopsyllus anomalus (Baker, 1904) (Allred, 1952; Beck, 1955) 

Hystrichopsylla dippier Rothschild, 1902 (Beck, 1955, Haas et al., 1973; Holland, 
19496, 1957; Tipton, 1950) 

Malaraeus bitterrootensis (Dunn, 1923) (Wiseman, 1955) 

Malaraeus euphorbi (Rothschild, 1905) (Allred, 1968a) 

Malaraeus telchinus (Rothschild, 1905) (Allred, 1952, 1968a; Beck, 1955; Haas 
et al., 1973; Hansen, 1964; Hartwell et al., 1958; Seidel and Booth, 1960; 
Stark, 1959; Tipton, 1950) 

Megabothris abantis (Rothschild, 1905) (Allred, 1952; Augustson, 19415; Beck, 
1955; Haas et al., 1973; Hansen, 1964; Hubbard, 1947, 1949c; Jellison 
and Senger, 1973; Kartman and Prince, 1956; Kinsella and Pattie, 1967; 
Stark, 1959) 

Megabothris asio (Baker, 1904) (Hansen, 1964; Holland, 1950; Hubbard, 1949c) 

Megabothris clantoni Hubbard, 1949 (Hansen, 1964; Hubbard, 1949) 

Megabothris lucifer (Rothschild, 1905) (Holland, 1941, 1949a, 19496; Jellison 
and Senger, 1976; Wagner, 1936) 

Meringis hubbardi Kohls, 1938 (Hansen, 1964) 

Meringis parkert Jordan, 1937 (Allred, 19682) 

Meringis shannon (Jordan, 1929) (Bacon, 1953) 

Monopsyllus eumolpi (Rothschild, 1905) (Allred, 1952; Beck, 1955; Hansen, 
1964; Stark, 1959) 

Monopsyllus wagner (Baker, 1904) (Allred, 1952, 1968a; Bacon, 1953; Beck, 
1955; Haas et al., 1973; Hansen, 1964; Stark, 1959) 

Nosopsyllus fasciatus (Bosc, 1801) (Allred, 1952; Beck, 1955) 

Opisodasys keeni (Baker, 1896) (Stark, 1959; Stark and Kinney, 1969) 

Oropsylla idahoensis (Baker, 1904) (Haas et al., 1973) 


Parasites 497 


Peromyscopsylla hamifer (Rothschild, 1906) (Haas et al., 1973; Johnson and 
Traub, 1954; Stark, 1959) 

Peromyscopsylla selenis (Rothschild, 1906) (Augustson, 19416; Haas, 1973; Haas 
et al., 1973; Hansen, 1964; Hopkins and Rothschild, 1971; Hubbard, 
1947, 1949c; Johnson and Traub, 1954; Stark, 1959; Stark and Kinney, 
1969) 

Thrassis bacchi (Rothschild, 1905) (Allred, 1968ca) 

Microtus ochrogaster 

Ctenophthalmus pseudagyrtes Baker, 1904 (Basolo and Funk, 1974; Batson, 1965; 
Buckner and Gleason, 1974; Hopkins and Rothschild, 1966; Jameson, 
1947; Jellison and Senger, 1973; Layne, 1958; Mumford and Whitaker, 
1982; Poorbaugh and Gier, 1961; Senger, 1966; Verts, 1961; Whitaker 
and Corthum, 1967) 

Epitedia wenmanni (Rothschild, 1904) (Basolo and Funk, 1974; Buckner and 
Gleason, 1974; Hopkins and Rothschild, 1962; Jameson, 1947; Poor- 
baugh and Gier, 1961; Verts, 1961; Whitaker and Corthum, 1967; Wil- 
son, 1957) 

Hystrichopsylla dippier Rothschild, 1902 (Hopkins and Rothschild, 1962) 

Malaraeus euphorbi (Rothschild, 1905) (Senger, 1966) 

Megabothris asio (Baker, 1904) (Verts, 1961) 

Monopsyllus wagnert (Baker, 1904) (Turner, 1974) 

Nearctopsylla hyrtaci (Rothschild, 1904) (Jellison and Senger, 1973; Senger, 1966) 

Nosopsyllus fasciatus (Bosc, 1801) (El-Wailly, 1967; Jameson, 1947) 

Orchopeas howardu (Baker, 1895) (Jameson, 1947) 

Orchopeas leucopus (Baker, 1904) (Buckner and Gleason, 1974; Easton, 1982; 
El-Wailly, 1967; Jameson, 1947; Jellison and Senger, 1973; Lampe et 
al., 1974; Poorbaugh and Gier, 1961; Rapp and Gates, 1957; Turner, 
1974; Verts, 1961) 

Orchopeas sexdentatus (Baker, 1904) (Rapp and Gates, 1957) 

Peromyscopsylla scotti 1. Fox, 1939 (Buckner and Gleason, 1974) 

Rhadinopsylla sectilis Jordan and Rothschild, 1923 (Senger, 1966) 

Stenoponia americana (Baker, 1899) (Buckner and Gleason, 1974; Hopkins and 
Rothschild, 1962; Poorbaugh and Gier, 1961; Verts, 1961; Whitaker and 
Corthum, 1967; Wilson, 1957) 

Muicrotus oeconomus 

Amphipsylla marikovskit Toff and Tiflov, 1939 (Fox, 19406 [reported as A. ewingz]; 
Holland, 1963; Hopkins and Rothschild, 1971; Hopla, 1965a, 1965d) 

Catallagia dacenkoi loff, 1940 (Hopkins and Rothschild, 1962; Hopla, 1965a, 
19656; Hubbard, 1960; Jellison and Senger, 1976) 

Ceratophyllus gare: Rothschild, 1902 (Hopla, 19656) 

Corrodopsylla curvata (Rothschild, 1915) (Haas et al., 1982; Hopla, 19655) 

Epitedia wenmanni (Rothschild, 1904)(Haas et al., 1979; Hubbard, 1960) 

Hystrichopsylla occidentalis Holland, 1949 (Campos and Stark, 1979; Haas et 
al., 1979; Holland, 1957) 

Malaraeus penicilliger (Grube, 1851) (Haas et al., 1979, Haas et al., 1982; 
Holland, 1958, 1963; Hopla, 1965a, 19656, 1980; Hubbard, 1960; 
Rausch et al., 1969) 


498 


Timm 


Megabothris abantis (Rothschild, 1905) (Haas et al., 1979, 1982; Rausch et al., 
1969; Schiller and Rausch, 1956) 

Megabothris calcarifer (Wagner, 1913) (Haas et al., 1979, 1982; Holland, 1958, 
1963; Hopla, 1965a, 19656, 1980; Hubbard, 1960) 

Megabothris groenlandicus (Wahlgren, 1903) (Hubbard, 1960) 

Megabothris quirini (Rothschild, 1905) (Hopla, 1965a, 19656, 1980) 

Monopsyllus vison (Baker, 1904) (Hopla, 19656) 

Orchopeas caedens (Jordan, 1925) (Hopla, 19656) 

Peromyscopsylla hamifer (Rothschild, 1906) (Quay, 1951) 

Peromyscopsylla oststbirica (Scalon, 1936) (Haas et al., 1982; Holland, 1958, 
1963; Hopkins and Rothschild, 1971; Hopla, 1965a, 19655, 1980; Hub- 
bard, 1960; Jellison and Senger, 1976; Rausch et al., 1969) 


Microtus oregoni 


Atyphloceras multidentatus (C. Fox, 1909) (Holland, 19494,; Hopkins and Roth- 
schild, 1962; Hubbard, 1941a, 1947) 

Catallagia charlottensis (Baker, 1898) (Holland, 19495; Hubbard, 1941a, 1947) 

Corrodopsylla curvata (Rothschild, 1915) (Holland, 19495; Hubbard, 1941a, 1947 
[reported as Doratopsylla jellisont Hubbard)]) 

Corypsylla ornata C. Fox, 1908 (Holland, 19495; Hopkins and Rothschild, 1962) 

Delotelis holland: Smit, 1952 (Hopkins and Rothschild, 1962; Smit, 1952) 

Delotelis telegoni (Rothschild, 1905) (Holland, 19496) 

Epitedia scapani (Wagner, 1936) (Hopkins and Rothschild, 1962; Hubbard, 
1941a, 1947 [reported as E. jordanzi]) 

Hystrichopsylla dippier Rothschild, 1902 (Hubbard, 1941a, 1947) 

Hystrichopsylla occidentalis Holland, 1949 (Campos and Stark, 1979; Holland, 
1957; Hopkins and Rothschild, 1962) 

Malaraeus dobbsi Hubbard, 1940 (Hubbard, 19406 [original description], 19414; 
Jellison and Senger, 1976) 

Megabothris abantis (Rothschild, 1905) (Holland, 19496, Hubbard, 1941a, 1947; 
Wagner, 1936a) 

Megabothris quirini (Rothschild, 1905) (Hubbard, 1947) 

Opisodasys keeni (Baker, 1896) (Holland, 19496) 

Peromyscopsylla hesperomys (Baker, 1904) (Hubbard, 1947; Johnson and Traub, 
1954) 

Peromyscopsylla selenis (Rothschild, 1906) (Holland, 1949; Hubbard, 19412) 

Rhadinopsylla sectilis (Jordan and Rothschild, 1923) (Holland, 19496) 


Microtus pennsylvanicus 


Amphipsylla marikousku Toff and Tiflov, 1939 (Hopla, 19652) 

Amphipsylla sibirica (Wagner, 1898) (Brown, 1944; Hopkins and Rothschild, 
1971; Jordan and Rothschild, 1913; Rothschild, 1905 [reported as Cer- 
atophyllus pollionis|; Wagner, 1936a) 

Atyphloceras bishopi Jordan, 1933 (Baker, 1946; Benton, 1980; Benton and Cer- 
wonka, 1960; Benton and Kelly, 1971, 1975; Benton and Smiley, 1963; 
Buckner and Blasko, 1969; Burbutis, 1956; Cressey, 1961; Fox, 1940a; 
Geary, 1959; Holland, 1949a, 1958; Holland and Benton, 1968; Hopkins 
and Rothschild, 1962; Jameson, 1943a; Jordan, 1933; Lawrence et al., 
1965; Main, 1970; Mathewson and Hyland, 1964; Miller and Benton, 
1973; Scharf and Stewart, 1980) 


Parasites 499 


Catallagia borealis Ewing, 1929 (Benton, 1980; Ewing, 19296 [original descrip- 
tion and type-host]; Fox, 1940a; Fuller, 1943a, 19436; Holland and Ben- 
ton, 1968; Hopkins and Rothschild, 1962; Main, 1970) 

Catallagia charlottensis (Baker, 1898) (Holland, 19496) 

Catallagia dacenkoi loff, 1940 (Holland, 1951; Hopkins and Rothschild, 1962; 
Hopla, 1965a) 

Catallagia decipiens Rothschild, 1915 (Easton, 1982; Holland, 19495; Hopkins 
and Rothschild, 1962) 

Catallagia jellisoni Holland, 1954 (Hopkins and Rothschild, 1962) 

Corrodopsylla curvata (Rothschild, 1915) (Robert and Bergeron, 1977; Verts, 
1961) 

Ctenophthalmus pseudagyrtes Baker, 1904 (Amin, 1973, 1976a; Baker, 1946; 
Batson, 1965; Bell and Chalgren, 1943, Benton, 1966; Benton and Kelly, 
1969, 1975; Benton and Krug, 1956; Benton and Timm, 1980; Benton 
et al., 1969; Brimley, 1938; Brown, 1944; Brown, 1968; Burbutis, 1956; 
Connor, 1960; Cressey, 1961; Cummings, 1954; Erickson, 1938a; Fox, 
1940a; Fuller, 1943a, 19436; Gates, 1945; Geary, 1959; Gyorkos and 
Hilton, 19826; Holland and Benton, 1968; Hopkins and Rothschild, 1966; 
Hubbard, 1949a; Jameson, 19436; Jordan, 1928; Joyce and Eddy, 1944; 
Judd, 1950; Knipping et al., 19505; Lawrence et al., 1965; Lovejoy and 
Gaughan, 1975; MacCreary, 1945a; Main, 1970, 1983; Main et al., 
1979; Mathewson and Hyland, 1964; Miller and Benton, 1973; Osgood, 
1964; Quackenbush, 1971; Rapp and Gates, 1957; Robert, 1962; Robert 
and Bergeron, 1977; Rothschild, 1904; Scharf and Stewart, 1980; Stew- 
art, 1928, 1933; Timm, 1975; Tindall and Darsie, 1961; Verts, 1961; 
Whitaker and Corthum, 1967; White and White, 1981; Woods and Lar- 
son, 1971; Wright, 1979) 

Delotelis telegoni (Rothschild, 1905) (Brown, 1944; Holland, 19495, Hopkins 
and Rothschild, 1962; Rothschild, 1905 [original description and cotype 
host]; Tiraboschi, 1907) 

Doratopsylla blarinae C. Fox, 1914 (Benton, 1966; Fox, 1940a; Main, 1970) 

Epitedia stanfordi Traub, 1944 (Hopkins and Rothschild, 1962) 

Epitedia wenmanni (Rothschild, 1904) (Allred, 1952; Baker, 1946; Beck, 1955; 
Benton and Kelly, 1971, 1975; Benton and Timm, 1980; Burbutis, 1956; 
Connor, 1960; Cressey, 1961; Fox, 1940a; Fuller, 1943a; Gabbutt, 1961; 
Geary, 1959; Holland, 19495; Holland and Benton, 1968; Hopkins and 
Rothschild, 1962; Joyce and Eddy, 1944; Knipping et al., 19506; Law- 
rence et al., 1965; Main, 1970, 1983; Main et al., 1979; Mathewson and 
Hyland, 1964; Mumford and Whitaker, 1982; Osgood, 1964; Stark, 1959; 
Timm, 19726; Tindall and Darsie, 1961; Verts, 1961; Whitaker and 
Corthum, 1967; Wright, 1979) 

Hoplopsyllus anomalus (Baker, 1904) (Allred, 1952; Beck, 1955) 

Hystrichopsylla dippier Rothschild, 1902 (Easton, 1981; Fox, 1940a; Holland, 
1957; Jordan, 1929; Timm, 1975) 

Hystrichopsylla occidentalis Holland, 1949 (Campos and Stark, 1979; Egoscue, 
1966) 

Hystrichopsylla tahavuana Jordan, 1929 (Benton, 1966; Benton and Kelly, 1975; 
Benton et al., 1969; Geary, 1959; Hopkins and Rothschild, 1962; Jordan, 


500 


Timm 


1929 [original description]; Main, 1970; Osgood, 1964; Quackenbush, 
1971) 

Malaraeus penicilliger (Grube, 1851) (Holland, 1952b; Hopla, 1965a) 

Megabothris abantis (Rothschild, 1905) (Holland, 19494; Rothschild, 1905 [orig- 
inal description and type host}) 

Megabothris acerbus (Jordan, 1925) (Benton and Kelly, 1975) 

Megabothris asio (Baker, 1904) (Amin, 1976a; Baker, 1946; Benton, 1966, 1980; 
Benton and Kelly, 1975; Benton and Krug, 1956; Benton and Timm, 
1980; Benton et al., 1969, 1971; Brown, 1968; Burbutis, 1956; Connor, 
1960; Cressey, 1961; Cummings, 1954; Florschutz and Darsie, 1960; 
Fox, 1939a, 1940a; Fuller, 1943a; Gabbutt, 1961; Geary, 1959; Gyorkos 
and Hilton, 19826; Harper, 1956, 1961; Holland, 1949a, 19496, 1950, 
1958; Holland and Benton, 1968; Jellison and Senger, 1973; Jordan, 
1929 [described as Ceratophyllus megacolpus, 1933]; Knipping et al., 19508; 
Lawrence et al., 1965; Lovejoy and Gaughan, 1975; MacCreary, 1945a; 
Main, 1970; Main et al., 1979; Mathewson and Hyland, 1964; Miller 
and Benton, 1973; Mumford and Whitaker, 1982; Osgood, 1964; Quack- 
enbush, 1971; Robert, 1962; Robert and Bergeron, 1977; Scharf and 
Stewart, 1980; Scholten et al., 1962; Timm, 1975; Tindall and Darsie, 
1961; Verts, 1961; Wagner, 1936a [reported as M. megacolpus]; Woods 
and Larson, 1969; Wright, 1979) 

Megabothris calcarifer (Wagner, 1913) (Holland, 1950, 1958; Hopla, 1965a) 

Megabothris groenlandicus (Wahlgren, 1903) (Holland, 1952a) 

Megabothris lucifer (Rothschild, 1905) (Brown, 1944; Genoways and Jones, 1972; 
Holland, 19495; Rothschild, 1905 [original description and cotype-host]; 
Woods and Larson, 1971) 

Megabothris quirini (Rothschild, 1905) (Benton, 1966; Benton and Kelly, 1975; 
Benton and Timm, 1980; Benton et al., 1969, 1971; Buckner, 1964; Fox, 
1940a; Fuller, 19432; Gabbutt, 1961; Geary, 1959; Gyorkos and Hilton, 
19826; Harper, 1956; Holland, 194945; Hopla, 19652, 1980; Hubbard, 
1947; Jordan, 1932; Knipping et al., 19505; Lawrence et al., 1965; Love- 
joy and Gaughan, 1975; Quackenbush, 1971; Robert, 1962; Timm, 1975; 
Wagner, 1936a; Whitaker and French, 1982; Woods and Larson, 1969; 
Wright, 1979) 

Monopsyllus eumolopi (Rothschild, 1905) (Jordan, 1932) 

Monopsyllus vison (Baker, 1904) (Robert, 1962) 

Monopsyllus wagneri (Baker, 1904) (Beck, 1955; Benton and Timm, 1980; Eas- 
ton, 1982; Genoways and Jones, 1972; Timm, 19726; Verts, 1961) 
Nosopsyllus fasciatus (Bosc, 1801) (Allred, 1952; Baker, 1946; Beck, 1955; Fuller, 
1943a; Geary, 1959; Holland and Benton, 1968; Jameson, 1943a) 
Opisocrostis bruner: (Baker, 1895) (Amin, 1973, 1976a; Benton et al., 1971; 

Benton and Timm, 1980; Woods and Larson, 1969) 

Opisodasys pseudarctomys (Baker, 1904) (Holland and Benton, 1968) 

Orchopeas howardi (Baker, 1895) (Main et al., 1979; Mathewson and Hyland, 
1964; White and White, 1981) 

Orchopeas leucopus (Baker, 1904) (Amin, 1973, 1976a; Benton and Kelly, 1975; 
Buckner, 1964; Cressey, 1961; Fox, 1940a; Fuller, 1943a; Gates, 1945; 
Geary, 1959; Genoways and Jones, 1972; Holland and Benton, 1968; 


Parasites 501 


Joyce and Eddy, 1944; Knipping et al., 19506; Lawrence et al., 1965; 
Main, 1970; Main et al., 1979; Mathewson and Hyland, 1964; Robert, 
1962; Timm, 1975; Verts, 1961; Whitaker and Corthum, 1967) 

Oropsylla arctomys (Baker, 1904) (Verts, 1961) 

Peromyscopsylla catatina (Jordan, 1928) (Baker, 1946; Benton and Kelly, 1975; 
Benton and Krug, 1956; Benton and Timm, 1980; Benton et al., 1969; 
Buckner, 1964; Buckner and Blasko, 1969; Easton, 1981, 1982; Fox, 
1940a; Fuller, 1943a; Geary, 1959; Harper, 1956; Holland and Benton, 
1968; Hopkins and Rothschild, 1971; Jordan, 1929; Lawrence et al., 
1965; Lovejoy and Gaughan, 1975; Mathewson and Hyland, 1964; Stew- 
art, 1933; Timm, 1975) 

Peromyscopsylla hamifer (Rothschild, 1906) (Benton, 1980; Benton and Miller, 
1970; Benton and Timm, 1980; Cressey, 1961; Haas and Wilson, 1973; 
Holland, 1958; Holland and Benton, 1968; Hopkins and Rothschild, 
1971; Hubbard, 1949a; Johnson and Traub, 1954; Knipping et al., 19506 
[originally reported as P. catatina]; Lawrence et al., 1965; Lovejoy and 
Gaughan, 1975; Main, 1970, 1983; Main et al., 1979; Miller and Benton, 
1973; Mumford and Whitaker, 1982; Timm, 1975; Whitaker and Cor- 
thum, 1967) 

Peromyscopsylla hesperomys (Baker, 1904) (Benton and Kelly, 1975; Johnson 
and Traub, 1954) 

Peromyscopsylla ostsibirica (Scalon, 1936) (Haas et al., 1982; Hopla, 1965a) 

Peromyscopsylla scotti 1. Fox, 1939 (Benton and Kelly, 1975) 

Peromyscopsylla selenis (Rothschild, 1906) (Hopkins and Rothschild, 1971; 
Johnson and Traub, 1954; Rothschild, 1906; Wagner, 1936a [reported 
as Ctenopsylla selenis]) 

Rhadinopsylla fraterna (Baker, 1895) (Hopkins and Rothschild, 1962; Smit, 1957) 

Rhadinopsylla orama Smit, 1957 (Benton, 1980; Fox 1940a [questionable iden- 
tification]; Fuller, 1943a; Miller and Benton, 1973; Smit, 1957 [original 
description; type collected in nest]) 

Stenoponia americana (Baker, 1899) (Benton and Kelly, 1971, 1975; Fox, 1940a; 
Fuller, 1943a; Hopkins and Rothschild, 1962; MacCreary, 1945a; Main, 
1983; Main et al., 1979; Miller and Benton, 1973; Quackenbush, 1971; 
Tindall and Darsie, 1961) 

Thrassis bacchi (Rothschild, 1905) (Easton, 1982) 

Microtus pinetorum 

Atyphloceras bishopi Jordan, 1933 (Benton and Kelly, 1975; Main et al., 1979) 

Ctenophthalmus pseudagyrtes Baker, 1904 (Benton, 1955a; Benton and Kelly, 
1969, 1975; Benton and Krug, 1956; Benton et al., 1969; Burbutis, 1956; 
Cressey, 1961; Fox, 1940a; Harlan and Palmer, 1974; Holland and Ben- 
ton, 1968; Hopkins and Rothschild, 1966; Jameson, 19436, 1947; Jordan, 
1928; Layne, 1958; MacCreary, 1945a; Main, 1970, 1983; Main et al., 
1979; Mathewson and Hyland, 1964; Miller and Benton, 1973; Morlan, 
1952; Mumford and Whitaker, 1982; Palmer and Wingo, 1972; Sanford 
and Hays, 1974; Schiefer and Lancaster, 1970; Tindall and Darsie, 1961; 
Whitaker and Corthum, 1967) 

Doratopsylla blarinae C. Fox, 1914 (Benton, 1955a; Benton and Kelly, 1975; 
Burbutis, 1956; Miller and Benton, 1973) 


502 


Timm 


Epitedia wenmanni (Rothschild, 1904) (Burbutis, 1956) 

Hystrichopsylla tahavuana Jordan, 1929 (Benton and Kelly, 1975; Benton and 
Smiley, 1963; Holland, 1949a, 1957) 

Megabothris asio (Baker, 1904) (Miller and Benton, 1973) 

Opisodasys pseudarctomys (Baker, 1904) (Holland and Benton, 1968) 

Orchopeas howardu (Baker, 1895) (Morlan, 1952) 

Orchopeas leucopus (Baker, 1904) (Benton and Kelly, 1975; Benton et al., 1969; 
Ellis, 1955; Holland and Benton, 1968; Jameson, 1947; MacCreary, 1945a; 
Main et al., 1979; Tindall and Darsie, 1961) 

Peromyscopsylla catatina (Jordan, 1928) (Benton et al., 1969; Holland and Ben- 
ton, 1968) 

Peromyscopsylla hamifer (Rothschild, 1906) (Main et al., 1979) 

Peromyscopsylla hesperomys (Baker, 1904) (Main, 1983) 

Rhadinopsylla orama Smit, 1957 (Benton, 1980; Benton and Kelly, 1975; Hol- 
land and Benton, 1968; Hopkins and Rothschild, 1962; Miller and Ben- 
ton, 1973; Smit, 1957) 

Stenoponia americana (Baker, 1899) (Benton and Kelly, 1975; Benton and Smi- 
ley, 1963; Burbutis, 1956; Hopkins and Rothschild, 1962; MacCreary, 
1945a; Main et al., 1979; Palmer and Wingo, 1972; Sanford and Hays, 
1974; Tindall and Darsie, 1961; Wilson, 1957) 


Mucrotus richardson 


Catallagia charlottensis (Baker, 1898) (Hubbard, 1947) 

Catallagia scullent Hubbard, 1940 (Holland, 19496) 

Hystrichopsylla dippier Rothschild, 1902 (Hubbard, 1947; Jellison and Senger, 
1973; Senger, 1966) 

Megabothris abantis (Rothschild, 1905) (Egoscue, 1966; Hubbard, 1947; Jellison 
and Senger, 1973; Kinsella and Pattie, 1967; Ludwig, 1984) 

Megabothris asio (Baker, 1904) (Ludwig, 1984) 

Monopsyllus eumolpi (Rothschild, 1905) (Ludwig, 1984) 

Monopsyllus wagneri (Baker, 1904) (Allred, 1952) 

Nearctopsylla hyrtaci (Rothschild, 1904) (Ludwig, 1984) 

Opisodasys keeni (Baker, 1896) (Stark, 1959) 

Peromyscopsylla hamifer (Rothschild, 1906) (Ludwig, 1984) 

Peromyscopsylla hesperomys (Baker, 1904) (Hubbard, 1947) 

Peromyscopsylla selenis (Rothschild, 1906) (Gresbrink and Hopkins, 1982; Hop- 
kins and Rothschild, 1971; Hubbard, 1947; Ludwig, 1984) 

Stenoponia americana (Baker, 1899) (Hopkins and Rothschild, 1962) 

Thrassis alpinus Stark, 1957 (Senger, 1966) 


Microtus townsend 


Atyphloceras multidentatus (C. Fox, 1909) (Holland, 19495; Hoplins and Roth- 
schild, 1962; Hubbard, 1947; Macchiavello, 1954) 

Catallagia charlottensis (Baker, 1898) (Holland, 19495; Hopkins and Rothschild, 
1962; Hubbard, 1947; Macchiavello, 1954; Svihla, 1941) 

Catallagia scullent Hubbard, 1940 (Hopkins and Rothschild, 1962) 

Corrodopsylla curvata (Rothschild, 1915) (Hubbard, 1947; Macchiavello, 1954) 

Corypsylla ornata C. Fox, 1908 (Holland, 19496) 

Corypsylla kohlsi Hubbard, 1940 (Fox, 1940c [described as Corypsylloides spi- 
nata]; Macchiavello, 1954) 


Parasites 503 


Delotelis hollandi Smit, 1952 (Hopkins and Rothschild, 1962; Smit, 1952 [orig- 
inal description and type-host]) 

Delotelis telegoni (Rothschild, 1905) (Holland, 194965; Hubbard, 1947; Jellison 
and Senger, 1976; Macchiavello, 1954) 

Epitedia scapani (Wagner, 1936) (Hopkins and Rothschild, 1962; Hubbard, 
1947; Macchiavello, 1954) 

Hystrichopsylla dippier Rothschild, 1902 (Hubbard, 1947; Macchiavello, 1954; 
Svihla, 1941) 

Hystrichopsylla occidentalis Holland, 1949 (Holland, 1957; Hopkins and Roth- 
schild, 1962) 

Megabothris abantis (Rothschild, 1905) (Hubbard, 1947; Macchiavello, 1954; 
Svihla, 1941; Wagner, 1936a) 

Megabothris quirini (Rothschild, 1905) (Hubbard, 1947) 

Monopsyllus wagner: (Baker, 1904) (Hubbard, 1947; Macchiavello, 1954) 

Opisodasys keen (Baker, 1896) (Holland, 19496; Macchiavello, 1954) 

Peromyscopsylla hesperomys (Baker, 1904) (Hubbard, 1947; Macchiavello, 1954) 

Peromyscopsylla selenis (Rothschild, 1906) (Hopkins and Rothschild, 1971; Svih- 
la, 1941) 

Rhadinopsylla sectilis Jordan and Rothschild, 1923 (Hopkins and Rothschild, 
1962; Hubbard, 19416, 1947 [reported as Muicropsylla goodi]; Macchia- 
vello, 1954) 


Directions for Future Research 


A review of the literature on parasites of North American M:- 
crotus contains over 485 primary references covering the 91-year 
period from 1894 to 1984. Most of these papers deal with the 
taxonomy of the various groups of parasites and their distribution 
on the hosts. Surprisingly, with this wealth of literature, we actually 
know very little about the biology of parasites on Microtus. Future 
research on systematic problems of many of the groups of parasites 
is needed, most especially of the mites, the most diverse and poorly 
known of the parasitic groups. 

One of the most productive areas for future research will be 
exploring aspects of the biology of hosts and parasites from an 
evolutionary perspective. Future research should address co-evolu- 
tion in the broadest sense between hosts and parasites, including 
co-accommodation, co-adaptation, and co-speciation. One of the most 
challenging, yet most fruitful directions will be in statistical quan- 
tification of the cost of parasitism. Hopefully, future studies will be 
able to directly or indirectly measure increased or decreased repro- 
ductive success by both host and parasites. Such questions might 
include: 1) What are the selective forces exerted by the host on the 


504 Timm 


parasites, and conversely, what are the selective forces exerted by 
the parasites on the host? 2) What is the cost of parasitism to the 
host? 3) How are the reproductive cycles of the parasites cued to 
the reproductive cycle of the host? 4) What is the role of parasites 
in the epidemiology of diseases among hosts? 5) Can parasites affect 
the behavior of the host? 6) Is there a genetic basis for resistance 
to parasitic infections by the host, and can this be selected for? 7) 
Can parasites play a role in regulating host populations? and 8) 
Can parasites or the diseases transmitted by them be responsible 
for delineating geographic ranges of species? Certainly we would 
expect massive infestations of parasites to alter the behavior or 
reproductive cycle of the host, but given lower “normal” levels of 
infestation, can the host be altered in more subtle ways through 
hormonal imbalance, odors, etc? The rapidly expanding field of 
biogeography has provided interesting and potentially productive 
directions for future studies in parasitology. The application of is- 
land biogeography theory to host-parasite systems leads to questions 
such as: Can an individual host, a population, or entire species be 
viewed as an island for parasites? 

The study of parasites has been a part of both our basic and 
applied sciences for decades, yet it is still an extremely fruitful area 
of future research. There remains much to learn about the biology 
of Microtus with respect to its parasites and about the biology of 
those parasites. 


Acknowledgments 


I thank A. H. Benton, J. B. Kethley, B. M. OConnor, R. L. 
Wenzel, and J. O. Whitaker for freely sharing with me their knowl- 
edge of and literature on parasites. B. L. Clauson, R. H. Tamarin, 
and J. O. Whitaker reviewed, in detail, the entire manuscript; R. 
L. Rausch reviewed the section on endoparasites and provided nu- 
merous references. J. S. Ashe reviewed the section on parasitic 
beetles. J. Shaw provided much assistance in locating obscure ref- 
erences. 


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Appendix A. Endoparasites 


Acanthocephalans 


Microtus ochrogaster 


Moniltformis clarkt (Ward, 1917) (Fish, 1972) 


Parasites 529 


Microtus pennslyvanicus 
Moniliformis clarki (Ward, 1917) (Benton, 1954; Fish, 1972) 
Polymorphus paradoxus Connell and Corner, 1957 (Platt, 1978) 
Microtus pinetorum 
Moniliformis clarki (Ward, 1917) (Benton, 1954, 1955a; Fish, 1972; Van Cleave, 
1953) 


Cestodes 


Microtus abbreviatus 
Andrya arctica Rausch, 1952 (Rausch and Rausch, 1968) 
Andrya macrocephala Douthitt, 1915 (Rausch and Rausch, 1968) 
Paranoplocephala infrequens (Douthitt, 1915) (Rausch and Rausch, 1968) (=Anop- 
locephaloides sp.; A. infrequens as presently understood is restricted to pocket 
gophers; at least two species of morphologically similar cestodes of the genus 
Anoplocephaloides occur in voles in the Arctic [R. L. Rausch, pers. comm.]) 
Paranoplocephala omphalodes (Hermann, 1783) (Rausch, 1976; Rausch and Rausch, 
1968) 
Taenia crassiceps (Zeder, 1800) (Rausch and Rausch, 1968) (larval stage) 
Microtus breweri 
Andrya macrocephala Douthitt, 1915 (Winchell, 1977) 
Microtus californicus 
Andrya macrocephala Douthitt, 1915 (Rausch, 19526; Voge, 1948 [reported as 
A. kirbyt]) 
Microtus chrotorrhinus 
Andrya macrocephala Douthitt, 1915 (Martin, 1972; Schad, 1954) 
Hymenolepis horrida (von Linstow, 1901) (Schiller, 1952a) 
Taenia crassiceps (Zeder, 1800) (Martin, 1972) (larval stage) 
Microtus longicaudus 
Andrya communis Douthitt, 1915 (Rankin, 1945) (=A. primordialis Douthitt, 1915) 
Hymenolepis diminuta (Rudolphi, 1819) (Rankin, 1945) 
Hymenolepis horrida (von Linstow, 1901) (Kinsella, 1967; Kuns and Rausch, 1950; 
Schiller, 1952a) 
Paranoplocephala infrequens (Douthitt, 1915) (Kinsella, 1967; Kuns and Rausch, 
1950) (=Anoplocephaloides troeschi Rausch, 1946) 
Taenia mustelae Gmelin, 1790 (Kinsella, 1967) (larval stage) 
Microtus mexicanus 
Paranoplocephala infrequens (Douthitt, 1915) (Rausch, 1952a)(=A. troeschi) 
Muicrotus miurus 
Andrya arctica Rausch, 1952 (Rausch, 1952a [original description]) 
Hymenolepis horrida (von Linstow, 1901) (Schiller, 1952a) 
Paranoplocephala infrequens (Douthitt, 1915) (Rausch, 1952a) (=Anoplocephaloides 
sp.) 
Paranoplocephala omphalodes (Hermann, 1783) (Rausch, 1952a, 1976) 
Taenia tenuicollis Rudolphi, 1809 (Rausch, 1952a) (=7. mustelae) (larval stage) 
Maicrotus montanus 
Andrya communis Douthitt, 1915 (Rankin, 1945) (=A. primordialis Douthitt, 1915) 
Andrya macrocephala Douthitt, 1915 (Kinsella, 1967; Kuns and Rausch, 1950) 


530 Timm 


Andrya primordialis Douthitt, 1915 (Kuns and Rausch, 1950) 

Hymenolepis horrida (von Linstow, 1901) (Kuns and Rausch, 1950; Schiller, 1952a) 

Paranoplocephala infrequens (Douthitt, 1915) (Kinsella, 1967; Kuns and Rausch, 
1950; Rausch, 1952a, 1976) (=A. troescht) 

Microtus ochrogaster 

Andrya macrocephala Douthitt, 1915 (Hansen, 1947 [reported as A. microti, 1950]; 
Lubinsky, 1957) 

Choanotaenia nebraskensis Hansen, 1950 (original description) 

Choanotaenia sp. (Rausch and Tiner, 1949) 

Hymenolepis horrida (von Linstow, 1901) (Schiller, 1952a) 

Hymenolepis sp. (Rausch and Tiner, 1949) 

Paranoplocephala borealis (Douthitt, 1915) (Rausch, 1952a) (=Anoplocephaloides 
sp.) 

Paranoplocephala infrequens (Douthitt, 1915) (Hansen, 1950; Whitaker and Adalis, 
1971) (=A. troescht) 

Paranoplocephala troeschi Rausch, 1946 (Whitaker and Adalis, 1971) (=A. troescht) 

Paranoplocephala sp. (Rausch and Tiner, 1949) (=Anoplocephaloides sp.) 

Taenia mustelae Gmelin, 1790 (Lubinsky, 1957 (larval stage) 

Taenia taeniaeformis (Batsch, 1786) (Rausch and Tiner, 1949; Whitaker and Ad- 
alis, 1971) (larval stage) 

Microtus oeconomus 

Andrya macrocephala Douthitt, 1915 (Rausch, 1952a) 

Echinococcus granulosus (Batsch, 1786) (Rausch and Schiller, 1951) 
(=E. multilocularis; larval stage) 

Echinococcus multilocularis Leuckart, 1863 (Ohbayashi, 1971; Vogel, 1957) (larval 
stage) 

Echinococcus sibiricensis Rausch and Schiller, 1954 (Rausch and Schiller, 1954 
[original description], 1956) (=E. multilocularis; larval stage) 

Echinococcus sp. (Rausch, 1952a; Rausch and Schiller, 1951) (=E. multilocularis; 
larval stage) 

Paranoplocephala infrequens (Douthitt, 1915) (Rausch, 1952a, 1957) (=Anoplo- 
cephaloides sp.) 

Paranoplocephala omphalodes (Hermann, 1783) (Rausch, 1976) 

Taenia polyacantha Leuckart, 1856 (Schiller, 1953) (larval stage) 

Taenia twitchelli Schwartz, 1924 (Rausch, 1977) (larval stage) 

Microtus pennsylvanicus 

Andrya communis Douthitt, 1915 (Douthitt, 1915 [original description]; Lubinsky, 
1957) (=A. primordialis) 

Andrya macrocephala Douthitt, 1915 (Hall and Sonnenberg, 1955; Kuns and Rausch, 
1950; Lubinsky, 1957; Mumford and Whitaker, 1982; Schad, 1954; Whitaker 
and Adalis, 1971) 

Andrya primordialis Douthitt, 1915 (Kuns and Rausch, 1950; Meggitt, 1924) 

Andrya sp. (Erickson, 19385; Hall and Sonnenberg, 1955) 

Cladotaenia globifera (Batsch, 1786) (Baron, 1971) (larval stage) 

Cladotaenia sp. (Whitaker and Adalis, 1971) 

Echinococcus multilocularis Leuckart, 1863 (Hnatiuk, 1966; Leiby, 1965; Leiby et 
al., 1970; Rausch and Richards, 1971) (larval stage) 


Parasites 531 


Hymenolepis evaginata Barker and Andrews, 1915 (Rausch and Tiner, 1949) 

Hymenolepis fraterna Stiles, 1906 (Rausch and Tiner, 1949) 

Hymenolepis horrida (von Linstow, 1901) (Kinsella, 1967; Lubinsky, 1957; Schill- 
er, 1952a) 

Hymenolepis johnsoni Schiller, 1952 (Rausch, 1952a; Schiller, 19526 [original de- 
scription and type-host]) 

Paranoplocephala borealis (Douthitt, 1915) (Rausch, 1952a) (=Anoplocephaloides 
sp.) 

Paranoplocephala infrequens (Douthitt, 1915) (Hall and Sonnenberg, 1955; Kin- 
sella, 1967; Kuns and Rausch, 1950; Lubinsky, 1957; Mumford and Whitaker, 
1982; Rausch, 1946, 1952a; Rausch and Schiller, 1949; Schad, 1954) (=A. 
troescht) 

Paranoplocephala troeschi Rausch, 1946 (Mumford and Whitaker, 1982; Rausch, 
1946 [original description and type-host], 1976; Rausch and Tiner, 1949) (=A. 
troescht) 

Paranoplocephala variabilis (Douthitt, 1915) (Kinsella, 1967; Lubinsky, 1957; Schad, 
1954) (=A. variabilis) 

Paranoplocephala sp. (Erickson, 1938a; Rausch and Tiner, 1949) (=Anoplocepha- 
loides) 

Paruterina candelabraria (Goeze, 1782) (Baron, 1971) (larval stage) 

Taenia crassiceps (Zeder, 1800) (Freeman, 1954, 1962; Leiby and Whittaker, 1966) 
(larval stage) 

Taenia mustelae Gmelin, 1790 (Lubinsky, 1957) (larval stage) 

Taenia taeniaeformis (Batsch, 1786) (Erickson, 19386; Kinsella, 1967; McBee, 1977; 
Rausch and Tiner, 1949) (larval stage) 

Taenia tenuicollis Rudolphi, 1809 (Schad, 1954) (=7. mustelae) 

Microtus pinetorum 

Hymenolepis pitymi Yarkinsky, 1952 (original description) 

Taenia taeniaeformis (Batsch, 1786) (Lochmiller et al., 19826) (larval stage) 

Taenia sp. (Erickson, 19385; Lochmiller et al., 19826; Whitaker and Adalis, 1971) 
(larval stage) 

Microtus richardsoni 

Andrya macrocephala Douthitt, 1915 (Kuns and Rausch, 1950) 

Andrya primordialis Douthitt, 1915 (Kuns and Rausch, 1950) 

Andrya sp. (Kuns and Rausch, 1950) 

Hymenolepis horrida (von Linstow, 1901) (Kuns and Rausch, 1950; Schiller, 1952a) 

Paranoplocephala infrequens (Douthitt, 1915) (Kuns and Rausch, 1950; Rausch, 
1952a) (=A. troescht) 

Microtus xanthognathus 
Taenia martis americana Wahl, 1967 (Rausch, 1977) (larval stage) 


Nematodes 


Microtus abbreviatus 
Heligmosomoides bullosus matthewensis Durette-Desset, 1967 (Durette-Desset, 1968) 
Heligmosomum nearcticum Durette-Desset, 1967 (Durette-Desset, 1968) 
Heligmosomum sp. (Rausch and Rausch, 1968) 


532 Timm 


Microtus californicus 
Heligmosomoides montanus Durette-Desset, 1967 (Durette-Desset et al., 1972) 
Pelodera sp. (Poinar, 1965) (larval stage in eyes) 

Microtus chrotorrhinus 

Capillaria hepatica (Bancroft, 1893) (Fisher, 1963) 

Chetropteranema sp. (Komarek and Komarek, 1938) 

Nematospiroides dubius Baylis, 1926 (Schad, 1954) 

Microtus longicaudus 

Aspiculuris tetraptera (Nitzsch, 1821) (Kinsella, 1967) 

Heligmosomoides microti (Kuns and Rausch, 1950) (Kinsella, 1967) 

Heligmosomoides montanus Durette-Desset, 1967 (Durette-Desset, 1968) 

Heligmosomum costellatum (Dujardin, 1845) (Kinsella, 1967) 

Mastophorus sp. (Kinsella, 1967) (=Protospirura sp.) 

Nematospiroides longispiculatus Dikmans, 1940 (Rausch, 1952a) (=Heligmoso- 
modes longispiculatus) 

Pelodera sp. (Kinsella, 1967) (larval stage in eyes) 

Syphacia obvelata (Rudolphi, 1802) (Kinsella, 1967; Rankin, 1945) (Quentin [1971] 
concluded that Syphacia nigeriana Baylis, 1928, is the only species of Syphacia 
parasitizing Microtus in North America; S. obvelata is restricted in occurrence to 
Rattus and perhaps other murids.) 

Microtus mexicanus 
Syphacia nigeriana Baylis, 1928 (Quentin, 1971) 
Microtus miurus 

Heligmosomum nearcticum Durette-Desset, 1967 (Durette-Desset, 1968) 

Rictularia microti McPherson and Tiner, 1952 (McPherson and Tiner, 1952 [orig- 
inal description]; Quentin, 1971) (=Pterygodermatites microtz) 

Rictularia sp. (Rausch, 1952a) 

Trichinella spiralis (Owen, 1835) (Rausch et al., 1956) (=7. nativa Britov and 
Boev, 1972) 

Muicrotus montanus 

Nematospiroides microti Kuns and Rausch, 1950 (Kinsella, 1967; Kuns and Rausch, 
1950 [original description]) (=Heligmosomoides micrott) 

Syphacia obvelata (Rudolphi, 1802) (Kinsella, 1967; Kuns and Rausch, 1950; Lei- 
by, 1962; Rankin, 1945) (=S. nigeriana ?) 

Microtus ochrogaster 

Boreostrongylus dikmansi Durette-Desset, 1974 (original description) 

Capillaria sp. (Dunaway et al., 1968) 

Longistriata carolinensis Dikmans, 1935 (original description) (=B. carolinensis) 

Syphacia obvelata (Rudolphi, 1802) (Rausch and Tiner, 1949) (=S. nigeriana ?) 

Trichuris sp. (Rausch and Tiner, 1949) 

Microtus oeconomus 

Heligmosomoides bullosus bullosus Durette-Desset, 1967 (Durette-Desset, 1968) 

Heligmosomum nearcticum Durette-Desset, 1967 (Durette-Desset, 1968) 

Pterygodermatites microti (McPherson and Tiner, 1952) (Quentin, 1971) 

Rictularia microti McPherson and Tiner, 1952 (original description) (=P. microtz) 

Sobolevingylus microti Rausch and Rausch, 1969 (original description and type- 
host) 

Syphacia nigeriana Baylis, 1928 (Quentin, 1971) 


Parasites yo}! 


Microtus pennsylvanicus 
Capillaria hepatica (Bancroft, 1893) (Freeman and Wright, 1960; Lubinsky et al., 
1971) 
Capillaria muris-sylvatic: (Diesing, 1851) (Rausch and Tiner, 1949) 
Dictyocaulus viviparus (Bloch, 1782) (Rausch and Tiner, 1949) 
Heligmosomoides longispiculatus (Dikmans, 1940) (Durette-Desset et al., 1972) 
Heligmosomoides wisconsinensis Durette-Desset, 1967 (Durette-Desset, 1968; Dur- 
ette-Desset et al., 1972) 
Heligmosomum costellatum (Dujardin, 1845) (Kinsella, 1967) 
Heligmosomum microti (Kuns and Rausch, 1950) (Kinsella, 1967; Kuns and Rausch, 
1950) (=Heligmosomoides microti) 
Heligmosomum nearcticum Durette-Desset, 1967 (Durette-Desset, 1968) 
Longistriata dalrymper Dikmans, 1935 (Dikmans, 1935 [original description]; 
Lichtenfels and Haley, 1968; Rausch and Tiner, 1949) 
Mastophorus muris (Gmelin, 1790) (Rausch and Tiner, 1949) (=Protospirura 
muris) 
Nematospira turgida Walton, 1923 (original description and type-host) 
Nematospiroides longispiculatus Dikmans, 1940 (original description) (=Heligmo- 
somoides longispiculatus) 
Nematospiroides sp. (Hall and Sonnenberg, 1955; Rausch and Tiner, 1949) (=He- 
ligmosomoides sp.) 
Oxyuris sp. (Stiles and Hassall, 1894) 
Rictularia coloradensis Hall, 1916 (Lubinsky, 1957) (=Pterygodermatites coloraden- 
SIS) 
Syphacia nigeriana Baylis, 1928 (Quentin, 1971) 
Syphacia obvelata (Rudolphi, 1802) (Erickson, 1938a, 19385; Kinsella, 1967; Kuns 
and Rausch, 1950; Rausch and Tiner, 1949; Schad, 1954) (=S. nigeriana ?) 
Syphacia sp. (Hall and Sonnenberg, 1955; Lichtenfels and Haley, 1968) 
Trichinella spiralis (Owen, 1835) (Holliman and Meade, 1980) 
Trichuris opaca Barker and Noyes, 1915 (Hall and Sonnenberg, 1955; Lichtenfels 
and Haley, 1968; Rausch and Tiner, 1949) 
Trichuris sp. (Hall and Sonnenberg, 1955) 
Microtus pinetorum 
Capillaria gastrica (Baylis, 1926) (Lochmiller et al., 1982a) 
Oxyuris sp. (Stiles and Hassall, 1894) 
Trichinella spiralis (Owen, 1835) (Zimmermann, 1971) 
Trichuris opaca Barker and Noyes, 1915 (Hall and Sonnenberg, 1955) 
Trichuris sp. (Benton, 1955a) 
Microtus richardsoni 
Nematospiroides microti Kuns and Rausch, 1950 (original description) 
Syphacia obvelata (Rudolphi, 1802) (Kuns and Rausch, 1950) (=S. nigeriana ?) 
Trichuris opaca Barker and Noyes, 1915 (Kuns and Rausch, 1950) 


Trematodes 


Microtus miurus 


Brachylaima rauschi McIntosh, 1951 (Rausch, 1952a) 


534 Timm 


Microtus montanus 
Quinqueserialis hassalli (McIntosh and McIntosh, 1934) (Kuns and Rausch, 1950) 
(=Q. quinqueserialis; Barker and Laughlin, 1911) 
Microtus oeconomus 
Quinqueserialis quinqueserialis (Barker and Laughlin, 1911) (Rausch, 1952a) 
Microtus pennsylvanicus 

Brachylaima sp. (Rausch, 1952a) 

Entosiphonus thompsoni Sinitsin, 1931 (Rausch and Tiner, 1949) 

Mediogonimus ovilacus Woodhead and Malewitz, 1936 (Rausch and Tiner, 1949; 
Woodhead and Malewitz, 1936 [original description]) 

Monostomum sp. (Stiles and Hassall, 1894) 

Plagiorchis muris Tanabe, 1922 (Kinsella, 1967; Schad, 1954) 

Quinqueserialis hassalli (McIntosh and McIntosh, 1934) (Harwood, 1939; Kuns 
and Rausch, 1950; McIntosh and McIntosh, 1934 [original description and type- 
host]; Rausch, 1952a; Rausch and Tiner, 1949) (=Q. quinqueserialis) 

Quinqueserialis quinqueserialis (Barker and Laughlin, 1911) (Edwards, 1949; Har- 
rah, 1922; Kinsella, 1967; Rausch, 1952a; Schad, 1954) 

Schistosomatium douthitti (Cort, 1915) (Price, 1931; Zajac and Williams, 1980, 
1981) 


PREDATION 
OLIVER P. PEARSON 


Abstract 


ICROTUS is killed and eaten by an enormous variety of verte- 
M brates of every class and of every size from shrews to bears. 
Some of its predators are generalists that consume numerous other 
kinds of prey, and some specialize on Microtus. Microtus is palatable 
to generalists and specialists alike, and, since it chooses to live in 
relatively open habitats, each individual is so vulnerable that the 
entire population is at risk. 

Most hawks are generalists, but several species of owls and kites 
are specialists on Microtus. One specialist (a male white-tailed kite) 
needed to hunt only an average of 8 min to catch a mouse. By 
hunting less than 20% of the daylight hours, he caught 21 mice in 
one day. 

Raptors frequently establish themselves in regions where Micro- 
tus is abundant; in such places raptor assemblages may reach den- 
sities as high as one raptor to each 1,300 Microtus. The impact of 
an individual raptor on a Microtus population can be estimated by 
the following relationship between body weight of the raptor and 
number of 35-g Microtus consumed/raptor/km? per day: 


Zl 
Wt?-°? 


Populations of raptors respond to changes in abundance of M:- 
crotus by adjusting their use of alternative prey (functional re- 
sponse) or by a numerical response achieved by immigration-emi- 
gration or by changes in nesting attempts and nesting success. 

Among mammalian predators, ermines (Mustela erminea) are 
Microtus specialists. In one study, 99% of their diet consisted of 
Microtus, which precluded a functional response; the numerical re- 
sponse resulted in ratios of as few as 42 voles/ermine to as many 
as 800. In another study of the impact of an assemblage of middle- 
sized, generalist carnivores during three cycles of Microtus abun- 
dance, the numerical response of the carnivores was between 6 and 


535 


Impact = 


536 Pearson 


47-fold and the functional response between 2.7- and 5.2-fold. The 
numbers of mice per carnivore varied from 5,400 during the in- 
crease phase of the vole cycle (very low predation pressure) to 24 
near the end of a crash (very high predation pressure). The desta- 
bilizing effect of such shifts in predation pressure suggests that 
carnivore predation may actually cause the multi-year Muicrotus 
cycles of abundance. 

Fishes, amphibians, and reptiles all prey on Microtus, but the 
intensity of this predation has been measured only for a few species 
of snakes. In one study, copperheads (Ancistridon) ate about 20 30-g 
Microtus/ha/year. Two of 14 other species of snakes in the same 
area were important predators on Microtus also. 

The summed effort of the numerous predators removes enormous 
numbers of Microtus from the population, but we are only begin- 
ning to measure the demographic results and to speculate about 
what strategies Microtus is using to minimize the impact of pred- 
ators. 


Introduction 


It is possible to find in nature an array of predator-prey systems 
that range from clumsy to deadly efficient. One end of the spectrum 
might be the predation of rats on humans. Every year, a few ne- 
elected babies or incapacitated adults are attacked by rats. Near the 
middle of the spectrum lies the mink-muskrat system in which mink 
capture primarily surplus muskrats, described by Errington (1946) 
as “a harassed and battered lot congregating about the fringes of 
areas dominated by muskrats already in residence.” At the deadly 
efficient end of the spectrum lie several systems involving Microtus, 
such as kite-Microtus and short-tailed weasel-Microtus systems. In 
fact, Microtus is sometimes so easy to capture that some species of 
predators catch not just the homeless and maladjusted but practi- 
cally every one. No terrestrial or avian predator is too large to prey 
on Microtus, and almost every predator large enough to subdue a 
Microtus does so occasionally, from 10-g shrews (Hamilton, 1940) 
to ospreys (Proctor, 1977) to grizzly bears (Sheldon, 1930). I do 
not try to document all of this carnage but mention a few of the 
interesting extremes and concentrate on examples that give excep- 
tional insight into the interaction between predator and prey, ex- 
amples in which an attempt was made to measure the intensity of 


Predation 537 


predation, and examples that contain information on the functional 
and numerical responses of a predator species. By functional re- 
sponse I mean change in the number of Microtus killed per unit 
time per individual predator, and by numerical response I mean 
change in the density of a population of predators in response to 
change in the density of Microtus (Holling, 1959). 

The reader will note that studies of predation on Microtus have 
not reached a sophisticated level. We are emerging from a century 
of reports on the contents of owl pellets (in which Microtus is fre- 
quently dominant), but we have barely begun to learn what seg- 
ments of vole populations are most vulnerable to which predators, 
what is the impact of different predators on vole densities in dif- 
ferent habitats or different seasons, and how voles have adapted 
their individual life styles and their social systems in response to 
what appears to be a vulnerability unusually high among mammals. 
Progress has been slow because of the difficulty of measuring the 
abundance and the hunting range of different predators, and of 
measuring the demographics of the Muicrotus populations them- 
selves. Such difficulties have not even permitted us to reach agree- 
ment on one of the central themes of microtine biology: the causa- 
tion of the multi-annual cycle of abundance observed in many 
populations of microtines. 


Predation by Birds 


An assortment of non-raptors is known to catch and eat Microtus, 
such as jays, crows, ravens, shrikes, gulls, and herons, but rarely 
does Microtus make up a large proportion of their diet. Shrikes, for 
example, seem to attack unselectively almost anything that moves, 
provided it is within a reasonable (but great) size range (Miller, 
1931). Under special circumstances some of these raptors may even 
consume a lot of mice, such as when gulls and crows follow the 
cutters in fields of artichokes infested with 1,000 or more Microtus 
californicus per ha (Gordon, 1977), or when large flocks of ravens 
select Microtus out of a mixed plague of Mus and Microtus (Hall, 
1927), but rarely do these non-raptor generalists have an important 
impact on Microtus populations. Even among the raptors themselves 
(hawks, owls, and kites) only a handful of species specialize year- 
round in the capture of mice. Snyder and Wiley (1976) listed the 
categories of prey captured by 44 species of raptors. More than 90% 


538 Pearson 


of the captures of eight of them consisted of mammals, usually mice, 
frequently Microtus. These eight species were the barn owl, great 
grey owl, hawk owl, long-eared owl, short-eared owl, saw-whet 
owl, boreal owl, and white-tailed kite. The diet of four other species 
of raptors was more than 50% mammal (ferruginous hawk, 85%; 
golden eagle, 72%; rough-legged hawk, 62%; and red-tailed hawk, 
51%), but the Microtus content of some of these would not be ex- 
pected to be high. I describe below a predator-prey system in which 
an entire assemblage of species of raptors seems to concentrate on 
Microtus, and another system in which the existence of one of the 
raptor species seems to depend completely on Microtus even though 
the diet is not entirely Microtus. 


Raptor Assemblages 


The most ambitious and most convincing measurement of the 
impact of avian predators on microtine populations were made in 
Michigan on a 93-km? township devoted primarily to dairy farming 
(Craighead and Craighead, 1956). The township consisted of wood- 
land (11% of the area), fields, and wet areas. An overwintering 
assemblage of raptors fed primarily on Microtus and was then large- 
ly replaced by a nesting assemblage. Raptors were censused visually 
while they were hunting or at their roosting or nesting sites. M:- 
crotus was censused on sample areas, then the population of the 
entire area was calculated taking into account the extent of the 
different qualities of Microtus habitat and the relative abundance 
of voles in each kind. During the autumn and winter of 1941, a 
year of Microtus abundance, good habitat was estimated to support 
343 Microtus pennsylvanicus/ha and the entire 93-km? study area 
a total of 303,000 Microtus. Six species of hawks and four species 
of owls preyed on this population. 

Table 1 illuminates some of the details of this unusually well- 
documented predation. During winter of 1942, 159 raptors preyed 
heavily on the abundant vole population, and Microtus made up 
87% of their diet. During the ensuing summer, voles made up only 
28% of the diet of the 63 pairs of breeding raptors. During winter 
of 1948, when voles were only one-quarter as abundant as before, 
the much-reduced raptor population (59 birds) included only 55% 
Microtus in its diet. This indicates both a numerical response and 
a functional response to Microtus abundance that resulted in a five- 
fold difference in the total number of Muicrotus eaten. In summer 


539 


Predation 


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540 Pearson 


of 1948 a raptor assemblage of about the same size as that in 1942 
included about the same proportion of Microtus in its diet. Since 
each individual and each species of the winter assemblage of raptors 
was feeding heavily on Muicrotus, the most timely information for 
every Microtus when it left its safe retreat was: how many of “us” 
are there and how many of “them”? This Microtus-raptor ratio 
during the winter of mouse abundance was about 2000:1. During 
the winter of lower Microtus density, the ratio was about 1300:1. 
Note that this lower number represents a moderately higher pre- 
dation pressure. In other words, predation pressure measured in 
this way (numerical ratio of mice to raptors) was greater in the 
winter of 1948 in spite of the fact that the raptors ate only one- 
fifth as many Microtus. In both winters they ate roughly the same 
proportion of the Microtus crop (26% in 1942 and 22% in 1948). 

The Craigheads emphasized the around-the-clock danger to M:- 
crotus from the diurnal hawk assemblage and the nocturnal owl 
assemblage. They also estimated the abundance of seven species of 
mammalian carnivores (fox, opossum, raccoon, skunk, badger, wea- 
sel, and mink), totalling between 277 and 346 individuals in the 93- 
km? township, and stated that during winter of 1941-1942 these 
carnivores were feeding largely on Microtus. They did not attempt 
to calculate the impact of these carnivores, but from metabolic con- 
siderations it is obvious that the carnivores were probably consum- 
ing as many Muicrotus as were the raptors. Their report did not 
include house cats, whose impact also may be considerable (see 
below). 

The data of Baker and Brooks (1981, 1982) in a study of over- 
wintering rough-legged and red-tailed hawks near the Toronto air- 
port confirm that the abundance of raptors reported by the Craig- 
heads is not unique. Muicrotus pennsylvanicus was present at 
measured densities about the same as on the best Microtus habitat 
on the Craigheads’ study area in Michigan during the winter of 
1942, and the two species of hawks had established themselves at 
Toronto at densities (0.33 to 0.72/ha) three to five times as great 
as the hawk assemblages on the study area in Michigan, or two to 
four times as dense as the entire raptor assemblage in Michigan. 
The greater density at Toronto was presumably made possible by 
the fact that three-fourths of the 827-ha study area consisted of 
good Microtus habitat undiluted by woodlots. My calculations of 
the predation pressure of these two species of hawks at Toronto fall 


Predation 541 


between 1,300 and 3,000 voles/hawk, which brackets the total pres- 
sure (1,905/raptor) in Michigan. The overwinter raptor catch ac- 
counted for 19% of the population loss during that period. The 
authors stated that diurnal raptor predation of this magnitude is 
not important in vole declines. 

There are many other reports of winter concentrations of avian 
predators on Muicrotus-rich areas. Many of these concern species 
that breed in the north and congregate farther south in winters 
following peak population of voles and lemmings. Davis (1937), for 
example, reported conspicuous 3- or 4-year peaks in the number of 
northern shrikes reported on Christmas bird counts in New En- 
gland, and noted that this cycle agreed exactly with maxima in the 
number of arctic fox pelts marketed. The fox population presum- 
ably was reflecting vole or lemming abundance in northern Canada. 
Snowy owl “invasions” during winter frequently have been related 
to the collapse of microtine populations in the north (Gross, 1947). 
These emigrant owls frequently establish themselves in regions 
where Microtus is available. An especially impressive winter assem- 
blage of owls was noted during the winter of 1978-1979 on 60-km’ 
Amherst Island in Lake Ontario (Sayr, 1980). The meadow vole 
population had exploded in the autumn, and owls were abundant 
throughout the winter. In March a census revealed 34 great gray 
owls, 22 long-eared owls, 20 short-eared owls, 13 snowy owls, and 
a dozen other owls of six different species, giving a total of .017 
owls/ha (one owl/59 ha). During the same winter great gray owls 
appeared on Neebish Island in Michigan, where they readily cap- 
tured Microtus through a considerable snow cover (Master, 1979). 
Pellets indicated a diet of 96% Mucrotus pennsylvanicus and 4% 
short-tailed shrews (Blarina brevicauda). 


Kites 


White-tailed kites (Elanus leucurus) prey almost entirely on small 
mammals, primarily Microtus, and are noted for being responsive 
to the abundance of Microtus (Waian and Stendell, 1970). They 
frequently remain at the same place all year long. Stendell (1972) 
took advantage of the relative ease of observing and censusing kites 
to provide many insights into the machinery of predation by this 
species. The kites studied were living on three islands in an area of 
rotational agriculture. The two most vulnerable and probably most 


542 Pearson 


abundant prey species, estimated from nearly 6,000 mice in pellets, 
were Microtus californicus (75% by frequency and 89% by biomass) 
and Mus musculus (21% frequency and 9% biomass). Relative num- 
bers of Microtus in the fields over which the kites were hunting 
were estimated during a 22-year period by a combination of counts 
of active runways, live-trapping, and grid-trapping, and were re- 
lated to the abundance of kites. Fluctuations in the number of M:- 
crotus tended to be approximately synchronous, but local highs of 
Mus could always be found. On Grizzly Island the numbers of mice 
trapped were 1,010 Microtus, 1,614 Mus, 22 Reithrodontomys, and 
3 Sorex. Mus may be the most abundant species but it apparently 
is not the preferred prey. The number of kites preying on these 
mice on Grizzly Island, which has a total area of 3,500 ha of which 
1,400 ha are suitable Microtus habitat, varied from three nesting 
pairs one year to 20 nesting pairs the next. The peak population 
was 72 kites, which then dropped to 10. The numerical interaction 
can be traced in Fig. 1 (top). While the Microtus population in- 
creased about five- or six-fold, the kite population increased by the 
same amount, initially by immigration, then by reproduction. Dur- 
ing the decline of the vole population, kite numbers remained sur- 
prisingly stable until the Microtus density became very low. At this 
time the kite population decreased rapidly as a result of emigration 
and mortality. Note (Fig. 1, top) the important role that was played 
at this time by Mus serving as an alternative prey. They probably 
kept the kites from leaving the area until the Microtus had declined 
to a very low density. 

Figure 1 (bottom) shows that Microtus made up at least 40% of 
the kite diet throughout the vole cycle, that it increased to about 
80-85% when Microtus was at its peak, and that it remained above 


= 


Fic. 1. Top: numerical response of a population of white-tailed kites to one cycle 
of abundance of Microtus californicus. The solid line and closed circles indicate re- 
sponse during the increase phase of the vole cycle; dashed line and open circles 
represent response during the decline phase; circled points indicate periods when 
large numbers of house mice (Mus musculus) were taken by kites. Bottom: functional 
response of a population of white-tailed kites to one cycle of abundance of Microtus 
californicus. The percentage differences between the indicated values and 100% were 
made up almost entirely by Mus musculus. Graphs are modified slightly from Stendell 
(1972). 


Number of Kites 


Voles in Pellets (%) 


80 


ee eo a _-decline phase 


6 9% Pec sad 

e) r) 
/ 
J 


Predation 


e 
vie 
“increase phase 


100 


10 20 30 40 a0) 60 
Stations with Active Runways (%) 


(= ABUNDANCE OF VOLES) 


decline phase 


10 20 30 40 50 60 
Stations with Active Runways (%) 


(= ABUNDANGE OF VOLES) 


543 


544 Pearson 


80% of the diet throughout much of the collapse of the vole popu- 
lation. Because the number of kites remained high during much of 
the decline of Microtus, and because the percentage of Microtus in 
the diet remained high also, it is obvious that as the Microtus pop- 
ulation collapsed the intensity of kite predation increased to about 
five times as much as it was when the vole population was beginning 
to increase. Other species of predators were present also, of course. 
For example, at dusk on a summer evening on 1,400-ha Jersey 
Island about 30 kites were hunting over a large field that contained 
an abundant population of Microtus but no Mus. Immediately after 
dusk, at least 10 barn owls were observed in the same area. These 
two species of raptors together must have been taking about 120 
Microtus/day, which would be the equivalent of the standing crop 
of a dense Microtus population on 0.5 ha. 

When Microtus was abundant on Grizzly Island in the summer 
of 1970, Stendell (1972) counted 50 kites, between 50 and 60 marsh 
hawks, between 35 and 40 short-eared owls, and as many as 8 barn 
owls. Although the island is not effectively isolated from the main- 
land, and therefore one cannot assume that all of the raptors were 
obtaining all of their food from the 1,400 ha of suitable Microtus 
habitat on the island, there can be no doubt that every Microtus 
had reason for concern because roughly 150 very competent raptors 
were hunting over 1,400 ha of mouse habitat—one raptor for each 
Or hia. 

The effectiveness of kites as Microtus hunters is documented by 
the performance of a male kite that was watched all day. He was 
hunting over a field that supported approximately 346 Microtus/ 
ha. He supplied almost all of the food for himself, his mate, and 
five 4-week-old nestlings. During his 899-min day he made 38 
hunting flights, 21 of which were successful (17 Microtus and four 
Mus). He needed an average of only 8 min to catch a mouse. One 
mouse was taken from him by a marsh hawk. Note that he was 
able to catch this many mice by hunting less than 20% of his total 
time during daylight hours (Table 2). Other species of raptors also 
find mouse-catching easy. A pair of barn owls brought an average 
of 1.8 mice/h to the nest (Smith et al., 1974). 

Stendell showed that most of the changes in density of kites oc- 
curred immediately prior to or during their breeding season. Num- 
bers at other times of the year were relatively stationary. Vole 
density during the initial stages of the kite nesting season deter- 


Predation 545 


TABLE 2 
ACTIVITY BUDGET OF A MALE KITE THROUGHOUT A Day IN WHICH HE MADE 38 
HUNTING FLIGHTS AND CAUGHT 17 Microtus AND 4 Mus (FROM STENDELL, 1972) 


Percent of 

Activity Time (min) total time 
Perched 681 75.8 
Flight (total) (218) 24.2 
Hunting 168 18.8 
Near nest 22 2.4 
Aggressive 6 0.6 
Courtship 3 0.3 
Miscellany* 19 2A 
Total 899 100.0 


* Mostly flights between perches. 


mined whether the kites remained in an area. In a year of dimin- 
ishing Microtus density, a population of 68 kites in late January 
decreased to 24 in mid-February and to less than 12 after April 1. 
Nesting success, however, was not lower in low vole years, but 
during vole abundance many pairs of kites fledged two broods. It 
is apparent, therefore, that the numerical response of kites to the 
highly fluctuating abundance of Microtus stems from both immi- 
gration—emigration and reproduction, and that the kite strategy is 
one of nomadism rather than site faithfulness. Long-term survival 
of kite populations depends upon asynchrony of the vole population 
over extensive areas and the kite’s ability to find local vole highs. 

In a quite different habitat at the Hastings Natural History Re- 
servation in California, a small number of kites hunted over grassy 
fields in which censuses of Microtus were being carried out (Stendell 
and Myers, 1973). During three successive summers in which den- 
sities of Microtus were 62/ha, 11/ha, and less than 2/ha, the pro- 
portion of Microtus in kite pellets remained above 83%. No Mus 
were present, but alternative prey were gophers, harvest mice, kan- 
garoo rats, pocket mice, birds, and insects. The kites persisted in 
hunting over the fields with Microtus densities lower than 2/ha and 
apparently survived by spending more time hunting for each mouse 
captured. 

Warner and Rudd (1975) studied kites hunting over agricultural 
land in central California and confirmed the ease with which cap- 
tures are made. During April and May when a male was supplying 


546 Pearson 


food for his mate and nestlings, he spent 15% of the day hunting, 
but later when males and females were hunting independently, they 
each spent only 5% of the day hunting. Thirty-nine percent of the 
hunting forays, which lasted an average of 6.1 + SE 0.7 min each, 
ended in a successful strike, and 63% of all strikes were successful. 
Half of the hunts were within 0.1 km of the nest tree, and 96% 
were within 1 km. 


Other Birds 


Boonstra (1977) gave information on the minimum amount of 
predation on a population of Microtus townsend living on an island 
near Vancouver. He marked almost all of the Microtus on three 
study grids with metal ear tags and looked for the tags in the pellets 
and feces of predators. He listed short-eared owls, great-horned 
owls, snowy owls, barn owls, marsh hawks, rough-legged hawks, 
red-tailed hawks, northern shrikes, great blue herons, cats, and 
raccoons. The latter two were destroyed on sight. His Table 2 
shows recovery of 3.1%, 5.9%, and 7.4% of the ear tags from mice 
that disappeared from the three grids during winter of 1972-1973, 
30.3% of those disappearing between October and December, 1973, 
and 19% of those disappearing between December of 1973 and 
April of 1974. Beacham (1979) carried out a similar study on a 
nearby island in 1977 and reported that the proportion of loss 
accounted for tended to be between 10 and 15% (10 to 15% of the 
tags were actually recovered). The intensity of predation was di- 
rectly proportional to the size of the Microtus population. He also 
supplied some of the best evidence concerning what segments of the 
Microtus population suffered the most severe predation. Small males 
tended to be the animals most likely to be caught by avian predators, 
whereas large females were least likely. The average duration of 
life, measured as the time between first and last capture, was higher 
in females (21.1 weeks) than in males (18.0 weeks). This is con- 
sistent with the predator selection of smaller and presumably youn- 
ger males. He attributed most of the predation to great blue herons 
and marsh hawks. On one occasion he saw seven herons on his 
0.84-ha trapping area. 

I have cited a number of studies that document a numerical 
response of raptors to changes in vole numbers, but none of them 
illuminates the role played by nesting in the numerical response as 


Predation 547 


effectively as a 16-year study by Hamerstrom (1979). She measured 
relative abundance of Microtus pennsylvanicus as it went through a 
series of population cycles. In spite of the fact that marsh hawks 
have a widely varied diet, the number of their nests increased dra- 
matically (2.7-fold) in years when vole numbers were high, and 
only in those years. The actual number of marsh hawks varied less 
(1.4-fold), probably because a smaller proportion of them nested 
during Microtus lows than at highs. Nesting success of the hawks 
was 62.1% at vole lows and 83.1% at highs, but the number of 
young per successful nest remained at 3.1 during highs and lows. 
Nevertheless, the total production of young hawks per unit area 
increased about 3.6-fold during Microtus highs. Some other species, 
such as kites (Stendell, 1972) and barn owls (Wallace, 1948), in- 
creased production of young during Muicrotus highs by repeat nest- 
ing. 

Owls locate their prey by sight when light is adequate—and it 
usually is. Great-horned owls and barn owls can see a dead mouse 
at light intensity of 13 x 10~° foot candles (Marti, 1974), which is 
about half as bright as a clear starlit night without any moon. A 
long-eared owl can see a dead mouse at 70 x 10~* foot candles 
(Marti, 1974), which is about as bright as in a forest on a hazy, 
moonless night. Burrowing owls, which are rather crepuscular, need 
about six times as much light as barn owls. All four of these species 
can also locate and capture live mice in total darkness. Payne (1962) 
and Konishi (1973) described the remarkable skill of barn owls in 
this kind of passive acoustical localization. Owls also are equipped 
with plumage that muffles their flight. This presumably prevents 
their prey from hearing their approach and at the same time may 
prevent interference with their own acoustical detection of noises 
made by the prey. 


Raptor Impact 


I noted above various examples of the pressure of raptors on 
Microtus populations. As a result of the fact that home ranges of 
raptors and food consumption are both closely related to body weight, 
it becomes possible to make a useful estimate of the impact of each 
individual raptor on a population of Microtus. Using the data in 
Newton’s (1979) Fig. 10 of home ranges of pairs of hawks plotted 
against body weight (in g), I calculated a relationship: 


548 Pearson 


Home range per 


oh bel ie cna .00026 x Wt!” (1) 


The slope of this curve is very close to that calculated by Schoener 
(1968) for predatory birds and by Harestad and Bunnell for mam- 
mals (1979). See also Jenkins (1981). 

From data given by Brown and Amadon (1968), Craighead and 
Craighead (1956), and Graber (1962), I calculated that for 17 species 
of raptors ranging in size from saw-whet owl to eagle: 


Number of Microtus consumed _ 0315 x W079 (2) 
per bird per day 


I assumed an average body weight of 35 g/Muicrotus, and where 

appropriate have allowed for discard of stomach and intestines of 

each Microtus (12% of body weight according to Stendell, 1972). 
Combining equations (1) and (2): 


Impact (number of Microtus consumed __ 121 
per bird per km? per day) Wt? 


(3) 


The number emerging from this equation is based on the assump- 
tion that the raptor is living entirely on Microtus. If Microtus pro- 
vides only 80% by weight of the diet, then the impact must be 
reduced by 20%. If only 20% of the home range of the raptor is 
Microtus habitat, then the impact figure could be refined by mul- 
tiplying by five to arrive at a figure for impact per bird per square 
km of Microtus habitat. Different average body weights of Microtus 
can be accommodated also by scaling up or down from 35 g. 

Note that the slope of the line representing this relationship is 
negative: the larger the raptor, the less its impact per km? of raptor 
home range (Fig. 2). For example, if a 1,500-g great-horned owl 
and a 245-g long-eared owl were living in the same region and 
were subsisting entirely on 35-g Microtus, the impact of the horned 
owl would be expected to be 0.79 Microtus/km?’/day (from equation 
3), and the long-eared owl would be expected to eat 3% times as 
many per km? (2.74 from equation 3). 

The impact of predation of the intensity calculated for a single 
long-eared owl on a non-breeding Microtus population of 1,000/ 
km? (=10/ha) amounts to about 2% of the population per week. I 
cited above an observation of a kite hunting persistently over a field 
with a Microtus density less than 200/km? (less than 2/ha). The 


Predation 549 


NUMBER OF MICROTUS PER DAY 


100 300 1,000 3,000 
BODY WEIGHT (GMS) 


Fic. 2. Number of 35-g Microtus consumed/day by individual raptors of differ- 
ent body sizes from saw-whet owls to golden eagles (dashed line), compared with 
the calculated number of Microtus removed per day per km? by individual raptors of 
different body sizes (solid line). 


impact of this one individual in this example would amount to 10% 
of the Microtus population per week. Levels of predation such as 
this are probably appropriate for the raptor nesting season during 
which territories such as those presented by Newton (1979) are 
maintained. At other seasons, however, raptors may gather at much 
greater densities, attracted by abundant and vulnerable prey. When 
one realizes that a Microtus specialist such as the white-tailed kite 
can support itself by hunting only 5% of the day (see above) or that 
a pair of barn owls can deliver an average of 1.8 mice/h to the nest 
(Smith et al., 1974), that a pair of barn owls may accumulate at a 
nest 67 uneaten mice in 8 days (Wallace, 1948), and that as many 
as 14 barn owls may roost in a single tree (Reed, 1897) or 300 


550 Pearson 


along 4.8 km of cliff (Dixon and Bond, 1937), then one marvels at 
the ability of Microtus to survive at all. It must be assumed that 
before the last Microtus is caught, the Microtus specialists either 
starve or move away in search of denser Microtus populations, and 
the generalists either emigrate or switch to other prey. The Microtus 
population survives by becoming sparse. 


Predation by Mammals 


Mammalian predators of Microtus hunt them with almost all the 
physical and sensory equipment of the avian hunters and resort to 
two additional skills: sense of smell and ability to dig. It is possible 
that mammalian vision and hearing are not as acute as in some 
raptors, but when combined with a sense of smell they enable even 
relatively clumsy carnivores such as badgers and skunks to catch 
voles. Pearson (1959) showed that there is enough traffic in Micro- 
tus runways so that a carnivore the size of a fox could, if it was as 
clever at detecting active runways as are osmatically dull humans, 
catch its daily food requirements just by sitting and waiting beside 
runways. Most mammalian predators either sit and wait or cruise 
slowly through suitable habitat looking, listening, and sniffing for 
clues to Microtus presence. When a mouse is detected, wolves, coy- 
otes, dogs, foxes, and cats use a characteristic high pounce, the 
purpose of which may be to force the mouse into making a com- 
mitment to its direction of escape and thereby decrease the number 
of variables that the predator must compute. Cats use this high, 
curved jump only in tall grass, but foxes use it even when the grass 
is short (Leyhausen, 1978). 

The mobility imparted by the power of flight would seem to give 
raptors a great advantage by enabling them to skim the easy catches 
off of a larger area. To the contrary, the home ranges of avian 
raptors are much smaller than the home ranges of mammalian 
carnivores of similar body size (based on a comparison of equation 
(1) above with the equation for mammalian carnivores given by 
Harestad and Bunnell, 1979). 


Shrews 


Because of their small size shrews are able to follow Muicrotus 
down its runways into its nests. Even small species of Sorex prob- 
ably eat newborn voles when they encounter them. Blarina, the 


Predation 551 


short-tailed shrew, is a more effective killer and can kill Microtus 
that are twice its size (Martinsen, 1969). Its venomous bite and 
pugnacious personality undoubtedly help to compensate for its small 
size, but it is uncertain how effectively it uses its venom to kill or 
to paralyze mice in nature (Pearson, 1942; Tomasi, 1978). Indeed, 
there are conflicting reports about how effective a Microtus predator 
it is in the wild. Hahn (1908) saw a successful attack by Blarina 
ona Microtus pinetorum that was larger than the shrew, and Maur- 
er (1970) interrupted an attack on M. pennsylvanicus. Shull (1907) 
found a Blarina nest with the remains of about 23 voles in and 
around it. Eadie (1952) identified the contents of hundreds of Bla- 
rina scats collected in Microtus habitat during five autumns and 
winters near Ithaca, New York. He found that voles formed a 
significant portion of the fall and winter diet in every year. Up to 
56% of the scats contained Microtus remains in some seasons. Shrews 
maintained a fairly high population density even after a prolonged 
depression in vole numbers. In fact, shrew densities seemed to ap- 
proximate or even exceed vole densities. Invertebrates served as 
alternative prey and permitted such a low Microtus/predator ratio 
during periods of Microtus scarcity. 

In contrast, Whitaker and Ferraro (1963) made a careful analysis 
of the contents of 221 stomachs of Blarina taken at Ithaca in the 
summer and found no mammal remains at all. Whitaker and Mum- 
ford (1972) found mouse remains in only one of 125 Blarina stom- 
achs collected in Indiana, none in 109 Cryptotis stomachs, none in 
50 Sorex cinereus, and none in seven S. longirostris. The low vole 
content in these extensive samples of Blarina, in contrast to Eadie’s 
scat samples, was probably due to a difference in habitats sampled 
(Blarina lives in both forests and fields) and a difference in seasons 
of collection. Platt (1976), studying Microtus and Blarina in large 
outdoor enclosures at Ithaca, found that Blarina foraged for Micro- 
tus in winter and switched to invertebrates in the spring. Barbehenn 
(1958) acknowledged that Blarina was an effective predator on M:- 
crotus, but noted that populations of the two species appear to fluc- 
tuate independently. They do not constitute, therefore, a closely 
coupled predator-prey system. 


Weasels 


Weasels are traditional enemies of Microtus, and even the smaller 
species such as Mustela nivalis (40 to 90 g) kill mice with great ease 


552 Pearson 


(Heidt, 1972). They kill and stockpile numerous mice in the wild 
but prefer to eat only Microtus (Ryszkowski et al., 1973). The small 
species seem to be vole specialists. 

An especially favorable field situation for studying weasels was 
exploited by Fitzgerald (1977). He studied a number of mountain 
meadows in California isolated by pine forests. The meadows were 
buried under 1-3 meters of snow throughout each of the four win- 
ters of his study. Microtus montanus were censused on mark-and- 
recapture grids in the autumn and spring, and their subnivean nests 
were censused each spring when the snow melted. ‘There was an 
average of slightly less than one nest for each vole censused in the 
autumn. At the spring census of nests, many of them had been 
occupied by ermines (Mustela erminea) and a few by long-tailed 
weasels (M. frenata). The ermine occupant would line the nest with 
the fur of his victims and leave skulls, feet, and other parts lying 
about. Fitzgerald found on the average the remains of 54 voles at 
the nests occupied by each ermine. Ermines were censused by track- 
ing in the snow. Average territories covered about 3.5 ha of mead- 
ow. Counts of the number of ermines were confirmed calorically: 
since 99% of the diet consisted of Microtus, the number of Microtus 
needed for over-winter survival of one ermine could be calculated, 
and this number was in good agreement with the tracking infor- 
mation and with the body-count of Microtus eaten during the win- 
ter. 

In some meadows population densities of Microtus varied as 
much as 100-fold during the study. The density was low in winter 
of 1966-1967, moderate in winter of 1967-1968, and high in 1968- 
1969. Table 3 summarizes, during the three winters, the pressure 
of ermine predation on Microtus in a cluster of six meadows total- 
ling 14 ha. A relatively low Microtus population of 292 individuals 
entered the winter of 1966-1967 at a ratio of 97 voles/ermine and 
emerged in the spring with a population of 126 Muicrotus at a ratio 
of 42/ermine. This high predation pressure then apparently re- 
laxed, through the loss of two ermines, and the population was able 
to build up to 783 Microtus in autumn, at which time only one 
ermine was present, and the pressure was reduced to 783:1. This 
pressure was enough to reduce the population only slightly to 722 
in the spring. The population entered the winter of 1968-1969 at 
a high density, but an increase in the number of ermine to a ratio 
of 198:1 was then associated with a reduction in the population to 


Predation 553 


TABLE 3 
ERMINE PREDATION AT THE ONSET AND END OF WINTER, BASED ON THE NUMBER 
OF VOLES AND ERMINE AND ON KNOWN VOLE MORTALITY (FROM FITZGERALD, 


1977) 
Winter 
1966-67 1967-68 1968-69 
Number of vole nests 292 783 793 
Number of ermine present 3 1 4 
Vole : ermine ratio in autumn 97:1 783:1 198:1 
Maximum voles surviving 126 722 386 
in spring 
Estimated vole : ermine 42:1 221 96:1 


ratio in spring 


386 in the spring. The spring ratio of 96:1 was followed by a 
depression of the Microtus population throughout the breeding sea- 
son of 1969. Minimum estimates of the percent of the vole popu- 
lation eaten by ermine during the four winters varied from 5.9% to 
54.3%. Predation was most severe when voles were at lowest den- 
sity. In two of the meadows during the winter of 1966-1967, at 
least 81% and 83% of the voles present in the autumn were eaten 
by ermines. 

Since such a high percentage of the diet of these ermines consisted 
of Microtus, the response of these predators to changes in Microtus 
density was almost entirely a numerical response. It had a magni- 
tude of about four-fold. Raymond and Bergeron (1982), studying 
an ermine—Microtus pennsylvanicus system in Quebec, found that a 
numerical response appeared within 12 months and could be at- 
tributed to both reproduction and immigration. However, this nu- 
merical response occurred only among male ermines. 

Tapper (1979) studied the little European weasel, Mustela ni- 
valis, on a 25-km? area in southern England. The Microtus arvalis 
in the area went through a 4-year cycle with densities 14 times 
greater at the peak than at the low. Weasel numbers varied by a 
factor of two, with females failing to reproduce during the year of 
lowest vole numbers. The weasel population seemed to be quite 
mobile, however, so that failure of reproduction was soon adjusted 
by immigration. The proportion of voles in the weasel diet increased 
3.4-fold from the lowest Microtus years to the highest. The com- 


554 Pearson 


bined numerical and functional response of this weasel population 
gives them a potential 2 x 3.4 = 6.8-fold range in amount of pre- 
dation on the Microtus population. 


Large Carnivores 


The larger carnivores usually have a varied diet and, although 
they may specialize on Microtus for a few weeks or months, usually 
switch, as do shrews, to other foods at other seasons. Nevertheless, 
large carnivores may be efficient mouse-catchers. Microtus, along 
with pocket gophers, was the staple food item in the diet of coyotes 
in Yellowstone Park from April to November (Murie, 1940). Mu- 
rie watched a coyote for 1% h, hunting on a snowfield in a meadow. 
It pounced 30 times without success, but also in the same interval 
caught and swallowed 11 animals, all of which appeared to be 
Microtus. By following trails of red foxes in the snow, Murie (1936) 
showed that location and capture of mice was easy, even under the 
snow. Rabbits, mice, and shrews were caught in excess and merely 
cached uneaten. At Mount McKinley in Alaska during a series of 
years when hares were scarce, voles made up nearly two-thirds of 
the red fox diet in summer and three-fourths in winter (Murie, 
1944). Even in a year when voles were scarce, they were dominant 
in the diet. Mullen and Pitelka (1972) reported on the uncanny 
ability of arctic foxes and red foxes to detect mouse carcasses under 
as much as 0.75 m of snow. Scott (1943) showed that red foxes 
preferred to eat Microtus and were more likely to cache or discard 
Peromyscus, shrews, weasels, and other prey. Their diet in Iowa 
(primarily rabbits and Microtus) was surprisingly similar to that of 
horned owls in the same area (Scott and Klimstra, 1955). 

Wolves frequently eat Microtus. Murie (1944) found as many as 
six mice in one wolf scat at Mount McKinley and saw as many as 
17 pounces in one h. He once fed up to 19 mice and two shrews in 
quick succession to a captive wolf pup. Mowat (1963) saw a wolf 
catch and eat six voles in 10 min, 23 in one feeding bout. 

Sheldon (1930) found mice in two of 10 stomachs of grizzly bears 
and described a grizzly hunting them in the snow, using its nose as 
a plow, then digging the mouse out and catching it with a paw. 
Murie (1944) found only one vole in 201 grizzly scats from the 
Mount McKinley area. 

Lynx canadensis in Newfoundland fed primarily on hares, but 


Predation 555 


14% of the stomachs and scats contained Microtus pennsylvanicus. 
The frequency was low in winter and higher in years of Microtus 
abundance (Saunders, 1963). 

Many domestic cats, in spite of gratuitous alternative “prey” in 
the form of table scraps and cat food, cannot resist the hunting urge. 
Capture of two to three voles/day is not unusual (Bradt, 1949; 
Toner, 1956). George (1974) tabulated the number of prey items 
brought home during 3 years by three cats living in his home in 
southern Illinois. Microtus ochrogaster and M. pinetorum were the 
most frequent of the 18 species of prey. Diurnal predation yielded 
half of the prey, crepuscular predation 20%, and nocturnal preda- 
tion 30%. The sex ratio of captured voles of each species was ap- 
proximately equal. Captures were much less frequent in winter, 
which George attributed to the fact that the cats had already cap- 
tured a considerable proportion of the voles on their hunting area. 
He estimated that the combined predation by domestic cats on farms 
in the midwest seriously reduces the carrying capacity of the envi- 
ronment for overwintering raptors. 

Christian (1975) marked a population of Microtus pennsylvanicus 
with metal ear tags and then looked for the tags in the droppings 
of 10 to 12 domestic cats that lived on a farm across a road from 
the study area and that were fed commercial cat food and table 
scraps by the owners. Losses due to predation by the cats accounted 
for at least 16% of those voles disappearing from the study area. 
Voles of different sex and age were preyed upon in the same pro- 
portion as they appeared in the trapped sample, indicating either 
that the predation by cats was non-selective or that its bias was the 
same as the trapping bias. 


Carnivore Assemblages 


Madison (1979) marked a total of 93 Muicrotus pennsylvanicus 
with radiotransmitters during three different summers in three dif- 
ferent areas. Thirty (32%) of the marked individuals were killed 
by predators. Domestic cats, snakes, and weasels were the three 
dominant predators. Another 11 telemetered voles disappeared. If 
all of these had been removed by predators, the rate would have 
been 44%, which is an upper limit for the intensity of predation 
during these 3-month periods. Predation was most intense on in- 
dividuals living close to suboptimal habitats. 


556 Pearson 


TABLE 4 
IMPACT OF CARNIVORES DURING THREE Microtus DECLINES ON 14 HA IN CALIFORNIA 
(FROM PEARSON 1964, 1966, 1971) 


1961 1963 1965 

Number of Microtus/ha 

(high-low) 312-<2 540-30 >25-<2 
Number of carnivores on 14 

ha (high-low) 8-0.17 4.4-0.4 2.16-0.35 
Numerical response of car- 

nivores 47x 11x 6x 
Functional response of car- 

nivores! — bax Dix 
Greatest monthly impact? >90% 20% 33% 
Percent of vole standing crop 

eaten 88% 25% 33% 
Mouse-carnivore ratio 

(min., max.) +550:1, 72:1 5,400:1, +500:1 880:1, 24:1 


‘Greatest monthly average number of Microtus eaten/day/carnivore divided by 
the corresponding lowest monthly average. 

2Number of Microtus recovered in scats divided by the number existing at the 
beginning of the month, x 100. 


Pearson (1964, 1966, 1971) censused Microtus californicus on 14 
ha of annual grassland during part of two population declines and 
during all of a third. The population density reached peaks of 314/ 
ha, 540/ha, and more than 25/ha with lows of less than 2/ha 
between (Table 4). Carnivores were censused by their droppings. 
The species present were feral cats, raccoons, striped skunks, spot- 
ted skunks, and gray foxes, approximately in that order of abun- 
dance. For the calculations, the carnivores were treated as a single 
species of 3-kg carnivore, since the source of each dropping was not 
determined. As many as 88% of one of the peak populations was 
eaten before the beginning of the next breeding season. The nu- 
merical response of the carnivores varied from 47-fold to six-fold 
in the three cycles and lagged behind the Microtus numbers by a 
few months. It took many months for the carnivore numbers to 
recover after their prey started to recover. The functional response, 
to the contrary, was rapid. As soon as the Microtus population 
began to increase, the carnivores switched promptly back to a high- 
Microtus diet. The functional response varied from 2.7-fold during 
one decline to 5.2-fold during another. Intensity of predation, as 


Predation 5 oi, 


measured by numbers of Microtus/carnivore, was lowest during the 
buildup of the Microtus population (5,000) and greatest (72, 500, 
224) late in the three declines. One morning when the 1961 peak 
had dropped to 18 voles/ha, none of them breeding, and the average 
carnivore was still eating three Microtus/day, I (Pearson, 1964) saw 
six feral cats hunting on the 14-ha study area. It would have re- 
quired the standing crop of Microtus on 1 ha every day to support 
these cats, not mentioning the other predators. By March, no M:- 
crotus could be trapped on the census grid. Study of these three 
cycles led Pearson (1971) to speculate that mouse—carnivore ratios 
of less than 100 would prevent growth of even maximally repro- 
ducing Microtus populations, ratios between 200 and 1,000 would 
slow the growth of breeding populations and cause abrupt declines 
in non-breeding populations, and ratios higher than 1,000 would 
be relatively ineffective in preventing increases of breeding popu- 
lations. 

The considerable variation of measurements in the three cycles 
(Table 4) arises from sources such as: the measuring period was 
not the same in the three cycles; the carnivore population was re- 
duced by park officials beginning in 1963; and no effort was made 
to estimate the impact of snakes and raptors, an impact that may 
have been unequal in the three cycles. Nevertheless, it is clear that 
through numerical and functional responses the carnivores had the 
potential to bring 16 (in 1965) and more than 200 (in 1961) times 
as much predation pressure to bear on the Microtus population at 
one stage of the cycle as at another. However, the carnivores used 
their reserve predatory power at an inappropriate time to “control” 
the vole population. The most intense predatory pressure was al- 
ways at the end of the vole decline, thereby depressing the popu- 
lation even farther. The presence of a limited supply of alternative 
prey, especially harvest mice and pocket gophers, enabled the car- 
nivores to persist in their search for the last Microtus. The fact that 
Microtus is the preferred prey is shown in that the population den- 
sity of Reithrodontomys megalotis frequently was greater than that 
of Microtus californicus, but Reithrodontomys was relatively ignored 
by the carnivores except when Microtus was scarce. The intense 
and persistent predation during and following the collapse of the 
Microtus populations showed that the carnivores were catching more 
than just “surplus” Microtus. This persistence, made possible by 
the presence of a limited amount of alternative prey, kept the car- 


558 Pearson 


nivores on the scene long enough to prevent a resurgence of the 
Microtus population for one or more breeding seasons and led me 
(Pearson, 1966) to suggest that carnivore predation is an essential 
component of the multi-annual microtine cycle. Raptors, in contrast 
to carnivores, tend to leave the scene when Microtus becomes scarce. 

Many people have resisted accepting the importance of predation 
in driving the microtine cycle because they have expected predators 
to have their influence at the peak of the cycle. In reality, other 
factors must help the predators stop a vigorously growing microtine 
population. The carnivores play their role during and following the 
decline by depressing the population to extremely low levels and 
delaying its recovery. The role of alternative prey may also be mis- 
understood if they are thought of as “buffer species.” If they are 
present in limited supply they increase rather than buffer the am- 
plitude of the microtine cycle. 


Predation by Fish, Amphibians, 
and Reptiles 


Microtus enters water voluntarily and swims competently (Blair, 
1939; Murie, 1960; Peterson, 1947). Consequently, it is exposed to 
predation by fish, turtles, and alligators. This predation surely has 
negligible population consequences. Bullfrogs are predation gen- 
eralists and have a reputation for eating any moving object that they 
can swallow or partially swallow. Korschgen and Baskett (1963) 
found that M. ochrogaster made up an average of 15.3% by volume 
of the stomach contents of bullfrogs, and during one summer month 
as much as 43.9%. Even salamanders eat Microtus. Wilson (1970) 
found a 98-g Dicamptodon ensatus that had swallowed a 27-g M:- 
crotus longicaudatus. Bury (1971) found two Muicrotus in 12 Di- 
camptodon stomachs examined. 

A microtine Pyrrhic victory has been called to my attention by 
my colleague Harry Greene. He found a large red-legged frog (Rana 
aurora) lying dead at the edge of a pond. A young-adult Microtus 
californicus had been half-swallowed, head first, the posterior half 
still protruding from the frog’s mouth. The partially decomposed 
and pickled frog, without mouse, weighed 48 g. 

Snakes are traditional enemies of mice, but their impact has 
rarely been quantified. Fitch (1960) provided data for three of 15 


Predation 559 


species of snakes on the University of Kansas Natural History Re- 
servation. The diet of copperheads (Ancistridon contortix) was 39% 
by weight Microtus ochrogaster, which makes this vole by far the 
most important food for this snake. Population density of copper- 
heads on the reservation in the autumn, after birth of the young, 
exceeds 12/ha, and Fitch estimated that a typical copperhead con- 
sumes eight meals totalling approximately twice its own body weight 
in the course of a growing season. I have calculated that the impact 
of copperheads in this habitat would be about 20 30-g M. ochro- 
gaster/ha/year. 

In the same habitat racers (Coluber constrictor) occupy grasslands 
at densities of 2.5-7.5/ha. Sixty-six percent of their diet by weight 
consists of small mammals, mostly Microtus (Fitch, 1963a). The 
pilot black snakes (Elaphe obsoleta) on the same reservation ate 
primarily small mammals, and the most frequent of these was M. 
ochrogaster (Fitch, 19636). Blacksnake densities varied between an 
annual minimum of 2.1/ha and an annual maximum of 4.2/ha. 
The combined population density of these three species of snakes 
averages about 11 individuals/ha; all of them are deadly Microtus 
predators. The density of Microtus during a 2-year census in the 
same fields varied between 360/ha and 62/ha (Martin, 1956) and 
dropped much lower in the following year. It is probable that in 
some seasons these three predators outnumber the voles. 

In another study, racers and pilot black snakes preyed on a pop- 
ulation of Microtus pennsylvanicus, 36 of which were equipped with 
radiotransmitters (Madison, 1978). During a 1-month interval, six 
of these Microtus were eaten and recovered from snakes. The snakes 
preyed selectively on lactating females and their litters and on large 
males. Madison (1978) suggested that boldness in the presence of 
a predator, or perhaps chemical signals, make these subgroups of 
vole populations especially vulnerable to predation by snakes. 


Discussion 


The preceding documentation demonstrates that many species of 
predators can and do catch Microtus with great ease and that in 
many situations a single species of avian or mammalian or reptilian 
predator catches a lot of Microtus. An assemblage of predators has 
an even greater impact. Capture of more than 20% of a vole pop- 
ulation per month is not uncommon. After a long non-breeding 


560 Pearson 


season, attrition of this severity sometimes places Microtus in the 
awkward position of starting the breeding season surrounded by 
persisting predators that can eat the offspring produced by the sur- 
viving Microtus faster than they can be produced. In spite of the 
quantities of Microtus harvested by predators, many people doubt 
that predation has any marked effect on Microtus numbers. Martin 
(1956), for example, censused Microtus ochrogaster on the Univer- 
sity of Kansas Natural History Reservation for 2 years and con- 
cluded: “Although voles were a common item of prey for many 
species of predators on the Reservation, no marked effect on the 
density of the population of this vole could be attributed to predation 
pressure. Only when densities reached a point that caused many 
voles to expose themselves abnormally could they be heavily preyed 
upon. Their normally secretive habits, keeping them more or less 
out of sight, suggest that they are an especially obvious illustration 
of the concept that predation is an expression of population vul- 
nerability, rising to high levels only when a population is ecologi- 
cally insecure, rather than a major factor regulating population 
levels.” 

In the same report he lists the following Microtus predators living 
on the Reservation: four species of snakes, 15 species of birds, and 
nine species of mammals. He gives no support for his disbelief in 
an effective pressure on the Microtus population. I believe that when 
measurements are available they will show that here, as elsewhere, 
many species of snakes and raptors and carnivores do not wait until 
the meadows are overflowing with insecure or maladjusted Micro- 
tus: they kill Microtus with great ease even when populations are 
low. If a particular predator is a resident generalist with access to 
alternative prey, or is a nomadic specialist (for example, kites or 
short-eared owls), its effect would be expected to stabilize vole den- 
sity, as pointed out by Andersson and Erlinge (1977). The effect of 
stabilizing predation on a prey population is not easily detected 
because its greatest expression leads to an absence of any change in 
the density of the prey. If, however, a predator is a resident spe- 
cialist, such as an ermine, its predatory effect would be to destabilize 
vole densities. Amplitude of change would be increased, and the 
period of the microtine cycle of abundance would be increased. 
Martin’s (1956) voles, which in 2 years underwent a five-fold change 
of density, were responding to predation from a mixture of spe- 
cialist-generalist and resident-nomadic species, as well as to other 
complex influences such as weather. 


Predation 561 


Most of the adaptations of Microtus seem to equip it for life in 
grasslands rather than for defense against predators. Its size is con- 
venient for a host of predators from shrews to grizzly bears. Speed, 
acceleration, and agility are relatively poor. Senses are probably 
less acute than in most of the other species of small mammals living 
nearby. It possesses scent glands that function for intraspecific com- 
munication but that are ineffective in masking its basic delicious 
flavor. It is primarily a grass-eater, so the more it eats the more it 
becomes exposed to its enemies. It does not hibernate or estivate to 
avoid difficult or dangerous seasons of the year, and it is active both 
day and night, so it exposes itself to risk from both nocturnal and 
diurnal predators. Few Microtus store food and so they must ven- 
ture out of their nests at frequent intervals. M. californicus in the 
wild is equally active day and night in winter but is primarily active 
early in the morning during summer. This change seems to be 
driven by moisture requirements rather than by predation (Pearson, 
1960). Males of M. californicus make more excursions out into the 
runways than do females, but the average male excursion is briefer. 
Daytime excursions last much longer than nighttime excursions. 
These and other differences in behavior affect the vulnerability of 
different subgroups of the population. The catch by still-hunters 
such as copperheads should show a bias toward males; sweeping 
hunters such as barn owls and marsh hawks should encounter a 
less-biased sex ratio. Field data on the vulnerability of different 
subsets of the Microtus population are needed urgently. 

A frequently mentioned stratagem against predators, one that is 
effective at the population level if not at the level of the individual, 
is a high rate of reproduction. Most species of Microtus have high 
(and elastic) reproductive potential. Litter size is not notably large, 
but post-partum breeding is common, and early sexual maturity, 
which through compounding is most important for rapid population 
growth, may be spectacular. I have caught 15-g M. californicus 
carrying conspicuous embryos. These females must have become 
pregnant at not more than two weeks of age. Most individuals of a 
Microtus population also initiate breeding in synchrony so that a 
pulse of young emerge at a presumably favorable season and over- 
whelm the appetites of the available predators. No predators are 
able to outbreed Microtus, so a numerical response of the carnivores 
usually lags behind an increasing vole population. 

The grassland in which most Microtus live is a relatively simple 


562 Pearson 


habitat that does not promote species diversity (Cody, 1966). Con- 
sequently, two or more species of Microtus rarely live in the same 
meadow and share the reproductive costs of saturating the preda- 
tors. In fact, the simplicity of grassland is probably a necessary 
condition for the microtine cycle of abundance. There are no multi- 
annual cycles of rodents in rainforest, a habitat so complex, with 
alternative prey so varied and abundant, that predators presumably 
are supported for long periods at a more constant density than in 
grasslands. 

Various social strategies found in Muicrotus restrict population 
growth and thereby tend to keep population density below a level 
that attracts nomadic predators. Cannibalism is one of these (Fitch, 
1957). Dispersal is another (Lidicker, 1975). Dispersal may occur 
at various stages in the cycle of abundance, at various seasons, and 
may involve different classes of the population. They may disperse 
into good, or marginal, or even submarginal habitat. All of these 
kinds of dispersers will have increased their vulnerability to pre- 
dation and can be thought of as dispersing into a sink that is the 
collective maw of their predators (Tamarin, 1978). 


Conclusions 


It will be many years before we fully understand the populational 
consequences of predation on microtines. We already know that 
predation is a vital concern at the level of the individual. A sophis- 
ticated Microtus, cowering in its retreat contemplating an excursion 
out into the grassland, could best calculate the probability of its 
survival for one more day in a dangerous world if it knew: How 
many of “‘us” are there? What is our sex ratio and age composition? 
How many of “them” are there? How many of them are generalists 
or specialists? How many resident or nomadic? How many noc- 
turnal or diurnal? How many are still-hunters? What is this week’s 
rate of change of their numbers and ours? How many alternative 
prey are there? He could then optimize the time, duration, and 
direction of his excursion. Leopold (1933) called attention to almost 
all of these variables that affect prey mortality, but in the ensuing 
50 years we have failed to provide more than the sparsest of field 
data. We are ready to document which predator catches which 
mouse, but not yet can we predict how that event will alter the 
course of the predator and prey populations. 


Predation 563 


Future research probably will focus on the complex effects of 
predation on the demographies of predator and prey. Progress may 
be slow because we are still waiting for mammalogists to provide 
us with a good method of measuring densities of Microtus, a good 
method of defining and measuring meaningful subcategories of the 
populations, a good method of anticipating future reproductive per- 
formance of populations and, consequently, an adequate method of 
predicting potential growth of a population. Achievement of these 
goals would simplify the design and interpretation of much-needed 
experimental manipulations of predator—Microtus systems. Mean- 
while, many “natural experiments” wait to be exploited. Islands 
with and without various predators could be investigated profitably 
and could be manipulated with the expectation of getting inter- 
pretable results. 

In view of the many marvelous interactions that have been de- 
scribed in other animal groups, it is not unreasonable to expect that 
coevolution, driven by the selective force of the intense predation 
documented in this review, has provided some fascinating predator- 
prey interactions waiting to be revealed. 


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4-93: 


POPULATION DYNAMICS 
AND CYCLES 


Mary J. TAITT AND CHARLES J. KREBS 


Abstract 


E address two questions about North American Microtus: 1) 
W what type of numerical changes occur in their populations? 
and 2) what factors must be invoked to explain these population 
changes? 

Historically, studies of Microtus population dynamics have cen- 
tered around descriptions of multi-annual cycles in abundance. Ex- 
amination of field data collected over the last two decades on species 
of Microtus in North America reveals three demographic patterns: 
annual fluctuations, multi-annual cycles, and both, in sequence. 
Out of a total of 106 years of data, we estimated 59% were years 
of annual fluctuations and 41% were cyclic. In two species exhib- 
iting both patterns in sequence there were 9 years of annual fluc- 
tuations and three multi-annual cycles. It appears that annual fluc- 
tuations in density are more common than multi-annual cycles in 
some Microtus populations. 

If we compare annual fluctuations and cycles, we find that the 
amplitude of numerical change is always less than five-fold for 
annual fluctuations and usually over 10-fold for cycles. Peak cyclic 
densities are typically three times greater than the maximum den- 
sities of annual fluctuations. Substantial spring declines in density 
are characteristic of annual fluctuations, whereas little or no spring 
decline (particularly in female numbers) occurs in years of cyclic 
peak densities. 

There are still problems associated with obtaining reliable esti- 
mates of population parameters for Microtus species. The use of 
more than one trapping technique, especially in high density pop- 
ulations, is strongly recommended. 

Microtus numbers increase when extra food is provided experi- 
mentally to field populations, but no one yet has prevented a cyclic 
decline by food addition. It is not yet certain whether plant second- 


567 


568 Taitt and Krebs 


ary compounds play any role in vole cycles. Predation interacts with 
cover to affect vole numbers, and predators can take large numbers 
of voles under certain conditions. Predators may prolong the phase 
of low vole densities but it is not clear that they can generate cycles. 

Spacing behavior operating through differential dispersal may be 
a key element in the adjustment of Muicrotus densities to available 
resources. Surplus voles exist in some populations, but we do not 
know what role such voles play in generating the population dy- 
namics observed. Spacing behavior could be under both genotypic 
and phenotypic control, which suggests a multi-factor component 
in vole population dynamics. There is renewed interest in physio- 
logical responses of voles and lemmings to stress, and speculations 
about its effect on suppression of the immune-inflammatory system, 
especially at high population densities. 

A brief consideration of two phenomena suggests how multi-factor 
explanations could be associated with population cycles in Microtus. 
Body weight may be heritable, but the expression of the trait could 
be modified by, for example, food conditions in the increase phase 
or population density at the peak. Mature female voles should per- 
haps be considered analogous to territorial male birds in maintain- 
ing space for production of offspring. The size of territories, and 
hence the number of mature females, may be determined partly by 
genetic predisposition and partly by behavioral adjustments to en- 
vironmental conditions and to local vole density. 

Future modeling and research on Microtus population dynamics 
should address the two patterns of fluctuation described. Herita- 
bility of growth, reproduction, dominance, and dispersal should be 
investigated in populations exhibiting both patterns of fluctuation 
in sequence as well as in predominantly cyclic and non-cyclic pop- 
ulations. Realistic multi-factor hypotheses must be formulated. ‘These 
should assign factors in a hierarchy over time to predict the patterns 
observed and be testable by field experiments. There is still much 
to do. 


Introduction 


Population dynamics of species in the genus Microtus have been, 
with other small rodents, the subject of several reviews. Historical 
descriptions of outbreaks and plagues were compiled by Charles 
Elton (1942) in his book “‘Voles, Mice and Lemmings.” The eco- 


Population Dynamics and Cycles 569 


nomic consequences of rodent population irruptions, curiosity about 
mechanisms of population regulation, and a desire to predict abun- 
dance have stimulated much research into rodent population dy- 
namics since Elton’s book. Most of the research done up to the early 
1970s was reviewed extensively by Krebs and Myers (1974). 

In the present review, we evaluate field studies that, for the most 
part, were conducted since the review by Krebs and Myers (1974), 
and are restricted to rodents of the genus Microtus in North Amer- 
ica. We attempt to answer two major questions in this chapter: 1) 
What type of population changes occur in Microtus species in North 
America? and 2) What factors must be invoked to explain these 
population changes? By a critical evaluation of past work we hope 
to provide a paradigm for future studies on these rodents. 


Methods of Study 


Voles of the genus Microtus typically live in underground burrow 
systems in grasslands. Where grass cover is dense, they develop 
extensive surface runways. Direct observation of individual voles in 
the field is, therefore, virtually impossible. Most population data 
are collected as a result of trapping individuals. 

Researchers in North America use snap-traps for census work 
and live-traps for continuous mark-recapture monitoring of vole 
populations. Most of the live-traps in use are Longworths (Chitty 
and Kempson, 1949), or Shermans (Morris, 1968), although pit- 
falls (Boonstra and Krebs, 1978; Kott, 1965) and multiple-catch 
traps are also used. 

Live-traps are usually placed in square grids with a specific dis- 
tance (often 25 ft, 7.62 m) between stations. One or two traps are 
put at each point on the grid, and positioned in active surface run- 
ways. In order to catch voles of some species, it is necessary to pre- 
bait for a period before commencing with a regular trapping pro- 
gram (for example, M. townsendu has to be pre-baited for four 
weeks before appreciable numbers are caught). In the pre-baiting 
period, food is put in each trap, which is then locked open and 
placed in position on the grid. Many studies over the last decade 
have used the field technique suggested by Krebs (1966). In this 
technique the traps are set with food and bedding (usually a handful 
of oats and cotton batting). A typical trapping session involves set- 
ting traps in the afternoon, checking them for voles the next morn- 


570 Taitt and Krebs 


ing, re-setting, and checking that afternoon, re-setting and checking 
for the last time the next morning. The traps are then locked open 
with a handful of oats as pre-bait over the interval until the next 
trapping session, normally two weeks later. In summer, the daytime 
trapping period is abandoned to avoid death from overheating of 
surface metal traps. This is not a problem with pitfall traps. 

When a vole is first caught, it is individually marked for future 
identification. This is most often done by placing a numbered fin- 
gerling fish-tag in one ear; alternatively, a system of toe-clipping is 
used. On first capture within a trapping session, individuals are 
sexed and weighed to the nearest g. Males are classified according 
to the position of the testes, either abdominal or scrotal. Females 
are checked for vaginal perforation: open or closed (estrus or anes- 
trus); size of nipples and amount of lactation tissue: small, medium 
or large (not lactating, beginning or end of lactation, mid-lactation); 
separation of the pubic bones: closed (immature), slightly open (pre- 
viously littered), or open (has just or is about to deliver). All preg- 
nancies and trap litters are recorded. In some studies the number 
of wounds is recorded; recent wounds are easily identified by blow- 
ing the fur and looking for small, usually paired, incisions which 
indicate the bite of another vole. Every time an individual is caught 
its number and grid location is recorded. 

There is a large literature on the problems of estimating popu- 
lation size in small mammals; we do not review it here (Seber, 
1982). The studies that we review are based on live-trapping with 
a single type of trap. There is now a suggestion in at least one 
species (M. townsendu at high density in summer when daytime 
trapping is not possible) that pitfall trapping is needed in addition 
to Longworth trapping to census adult populations (Beacham and 
Krebs, 1980; Boonstra and Krebs, 1978). In these two studies of 
peak populations, 40-45% of the adult voles were captured only in 
pitfall traps. We do not know if these adults could have been caught 
in Longworth traps if the number of Longworths had been doubled 
or quadrupled. Nor do we know whether this problem is specific 
to M. townsendii, but it is clear that future studies should use two 
different trapping techniques whenever possible. Alternatively, 
multiple-capture traps could be used. 

Details of trapping methods might be less critical in vole popu- 
lation studies if we could use mark-recapture methods such as the 
Jolly-Seber model (Jolly, 1965; Seber, 1982). Because of early in- 


Population Dynamics and Cycles 571 


dications that Microtus does not respond randomly to traps (Krebs, 
1966; Leslie et al., 1953) many workers have used enumeration to 
provide an estimate of abundance. Enumerated densities (minimum 
number alive) have a negative bias. Hilborn et al. (1976) estimated 
at least a 10-20% bias in enumerated densities of five species of 
Microtus but pointed out that if unmarked animals had very low 
probabilities of capture, the minimum-number-alive estimator would 
seriously underestimate the true number. This is another way of 
emphasizing the need for pitfall trapping or additional techniques 
for sampling voles which might not be caught in normal live-traps. 

Jolly and Dickson (1983) argued for the use of Jolly-Seber es- 
timates in populations whose individuals show unequal catchability. 
The Jolly-Seber estimates will have a negative bias under these 
conditions, but less of a bias than enumeration techniques. Caroth- 
ers (1973, 1979) showed that unequal catchability has only a very 
small effect on Jolly-Seber estimates of numbers and survival, if the 
probability of capture is above 0.5 in each trapping session. These 
studies suggest that small mammal ecologists should use Jolly-Seber 
estimates to estimate numbers rather than enumeration methods, 
but it is important to qualify this recommendation with the re- 
minder that no statistical method can provide accurate estimates of 
abundance when a large fraction of the population does not enter 
the traps at all. 

Many factors can affect trapping success in small rodents and 
odors associated with traps is one possibly important factor (Boon- 
stra and Krebs, 1976; Stoddart, 1982). In M. townsendit, individuals 
entered dirty Longworth traps more than clean traps during the 
breeding season. Voles also may avoid traps visited by other species. 
Boonstra et al. (1982) showed that M. pennsylvanicus was much 
less likely to be caught in a Longworth trap previously occupied by 
Blarina, Mus, Zapus, or Peromyscus. Stoddart (1982) claimed that 
unmarked M. agrestis was more readily caught in clean traps than 
in dirty ones, but his conclusions cannot be accepted because of 
faulty experimental design (no pre-baiting) and no suitable controls 
to measure late summer recruitment of young (cf. Chitty and Phipps, 
1966:323). Further work on the effects of odor on trapping success 
in Microtus will be useful particularly if it addresses how present 
trapping techniques could be improved. 

We assume in this chapter that population data obtained by live- 
trapping is a reliable index of actual changes in numbers if sam- 


572 Taitt and Krebs 


pling is done at least monthly with an excess of live-traps and a 
probability of capture above 50% for adult animals. Attempts to 
sample at a lower intensity have so far proven unreliable at pro- 
viding a detailed picture of population dynamics, although they may 
reveal large-scale trends. 


Observed Population Patterns 


In the last decade, field studies have been conducted on popula- 
tions of Microtus in North America at locations shown in Fig. 1. 
These empirical studies tend to be short-term and are usually con- 
ducted in man-made grasslands where grass cover is dense and the 
number of voles can be substantial in a 2-3 year period (average 
workspan of a graduate student). This raises an important general 
question: are the population dynamics observed in these habitats 
typical? Bearing this in mind, and trying to allow for differences 
in trapping regime, sampling periods, and grid size, we ask what 
population patterns have been observed in the North American 
species of Microtus. 

In Tables 1-6, we summarize the demographic patterns observed 
on control areas in studies of North American Microtus populations. 
We calculated densities of voles by adding a boundary strip one- 
half the inter-trap distance to each edge of the live-trapping area. 
In some cases authors have already presented population data as 
densities and we used these when given. In all cases we rounded 
densities to the nearest 5/ha because of the error in estimating 
numbers from published graphs, so the density estimates we give 
should be viewed as approximations only. We divided demographic 
patterns into two classes: 1) annual fluctuations, and 2) multi- 
annual cycles. Annual fluctuations generally have an autumn or 
winter, end-of-breeding season maximum, and a spring, or onset- 
of-breeding, minimum. Cycles are defined by a low-peak-decline 
sequence over at least two years, and by additional demographic 
criteria defined by Krebs and Myers (1974) when such data are 
available. When long-term, detailed data are available (Figs. 2, 3), 
the classification of annual versus cyclic patterns is usually clear. 
Problems arise in classifying some studies, particularly short-term 
ones. We think that these two patterns could be quantified by ana- 
lyzing the variance of spring breeding densities, or more precisely 
the variance of the natural logarithms of spring densities. For an- 


Population Dynamics and Cycles 573 


Fic. 1. Population study sites of Microtus in North America. Numbers refer to 
studies identified in Tables 1-6. 


Taitt and Krebs 


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Population Dynamics and Cycles 575 


nual fluctuations we expect this variance to be less than 0.5, and 
for cycles, greater than 1.0. Note that spring densities are critical, 
not autumn densities (Krebs and Myers, 1974). We do not know 
whether the dichotomy between annual and cyclic populations is 
real, or whether there is a continuum between the two extremes. 
In the following, we discuss demographic patterns for each species. 


M. townsendii 


All of the long-term population data on this species come from 
the Vancouver area of British Columbia. We identified (Table 1) 
four probable cycles in four populations of this species and 13 an- 
nual fluctuations in three populations. Figure 2 illustrates popu- 
lation changes on one area that was monitored for 11 years. A cyclic 
peak is evident in 1975 but in most years annual fluctuations occur. 
Cyclic peaks in this species ranged from 525 to 800/ha, averaging 
697 voles/ha (Longworth-trapped population only). Annual fluc- 
tuations had average maximums of 239 voles/ha and minimums of 
94 voles/ha. Most of the communities studied consisted only of this 
vole species. One area (grid E; see Krebs, 1979:Fig. 3) contained 
Peromyscus maniculatus and M. oregoni when M. townsendi was at 
low numbers, but both these potential competitors disappeared when 
M. townsendii increased above 100/ha. 


M. pennsylvanicus 


Studies on M. pennsylvanicus have been conducted over a broad 
geographic range (Fig. 1) and an array of demographic patterns 
has been described. There are large differences in average density 
of this species in different areas and these regional differences can- 
not be due simply to techniques (Table 2). In Ontario, recent work 
indicates that annual fluctuations are common with maximum den- 
sities averaging 410/ha and minima averaging 120/ha. Boonstra 
and Rodd (1983) provided 3 years of data from Toronto showing 
annual fluctuations at high densities. A striking population pattern 
was observed by Iverson, Turner and Mihok in Manitoba (Fig. 3; 
Mihok, in press). This population exhibited a cycle, a cyclic low 
density followed by another cycle, then three annual fluctuations. 
In Manitoba, densities were very low, averaging 90/ha at cyclic 
peaks and 10/ha at cyclic lows; annual fluctuations averaged 55/ 
ha at maximum and 30/ha at minimum. 


Taitt and Krebs 


576 


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Population Dynamics and Cycles MT 


Indiana data on M. pennsylvanicus are almost intermediate be- 
tween cyclic and annual fluctuations and we interpret them as 2-year 
cycles. The cyclic maxima averaged 180/ha and the minima aver- 
aged 40/ha. These figures are similar to those obtained by Tamarin 
(1977) in Massachusetts. Virginia data on this species seem to show 
the end of one cycle and then 2 years of annual fluctuations aver- 
aging 85/ha maximum and 35/ha minimum. In Minnesota, 2 years 
of annual fluctuations averaged 85/ha maximum and 10/ha min- 
imum. In Illinois, M. pennsylvanicus invaded habitats formerly oc- 
cupied by M. ochrogaster; to date, populations are sparse, with max- 
ima averaging only 30/ha. From these studies we estimate that, for 
33 years of data, 17 years showed annual fluctuations and 16 years 
were cyclic. There is no clear evidence of a competitive density 
reduction in those areas in which a second Microtus species oc- 
curred. 


M. ochrogaster 


Populations of M. ochrogaster have been studied extensively in 
Kansas, Illinois, and Indiana. Most populations studied in IIlinois 
and Indiana showed 2-4 year cycles in numbers, averaging 130 
voles/ha at the peak and often falling to local extinction during 
cyclic lows (average 4/ha). In Indiana and, since 1975 in Illinois, 
there was potential competition from M. pennsylvanicus. Krebs 
(1977) could find no clear evidence of competition between these 
two species in Indiana. But in Illinois the 1975 M. ochrogaster peak 
(M. pennsylvanicus present) was only half that of the 1972 peak 
when M. pennsyluvanicus was absent (Getz et al., 1979:fig. 1). In 
Kansas after an initial 3-year cycle (Gaines and Rose, 1976), M. 
ochrogaster populations exhibited a series of annual fluctuations 
averaging 55/ha at the maximum and 15/ha at the minimum 
(Gaines et al., 1979). Densities in Kansas were higher in the one 
cyclic peak observed (120/ha), and fell to less than 5/ha in the 
cyclic low. Other studies in Kansas (Martin, 1956) reported an 
absence of cycling in M. ochrogaster during 4 years. For the studies 
that are included in Table 3 we tallied 13 years of cyclic populations 
out of 20 total years of data. 


M. californicus 


The California vole (Table 4) has a restricted geographical dis- 
tribution but has been studied extensively by the research group at 


Taitt and Krebs 


578 


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Pinawa, Manitoba (reproduced, with permission, from Mihok, in press). 


Berkeley led by Pearson, Lidicker, and Pitelka. Unfortunately, like 
most vole population studies, techniques have not been standardized 
and we can only hope that results are comparable, as Pearson (1971) 
demonstrated for two studies. Lidicker (1973) reported the longest 
time series for this species (13 years), but we consider only the first 
5 years to be sufficiently accurate for this analysis. Lidicker (1973) 
found annual fluctuations to be common on Brooks Island and 
Krebs (1966) reported cases of annual fluctuations on the mainland. 
Krohne (1982) recently reported annual fluctuations in perennial 
grasslands in northern California. Densities varied greatly in dif- 
ferent areas. Lidicker’s (1973) Brooks Island densities were 3-10 
times those reported in areas on the mainland. This difference may 
be due to an island effect or a difference in techniques. For main- 
land sites, cyclic peak densities averaged 570 voles/ha, and cyclic 
lows average 15/ha. Annual fluctuations on the mainland reached 
average maxima of 85/ha and average minima of 20/ha. We do 
not know if M. californicus cycles in southern California. Blaustein 
(1980) reported declines that could be either cyclic or the result of 
an irregular annual fluctuation with frequent extinctions. For the 
studies summarized in Table 4, we suggest that there were 7 years 


581 


Population Dynamics and Cycles 


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Population Dynamics and Cycles 583 


of cycles and 7 years of annual fluctuations reported in this species. 
There are no apparent competitors of M. californicus, which seems 
to dominate all other rodents in its grassland habitat (Blaustein, 
1980; DeLong, 1966; Lidicker, 1966). We did not include Garsd 
and Howard’s (1982) analysis of pit-trap data; we do not know 
whether their pitfall technique adequately measures vole population 
densities. 


M. oregoni 


The Oregon vole is unusual for Microtus species because it lives 
in a variety of habitats from virgin conifer forests to clearcut areas 
in forests and grasslands (Hawes, 1975). It has never been recorded 
at high densities (Table 5), so it illustrates the difficulty of trying 
to determine if cycles are present. There is no clear evidence for 
cycles except for two cases reported in Sullivan and Krebs (1981). 
Gashwiler (1972) reported some fluctuations in M. oregon: in clear- 
cut habitats but little fluctuation in virgin timber areas. Hawes 
(1975) found only annual fluctuations in M. oregon: and showed 
that this species was reduced in density when it came into compe- 
tition with M. townsendii. Petticrew and Sadleir (1974) reported a 
possible cycle of M. oregoni in a Douglas-fir plantation; Taitt (1978) 
found M. oregoni invading a forest trapping area in 1 of 3 years of 
study. We conclude that M. oregon: populations may cycle, but they 
most frequently have annual fluctuations that average 32/ha at 
maximum and 7/ha at minimum density. Cyclic populations are 
suggested to have peak densities 2-3 times the annual maxima 
(Table 5). 


M. breweri 


This island species was shown to have annual fluctuations on 
Muskeget Island (Tamarin, 1977); the average peak was 170 voles/ 
ha and the average minimum was 68/ha (Table 6). 


M. longicaudus 


Few studies of M. longicaudus have been carried out (Table 6). 
In Alaska, an annual cycle at low density seemed to occur in logged 
areas (Van Horne, 1982). Densities averaged 33/ha at maximum 
and 11/ha at minimum. Conley (1976) reported a possible cyclic 
peak of this species at 105/ha in a New Mexico grassland. In the 


Taitt and Krebs 


584 


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Population Dynamics and Cycles 


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586 Taitt and Krebs 


southwestern Yukon we found only one high-density population of 
M. longicaudus in 5 years of snap-trapping (Krebs, unpublished). 


M. mexicanus 


A single study of this interesting species by Conley (1976) sug- 
gested annual density fluctuations between a low of 15/ha and a 
high of 50/ha (Table 6). 


M. oeconomus 


This species fluctuates cyclically in Finland, and Whitney (1976) 
suggested one cyclic decline in central Alaska with a peak density 
around 70-80 voles/ha (Table 6). 


M. xanthognathus 


One 3-year study of this enigmatic vole by Wolff and Lidicker 
(1980) in central Alaska showed only annual density fluctuations 
and no evidence of cyclic changes. 


General Conclusion 


We present a synopsis of density changes in the species of M:- 
crotus for which the data indicate a clear population pattern in 
Table 7. Two major conclusions emerge from this analysis. First, 
annual fluctuations are common in most Muicrotus species. Of a 
grand total of 106 years of data on all species, 59% of the years had 
annual fluctuations and 41% were part of cycles. Second, both the 
amplitude and maximum density are higher in cyclic populations 
of a species than in annual fluctuations of the same species. The 
amplitude is always less than five-fold for annual fluctuations and 
usually well above 10-fold for cyclic fluctuations. The summary 
statistics given in Table 7 cannot be assumed to be more than 
general indications of the types of dynamics observed in each species. 
The available data show that M. townsend sustains the highest 
average densities of any North American Microtus, closely followed 
by M. californicus. These trends do not apply to all populations of 
these species, as Krohne (1982) pointed out for M. californicus. We 
conclude that we must explain both patterns of fluctuation, espe- 
cially because data for the two longest-term Microtus studies (Figs. 


Population Dynamics and Cycles 587 


TABLE 7 
SUMMARY OF POPULATION PATTERNS 


Average : 
pean aia No. Proportion 
Maxi- Mini- (max./ _ years of years 
Species Pattern mum mum _ min.) data cyclic 
M. townsendi Annual 239 94 2.5 12 0.29 
Cycle 697 48 14.5 5 
M. pennsylvanicus Annual Le Di 3.0 Wi, 0.48 
Cycle 156 23 6.8 16 
M. ochrogaster Annual 59 2 5.0 7 0.65 
Cycle 129 2 51.6 13 
M. californicus Annual 167 38 4.4 7 0.50 
Cycle 427 12 35.6 if 
M. oregoni Annual 32 7 4.6 10 <()E22 
M. breweri Annual 170 68 25 ) 0 
M. longicaudus Annual 33 11 3.0 Z 0 
M. mexicanus Annual 50 15 3.3 2 0 
M. oeconomus Cycle Us 0 ? 3 1:0 
M. xanthognathus Annual 100 55 1.8 2 0 


2, 3) show that individual populations can exhibit both patterns 
over time. 

In the fifth column of Tables 1-6, we summarize the spring 
dynamics of each Microtus population study. The spring dynamics 
of M. townsendii show two patterns associated with the two forms 
of population fluctuation (Fig. 2). An annual fluctuation is preceded 
by a substantial spring decline. By contrast, in cyclic peak years 
(1975, 1977; Table 1) the spring decline is slight (Fig. 2). Taitt (in 
press) suggested that the form of the spring decline may indicate 
the type of population pattern shown by this species. A similar 
suggestion was made by Hansson (1971) for M. agrestis in south 
Sweden. The data for M. townsendu also indicate that the sexes 
have two patterns of spring decline: both male and female numbers 
decline in the spring of an annual fluctuation, but females do not 
decline in a cyclic peak spring (Fig. 2). 

Spring densities of M. pennsylvanicus in Manitoba, Indiana, 
Massachusetts, Minnesota, and Illinois tend to be lower in years of 


588 Taitt and Krebs 


annual fluctuation than in years of cycles (Table 2). This pattern 
also is seen in M. ochrogaster (Table 3), M. californicus (Table 4), 
and M. brewer: (Table 6). Few of the studies in Tables 2-6 pro- 
vided data on density change according to sex. But in six cases male 
M. pennsylvanicus declined more than females in the spring of cyclic 
years. Data for other species listed in Tables 5 and 6 are inadequate 
to establish whether this pattern is a general one. However, we 
know of no exceptions to the pattern of a strong spring decline 
being associated with annual fluctuations and weak spring declines 
being associated with cyclic peak populations. 


Hypotheses to Explain Population Patterns 


Since the review of Krebs and Myers (1974), there has been 
considerable development of hypotheses that account particularly 
for cyclic fluctuations in voles. We first state the hypotheses and 
then review the evidence in favor of each one. 


Food Hypotheses 


There are at least three food hypotheses now in the literature: 


1) food quantity, 
2) food quality, 
3) secondary compounds. 


The food-quantity hypothesis states that fluctuations in popula- 
tion size are produced by changes in the amount of available food. 
It was discussed by Elton (1942) and put forward by Lack (1954) 
as an explanation of cycles. In nutritional terms, it states that cal- 
ories limit populations, and that malnutrition causes changes in 
birth and death rates. 

The food-quality hypothesis arose in opposition to the simple 
world-is-green argument, and states that even though food supplies 
are abundant, they may be deficient in one or more nutrients that 
will stop reproduction and growth or accelerate mortality (Pitelka 
and Schultz, 1964). For example, Kalela (1962) postulated that 
fluctuations in boreal small rodents may be triggered by plant 
rhythms in production and growth. The food-quality hypothesis is 
now a family of hypotheses that explain population fluctuations by 
one or more macro- or micro-nutrients such as nitrogen, potassium, 


Population Dynamics and Cycles 589 


phosphorus, or sodium. For example, White (1978) argued that 
herbivores are limited by a relative shortage of nitrogenous food for 
young animals. 

Plant secondary compounds can affect herbivores in three general 
ways. They can alter digestibility of forage and thus cause symp- 
toms of food-quality deficiencies, they can be toxic directly and cause 
death, or they can inhibit (Berger et al., 1977) or stimulate (Berger 
et al., 1981) reproduction. Freeland (1974) was the first to suggest 
the toxic-compound hypothesis. General hypotheses about the role 
of plant secondary compounds were presented by Freeland and 
Janzen (1974). Haukioja and Hakala (1975) and Haukioja (1980) 
suggested that production of some compounds may be induced by 
herbivore grazing. 


Predation Hypotheses 


Predation on small mammals is postulated to determine the am- 
plitude and timing of cycles (Pearson, 1971). Predation is not thought 
to act on increasing populations to stop their increase but rather to 
accelerate declines and hold numbers low. Mammalian predators 
are thought to be more effective than avian predators at hunting 
low-density populations (see Pearson, this volume). 

Avian predation is one component of the effect of vegetative cover 
on vole populations. Birney et al. (1976) presented a two-threshold 
model called the ‘‘cover level hypothesis.”” Below the lower thresh- 
old of cover no population can exist. Non-cyclic populations with 
annual fluctuations are found at medium levels of cover. Cover can 
influence predation, available food supply, and behavioral interac- 
tions (Taitt and Krebs, 1983); it is reconsidered when we discuss 
multi-factor hypotheses. 


Spacing-Behavior Hypotheses 


The possibility that animals might limit their density by terri- 
torial behavior has been argued by ornithologists for 60 years. 
Wynne-Edwards (1962) elevated this idea to the general hypothesis 
that animals adjust their population density to available resources 
through social behavior. Watson and Moss (1970) provided an op- 
erational set of criteria that could be applied to field populations to 
determine whether breeding density is regulated by spacing behav- 
ior (Table 8). 

The spacing-behavior hypothesis has been closely associated with 


590 Taitt and Krebs 


TABLE 8 
THE CRITERIA SUGGESTED BY WATSON AND Moss (1970) TO DETERMINE WHETHER 
SPACING BEHAVIOR LIMITS BREEDING DENSITY OF A POPULATION 


> 


. A substantial part of the population does not breed; they die, are unsuccessful at 
breeding, are inhibited from breeding, or they breed later. 
Such non-breeders are capable of breeding. 
. Breeding animals are not resource limited. 
. Spacing behavior is compensatory. 
If A to D are true, and densities change according to shifts in food availability, 
then both spacing behavior and food limit the number of breeders. 


myaw 


the role of dispersal in microtine population regulation. Spacing 
behavior in field populations produces dispersal. Lidicker (1975) 
recognized pre-saturation, saturation, and frustrated dispersal (Lid- 
icker, this volume). Abramsky and Tracy (1979) suggested that 
immigration was necessary to produce population cycles. Popula- 
tions with emigration but no immigration showed annual density 
fluctuations. Gaines and McClenaghan (1980) recently reviewed 
dispersal in small mammals. Anderson (1980) also reviewed dis- 
persal in microtines but did not discuss how dispersal affects pop- 
ulation fluctuations or cycles. The exact mechanism by which spac- 
ing behavior produces population declines has not been specified. 

There are two other groups of social-behavior hypotheses which 
we call phenotypic-behavior and genotypic-behavior hypotheses. We 
tentatively separate these hypotheses from spacing behavior in this 
review because they suggest specific mechanisms for the cyclic de- 
cline. Watson and Moss (1970) discussed the important role of 
“surplus” animals in their criteria (Table 8), but neither Christian 
(1978) nor Chitty (1967) discussed them. We suggest that the cri- 
teria of Watson and Moss (1970) will be essential to testing both 
of these groups of hypotheses. 


Phenotypic-Behavior Hypotheses 


These hypotheses state that social behavior limits breeding den- 
sity and that the relevant behaviors are under phenotypic (non- 
heritable), physiological control. The best known is the stress hy- 
pothesis or neurobehavioral-endocrine mechanism of regulation of 
population growth, which was discussed in detail by Christian 


Population Dynamics and Cycles 591 


(1978, 1980). This hypothesis was the first proposed to explain 
population fluctuations by an intrinsic mechanism (Christian, 1950). 
At high density a high rate of interaction results in a stress response, 
which leads to increased mortality and decreased reproduction and 
hence to population declines. 

Social behavior often is mistakenly identified with aggressive be- 
havior, but it includes any type of dominance or spacing behavior 
that affects an individual’s chances of surviving and breeding. Thus, 
social structure, as discussed by Getz (1978), can affect rates of 
sexual maturation through pheromones or can affect familiarity 
among individuals and dispersal (Bekoff, 1981). The problem is 
that social behavior can have such varied effects on animals that we 
cannot determine without field experiments whether the effects of 
social behavior are relevant to understanding population fluctua- 
tions. For example, in peak populations of M. pennsylvanicus, age 
at sexual maturity is increased. Is this increase due to malnutrition, 
to maturation-retarding pheromones, or to adrenal-pituitary stress? 
We must do field experiments to answer specific questions of this 
type. 

Since the early work of Frank (1957), there have been sugges- 
tions that social organization changes during population cycles. 
Populations exist in socially-stable configurations (individual ter- 
ritories) or in unstable configurations (group territories or domi- 
nance hierarchies), which produce cyclic peaks and overpopulation. 
Getz (1978) suggested that M. ochrogaster changes from a monog- 
amous, territorial system, to a polygamous mating system in the 
increase phase of a cycle. One difficulty of this model is that other 
Microtus species, such as M. pennsylvanicus, are polygamous at all 
times and yet also cycle (Getz et al., 1979). Nevertheless, the general 
hypothesis that a variable social system underlies the differences 
between annual and cyclic populations is an important one that 
needs testing. 

Hamilton (1964) discussed how kin selection could affect the 
evolution of social behavior. Charnov and Finerty (1980) applied 
these ideas to vole cycles and argued that aggression should be low 
among close relatives and should become high when individuals 
interact with many non-relatives, as they would in a population 
with high dispersal rates. Note that this kin-selection hypothesis is 
not a genotypic-behavior hypothesis but a phenotypic one, because 
individual voles are not genetically programmed to act any differ- 


592 Taitt and Krebs 


ently in increasing or declining populations. Individuals simply ap- 
ply a general rule at all times: be aggressive to non-relatives and 
docile to relatives. 


Genotypic-Behavior Hypotheses 


Genotypic-behavior hypotheses are similar to phenotypic ones in 
assuming that changes in population size are caused by changes in 
social behavior, but they differ in ascribing the changes to shifts in 
allelic frequencies of genes that affect behavior. Genotypic hypoth- 
eses do not deny the physiological machinery behind the behavioral 
changes but assume that there is an array of genotypes in natural 
populations with differing social behaviors and that these genotypes 
are alternately favored or disfavored by natural selection. . 

The Chitty hypothesis is the best known of the genotypic-behavior 
hypotheses (Chitty, 1967); the hypothesis was reviewed recently by 
Krebs (1978a). A second hypothesis involving heterozygosity was 
suggested by Smith et al. (1975). Increasing heterozygosity in nat- 
ural populations is associated with outbreeding, population growth, 
and increasing aggressive behavior. Smith et al. (1978) discussed 
predictions that follow from their model. 

If the genotypic-behavior hypothesis is correct, it allows us to 
predict which populations will show annual fluctuations and which 
will show cycles. Krebs (1979) suggested that there was a positive 
correlation between the amount of fluctuation in population density 
and the heritability of spacing behavior. Populations with strong 
cycles should show a high additive genetic variance in spacing be- 
havior, and this genetic variance should provide the time lag nec- 
essary to generate a cycle. 


Multi-factor Hypotheses 


“In the case of every species, many different checks, acting at 
different periods of life, and during different seasons or years, prob- 
ably come into play” (Darwin, 1859). The multi-factor hypothesis 
is an old idea which has become popular in vole research (Batzli, 
in press; Christian, 1978; Getz, 1978; Lidicker, 1973, 1978; Taitt, 
in press; Tamarin, 1978a). We recognize two variants of the multi- 
factor hypothesis. The Lidicker model is diagrammed in Lidicker 
(1978:135) and is a generalized version of the multi-factor hypoth- 
esis first suggested by Darwin. We do not accept this model as 


Population Dynamics and Cycles 593 


being useful for further research and agree with Tamarin’s (19786) 
criticism of Lidicker’s model. We are not questioning the truth of 
the model but rather its utility. 

Another variant of the multi-factor model was presented by Taitt 
(in press) and is shown in Fig. 4. The value of this model is two- 
fold. First, it integrates intrinsic and extrinsic variables through 
spacing behavior, and thus begins to specify a hierarchical type of 
systems model appropriate for explaining population changes. Sec- 
ond, it is experimentally oriented and suggests entry points for 
manipulation of populations. Thus, it avoids the major pitfall of 
most multi-factor models: they are a posteriori and untestable. 

A general problem with many hypotheses in vole research is that 
they are often stated in vague terms. For example, Lidicker (1978: 
135) stated that the multi-factor hypothesis can ‘“‘explain densities” 
and population “regulation.”” We know of no hypothesis that can 
do this. Instead, we can only explain changes in density over time, 
or differences in density over space (Chitty, 1960). 

Multi-factor approaches have been useful for recognizing the 
possible role of spatial heterogeneity in vole population fluctuations. 
Soviet ecologists have emphasized the role of spatial variation in 
habitat quality (for example, Naumov, 1972). A variety of terms 
has been used to describe habitat variations: central and marginal, 
optimal and suboptimal, primary and secondary, donor and recep- 
tor, survival and colonization (Anderson, 1980; Hansson, 1977; 
Smith et al., 1978; Wolff, 1981). The major distinction is whether 
the habitat is permanently occupied or not. There is no agreement 
about the role of chance in spatial heterogeneity, and this has led 
to circularity. Do we distinguish optimal habitats by their vegeta- 
tion characteristics or by the fact that they always contain voles? Is 
it possible in a cyclic population to have empty primary habitats 
and occupied secondary habitats simultaneously? As Hansson (1977) 
recognized, only a spatially extensive mark-recapture program can 
answer these questions about the role of spatial variation. 


Tests of Hypotheses 


In the last decade, numerous experimental studies have been 
conducted on Microtus populations in an attempt to test explicitly 
some of the hypotheses outlined above. 


594 Taitt and Krebs 


ENVIRONMENT 
Food, cover, space, -- Sex, age, size, 
predators, competitors maturity, genotype 


FEMALE wd) \ 


MALE SPACING 
SPATIAL ORGANISATION 


. Vv 


RESIDENT BREEDING 
MALES AND FEMALES| [SURPLUS 


SOCIAL BEHAVIOUR 


ENVIRONMENT 
Food, cover, 


space, predators 


,© 


LOW BREEDING DENSITY HIGH BREEDING DENSITY 
ANNUAL FLUCTUATION CYCLE 


Fic. 4. General model of population dynamics for Microtus townsendi indicating 
how sex-specific spacing behavior may “‘decide” the potential surplus and how en- 
vironmental conditions may “determine the fate” of the surplus and hence the pop- 
ulation pattern (modified from Taitt, 1978, in press). 


Food Experiments 


Three food-addition experiments were conducted recently on M:- 
crotus populations. In spring 1973, we added two levels of food to 
populations of M. townsendi (Taitt and Krebs, 1981). The control 


Population Dynamics and Cycles 595 


population was fluctuating at low density, but experimental pop- 
ulations reached and maintained densities two (low food addition) 
and five times (high food addition) that of the control. An inter- 
mediate level of food the following year resulted in a doubling of 
density over the control, even though the control was then increasing 
to a cyclic peak density. Voles with extra food increased in weight 
and more were reproductive, and they had reduced home ranges in 
proportion to the level of food added. It is fairly certain (see density- 
controlled food experiment by Mares et al., 1982) that the reduction 
of resident home ranges in response to food enabled immigrants to 
settle on food grids and colonize new habitat in proportion to the 
extra food available. 

A single level of extra food was supplied to M. ochrogaster (Cole 
and Batzli, 1978) and M. pennsylvanicus (Desy and Thompson, 
1983) with similar results. But in both studies the control popula- 
tion cycled and, although grids with extra food reached higher den- 
sities, they declined at the same time as the controls. Cole and Batzli 
(1978) noted that erratic declines on their high-density food grid 
were associated with periodic concentrations of predators; however, 
they did not mention this as a cause of the severe cyclic decline. If 
feeding experiments are done on other cyclic species, attempts should 
be made to have a replicate food grid from which all predators are 
removed. 

We conclude that these Microtus species do respond to an increase 
in food. They reach higher densities than controls because of in- 
creased growth, reproduction, and immigration. But so far extra 
food has not prevented cyclic declines in density. 

Six 1-ha plots of shortgrass prairie were manipulated for 6 years 
in eastern Colorado as part of the IBP Grassland Biome study 
(Abramsky and Tracy, 1979; Birney et al., 1976). M. ochrogaster 
density on the control remained low (average maximum of 3.5/ha) 
throughout. No Microtus were trapped on plots receiving 50 kg/ha 
of ammonium nitrate. Grids treated with water had 14 M. ochro- 
gaster/ha by the fourth year of treatment. Plots with both nitrogen 
and water added maintained the highest density (average maximum 
of 80/ha) of M. ochrogaster and had three times as much cover as 
the control. However, voles simply may have responded to cover 
and not to food quality (Birney et al., 1976). 

In Fennoscandia, long-term monitoring studies indicate that peaks 
of plant flowering coincide with cyclic increases of rodent numbers 


596 Taitt and Krebs 


(Laine and Hettonen, 1983). It is not known if this correlation is 
a causal one or not. 

The role of plant secondary compounds in vole population dy- 
namics is difficult to assess. Although voles show food preferences 
(Batzli, in press), it is difficult to decide what is toxic to voles (Batzli 
and Pitelka, 1975; Freeland, 1974). Schlesinger (1976) challenged 
Freeland’s (1974) first tenet, that voles must prefer non-toxic plants. 
But he agreed that M. pennsylvanicus (Thompson, 1965) and M. 
californicus (Batzli and Pitelka, 1971), both cited by Freeland, avoid 
toxic plants. The only other Microtus data considered by Schlesinger 
(1976) was for M. ochrogaster, which did not avoid toxic plants. 
However, Zimmerman (1965) found that M. pennsylvanicus avoid- 
ed three toxic plant species. Problems of sample size, and the fact 
that seeds (which made up 66-86% of stomach contents) were not 
identified to species (Batzli and Pitelka, 1975) have made tests of 
Freeland’s (1974) hypothesis inconclusive. Bergeron (1980) report- 
ed that M. pennsylvanicus increases its consumption of toxic plants 
at peak densities, as Freeland (1974) predicted, but whether these 
toxic food items are responsible for cyclic declines in numbers is 
not clear. 

Details of the factors controlling reproduction and growth are 
discussed in other chapters (see Keller, this volume; Batzli, this 
volume). Since the duration of the breeding season is an important 
variable that can affect population changes, we need to know what 
factors start and stop breeding in Microtus. Negus and Berger (1977) 
reported that M. montanus populations given access to sprouted 
wheatgrass in mid-winter became reproductive in two weeks while 
controls remained non-reproductive. They isolated the causal chem- 
ical as 6-methoxybenzoxalinone (6-MBOA). Rose et al. (in press) 
fed oats impregnated with 6-MBOA to a M. pennsylvanicus pop- 
ulation in January and reported 42% of females pregnant compared 
with 10% in a control population 5 weeks later. No field tests have 
been conducted on the phenolic compounds that inhibit reproduc- 
tion in M. montanus (Berger et al., 1977). 

Induction of secondary chemicals in plants eaten by Microtus has 
not been demonstrated. However, Haukioja (1980) suggested that 
induction of such chemicals could be ruled out if a vole population 
was able to increase immediately after being transferred to an area 
that previously had been heavily grazed. Myers and Krebs (1974) 
introduced M. ochrogaster into a fenced enclosure in which a pop- 


Population Dynamics and Cycles DOF, 


ulation of this species had previously reached 5-times natural den- 
sity (caused by a fence effect). The new M. ochrogaster population 
increased in 1 year to more than 10 times the density of the 
unenclosed control. Krebs (1966) showed that, if new voles were 
introduced, a population increase of M. californicus could be induced 
in an area that had just suffered a decline in density. 

In summary, three Microtus species responded to experimental 
addition of food. Increases in other rodent populations were cor- 
related with improved plant quality. Reproduction of M. montanus 
and M. pennsylvanicus was stimulated by the presence of 6-MBOA. 
Grazing-induced secondary compounds appear not to be impor- 
tant in two Microtus species. No data indicate that food is more 
than a necessary condition for Microtus population increase. Future 
research needs to determine whether changes in food quantity or 
quality are sufficient to cause cycles. 


Evidence for Predation 


Recent work on predation has taken into account the importance 
of cover as protection against predation. Reduced cover caused by 
cattle grazing results in low-density Microtus populations (Birney 
et al., 1976). Baker and Brooks (1981) observed high raptor den- 
sities in habitats with high numbers of M. pennsylvanicus, but the 
amount and distribution of cover affected prey availability. We ex- 
perimentally increased cover by adding straw (Taitt et al., 1981), 
with the result that M. townsendi populations increased. We also 
reduced cover by mowing (Taitt and Krebs, 1983), and populations 
declined. 

Avian predation is easier to quantify than mammalian predation 
because bird pellets tend to be localized at roosts. The most useful 
data on predation combine field studies of vole demography (where 
voles are identified by metal ear tags) and collection of as many 
pellets as possible in the immediate area of the vole grids. Two 
studies on M. townsendii (Beacham, 1979b; Boonstra, 1977a) in- 
dicate that avian predators take more males than females and select 
small voles. Still, such studies are limited because one can never 
find all predator pellets or scats, so the estimates of predation will 
always underestimate the impact of predation on tagged animals. 
However, Beacham (19796) recorded an impressive 25% loss of M. 
townsendu to avian predation in a 1-week period of his study. Bea- 


598 Taitt and Krebs 


cham found a density-dependent correlation (r = 0.99; P < 0.02) 
between avian predation and densities of M. townsendu. 

Pearson (1971, this volume) argued that carnivore predation on 
M. californicus operated in an inverse density-dependent manner, 
so that the major effects were on low-density populations. Erlinge 
et al. (1983) measured both avian and mammalian predation of M. 
agrestis populations in south Sweden. They calculated that total 
annual predation was of the same magnitude as annual rodent 
production. Their result confirms Hansson’s (1971) suggestion that 
small rodents in south Sweden are prevented from cycling by pre- 
dation. Future predation studies must include both avian and mam- 
malian species. Attempts should be made to experimentally manip- 
ulate predation, particularly at important periods during vole 
demographic changes (for example, at the onset of breeding; Taitt 
and Krebs, 1983); only then will we be able to judge the true impact 
of predation on vole population dynamics. 


Spacing-Behavior Experiments 


Krebs et al. (1976) were the first to apply the Watson and Moss 
(1970) criteria to determine whether spacing behavior limits the 
breeding density of a microtine population. They demonstrated that 
surplus M. townsendi existed that were capable of breeding (Con- 
dition A and B, Table 8) but did not do so. We now discuss briefly 
other recent Microtus studies that support the criteria of Watson 
and Moss (1970) in Table 8. A more detailed review recently was 
published by Tamarin (1983). 

Condition A.—Voles occupy home ranges. If residents are re- 
moved, new voles colonize the vacant area (Baird and Birney, 1982; 
Krebs et al., 1976; Myers and Krebs, 1971). It is not certain wheth- 
er colonizers are surplus from resident populations, but Krebs et 
al. (1978) found that new colonizers showed more subordinate be- 
havior than control residents. 

Condition B.—If new colonizers are allowed to remain in an area, 
they establish a breeding population (M. ochrogaster [Gaines et al. 
1979]; M. townsendii [Krebs et al., 1978]). 

Condition C.—No direct evidence has been collected for this con- 
dition in Microtus species. But when a vole population is fenced in, 


Population Dynamics and Cycles 599 


the enclosed habitat supports a much higher population than unen- 
closed controls (M. pennsylvanicus [Krebs et al., 1969]; M. town- 
sendi [Boonstra and Krebs, 1977]). This suggests that food, space, 
and nest sites are not limiting voles directly in open control popu- 
lations. 

Condition D.—It is difficult to demonstrate behaviorly induced 
mortality in voles. If a vole ceases becoming trapped, it may have 
emigrated or died, or it simply may be avoiding traps. However, in 
a recent experiment on M. townsendi (Taitt and Krebs, 1983), we 
counted all such voles as “disappeared,” and found that the number 
of voles that ‘‘disappeared” from five populations over the month 
of onset of breeding in females was correlated (7 = 0.93; P < 0.05) 
with density of voles. Reproduction is compensatory (presumably 
behaviorally induced) in several species (M. californicus [Batzli et 
al., 1977]; M. montanus, M. ochrogaster, M. pennsylvanicus [Schaffer 
and Tamarin 1973]). We believe that these observations indicate 
that voles may show compensatory spacing behavior. 

Condition E.—In one species (M. townsend), we have some evi- 
dence for conditions A to D. Watson and Moss (1970) suggested 
that, if these populations respond to changes in food, they are reg- 
ulated by both spacing behavior and food. Populations of M. town- 
sendu increased to different densities in response to the amount of 
food added, and also colonized new habitat in response to food levels 
(Taitt and Krebs, 1981). 

If we use the criteria in Table 8, populations of M. townsend 
appear to be regulated by both spacing behavior and food. This, 
and the fact that females were more responsive to food availability, 
led to the formulation of the model in Fig. 4. The habitat patchiness 
(induced by winter rainfall) may be unique, but we feel that some 
of the mechanisms invoked (for example, cessation of reproduction 
through increased interaction as a result of winter flooding [Taitt 
and Krebs, 1981], and perhaps simultaneous settlement of breeding 
females in spring of cyclic years [Taitt and Krebs, 1983]), may be 
of general importance in other annual-cyclic species. 

A study in Finland by Pokki (1981) on M. agrestis is particularly 
interesting because it is suggests the possible influence of dispersal 
on the fate of surplus animals and population fluctuations. Pokki 
(1981) observed that island colonization was by inter-island dis- 
persal from small islands (isolated patches of grassland) over as 
much as 1 km of open water. However, dispersal on large islands 


600 Taitt and Krebs 


was within islands between grassland and marginal habitat (wood- 
land). Also, more inter-island dispersers colonized large islands than 
small ones. Pokki (1981) did not observe cycles on small islands, 
but M. agrestis appeared to be cyclic on the largest islands. This 
study gives a dramatic illustration of the dispersal ability of M. 
agrestis, and may provide evidence for an hypothesis about cycles 
(Fig. 4). If dispersers are surplus animals, can the observed popu- 
lation patterns be partly the result of elimination of surplus voles 
(on small islands), which leads to an absence of cycles, whereas 
survival of surplus voles (on large islands) results in cycles? Tam- 
arin (1978a) suggested that the presence of a vole surplus explained 
the absence of cycling in M. brewer: populations on Muskeget Is- 
land, but the two situations may not be comparable. Muskeget is 
isolated, and has been for 2,000-3,000 years. Experimental work 
is needed on island populations to test these interpretations. 


Phenotypic-Behavior Experiments 


A premise for both the phenotypic- and genotypic-behavior hy- 
potheses is that the rate of interaction of individuals increases with 
population density. Pearson (1960) reported that M. californicus 
built more runways as numbers increased. Carroll and Getz (1976) 
also found that the number of active runways was correlated with 
population density of M. ochrogaster. However, it is not known if 
voles confine all their activities to runways. In fact, Crawford (1971) 
observed M. ochrogaster climbing low branches of trees and engag- 
ing in fighting outside burrows during a cyclic peak. In addition, 
interactions need not always be through direct contact, because voles 
probably use indirect methods such as marking (Richmond and 
Stehn, 1976) and vocalizations that enable them to react to increases 
in density. 

Adrenocortical function has been evaluated indirectly in Microtus 
populations by measuring adrenal weight. But adrenal weight var- 
ies with sex, season, maturity, diet, and body weight. To and Tam- 
arin (1977) found that adrenal weights of sexually mature M. brew- 
ert from non-cyclic, island populations were significantly influenced 
by population density. But mainland, cyclic M. pennsylvanicus 
showed no clear adrenal response to population density in their 
study. However, Geller and Christian (1982) found that “mean 
relative adrenal weight” of mature female M. pennsylvanicus was 


Population Dynamics and Cycles 601 


correlated with mean population density in spring (April to June). 
It is difficult to compare densities in these studies, but it appears 
that To and Tamarin’s (1977) M. pennsylvanicus densities were 
lowest, their M. brewer: densities were higher, and Geller and 
Christian’s (1982) M. pennsylvanicus densities were highest. An 
interesting common trend in these studies is that, in populations 
where there is a relationship between adrenal weight and density, 
mature females showed a stronger relationship than males. Geller 
and Christian (1982) speculated that pregnant females, in popu- 
lations at different densities, may affect fetal immune development. 

Field studies on Antechinus stuarti in Australia indicate that 
males are extremely aggressive toward one another during mating 
(Braithwaite, 1974). This behavior is correlated with a marked 
increase in blood androgen (Moore, 1974). Bradley et al. (1980) 
showed that high free glucocorticoid concentrations in plasma result 
from increased total glucocorticoid and reduced plasma corticoste- 
roid binding which, in turn, suppress the immune and inflamma- 
tory system. The consequence is that all males die after mating 
from gastro-intestinal hemorrhage and infection from parasites and 
microorganisms. No field studies on Microtus have demonstrated 
death on this scale from these causes. But such physiological re- 
sponses to stress have been reported for M. montanus in the labo- 
ratory (Forslund, 1973). The period of spring decline is probably 
stressful in M. townsendiu (coincides with a peak in male wounding 
and pregnancy of the first females). McDonald and Taitt (1982) 
found that a small sample of voles from such a population had high 
levels of free corticosteroids, but the highest levels were found in 
mature females. 

Hormonal manipulation of behavior in the field has been at- 
tempted in M. townsend (Gipps et al., 1981; Krebs et al., 1977; 
Taitt and Krebs, 1982). Pellets or silastic implants of testosterone 
in males had no significant effect on demography. But silastic im- 
plants of scopolamine HBr, which have been shown to reduce male 
aggressive behavior in M. townsendi (Gipps, 1982), reduced the 
rate of spring decline in males. Males also survived better in a 
population in which females were fed a synthetic steroid (mestra- 
nol), which rendered them anestrous. Female wounding is uncom- 
mon in M. townsendii, but females with implants of testosterone 
had more wounds than males, and, like males, had low survival in 
spring. These results suggest that male M. townsend are responsive 


602 Taitt and Krebs 


to the level of overt aggression (male or female). Normally, females 
may rely less on overt aggression (Caplis, 1977) and more on site- 
specific defensive behavior. If true, it might explain, for example, 
why females respond more quickly to increased food. Also, if in- 
creased vole density means more challenges to site-specific individ- 
uals, then females may be stressed more by increased population 
density than males. 

Behavioral interactions may affect density through reproductive 
effects as well as through survival. The Bruce effect (pregnancy 
blockage) is perhaps the best known. Keller (this volume) reviewed 
these mechanisms and concluded that they may be important in 
field populations but that the evidence does not suggest a major role 
in generating population fluctuations. Taitt and Krebs (1981) sug- 
gested that M. townsendi may be driven to an annual fluctuation 
in most years because of winter cessation of reproduction. ‘They 
hypothesized that rain causes the water table to rise to the point 
that voles cannot maintain deep burrows; they are forced into less 
space, which results in increased interaction, weight loss, and ces- 
sation of reproduction. 

Social suppression of growth and reproduction may vary in dif- 
ferent species of Microtus (Facemire and Batzli, 1983). Species like 
M. californicus and M. ochrogaster, which have a monogamous social 
system, show social suppression of growth when siblings are caged 
together. Species like M. oeconomus and M. pennsylvanicus, which 
are promiscuous and show no male parental care, do not exhibit 
social suppression of growth and reproduction. The possibility that 
social suppression changes over the period of a population cycle 
needs investigation in these species. 

Future research on phenotypic behavior should concentrate more 
on female behavior (see section on Multi-factor Tests). Manipu- 
lations of behavior should be attempted in the field to increase or 
decrease stress. The consequences of such experiments may shed 
more light on the possibility of phenotypic maternal transfer of 
stressed conditions. 


Genotypic-Behavior Experiments 


Tests of the polymorphic behavior hypothesis typically have pro- 
ceeded in two steps. First, measurable behavioral differences are 
demonstrated between populations changing over time. Standard- 


Population Dynamics and Cycles 603 


ized laboratory tests of agonistic or exploratory behavior are done. 
Second, these behaviors are shown to be heritable so that natural 
selection can operate on them. 

Both agonistic and exploratory behavior changed with population 
density in M. ochrogaster and M. pennsylvanicus in Indiana (Krebs, 
1970). Myers and Krebs (1971) found behavioral differences be- 
tween resident and dispersing individuals of these same species. 
Hofmann et al. (1982) tried to repeat these observations on both 
species in Illinois but were unable to verify changes in behavior 
over a cycle. Rose and Gaines (1976) failed to find a relationship 
between wounding and density during a population cycle of M. 
ochrogaster in Kansas. Rasmuson et al. (1977) measured locomotory 
behavior in M. agrestis from cyclic and non-cyclic populations in 
Sweden and found strong differences between populations. ‘hey 
also demonstrated that locomotor activity was highly heritable. An- 
derson (1975) estimated heritability of agonistic behavior in M. 
townsendi as zero. There are no other estimates of the heritability 
of any component of spacing behavior in any Microtus species. Con- 
sequently, it is not yet possible to test the suggestions of Krebs 
(1979) that annual fluctuations are associated with low heritabili- 
ties of agonistic behavior and that cyclic fluctuations are associated 
with high heritabilities. 

Several attempts have been made to test Chitty’s (1967) hypoth- 
esis with electrophoretic markers in blood proteins. But because we 
do not understand the physiological effects associated with most 
electrophoretic markers or their linkage groups, changes in electro- 
phoretic allele frequencies may no longer be necessary or sufficient 
to verify the hypothesis. At best, electrophoretic markers indicate 
the intensity of selection in field populations. LeDuc and Krebs 
(1975) manipulated the frequency of a leucine-aminopeptidase 
marker in field populations of M. townsend and found no mea- 
surable effects of altered allelic frequencies on population density. 
We now think that experiments of this type are unlikely to be 
fruitful because of the difficulty of assessing linkage groups in nat- 
ural vole populations. 

Several attempts have been made to determine if dispersers differ 
in allelic frequencies from resident voles. Gaines and McClenaghan 
(1980) recently reviewed these studies, and concluded that electro- 
phoretic markers are not likely to be useful in determining whether 
dispersal behavior is heritable. Three attempts to estimate the her- 


604 Taitt and Krebs 


itability of dispersal tendencies in Microtus populations produced 
suggestions of high heritability (Anderson, 1975; Beacham, 1979c; 
Hilborn, 1975), but the results may have been caused by maternal 
effects. If dispersal tendency is highly heritable and dispersal is 
critical for population fluctuations, we will have strong support for 
the polymorphic behavior hypothesis. 

Chitty (in press) suggested that adult body size in M. townsendit 
is controlled by a single major gene; large voles are homozygotes 
(AA) and so are small voles (aa). If this simple major gene effect 
can be shown to underlie cyclic changes of body size in Microtus, it 
will be critical to study spacing behavior of these genotypes. Chitty 
(in press) suggested that the large-bodied homozygotes are in fact 
the hypothesized docile genotypes that dominate populations 
undergoing density increases. These ideas have not been confirmed 
for any Microtus species. 

Attempts to test the genotypic-behavior hypothesis must rest on 
an estimation of the heritability of traits of dominance and spacing 
behavior for which few data exist at present. The most critical 
experimental approach would be to conduct an artificial selection 
experiment in a natural population, selecting for or against some 
form of spacing behavior and observing the demographic conse- 
quences. 


Multi-factor Tests 


In practice, those who invoke multi-factor hypotheses fall into 
two general groups. To the first group a multi-factor model com- 
prises food and predators almost exclusively, with perhaps some 
climatic effects included (for example, Keith, 1974; Oksanen and 
Oksanen, 1981; Stenseth, 1978). In principle, there is no difficulty 
in testing such two-factor hypotheses experimentally, but no one 
seems to have done so. 

To the second goup a multi-factor model involves food, predators, 
and social behavior. Lidicker’s (1973) discussion on M. calzfornicus 
dynamics is a good example of this approach. Social behavior can 
be looked at in two ways when it is part of a multi-factor hypothesis. 
Some authors view social behavior as a way of partitioning re- 
sources, so that it is the resources (usually food) that are critical 
(Lack, 1954). Others view social behavior as part of the life-history 
strategy in which individuals are trying to maximize their fitness. 


Population Dynamics and Cycles 605 


In these situations individuals may compete for “‘social status,” which 
is related only tenuously to resources (Wynne-Edwards, 1962). The 
central issue has become whether social behavior can regulate den- 
sity below the carrying capacity dictated by food and predators 
(Zomnicki, 1978; Verner, 1977). Since social behaviors can be in- 
fluenced by many variables (both phenotypic and genotypic), some 
population changes may occur in ways unrelated to resource levels. 

It is difficult to test multi-factor models that include social be- 
havior. Getz (1978) and his research group tested social-behavior 
hypotheses on laboratory populations of M. ochrogaster and are now 
applying them to field populations. Taitt and Krebs (1981, 1982, 
1983) tried to test a complex multi-factor model on M. townsend 
directly in field populations (Fig. 4). We do not know what factors 
determine the number of surplus voles in field populations or what 
factors determine the fate of surplus animals. We can gain insight 
by measuring social behavior while manipulating food and preda- 
tors, and vice versa. Because dispersal is a critical element in these 
population systems, open populations must be the experimental 
units. 

In what follows we consider two features associated with vole 
population dynamics for which multi-factor considerations may be 
most appropriate. The first, body weight, has a long association 
with the literature on small mammal cycles; the second, the role of 
females, has begun to receive attention over the last decade. 

Body weight.—Chitty (1952) observed that peak-density popu- 
lations of M. agrestis contained individuals of high body weight that 
were absent in low-density populations. All but one of the studies 
on Microtus listed as reporting cycles in abundance (Tables 1-6) 
found larger animals in peak populations. The exception was Gaines 
and Rose (1976), who reported no shift to heavier M. ochrogaster 
in a peak population. We do not know what the adaptive advantage 
of large size is for voles (Boonstra and Krebs, 1979); two contra- 
dictory hypotheses involving r-selection (Chitty, 1967) and a-selec- 
tion (Stenseth, 1978) have been suggested. 

Recent studies indicate that growth in voles is influenced by ex- 
trinsic factors. Iverson and Turner (1974) showed that mature M. 
pennsylvanicus lost weight in winter. Petterborg (1978) reported 
that M. montanus grew at a slower rate under a short photoperiod 
than under a long photoperiod. Beacham (1980) found that M. 
townsendi born in spring had higher growth rates than voles born 


606 Taitt and Krebs 


in any other season. M. townsendi in open populations grew 20% 
faster than voles in enclosures (Beacham, 19796); the density in the 
enclosures was higher than in the open populations (Beacham, 
1979a). Finally, Batzli et al. (1977) found that growth was sup- 
pressed by social conditions in M. californicus and M. ochrogaster. 
These results indicate that weight cannot be correlated simply with 
age. However, Mallory et al. (1981) used lens weight to age Di- 
crostonyx and found that lemmings in the peak year were signifi- 
cantly older and heavier than lemmings in low years, suggesting 
that high body weights in the peak year could be the result of age. 
Anderson (1975) did not find a strong genetic influence on growth 
rate or maximum body size in M. townsendi. Instead, she found 
that environmental effects made siblings resemble one another in 
growth rate, and that maximum size of offspring correlated with 
size of mothers. Further, female body weight is correlated positively 
with litter size in this species (Anderson and Boonstra, 1979). 
Iverson and Turner (1974) suggested that loss of weight in old 
and lack of weight gain in young M. pennsylvanicus in winter were 
adaptive responses possibly cued by day length. They suggested that 
these were general phenomena among north temperate small ro- 
dents. But both deermice (Peromyscus maniculatus; Taitt, 1981) and 
Townsend’s voles (M. townsendu; Taitt and Krebs, 1981) respond- 
ed immediately to extra food in winter by gaining weight, suggest- 
ing that winter weight loss simply could be a proximate response 
to food availability. Beacham (1980) reported that “heavy” male 
M. townsendiu (using =70 g as peak weights) in his cyclic popula- 
tion were animals that had gained weight throughout the preceed- 
ing (“increase’’) winter. Yet M. townsendi, given extra oats in late 
winter, gained weight so that mean weights of males and females 
were significantly higher than those on the control after only 2 
weeks. In this short period, 63% of the males became “heavy” (=70 
g) compared with 23% on the control (Taitt and Krebs, 1983). 
These results indicate that growth rates are highly labile. Work 
on M. townsend indicates that animals with sufficient food can 
maintain positive growth rates in winter and become “heavy” an- 
imals. Because the spring decline in numbers in the peak year is 
slight, many of these animals may survive so that some voles in the 
peak population are older and heavier, whereas animals born at the 
peak have reduced growth rates because of high population density. 


Population Dynamics and Cycles 607 


Such an explanation does not rule out a genetic basis for the morphs 
in peak populations (Chitty, in press). It could be that genotypes 
yielding potentially large body weight are not expressed phenotyp- 
ically until food conditions are adequate, particularly in the winter 
preceeding a peak. Body weight in laboratory mice is highly her- 
itable, but Roberts (1981) suggested that there may be a range of 
variation in weight over which there is little natural selection in 
wild populations. Also, Fulker (1970) suggested that maternal ef- 
fects (behavioral and endocrine) could act as a buffering mechanism 
on the expression of offspring genotypes in rodents. 

The phenomenon of body-weight changes in cyclic populations 
of Microtus will be understood only when both environmental and 
genetic influences on growth and weight are measured. 

Role of females.—“‘Little work has been done on female aggressive 
behaviour ....” (Krebs and Myers, 1974). This situation has be- 
gun to change in the last decade, although the challenge to do so 
had been made much earlier. Frank (1957) made the following 
observations on M. arvalis in Germany: 1) breeding females occu- 
pied a range around their burrows from which they drove out all 
other voles; 2) females tolerated a strange male in their home ranges 
only when they were in heat; 3) males inhabited irregular large 
areas in which they wandered from female to female in order to 
mate; 4) in spring, young males without exception disappeared from 
their mothers’ territory, but young females settled in the immediate 
vicinity; and 5) “great families” arose every autumn when the last 
two to three litters remained in the maternal home range to over- 
winter. In addition, Frank (1957) suggested that the social behavior 
of females—their tendency to remain together even if they move— 
might explain how peak populations arise. 

One way to determine the role of females in natural populations 
is to alter sex ratios by removal experiments. Redfield et al. (1978) 
began sex-specific removal experiments on field populations of M. 
townsendu in 1972. They found that female recruitment was re- 
duced in a population containing a majority of females and that 
there was an inverse relationship between the number of young 
voles recruited and the density of mature females (but not males). 
Further experiments on M. townsendi showed that juvenile survival 
was dependent on female (not male) densities (Boonstra, 1978), and 
that females responded before males to the addition of food (Taitt 


608 Taitt and Krebs 


and Krebs, 1981, 1983). Also, males exhibited better survival in a 
population of “‘passive” females (Taitt and Krebs, 1982) and “pas- 
sive’ males (Gipps et al., 1981). 

Research on other Microtus species also indicates that Frank’s 
(1957) observations may apply to species other than M. arvalis. 
Radiotelemetry work by Madison (1980) showed that mature fe- 
male M. pennsylvanicus occupy exclusive home ranges. Males, on 
the other hand, had large, overlapping, and more variable home 
ranges. Males also moved temporarily into areas occupied by es- 
trous females. These observations were confirmed by Webster and 
Brooks (1981) for M. pennsylvanicus in Ontario. Field observations 
on other small mammals indicate that mature females exert control 
on population growth by excluding subordinates (Leuze, 1976; Vi- 
itala, 1977), or tolerating those that delay maturity (Bujalska, 1973; 
Jannett, 1978; Saitoh, 1981). In the laboratory, Batzli et al. (1977) 
found that females had more influence than males on the suppres- 
sion of growth in M. californicus and M. ochrogaster. Finally, recent 
results on stress responses at high density also indicate that females 
are more responsive to stress and may subsequently affect their 
offspring accordingly (Geller and Christian, 1982). 

Perhaps mature females in the breeding season can be considered 
the equivalent of territorial male birds. They secure an area for 
raising young (Boonstra, 19776; Jannett, 1978), including ample 
food for lactation and space free from intraspecific intrusion. Pher- 
omones may be the advertising currency equivalent to bird song. 
Male Microtus are forced to forage in the interstices of these female 
territories (Madison, 1980) and compete among themselves for es- 
trous females (Boonstra, 1978; Krebs, 19785; Madison, 1980; Web- 
ster and Brooks, 1981). Although these features suggest a polyga- 
mous mating system, the degree of polygyny could be dependent on 
population density (Getz, 1978). 

Greenwood (1980) suggested that philopatry favors the evolution 
of cooperative traits between members of the sedentary sex. One 
such trait may be the phenomenon described by Frank (1957) in 
M. arvalis in which sisters from “great families,” and sometimes 
their mother, remain together and breed on a common territory 
when conditions are optimal. Frank (1957) postulated that this 
“condensation potential” enabled M. arvalis populations to reach 
outbreak densities. Taitt and Krebs (1983) suggested another fe- 
male behavior that might contribute to outbreaks. They argued that 


Population Dynamics and Cycles 609 


if conditions were favorable, all females may become reproductive 
simultaneously and that this might precipitate simultaneous settle- 
ment at higher than normal density, as observed in the spring of 
cyclic years in M. townsend (Fig. 2). Large simultaneous pulses 
of young could be produced; the offspring, in turn, might simulta- 
neously colonize any available habitat and so result in a spreading 
outbreak. Simultaneous settlement has been observed in territorial 
male birds by Knapton and Krebs (1974) and Tompa (1971). 

Female behavior, like growth rates, appears to be influenced by 
extrinsic and intrinsic variables. Do Frank’s (1957) observations 
apply to all species of Microtus? If so, what changes in territorial 
social organization precipitate a cycle in abundance? How do fe- 
males respond to stress at peak density, and how does this affect 
survival of offspring? We suggest that answers to these questions 
will probably be needed before we can understand cyclic fluctua- 
tions. 


Mathematical Models 


In spite of the recent increase in mathematical modeling of bi- 
ological populations, little work has been done on models of rodent 
populations. May (1981) summarized models for single-species 
populations. Beginning with a simple logistic model, one can add a 
time-lag and produce population curves that vary from stable to 
cyclic. The critical parameter is the time delay in the feedback 
mechanism that regulates population size. If the time delay is 9- 
12 months, the resulting populations trace cycles with a period of 
3-4 years. The simple message is that for voles, which have a 
similar range of values for innate capacity for increase (r), we are 
looking for a delayed density-dependent factor that lags 9-12 months 
behind population density in order to establish a cyclic population. 
For shorter time lags an annual cycle would be produced. The 
problem with this simple approach is that we cannot evaluate easily 
any of the suggested biological mechanisms producing time delays 
in real vole populations. 

Models of the food hypothesis were suggested by Rosenzweig 
and Abramsky (1980) based on a predator-prey interaction between 
voles and their food plants. Batzli (in press) used loop analysis to 


610 Taitt and Krebs 


analyze the brown-lemming cycle in northern Alaska and suggested 
that, if vegetation quality is important in generating population 
cycles, it is likely to be a function of plant secondary compounds 
rather than delays in nutrient recycling. Stenseth et al. (1977) pro- 
duced the most comprehensive and realistic model for a Muicrotus 
population. This model was based on the nutritional balance of 
individuals and how nutrition affects birth, death and dispersal. It 
includes some effects of predation and habitat heterogeneity, and 
thus begins to approach a multi-factor model. However, the model 
is intractable because it “is impossible to analyze in a manner pro- 
viding intelligible results or predictions” (Stenseth, pers. comm.). 

Models of the Chitty (1967) hypothesis have been analyzed re- 
cently by Stenseth (1981) to see if population cycles could be gen- 
erated by a genetic polymorphism. Stenseth (1981) argued that 
intrinsic factors alone cannot generate a cycle, and that the only 
tenable hypothesis is that population cycles are caused by the in- 
teraction of intrinsic and extrinsic factors. Stenseth (1978) shows 
how this type of model can lead to cycles or annual fluctuations. 
The relevant extrinsic factors are not identified in his model; pre- 
sumably weather, food, predators, or parasites could be involved. 

The general tendency in population modeling has been to make 
the models more complex and include many factors. The result has 
not been very useful for guiding field work on Microtus. The most 
comprehensive recent effort by Finerty (1980) on population cycles 
includes the use of loop analysis. But almost none of these modelling 
studies has suggested a critical experiment, and they remain largely 
a posteriori analyses. 


Discussion 


In their review, Krebs and Myers (1974) challenged the existence 
of non-cycling populations of microtines. However, the pattern of 
fluctuations revealed in the present review indicate that field pop- 
ulations of Microtus in North America (Tables 1-6) show annual 
fluctuations, multi-annual cycles, and sometimes both in combina- 
tion (Figs. 2, 3). We must, therefore, search for hypotheses which 
will allow a range of possible outcomes for density changes. 

We are now more knowledgeable of the affect of temporal het- 
erogeneity in population dynamics, but we are less well versed in 
understanding spatial heterogeneity. This is partly because most 


Population Dynamics and Cycles 611 


studies have been carried out in favorable habitats, and because it 
is difficult to trap in areas large enough to encompass several hab- 
itats. Habitat variation is interwoven with dispersal in population 
dynamics (Hansson, 1977), so it is not surprising that both these 
elements are poorly understood in vole populations. 

The history of Microtus population studies is checkered by a 
series of arguments about the role of single factors in causing pop- 
ulation fluctuations. We think that perhaps these arguments should 
be left to the past and that a new synthesis should be attempted. 
Perhaps this synthesis could be based on the premise that both 
extrinsic and intrinsic factors are involved in Microtus population 
fluctuations. A second premise could be that dominance and spacing 
behavior play a central role by potentially apportioning resources 
differentially among members of the population. 

The investigation of Microtus population dynamics, and rodents 
in general, is still an expanding field of ecological research. Useful 
advances in the future will come largely from field experiments 
designed with a strong hypothesis-testing structure. Many of these 
tests will be difficult to formulate because they must be done on a 
complex system and we do not, in general, know the degree of 
complexity. 

The present review of Microtus population dynamics reveals that: 
1) annual fluctuations reach maximum densities typically one-third 
of cyclic densities; 2) the amplitude of an annual fluctuation tends 
to be less than five-fold, whereas that of a cycle can be more than 
ten-fold; and 3) substantial spring declines (of both sexes) may be 
characteristic of annual fluctuations, whereas reduced spring de- 
clines (sometimes confined to males) accompany cycles. 

A number of specific questions has arisen from this review. Do 
dominance and spacing behaviors limit the breeding density of all 
Microtus populations? What restricts a population to a five-fold 
increase in density one year and yet allows it to reach a ten-fold 
increase to cyclic density in another year? If surplus voles are pro- 
duced by spacing behavior, is it simply their fate at the onset of 
breeding that produces the two patterns of spring decline? What is 
the role of environmental factors on the fate of surplus animals and 
what bearing does this have on the population dynamics exhibited 
by a population? Why is body-weight distribution different in the 
two population patterns? Are “heavy” voles genetically different or 
do favorable conditions prior to peak density contribute to weight 


612 Taitt and Krebs 


gain and longer lifespan? Are females more sensitive than males to 
environmental conditions such as food and cover? If so, is the spac- 
ing behavior of mature females the proximate mechanism of M:- 
crotus population regulation? Can maternal responses to stress be 
transferred to offspring? If so, what are the consequences at cyclic 
peak densities, and what is the time-lag of such responses? 

Answers to these questions may be incomplete if they ignore the 
possible genetic basis of the relevant ecological variables—growth, 
reproduction, response to stress, dominance and dispersal behavior. 
Future research should emphasize the heritability of these variables 
in individuals from populations exhibiting both annual fluctuations 
and cycles in abundance (for example, see Rasmuson et al., 1977). 

The paradigm suggested by this review is that future studies of 
Microtus population dynamics must address the two patterns of 
fluctuation. Field manipulations should be designed to test the in- 
teractions suggested, particularly between spacing behavior, food, 
and predation. The results should be related to the dispersal abil- 
ities of voles that enable them to exploit temporally favorable hab- 
itat, and to their potential to reach outbreak densities. 


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Population Dynamics and Cycles 619 


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MANAGEMENT AND CONTROL 
Ross E. BYERS 


Abstract 


URRENT Microtus control technology is reviewed with specific 
GC information on rapid population monitoring methods; chemi- 
cal, cultural, and biological control methods; economic threshold 
levels, rodenticide residues and environmental hazards. The merits 
of control methods based on barriers, habitat manipulation, repel- 
lents, predators, grazing of hoofed animals, trapping, baits, and 
ground-cover sprays are discussed. 


Introduction 


The national economic impact of vole damage to trees, shrubs, 
and agronomic crops has been a significant factor in crop produc- 
tion. Most of the information presented in this chapter pertains to 
the technology developed for controlling the pine vole (Microtus 
pinetorum) in apple orchards. 

From a control point of view there are two classes of voles in- 
festing orchards: 1) subterranean voles which burrow deep in the 
soil and which damage the plant below the soil level such as the 
pine vole (Microtus pinetorum) in the eastern U.S., and 2) surface 
running voles that damage at or above the soil level, such as the 
meadow vole (Microtus pennsylvanicus), montane vole (Microtus 
montanus), and the California vole (Microtus californicus). The prai- 
rie vole (Microtus ochrogaster) of the midwestern states develops 
runs on the surface similar to the meadow vole but also has a deep 
tunnel system similar to the pine vole. Vole feeding habits, however, 
vary considerably depending on availability of cover, loose soil for 
tunnelling, and the location and type of desirable food supplies 
(Bailey, 1924; Byers, 1979a; Dimmick, 1978; Hamilton, 1938; 
White, 1965). For example, M. californicus in plowed potato, sugar- 
beet, or artichoke fields is found largely underground or in the 
plants, whereas in orchards where tilling is minimal, in alfalfa, or 


621 


622 Byers 


in herbaceous cover, M. pennsylvanicus feeds largely along runways 
on the surface. Control and management of any vole species often 
requires an integrated knowledge of the crop being protected, the 
habits of the animals in the cultural system, the control methods 
available, and the potential hazard to man or non-target animals. 

Numerous reports indicate that voles may cause serious economic 
losses to apple, peach, pear, citrus, blueberry, nursery, ornamental, 
and strawberry crops by girdling the roots and stems, causing plant 
death. By direct feeding, voles may also cause serious damage to 
flower bulbs, tubers, vegetables, sugar beets, grain, sagebrush, al- 
falfa, pasture land, and hay crops (Bailey, 1924; Batzli and Pitelka, 
1970; Cummings and Marsh, 1978; Dana and Shaw, 1958; Little- 
field et al., 1946; Morrison, 1953; Mueggler, 1967; Piper, 1908, 
1928; Sariz,. 1970; Spencer, 1959:. Spencer et al.,/1953). 

Ferguson (1980) estimated from a 1978 national survey that ap- 
ple growers lost 123,000 trees to vole injury, of which 37% of the 
trees were of bearing age. In perennial crops the loss of an economic 
unit (such as an apple tree) influences the profitability of the plant- 
ing for its productive life (Byers 1979a). Even sporadic annual 
losses of less than 1% in tree fruit crops can result in a 20-30% 
tree loss in the most profitable years for the crop which is at 25- 
30 years of age. In orchards, serious vole damage usually occurs in 
a single year when growers are unaware of rising vole populations. 
In these situations it is likely that 30% of the trees may be com- 
pletely girdled in a single season while another 20% or more may 
be seriously injured. In plantings sustaining this level of damage, 
all trees (good ones as well) often must be removed (bulldozed) due 
to the uneconomical operation of the block. Thus, in many cases 
twice as many trees may be removed as are actually damaged. As- 
sessment of long-term production losses from single season surveys 
are difficult because growers usually remove vole-damaged trees 
quickly. Good tree stands must be maintained throughout the life 
of an orchard, forest, or ornamental planting in order to remain an 
economic unit. In addition, replacement trees planted in older vole- 
infested orchards are very difficult to protect from vole injury. Re- 
planted trees usually do not survive because inadequate attention is 
taken to prepare individual soil planting sites as is recommended 
for establishing new trees on old orchard sites. 

Anthony and Fisher (1977) estimated that Pennsylvania apple 
growers spent approximately $270,000 in 1974 for control of pine 


Management and Control 623 


and meadow voles. No estimate was made of the economic losses 
caused by vole damage to fruit trees for that year. 

Byers (1974a) estimated that the national apple market value 
losses caused by pine-vole damage in the eastern and midwestern 
apple-producing areas were approximately $40 million in the geo- 
graphic range of this species, while an additional $3.3 million was 
spent on control measures for that year. 

The use of toxicants, habitat manipulations, and barriers have 
been the traditional methods of arresting damage over the last 50 
years for most agricultural crops (Hamilton, 1935). The use of 
predators, repellents, and trapping have had limited use as com- 
mercially acceptable agricultural practices; however, trapping can 
be quite useful to home owners and small orchardists with fewer 
than three acres. 

For most agricultural crops the presence of voles may or may not 
pose an immediate threat. In many fruit-tree and ornamental plant- 
ings, vole damage is restricted to the dormant period from Novem- 
ber through April except during a drought or extremely high pop- 
ulation levels. In the late spring, summer, or early fall, more desirable 
food sources than tree roots and bark are plentiful. More important, 
however, may be more desirable temperatures which allow voles to 
forage over a greater range, accessing more desirable plant material, 
thus making the crop plant less vulnerable to damage. With mono- 
cultured crops such as vegetable or hay crops, damage is usually 
dependent on vole population levels and the developmental stage of 
the crop. In orchards, if control measures are not taken, vole damage 
is likely to occur annually. For this reason, the development of 
control methodology for eastern voles has been more intensive for 
apple orchards than for any other crop. 


History of Vole Control 
in Orchards 


Prior to 1935 voles were controlled largely through clean culti- 
vation of the entire orchard floor, tree guards, and hand-placed 
poison baits made of strychnine or arsenic (Hamilton, 1935). Bait- 
carriers composed of fresh vegetable matter were thought to be more 
desirable than grain or oat carriers for toxicants. Although repel- 
lents, natural enemies, trapping, and gassing were suggested meth- 


624 Byers 


ods for the period, rarely were these methods relied upon as the 
sole commercially acceptable vole control measure. 


Monitoring 


Regular assessment of vole populations in crops susceptible to 
vole damage requires rapid assessment of large acreages in short 
intervals of time. In high-valued crops, a preventive vole control 
program should be followed because the economic threshold for 
damage is at low population levels. The loss of a single 15-year- 
old apple tree in a 50-ha block may reduce the gross value of the 
crop by $2,500 over the subsequent 20 years of the planting. If 
season-long control can be achieved by a single rodenticide treat- 
ment costing $25/ha, 100 ha of this age tree could be treated to 
prevent the loss of a single tree. As the age of the planting gets 
older, the value of trees decreases, and thus the economic threshold. 
Since a single animal residing at or near a tree may cause significant 
damage or tree loss, the economic threshold population is at a very 
low level. Thus, a highly effective and reliable preventative pro- 
gram is essential for avoiding damage to perennial tree crops (Byers, 
in press). Regular monthly inspections just prior to the damaging 
period and after treatments can provide the grower with an accurate 
view of future potential hazard (Barden et al., 1982). 

Examination of the ground cover for vole runways and holes can 
quickly give an indication of the recent presence of voles. Obser- 
vations based on vole signs (fresh digging, trails, feeding on plant 
material, defecation) are not adequate, because immediately after 
treatment runways and holes still may appear to be active but voles, 
in fact, may be eliminated. If voles are present in the runway sys- 
tems, it must be assumed that a potential for vole damage exists in 
high-valued crops. Vole population levels and damage potential can 
change rapidly because of increased animal survival rates, increased 
reproduction levels, or changes in other environmental stress factors 
(snow, drought, soil freezing, ground-cover dormancy), and a sim- 
ple, rapid, and accurate method for determining animal presence is 
desirable for researchers and growers as well. 

The apple indexing method has been used in orchards for many 
years to determine the percentage of trees infested with voles (Bar- 
den et al., 1982). An apple with a 2.5-cm diameter slice removed 
from the cheek may be placed in a run or a hole for meadow voles 
or 5-15 cm below the soil surface in a tunnel for pine voles. Apples 


Management and Control 625 


Voles/ site 


Fic. 1. Regression of percent activity on pine voles/site based on percent of 
apples having vole tooth-marks when placed 2/tree in runways 24 h previous. Plots 
(87 plots in four experiments in 1975 and 1976) were snap-trapped for a 5-day 
period following apple-activity reading. The apple-monitoring method was highly 
correlated with pine-vole population densities (R? = 0.77, y = 7.5 + 78.0x — 17.7x?; 
from Byers, 1981). 


can be observed for vole tooth-marks 24 h after placement and the 
percentage of trees infested can be calculated easily. This calculation 
can give a direct estimate of the percentage of trees that could be 
damaged, given the proper environmental conditions. In addition, 
vole population densities correlate strongly with the percentage of 
active sites (Fig. 1). This method has been used to evaluate exper- 
imental plots and general orchard populations pre- and post-treat- 
ment (Byers, 1975a, 1978, 1981). When assessing chemical control 
treatments, a reading of pre-treatment activity taken prior to and 
again approximately 3 weeks after treatment can be used to deter- 
mine if a reduction in the percentage of infested trees has occurred. 

In order to increase the quantitative measure of the number of 


626 Byers 


animals at each feeding station, the apples are weighed prior to 
placement and after 24 h. Weighing the apple gives the grams of 
apples consumed on an individual tree basis. We determined that 
the amount of apple consumed for pine and meadow voles/24 h is 
approximately 0.5 g of apple per gram of body weight. The average 
pine vole should consume approximately 13 g/animal and the av- 
erage meadow vole about 20 g/animal. 


Barriers 


Currently, tree guards are used to control damage from prairie 
and meadow voles but not pine voles, since the latter species can 
easily tunnel under barriers (Caslick and Decker, 1978; Hamilton, 
1935; Hunter and Tukey, 1977). Crushed stone is used when in- 
stalling tree guards so that nesting and trailing near the tree trunk 
is discouraged (Bode et al., 1981). In conjunction with tree guards, 
clean herbicide culture of 1.2 to 2-m wide strips in young plantings 
inhibits meadow voles from ranging near the tree trunk. As the tree 
enlarges, removal of the tree guard becomes necessary in order to 
prevent the guard from girdling the tree. The tree then becomes 
vulnerable to vole attack, particularly under snow cover. 


Habitat Manipulation 


In orchards the major food sources for voles are normally not 
apple trees, but include roots, stems, petioles, and leaves of a di- 
versity of plants living on or below the soil surface (Cengel et al., 
1978). Laboratory studies showed that, given sufficient water, pine 
voles cannot survive for more than about 4 days on 1-year-old 
stem or root tissue from apple trees (Byers, 19746). Logically, if 
voles under field conditions cannot survive without a supplementary 
food source to apple trees, “‘clean culture” should reduce vole pop- 
ulations. 

Fifty years ago the term “clean culture” referred to total destruc- 
tion of the orchard-floor plant material through cultivation tech- 
niques. However, today, herbicide or cultivated strips from 5 to 12 
ft wide within the tree rows and close mowing between rows is 
classified as clean culture (Byers and Young, 1978; Davis, 1976a, 
19766). 

Field experiments have shown that clean culture can greatly as- 
sist in reducing existing pine vole population levels (Byers and 
Young, 1974, 1978; Byers et al., 1976). Techniques used to achieve 


Management and Control 627 


TABLE 1 
EFFECT OF AN ANNUALLY-APPLIED HERBICIDE STRIP ON AVERAGE PINE-VOLE AC- 
TIVITY PER TREE AFTER THE TENTH YEAR IN A COMMERCIAL APPLE ORCHARD 
(AFTER BYERS AND YOUNG, 1974)* 


No. sites No. active sites No. voles caught 

Herbi- Herbi- Herbi- 
Tree no. Control cide Control cide Control cide 
1 2.00 O75) 1.00 O25 1.50 0.50 

2 2.00 0.00 175 0.00 1.50 0.00 

3 2.00 0.00 1.50 0.00 1.50 0.00 

4 175 0.75 1275 0.25 2.00 0.25 
Average 1.96 0.40 1.50 Ons 1.64 0.20 


* Treatments and controls were initiated in the first year of planting and monitored 
for vole activity after the tenth annual application of herbicide culture. Eight blocks 
of four tree spaces each were alternated in a single row; thus tree 1 and 4 were 
adjacent to the other treatment. There were 15 trees in the herbicide treatment group 
and 14 controls (no herbicide). A site refers to a vole run or hole below the soil level 
which appeared to be active. A limit of two sites/tree was counted. Active sites were 
those having characteristic vole tooth-marks on an apple placed in a run or hole 
approximately 24 h previous. 


clean culture vary considerably between orchardists and years. Some 
of the variables are related to type of equipment used, frequency of 
the practice, soil characteristics (particularly rockiness, depth of 
friable soil, terrain), tree age, planting distances, width of herbicide 
(or cultivated) band, ground-cover flora, and weather conditions 
(Byers and Young, 1978). 

The use of clean culture may provide some degree of preventive 
protection from voles when 1) started in the first year of orchard 
planting, 2) the planting site has never been previously infested, 3) 
a wide strip of herbicide or cultivation is maintained in the tree 
row, and 4) regular close mowing of middles is practiced. 

The use of wide-band cultivation can be advantageous for the 
control of pine voles (Byers and Young, 1978; Byers et al., 1976). 
However, the tilling of soil usually provides conditions for meadow 
voles to tunnel in the loose soil; thus the animals obtain a below- 
soil accessibility to roots and trunk (Byers, 1979c). 

Three experiments at different locations showed that clean cul- 
ture achieved with wide-band residual herbicides (Table 1), wide- 
band cultivations (Fig. 2), or combinations of the two (Fig. 3), in 
conjunction with regular mowing between rows, can greatly reduce 


628 Byers 


Adjoining 
orchard 
cultivated 


O Uncultivated 
O Cultivated 


% Activity 


5 6 7 8 9 10 tl 12 7 8 3 
| 1973 | 1974 | 1975 


Fic. 2. Effect of wide-band cultivation and chlorophacinone (CPN) hand-placed 
bait on pine-vole activity. Symbols with arrows refer to time of application. Percent 
activity refers to percent of apples having vole tooth-marks when placed in runways 
24 h previous (from Byers et al., 1976). 


existing vole populations and subsequent hazard to trees. However, 
some locations are apparently more amenable to control of voles 
through cultural means than others (Byers and Young, 1974, 1978; 
Figs. 2, 3). If regular mowing is not practiced, voles may become 
abundant in row middles and may easily move under snow cover 
to damage tree trunks. 

Costs of maintaining clean culture are almost prohibitive and 
were determined to be as much as three times as costly as a hand- 
placed toxicant or broadcast-bait program (Byers, 1977a, in press; 
Sullivan; 1979): 


Hoofed Animals 


Cattle, sheep, and swine have been used to a limited extent for 
control of pine and meadow voles in eastern U.S. orchards (Hors- 
fall, 1953; Woodside et al., 1942). The disadvantages usually great- 
ly outweigh advantages. Spray materials used in orchards may con- 
taminate the ground cover so that meat or milk cannot be used for 
human consumption. Action by hoofed animals is usually incom- 
plete, slow, and swine or cattle may severely damage trees. 


Repellents 


Repellents have been extensively used for rabbit, deer, and wood- 
chuck damage control, but seldom used for vole control. Repellents 
were shown to be superior to rodenticides in tank studies where 
rodents were confined to repellent-treated trees, including roots 


629 


Management and Control 


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630 Byers 


(Luke and Snetsinger, 1975). In practical use, however, tunnelling 
voles gnaw on roots and stems below soil level where repellents 
cannot be applied. In addition, repellents may wash off during the 
course of the winter or may not be reapplied if snow is present. 

Horticulturists recognize that fruit tree species are different in 
their susceptibility to vole damage. Hunter and Tukey (1977) rated 
apple, pear, peach, cherry, apricot, and plum in descending order 
of preference, but no definitive data are available in the literature. 
Laboratory studies showed that a great deal of difference existed 
between susceptibility of various clones to vole damage. Crosses of 
R5 or PI 286613 with Malus pumila Mill were found to be less 
susceptible to damage when compared to Golden Delicious apple 
stems (Byers and Cummins, 1977; Cummins et al., 1983; Geyer 
and Cummins, 1980; Wysolmerski et al., 1980). 


Predators 


Because the economic threshold for vole damage occurs at very 
low population levels (Byers, in press) and because predator pop- 
ulations (snakes, owls, hawks, skunks, etc.; see Pearson, this vol- 
ume) usually lag behind the prey, natural predatory control never 
has been considered commercially important. Vole populations are 
usually lowest in late winter and early spring when predators are 
reproducing and defining territories. Thus when voles are increas- 
ing during late summer and fall, predators may no longer be re- 
producing (Hamilton, 1935; Howard et al., 1982). 

Mowing, spraying, picking, and post-harvest removal of dropped 
apples interefere with predator population increases. These activi- 
ties disturb all types of wildlife, including voles. Rotary mowers are 
particularly devastating to snake populations and larger mammals 
within an orchard. 


Trapping 

Snap-traps have been used extensively for estimating vole pop- 
ulations (Chapman and Overton, 1966) in experimental plots be- 
cause almost complete removal of all animals can be achieved in a 
3—5 day period (Byers, 1975a, 1978, 1981) if done at critical periods 
when voles are susceptible to trapping. Many vole species, however, 
may not be as susceptible to trapping in summer when temperatures 
are high, during dry conditions, or when underground burrow sys- 


Management and Control 631 


tems have been developed. In fall when temperatures are ideal for 
vole movements, and in late winter while the soil is thawing, even 
pine voles can be trapped easily. ‘Trapping success can be enhanced 
by pre-baiting with apples, using covers over traps, and by placing 
traps in active runs at intervals (for example, at every tree, 100/ 
ha). Split tires can be used satisfactorily as trapping stations because 
they are convex and may be easily located in the fall when leaves 
may cover other types of flat stations. Because tires are black they 
retain heat, thus providing a warm, protected location for voles in 
adverse weather. Tires may be obtained without cost at many auto 
service centers or from commercial dumps where tires are split 
before covering. Commercial tire-splitting equipment is also avail- 
able for purchase. 


Chemical Controls 


During the post-1935 period, zinc-phosphide grain and vegetable 
baits developed by the U.S. Fish and Wildlife Service were impor- 
tant for the control of meadow voles in many agronomic and tree- 
fruit crops. Zinc-phosphide grain formulations, however, have not 
given adequate control of pine voles under most circumstances (Byers 
et al., 1976, 1982; Merson and Byers, 1981). Broadcast baiting 
with zinc-phosphide (Zn,P,) grain baits was found to kill only 50- 
60% of pine voles in a population (Byers et al., 1982). The failure 
of Zn,P, to adequately control pine voles was previously thought to 
be related to the differences between the two species, their accep- 
tance of grain carriers, or the inadequate exposure of pine voles to 
surface applied bait. 

Recent laboratory and field evaluations of zinc-phosphide pellet- 
ed bait show that wide differences exist between formulations. At 
least 27 formulations of Zn,P, are now listed with the Environ- 
mental Protection Agency, but very few have been compared for 
their lethality to any species in the laboratory or field. Greater 
differences in mortality have been shown to exist between formu- 
lations than between species for a number of Zn,P, formulations 
(Merson and Byers, 1981). The zinc-phosphide Rodent Bait AG 
formulation made by Bell Laboratories, Inc., recently has become 
extremely important to the fruit industry as a hand-placed and 
broadcast bait against both meadow and pine voles. Further im- 
provement of zinc-phosphide formulations through encapsulation 


632 Byers 


of the Zn,P, or changes in inert ingredients may continue to im- 
prove the lethality of this old toxicant and provide a different mode 
of action from the anticoagulants. 

In 1955 endrin became available to the apple industry as a ground- 
cover spray at the rate of 2.4 lbs/acre. Horsfall (1956a, 19566) was 
instrumental in determining rates, application techniques, and the 
significance of the ground-cover plant communities in the successful 
application of ground-cover sprays (Horsfall et al., 1974). After 10 
years of annual endrin use, growers complained about inadequate 
vole control and subsequent tree losses. Investigations in Virginia 
showed that some vole strains were 10 times more resistant to en- 
drin than voles taken from untreated orchards (Hartgove and Webb, 
1973; Webb and Horsfall, 1967; Webb et al., 1972, 1973). How- 
ever, in other eastern U.S. states (North Carolina, Pennsylvania, 
New York) where endrin was less frequently used, resistance was 
not reported to be a major problem in most orchards by the early 
1980s (Byers 1979b, 1980). 

By the late 1960s the vole problem became a major threat to the 
Virginia apple industry because of the development of endrin re- 
sistant pine voles. Since no alternative measure existed for the con- 
trol of the pine vole, Horsfall et al. (1974) investigated a number 
of toxicants and found the anticoagulant, chlorophacinone, was 
effective at 0.2 lbs/acre and above as a ground-cover spray. Since 
anticoagulants were rather expensive, the lowest rate of chloro- 
phacinone (CPN) that gave control was given use clearances by 
several states in 1974. Inconsistent results were obtained with CPN 
ground sprays in the years following its initial introduction (Byers, 
1975a, 19756; Byers et al., 1976). By the early 1970s the Environ- 
mental Protection Agency was not favorable toward the clearance 
of new ground-sprayed rodenticides for replacement of endrin. In 
addition, changes in orchard spray equipment for insect and disease 
control from high-pressure machines to low pressure and low-water 
volumes caused an increase in the costs of rodenticide applications 
and lower cost methods were developed. 

During the 1970s new bait formulations, cultural control meth- 
ods, and animal habits and biology were under intensive investi- 
gation with emphasis on finding new solutions to the tree damaging 
problem (Byers, 19776). Rodenticide-bait formulations developed 
by chemical companies for the commensal rodent trade were adapt- 
ed for use in agriculture. This resulted in state approval for many 


Management and Control 633 


anticoagulant baits and caused a return to hand-placed and broad- 
cast baiting followed by an understanding of the failure of previous 
zinc-phosphide bait programs. Excellent control with broadcast an- 
ticoagulent bait programs showed that the failure of Zn,P, broad- 
cast baiting programs was related to poor acceptance of the for- 
mulation and not access of animals to bait (Byers, 1981; Byers et 
al., 1982; Merson and Byers, 1981). 

Great differences between toxicants, formulations, and consump- 
tion time required for lethal doses resulted in some formulations 
outperforming others in vole field tests (particularly anticoagulants; 
Byers, 1978, 1981; ‘Table 2; Fig. 4). Due to lack of laboratory 
methods for testing formulations, the evaluations of toxic baits were 
conducted primarily in the field where population levels, weather, 
and animal access to highly preferred alternate food sources (apples 
and lush ground cover) were a part of the testing program (Byers, 
1978, 1981; Byers and Young, 1975). However, concurrent labo- 
ratory studies could have provided much useful information relative 
to quantities and exposure times required to achieve lethal doses 
from various bait formulations. 

Since the hoarding of toxic-pelleted baits by pine voles was quite 
strong in the field, this behavioral characteristic was incorporated 
into control methodology (Byers et al., 1976). Using radiotelemetry 
techniques, transmitters were implanted in pelletized Chloropha- 
cinone baits and placed in pine-vole runway systems. Pelleted bait 
placed with the transmitter was removed from the placement sites 
to more centralized caches near the pine-vole nests and located 25 
cm or more below the soil surface (Byers et al., 1976). Wax-block 
formulations (2.5 x 5 x 5 cm) used in rat-control programs were 
found less effective presumably because the bait was fed upon only 
at the placement site (Byers et al., 1976). Pelletized baits became 
accepted by the fruit industry very quickly because of their relatively 
low cost, ease of handling, and the need for more effective control 
measures. 

It was not until the 1980s that field experiments were conducted 
to determine if the caching behavior differed between pine and 
meadow voles. Laboratory-tank tests and caged trials showed both 
species exhibited a strong caching behavior (Merson and Byers, in 
press). However, in one field experiment three different pellet sizes 
were placed at 20 sites each. Using live-trap, toe-clip, and release 
methods, sixty pine voles were trapped over a 5-day period in one 


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Management and Control 635 


OPN 
hand bait 


Endrin Spray 
"aN 


OPN 


U hong bait 


OPN 
ri v0 ome 


cen 


hand bait 


Endrin spray 
CPN spray 

OPN hand bait 
CPN hand bait 
BFC hand bait 


< 35rc 
hand bait 


%e Activity 


& CPN 
hand bait 


oo0m80D 


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3 4 5 6 7 8 7 8 9 10 It 12 
Month (1974-1975) Month (1976-1977) 


Fic. 4. Endrin applied at 2.7 kg/ha (2.4 lb/acre) did not control pine voles 
(probably because of endrin resistance). Symbols with arrows refer to time of treat- 
ment. Percent activity is percent of apples having vole tooth-marks when placed in 
runways 24 h previous. Chlorophacinone (CPN) ground spray applied at 0.2 kg/ha 
(0.2 lb/acre) gave some control. Both chlorophacinone and diphacinone (DPN) hand- 
baits at 11.2 kg/ha (10 lbs/acre) were effective when applied in Feburary 1975. 
Endrin applied in November 1976 did not give adequate control. Two applications 
of DPN bait did not give adequate control in 1977 but bromodialone (BFC) gave 
excellent control (from Byers, 1978). 


orchard and in another orchard 50 meadow voles were trapped. 
(Using the Schnabel estimator 91 [60 to 136] pine voles and 47 [36 
to 62] meadow voles existed in the plots, respectively). In the pine- 
vole orchard approximately 60% of the sites had animals which 
cached half or more of the 50 g placed at the sites within a 24-h 
period. Less than 1% of the sites in the meadow-vole orchard had 
cached bait. This study took place in December 1980 near the end 
of the normal fall control period when caching by both species 
should have been strong (Merson and Byers, in press). Obviously, 
if the majority of meadow voles are sporadic feeders (not feeding 
from cached bait), they probably would not obtain a lethal dose of 
weak multi-dose anticoagulants if bait were placed at only one or 
two sites within the vole range. Anticoagulants such as chloropha- 
cinone or diphacinone may be expected to give better control of pine 
voles since they could be fed upon from bait cached near nests. 
Much work on the caching response under field conditions is needed 
to understand better the success and failure of different toxicants 
and pelleted formulations for each species. 

Recent data have shown that both acute and chronic baits control 
voles equally well when used against pine voles, whether applied 
as a broadcast or a hand-placed bait (Table 2). When baits are 
broadcast, the quantity of bait required on the orchard floor may 


636 Byers 


depend on the lethality of the bait as well as pellet density. The 
notion that pine voles do not sufficiently surface and thus do not 
retrieve sufficient surface-applied bait has been disproven in recent 
years in Virginia orchards (Byers et al., 1982; Table 2). The gen- 
eralization that broadcast applications are effective in all orchard 
or agricultural situations for microtines can be seen from these 
experiments to be an over-simplification. For example, voles cannot 
be controlled by surface-broadcast baits in bluegrass sods that pro- 
mote trailing below a thatch cover. 

Pelletized-bait formulations absorb moisture readily and are more 
susceptible to water deterioration in rainy weather than whole or 
cracked grains. Laboratory data have shown that 3 days of contin- 
uous feeding and consumption of approximately 10 g of chloropha- 
cinone bait/pine vole are required for 90% of animals to receive a 
lethal dose (Byers, 19766, 1978). Field results have shown reduced 
control where chlorophacinone (CPN) bait has been broadcast 1 
day prior to a rain, and 3 days without rain are thought to be 
required for adequate pine vole exposure and caching of bait. Res- 
idue analysis of voles from an orchard treated with the single-dose 
anticoagulant, brodifacoum (BFC) bait, showed that 95% of the 
meadow voles contained a detectable level of toxicant 1 day follow- 
ing treatment (Merson et al., 1984). Toxicants such as warfarin, 
which require numerous days of continuous feeding, probably would 
have limited usage when applied as hand-placed or broadcast baits 
because spoilage probably would occur before voles received a lethal 
dose. 

In order to develop low-cost and effective bait formulations for 
field use, these factors must be considered: 1) the time required for 
the population to contact the bait, 2) the consumption required to 
deliver a lethal dose, 3) weatherability of the bait in the field, and 
4) pellet sizes and density for optimum caching and feeding. Acute 
baits like 2% zinc phosphide, which have a quick action and taste 
aversion, have the advantage of low consumption for lethality (0.25 
g/vole) but the disadvantage of poor acceptance. Theoretically, the 
“acute” baits should require rates that are sufficient only to expose 
the vole to a single pellet within its home range (5 kg/ha or less), 
whereas bait that requires relatively large consumptions over a pe- 
riod of days may be more dependent on the quantities presented 
within the home range of the vole. 

Spoilage of bait in the field within 2 weeks after application has 
both advantages and disadvantages. Hazard to non-target species is 


Management and Control 637 


increased with highly weather-resistant formulations, which might 
last months or years, but reduced effectiveness may occur if weath- 
erability is not adequate. Packaging of bait in plastic packages has 
been shown to repel moisture while still being available to the voles. 
Placement of packaged bait under substantial bait-station covers 
(e.g., split tires, rubber mats, shingles) is desirable to prevent a non- 
target primary hazard. ‘Testing of two packet types against pine 
voles in field trials showed that voles did not open packets at ap- 
proximately 5% of the placement sites even though animals were 
known to be present (Byers, 1981; Byers et al., 1982). Sufficient 
numbers of animals appeared to be present to repopulate the or- 
chard because packets were continuously being opened in the post 
treatment period (Fig. 5). ‘The use of automobile tires split longi- 
tudinally and small open-top plastic cups to prevent soil contact 
with bait promotes good baiting conditions for at least 6 months 
(Merson and Byers, unpubl. observ.). Shingles or rubber mats that 
lay flat on the soil are easily covered by leaves, making baiting 
difficult. Since tire stations may be 6-10 cm above the soil level 
they may be easily located by personnel, but may cause difficulty 
for close mowing or cultivation operations. The use of smaller, 
compact automobile tires allows closer and less inhibited mowing 
operations. The black automobile tire retains heat and provides an 
ideal location for placement of bait in winter. 

Some orchardists place tires in the tree row while using band- 
herbicide applications wider than the tire. The disadvantage of this 
system is the poor exposure of voles to tires, because voles are 
seldom active in the herbicide band. If the herbicide band is nar- 
rower than the tire, some of the tire extends into the vegetation 
strip where the voles range. If a wide band herbicide strip is used, 
movement of the tire into adjacent cover is necessary when baiting. 

Invasion of voles from nearby fields can be reduced by perimeter 
baiting of orchards with tire stations. This system also provides 
some year-round protection even under heavy snow cover. If acute, 
rapid-kill baits are used, as little as 1 lb of formulated material/ 
acre (Byers et al., 1982) is required. However, the potential for 
bait shyness with toxicants like zinc phosphide requires rotation to 
toxicants that do not promote this characteristic. 

Several chemicals have potential use as rodenticides for vole con- 
trol. ‘Their eventual commercial use depends upon several factors: 
1) clearance from federal and state agencies, 2) non-target hazards, 
3) effectiveness, 4) profit potential as a world wide vertebrate con- 


100 oA @ % Active Apples -Tires Ni 
/ 4 % Active Apples - Blocks 
90 © O Hee O % Packets Opened - Tires ' 
AG o o 7 o o QO % Packets Opened - Blocks A 
7a 0 
70 a 


% Active Sites 


10 iP Xe) 
or 1180 
Ae Z a ae ee es Va ne 91) 


A M J J A S O N D J F M A M J J A S O N OD 
Month (1979-1980) 
Fic. 5. Effect of bromodialone (BFC) and Zn,P,zp packets on percent activity, 


which refers to percent apples with vole tooth-marks ( ) or percent packets opened 
(---) by voles when either was placed under cinder blocks or split-tires 24 h 


previous. Note that pine-vole populations were maintained uniformly low, but were 
not eliminated. In addition, a large percentage of packets was opened during summer, 
which indicates presence of voles under most trees and the annual need for placement 
of packets. Points followed by the same letter for percent activity (small letters) or 
percent packets opened (capital letters) are not statistically different for each sample 
date by Duncan’s multiple range test (P > 0.05) (from Byers et al., 1982). 


trol agent, and 5) consistent supply. In recent years, antimetabolites 
of vitamins B, C, and K, anticoagulants, chlorinated hydrocarbons, 
chemosterilants, inorganic toxicants, fumigants, organic phosphates, 
narcotics and inhibitors of feeding and functions of heart, muscle, 
and immune systems, intestinal microflora inhibitors, and mechan- 
ical action materials that cause a blockage in the digestive system 
have been studied for their rodenticide potential (Benjamini, 1982; 
Gutteridge, 1972; Marsh and Howard, 1976; Meehan, 1980a, 
19806; Merson and Byers, unpubl. observ.; Stehn et al., 1908; Ti- 
etjen, 1969). Many of these chemicals have great potential as safe 
and reliable rodenticides, but many have been discarded because of 
taste aversion and bait shyness. 


Mechanical Spreaders 


The degree of control achieved by broadcasting bait with a ground 
or aerial spreader may be quite variable since the types of distri- 


Management and Control 639 


bution equipment vary greatly in 1) placement accuracy under tree 
limbs where vole runways exist, 2) rate of distribution when weight 
of bait in the hopper changes, 3) degree of pulverization of pellet- 
ized bait before distribution, 4) precision of control over hopper 
opening of the distribution box, 5) clogging of hopper opening by 
irregular pellet sizes, and 6) throwing distance and pattern of dis- 
tribution by the spreader. 

Burrow-builder equipment has been used successfully in some 
forest and agronomic crops for distribution of grain bait (Anony- 
mous, 1957, 1968); however, they have not been very useful in 
orchards because of the wide variation in soil type, sod density, and 
rock content. 


Combination of Control Methods 


The use of toxicants, cultivation, herbicide strips, barriers, close 
mowing, and predators may have additive or counterproductive ef- 
fects on reducing populations. The application of broadcast bait or 
ground-cover sprays to cultivated or herbicided strips may greatly 
reduce the exposure of the population to the chemical. Integration 
of the rodenticide program with regard to the cultural system is 
extremely important for good results. Even though the use of cul- 
tural programs may reduce the vole hazard, the costs associated 
with the cultural program are questionable if chemical control is 
required (Byers, in press). 


Environmental Hazards and 
Chemical Residues 


The hazards of using rodenticides in low-acreage, high-valued 
crops is often confused with large acreage usage such as in forest 
or other areas where wildlife may have a high priority in the scheme 
of things (Anthony and Fisher, 1977; Bailey et al., 1970). Simply 
plowing a field, cultivating an orchard, or picking fruit in an or- 
chard interrupts and disturbs more existing wildlife than the ap- 
plication of a rodenticide. Only recently has man become aware or 
concerned about the encroachment of houses, buildings, and con- 
crete on agricultural crop and forest lands. Orchard acreage has not 
changed in the U.S. in the last 30 years even though production 
has increased. I suggest that the problems associated with wildlife 


640 Byers 


are much more affected by housing, industrial zoning, highway 
construction, and increasing human population levels than the use 
of rodenticides for a specific low-acreage high-valued crop. Toxi- 
cants used to kill mammalian pests may have some degree of risk, 
depending on how they are used, to other wildlife present. We must 
recognize that cultural practices may affect wild animal populations 
to a much greater extent than chemicals; overreaction to some wild- 
life kill may not be justified. Proper labelling and use-patterns of 
rodenticides may require the acceptance of some reasonable risks 
when costs or production benefits are significant. 

The current use of most rodenticides in orchards during the dor- 
mant season has been classified as non-food usage because they are 
not applied directly to the edible plant part during the growing 
season and are not translocated through plants. Some crops such as 
artichokes, vegetables, grains, and hay require food-usage labels or 
specific application directions to avoid contact with the food product. 

Of the toxicants used as a ground-cover spray in orchards, Endrin 
has been the most toxic and persistent. Much controversy surround- 
ed the use of this material after its clearance in 1956 (Driggers, 
1972; Eadie, 1961). Regardless, Endrin was used widely throughout 
the world for about 15-20 years. Many European countries and 
some states of the United States since banned its use for vole control. 
Poor handling of empty containers and Endrin spills into farm 
ponds or streams leading to larger bodies of water resulted in some 
fish kills and a ‘‘bad name’”’ for this material. However, when En- 
drin was used according to labeled directions, few if any problems 
were documented. 

The acute toxicant Zn,P, has been considered one of the more 
safe secondary hazard toxicants. Bell and Dimmick (1975) showed 
little hazard to red and gray foxes and great horned owls that fed 
on prairie voles poisoned with Zn,P,. This compound was limited 
in its use for vole control to a single treatment because of its taste- 
aversion properties, which produce bait shyness in the surviving 
population. In addition, only recently have formulations of Zn,P, 
been available (ZP Rodent Bait from Bell Labs) that are sufficiently 
effective to be considered good field rodenticides. 

The potential for primary or secondary hazards of the anticoag- 
ulants to non-target animals was demonstrated in the laboratory 
(Evans and Ward, 1967; Mendenhall and Pank, 1980), but evi- 
dence for significant primary or secondary hazards to pets and wild- 


Management and Control 641 


life under proper label use patterns in the field has not been dem- 
onstrated nor compared to existing toxicants such as zinc phosphide 
(Kaukeinen, 1982). Certainly any toxicant poses a risk or hazard 
under some circumstances or with improper usage. The degree of 
hazard and its value to society must be kept in proper perspective 
with existing technology. 

Because of the increased cost of obtaining federal approval for 
minor-use rodenticides and the low potential profit for chemical 
companies, the continued development of safer and more effective 
rodenticides has been greatly curtailed in the last 10-15 years. Ob- 
viously, when new rodenticide development is inhibited, older and 
inferior technology must be relied upon. 

Increasing EPA requirements for chemical-fate and non-target 
hazard evaluation of agricultural rodenticides has caused chemical 
companies to apply for state permits. Because of the sporadic use 
pattern of most agricultural rodenticides on high-valued, low-acreage 
crops, state labels have been important to the introduction of new 
toxicants, which allows companies to sell the product while con- 
tinuing to collect data on various aspects of its use pattern. 


Concluding Remarks 


Effective rodent-control methodology for use in agriculture has 
not developed as rapidly as insect, disease, and weed-control 
methodology for several reasons. First, rodents affect crops more 
sporadically and inflict less damage in major agricultural crops. 
Second, because rodents are on a high evolutionary scale, chemical- 
control agents are more likely to be hazardous to other mammals 
or man. Third, the profitability of a new agricultural rodenticide 
may not warrant chemical-company research and development costs 
considering the limited and diverse markets for such products. 
Fourth, the organization of animal control agencies with the U.S. 
government is within the Department of Interior, whose primary 
responsibility is conservation of wildlife. The U.S. Department of 
Agriculture has the primary responsibility to develop methods for 
crop protection from pests but does not have the responsibility in 
cases in which wildlife is involved. In the past, most rodent-control 
efforts have been crash programs designed to find an immediate and 
economical solution to an agricultural pest problem. Even though 


642 Byers 


overlapping responsibility should exist between the U.S. Depart- 
ment of Agriculture (USDA) and the U.S. Department of Interior 
(USDI), the USDA does not have a pest-mammal control section. 
Instead, commodity-oriented specialists within the Land Grant state 
universities have been pressured in the past by agricultural groups 
to find methods of control. Even though animal biologists and ecol- 
ogists may be equipped better to develop new and innovative tech- 
nology, in the past they did not address the problem with vigor. 
The organization of wildlife damage-control responsibilities within 
the universities also does not encourage the development of control 
technology since most wildlife departments are more conservation 
minded. In addition, since no direct relationship exists between 
professional wildlife specialists and growers, the luxury of not hav- 
ing to solve an immediate pest problem exists. If effective animal 
control methods are to be developed, we must recognize that long 
periods of time, financial commitment, and priority reorganization 
will be required before cost effective, easily applied methods are 
available. 


Literature Cited 


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Serv., Boston, Massachusetts, 13 pp. 

1968. Orchard mice... the underground suboteurs. Amer. Fruit Grower, 

88:17-19, 26. 

ANTHONY, R. G., AND A. R. FISHER. 1977. Wildlife damage in orchards—a need 
for better management. Wildl. Soc. Bull., 5:107-112. 

BAILEY, S., P. J. BUNYAN, C. M. JENNINGS, AND A. TayLor. 1970. Hazards to 
wildlife from the use of DDT in orchards. Pesticide Sci., 1:66-69. 

BaiLey, V. 1924. Breeding, feeding, and other life habits of meadow voles (Micro- 
tus). J. Agric. Res., 27:523-541. 

BARDEN, J. A., et al. 1982. Virginia spray bulletin for commercial tree fruit grow- 
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15-16. 

Batz.i, G. O., AND F. A. PITELKA. 1970. Influence of meadow mouse populations 
on California grassland. Ecology, 51:1027-1039. 

BELL, H. B., AND R. W. Dimmick. 1975. Hazard to predators feeding on prairie 
voles killed with zinc phosphide. J. Wildl. Mgmt., 39:816-819. 
BENJAMINI, L. 1982. Biocontrol of rodents: the use of immunosuppressants as a 
control agent. Pp. 22, in Abstracts of papers, Third Internatl. Theriol. 
Congr. (A. Myllymaki and E. Pulliainen, eds.). Helsinki, Finland, 313 


es 

Bopbe, W. M., et al. 1981. Tree fruit production guide. Pennsylvania State Univ. 
Coop. Ext. Bull., 88 pp. 

Byers, R. E. 1974a. Pine mouse control in apple orchards. Mountaineer Grower, 
335:3-13. 


Management and Control 643 


—. 19746. Susceptibility of apple and peach stems to attack by pine voles. 
Hortscience, 9:190-191. 

—. 1975a. A rapid method for assessing pine vole control in orchards. Hort- 
science, 10:391-392. 

——. 19756. Effect of hand baits and ground sprays on pine vole activity. 
Hortscience, 10:122-123. 

——. (ed.). 1977a. Proceedings of the first eastern pine and meadow vole sym- 
posium (R. Byers, ed.). Winchester, Virginia, 113 pp. 

———. 1977b. Pine vole control research in Virginia. Pp. 88-100 in Proceedings 
of the first eastern pine and meadow vole symposium (R. Byers, ed.). 
Winchester, Virginia, 113 pp. 

———.. 1978. Performance of rodenticides for the control of pine voles in orchards. 
J. Amer. Soc. Hort. Sci., 103:65-69. 

——. 1979a. Highlights of pine vole research in Virginia. Mountaineer Grower, 
394:12-15. 

——. 19796. Highlights of the third eastern pine and meadow vole symposium. 
P. i, in Proceedings of the third eastern pine and meadow vole symposium 
(R. Byers, ed.). New Paltz, New York, 86 pp. 

———. 1979c. Controls to stop voles. Amer. Fruit Grower, 99:14-15, 22-23. 

—. 1980. Highlights of the fourth eastern pine and meadow vole symposium. 
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sium (R. Byers, ed.). Hendersonville, North Carolina, 91 pp. 

———. 1981. Pine vole control with anticoagulant baits in orchards. J. Amer. 
Soc. Hort. Sci., 106:101-105. 

———. In press. Economics of Microtus control in eastern U.S. orchards. /n The 
organization and practice of vertebrate pest control (Tropical Pest Man- 
agement, ed.). Center Overseas Pest Res., London, England. 

Byers, R. E., AND J. N. Cummins. 1977. Variations in susceptibility of apple 
stems to attack by pine voles. J. Amer. Soc. Hort. Sci., 102:201-203. 

Byers, R. E., AND R. S. YouNG. 1974. Cultural management of pine voles in 

apple orchards. Hortscience, 9:445-446. 

1975. Pine vole control with anticoagulant baits. J. Amer. Soc. Hort. Sci., 

100:691-694. 

——.. 1978. Effect of orchard culture on pine vole activity. J. Amer. Soc. Hort. 
Sci., 103:625-626. 

Byers, R. E., M. H. MERSON, AND S. D. PALMATEER. 1982. Control of orchard 
voles with broadcast baits. J. Amer. Soc. Hort. Sci., 107:631-637. 

Byers, R. E., R.S. YOUNG, AND R. D. NEELy. 1976. Review of cultural and other 
control methods for reducing pine vole populations in apple orchards. Pp. 
242-253, in Proceedings of the seventh vertebrate pest conference (C. Siebe, 
ed.). Monterey, California, 323 pp. 

CasLick, J. W., AND D. J. DECKER. 1978. Control of wildlife damage in orchards 
and vineyards. Cornell Univ. Coop. Ext. Inf. Bull., 146:1-18. 

CENGEL, D. J., J. ESTEP, AND R. L. KIRKPATRICK. 1978. Pine vole reproduction 
in relation to food habits and body fat. J. Wildl. Mgmt., 42:822-833. 

CHAPMAN, D. G., AND W. S. OVERTON. 1966. Estimating and testing differences 
between population levels by the Schnabel estimation method. J. Wildl. 
Memt., 30:173-180. 

CUMMINGS, M. W., AND R. E. MarsH. 1978. Vertebrate pests of citrus. Jn The 
citrus industry (W. Reuther, L. D. Batchelor, and H. J. Webber, eds.). 
Univ. California Press, Berkeley, 4:237-273. 

Cummins, J. N., H. S. ALDWINCKLE, AND R. E. BYERS. 1983. ‘Novole,’ an apple 
stock resistant to environmental hazards. Hortscience, 18:772-774. 


644 Byers 


Dana, R. H., AnD D. H. SHAW. 1958. Meadow mouse control in holly. Bull. 
California Dept. Agric., 48:224-226. 

Davis, D. E. 1976a. Management of pine voles. Pp. 270-275, in Proceedings of 

the seventh vertebrate pest conference (C. Siebe, ed.). Monterey, Califor- 

nia, 323 pp. 

19766. Management of pine voles. North Carolina Agric. Ext. Serv., Zool. 

Series, 9:1-2. 

Dimmick, R. W. 1978. Microtine rodents in Virginia pine plantations: their ecol- 
ogy and measures for population control. /n Proceedings of the symposium 
on management of pine of the interior south, Knoxville, Tenn. USDA 
Forest Serv. Tech. Publ., SAT P2:130-134. 

DriGcErRs, B. F. 1972. Ground spraying with endrin to control orchard mice may 
result in severe tree damage by the meadow mouse, Microtus. Hort. News, 
52:18-20. 

Eapig, W. R. 1961. Control of wildlife damage to orchards. Cornell Univ. Ext. 
Bull., 1055:1-16. 

Evans, J., AND A. L. WARD. 1967. Secondary poisoning associated with antico- 
agulant-killed Nutria. J. Amer. Vet. Med. Assoc., 151:856-861. 
FeRGuSON, W. L. 1980. Rodenticide use in apple orchards. Pp. 1-8, in Proceedings 
of the fourth eastern pine and meadow vole symposium (R. Byers, ed.). 

Hendersonville, North Carolina, 91 pp. 

Geyer, L. A., AND J. N. CUMMINS. 1980. Textural and taste influences on gnaw- 
ing by pine voles. Pp. 43-49, in Proceedings of the fourth eastern pine 
and meadow vole symposium (R. Byers, ed.). Hendersonville, North Car- 
olina, 91 pp. 

GUTTERIDGE, N. J. A. 1972. Chemicals in rodent control. Chem. Soc. Rev., 
1:381-409. 

HAMILTON, W. J., JR. 1935. Field mouse and rabbit control in New York orchards. 

New York (Cornell) Ext. Bull., 338:1-24. 

1938. Life history notes on the northern pine mouse. J. Mamm., 19:163- 

170: 

HaArRTGROVE, R. W., AND R. E. Wess. 1973. The development of benzyprene 
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HorsFA.L, F., JR. 1953. Mouse control in Virginia orchards. Virginia Polytech. 
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—. 1956a. Pine mouse control with ground-sprayed endrin. Proc. Amer. Soc. 

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1956b. Rodenticidal effect on pine mice of endrin used as a ground spray. 

Science, 123:61. 

HorsFA.l, F., JR., R. E. WEBB, AND R. E. Byers. 1974. Dual role of forbes and 
rodenticides in the ground spray control of pine mice. Pp. 112-125, in 
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Howarp, W. E., R. E. MARSH, AND C. W. CorBETT. 1982. Raptor perches: their 
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Hunter, R. E., AND R. B. TUKEY. 1977. Mouse control in Washington orchards. 
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KAUKEINEN, D. 1982. A review of the secondary poisoning hazard potential to 
wildlife from the use of anticoagulant rodenticides. Pp. 151-158, in Pro- 


Management and Control 645 


ceedings of the tenth vertebrate pest conference (R. Marsh, ed.). Monterey, 
California, 245 pp. 

LITTLEFIELD, E. W., W. J. SCHOOMAKER, AND D. B. Cook. 1946. Field mouse 
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Luke, J. E., AND R. J. SNETSINGER. 1975. Apple trees protected from voles with 
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Marsh, R. E., AND W. E. Howarb. 1976. New perspectives in rodent and mam- 
mal control. Pp. 317-329, in Proceedings of the third international bio- 
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MEEHAN, A. P. 1980a. The rodenticidal activity of reserpine and related com- 

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19806. Effect of temperature, body size, bait age and long-term feeding 

response of mice to reserpine. Pesticide Sci., 11:562-567. 

MENDENHALL, V. M., AND L. F. PANK. 1980. Secondary poisoning of owls by 
anticoagulant rodenticides. Wildl. Soc. Bull., 8:311-315. 

Merson, M. H., AND R. E. Byers. 1981. Laboratory efficacy of some commercial 
zinc phosphide baits used for control of meadow and pine voles in orchards. 
Hortscience, 16:49-51. 

—. In press. Pellet size and the effectiveness of rodenticides against orchard 
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Merson, M. H., R. E. BYERS, AND D. KAUKEINEN. 1984. Residues of the roden- 
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Morrison, H. E. 1953. The meadow mouse (Microtus californicus) problem in 
Sacramento County. California Dept. Agric. Bull., 42:59-62. 

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1928. The mouse infestation of Buena Vista Lake basin. Monthly Bull., 

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SPENCER, D. A. 1958. Preliminary investigation of the Northwestern Mucrotus 

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STEHN, R. A., E. A. JOHNSON, AND M. E. RICHMOND. 1980. An antibiotic roden- 
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SULLIVAN, W. T. 1979. Cost of controlling pine voles by different methods. Pp. 
66-68, in Proceedings of the third eastern pine and meadow vole sympo- 

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TIETJEN, H. P. 1969. Orchard mouse control—a progress report. Ann. Rept., Mas- 
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Wess, R. E., AND F. HorsFALL, JR. 1967. Endrin resistance in the pine vole. 
Science, 156:1762. 

WEBB, R. E., W. C. RANDOLPH, AND F. HorSFALL, JR. 1972. Hepatic benzpyrene 


646 Byers 


hydroxylase activity in endrin susceptible and resistant pine mice. Life 
Sci., 11:477-483. 

Wess, R. E., R. W. HARTGROVE, W. C. RANDOLPH, V. J. PETRELLA, AND F. 
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Control of field mice in apple orchards. Virginia Polytech. Inst., Virginia 
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WYSOLMERSKI, J. C., R. E. BYERS, AND J. N. CUMMINS. 1980. Laboratory eval- 
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Amer. Soc. Hort. Sci., 105:675-677. 


LABORATORY MANAGEMENT AND 
PATHOLOGY 


FRANK F. MALLORY AND 
ROBERT A. DIETERICH 


Abstract 


HIS chapter discusses and describes laboratory management 
T procedures and possible pathogens associated with the genus 
Microtus. 

The successful maintenance of active breeding colonies is outlined 
with respect to housing, cleaning, feeding, breeding and photope- 
riod, temperature, and humidity. Surgical procedures are discussed 
also. 

A literature survey indicates that this genus may be host to a 
wide variety of pathogens, including 15 viral diseases, 13 bacterial 
diseases, three protozoal diseases, and one fungal disease. In addi- 
tion, 28 varieties of neoplasms and approximately 22 constitutional 
disorders have been described. 

Although the number of pathogens associated with these micro- 
tines should concern us all, ten years of laboratory experience sup- 
ports the conclusion that pathogenic problems in colonies and per- 
sonnel are minimal, and that voles have many characteristics which 
make them ideal laboratory mammals. 


Introduction 


Although small mammal populations have been studied since the 
turn of the century under natural conditions (Elton, 1942), the last 
decade has witnessed a major shift in research emphasis. Increas- 
ingly, wild species have been introduced to the laboratory and raised 
under artificial conditions. Among the more popular are a group of 
rodents of the subfamily Microtinae, genus Muicrotus, which are 
readily available by live-trapping. As indicated in Table 1, almost 


647 


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652 Mallory and Dieterich 


half of all the Nearctic species, as defined by Hall (1981), have 
been reared successfully in the laboratory during the past ten years. 
In view of the current interest in rodent population fluctuations, 
detailed information on demographic parameters is needed. Al- 
though certain aspects of changes in abundance can be studied in 
the field, information on genetic, physiologic, reproductive, and be- 
havioral indices can often be understood best from breeding and 
experimentation in captivity (Richmond and Conaway, 1969). Thus, 
the first objective of this chapter is to review the current practices 
of laboratory management for the genus Microtus and to make rec- 
ommendations that can be used as a general guide for future re- 
searchers. The second objective is to.examine our knowledge of 
pathogens and pathogenic conditions associated with Mucrotus, 
which, in addition to being a requirement for sound laboratory 
management, is especially important as more and more people may 
be exposed to these pathogens under confined conditions. 


Laboratory Management 


The easiest means of transport from the field is to carry the 
animal in the live-trap in which it was caught; however, if long 
distances are involved, special transport cages may be necessary. On 
reaching the laboratory, animals should be housed individually in 
cages containing bedding and cover. Additional cover appears to 
reduce the incidence of stress-related mortality, which can affect up 
to 50% of the animals within the first 2 weeks after capture. Ani- 
mals housed together often fight, aggravating stress-related prob- 
lems (Mallory, pers. observ.). A variety of both dry and fresh foods 
should be introduced to the cage, including the commercial chow 
on which the colony is maintained. Over a 2-week period, selec- 
tion of foods should be reduced to that of the commercial chow. 
Water should be provided in a bottle with a lick tube and in a small 
dish in the cage, as it takes a little time for some individuals to 
learn to use standard water bottles. After a few days the dish can 
be removed. Recently captured animals should be quarantined from 
the colony for a 2-week period, during which time the cages should 
be cleaned twice a week. This procedure removes most ectopara- 
sites, which are discarded in bedding, and allows one to assess the 
health of individual animals. Handling should be kept to a mini- 


Laboratory Management and Pathology 653 


mum, and photoperiod and temperature should be intermediate 
between that of the colony and the field situation. 


Records 


Although recorded information will vary with the desires and 
needs of each researcher, a general description of standard proce- 
dure may be of value. Records should be kept in both a daily log 
book and on cards attached to each cage. This duplication, though 
tedious, is often invaluable when important data are lost in one or 
the other system (most frequently the card is lost). Generally, each 
individual is identified by species, number, and sex, and where 
known, date of birth, date of weaning, and number of mother. In 
females, dates of pairing with males, dates of parturition, and litter 
sizes at parturition and weaning are important, and in males, pair- 
ing dates and offspring produced are often of value. Records should 
be used by the researcher to minimize inbreeding and genetic drift 
within the colony, unless otherwise desired. Wild caught animals 
should be introduced to the colony at regular intervals to keep it as 
representative of the natural population as possible. 


Housing, Cleaning, and Food 


As evident from Table 1, microtines have been maintained suc- 
cessfully in a wide array of containers, ranging from gallon cans 
(Jannett, 1974) to glass aquaria (Schadler, 1980). However, the 
majority of researchers have found standard plastic mouse cages 
with wire tops and a floor area ranging between 500 to 1,000 cm? 
most convenient. 

In addition, breeding pairs and nursing females with litters should 
be placed in larger cages; solid bottom cages are preferred over those 
with wire (Richmond and Conaway, 1969). Sawdust or wood shav- 
ings approximately 2 cm deep is the most common bedding, al- 
though other absorbent materials such as San-i-cel, corn grit, hay, 
peat, and soil may be used. Because these animals are semi-fossorial 
and spend a considerable amount of time digging, the finer bedding 
materials have the disadvantage of creating a dust problem (Mal- 
lory, pers. observ.). 

The most commonly used material for nesting and cover is cotton 
batting, although facial tissue (Dieterich and Preston, 1977a) and 
straw (Stehn and Jannett, 1980) have been employed. A number 


654 Mallory and Dieterich 


of recent researchers have refrained from using nesting material 
(Schadler, 1980; Webster et al., 1981), which has been our pref- 
erence for the past five years, because cotton can become wrapped 
around the limbs of neonates resulting in amputation or maiming 
(Mallory, pers. observ.). 

The frequency of cage cleaning (Table 1) may be from twice a 
week (Clulow and Mallory, 1970) to whenever necessary (Rich- 
mond and Conaway, 1969). Problems associated with changing cages 
are generally ones of disturbance and the negative effect it has on 
the pregnancy rate in the colony and the survival of neonates. Rich- 
mond and Conaway (1969) noted that female M. ochrogaster with 
neonates often killed their offspring after having their cage cleaned. 
In their laboratory, the incidence of this phenomenon was lowered 
by leaving a small amount of soiled bedding in the new cage. Mal- 
lory and Brooks (1980) demonstrated that handling gravid females 
of the lemming, Dicrostonyx groenlandicus (as one would do during 
cage changes), significantly reduced the number of pregnancies 
reaching parturition. Although the frequency of cage cleaning may 
vary with researcher and experimental design, current data suggest 
that colony productivity will be increased if gravid and lactating 
females are disturbed as little as possible. Cages should be washed 
according to standard mouse-colony procedure with a disinfecting 
detergent and rinsing (Les, 1966). 

In all colonies studied, food and water were provided ad lib., and 
the majority of researchers provided their animals with both dry 
and fresh food (Table 1). Commercial dry food is more convenient 
than other combinations, and a number of different types have 
proved successful, including standard mouse chow, mouse breeder 
chow, rat and hamster chow, and rabbit and guinea-pig pellets. 
Batzli (pers. comm.) has suggested that rabbit and guinea-pig pel- 
lets, composed largely of alfalfa and having high fiber and low fat 
content, are preferable to rat or mouse chows (Batzli, this volume). 
Fresh food may include barley, oats, barley and wheat sprouts, 
sunflower seeds, carrots, lettuce, and apples. Supplements of fresh 
food are recommended, because reproduction is enhanced in M. 
montanus fed fresh plant greens or their extracts (Berger et al., 
1981; Hinkley, 1966; Negus and Pinter, 1965, 1966; Pinter and 
Negus, 1965; Sanders et al., 1981). In one colony of M. pennsyl- 
vanicus, salt cubes were made available (Lee et al., 1970). 


Laboratory Management and Pathology 655 


Photoperiod, Temperature, and Humidity 


Control of photoperiod is essential if high rates of reproduction 
and sexual maturity are to be sustained throughout the year. The 
majority of successful colonies have been maintained on a long-day 
photoperiod ranging between 14 and 18 h of light/24-h period 
(Table 1). No colonies were given less than 12 h of light/day. Imel 
and Amann (1979) demonstrated that reproductive function and 
body weight in M. pennsylvanicus were significantly greater at a 
16L:8D photoperiod, and were more favorable than 14L:10D and 
18L:6D, at 22°C. Because evidence supports the conclusion that 
members of the genus Microtus are long-day breeders (Clarke and 
Kennedy, 1967; Iverson and Turner, 1974; Petterborg, 1978; 
Vaughan et al., 1973), the 16L:8D photoperiod may be best for 
most mid-latitude species. Light intensities inside cages of 40-75 
lux and 100 lux were reported by Lee et al. (1970) and Imel and 
Amann (1979), respectively. Virtually no work has been done on 
the effect of different spectral emissions. Temperature of colonies 
generally varied between 20 and 25°C (range —12 to 27°C); Rich- 
mond and Conaway (1969) maintained a constant humidity of 
Gore 76. 


Breeding and Weaning Procedures 


A survey of the literature indicates that most laboratories house 
their breeders as single pairs rather than in mixed groups. Stud 
males have been left successfully with gravid females throughout 
gestation and lactation (Morrison et al., 1977a, 19776), often in the 
presence of previous litters. Other researchers removed the males 
on day 7 post coitum (Imel and Amann, 1979) or after the birth of 
the litter (Batzli et al., 1977). Maintaining a pair together is ad- 
vantageous in that females most often mate at post-partum estrus, 
which occurs on the first day after parturition (Hasler, 1975). Two 
other factors that can reduce reproductive output in microtine col- 
onies are pregnancy failure, which occurs when pregnant females 
are exposed to strange males (Clulow and Langford, 1971; Mallory 
and Clulow, 1977; Schadler, 1981; Stehn and Richmond, 1975), 
and infanticide, which can occur when strange males or females are 
introduced into cages holding females and their neonates (Mallory 
and Brooks, 1978, 1980; Webster et al., 1981). Laboratory person- 


656 Mallory and Dieterich 


nel should be aware of these potential problems, which may become 
important during cage changes, when establishing new pairings, or 
when introducing new animals to the colony. 

Weaning young from the maternal cage usually is accomplished 
at approximately 3 weeks post partum (range 17 to 35 days); how- 
ever, in some instances up to three successive litters were left with 
the parents (Richmond and Conaway, 1969). The size and com- 
position of post-weaning groups of immature animals has been 
shown to significantly influence rate of maturation and propensity 
to mate. Immature M. californicus, M. ochrogaster (Batzli et al., 
1977), and M. pinetorum (Schadler, 1980) exhibited suppressed 
sexual development and growth when housed in groups. In addi- 
tion, female M. ochrogaster developed the least when paired with 
littermate weanling males as compared to non-littermate adult males 
(Hasler and Nalbandov, 1974), and incest avoidance may occur in 
this species when siblings are housed together (McGuire and Getz, 
1981). Thus, to maximize colony productivity, immature males 
should be housed individually and immature females should be 
paired with non-related adult males or non-littermate immature 
males (Baddaloo and Clulow, 1981; Batzli et al., 1977). 


Other Procedures 


Surgical procedures such as adrenalectomy, splenectomy, vasec- 
tomy, and castration have been successfully performed on microtines 
with minimum equipment (Richmond and Conaway, 1969). Both 
ether and sodium pentabarbital have been used successfully as an- 
esthetics. Sodium pentabarbital at a dosage of 0.06 mg/g body weight 
administered intraperitoneally is sufficient to keep an animal im- 
mobilized for 3 h. Lower dosages have little effect and higher dos- 
ages increase mortality. Post-operative care requirements are min- 
imal; however, a heat lamp over recovering animals increases 
survival. 

Although ectoparasites are generally eliminated by the cleaning 
procedures described above, the follicle-inhabiting mite, Psorergates 
simplex, has been a problem on occasion (Lee and Horvath, 1969). 
Infestations can be suppressed successfully by treating animals and 
cages with a 2% aqueous solution of a wetable powder containing 
15% Aramite [2-(p-tertbutylphenoxy)isopropyl 2-chloroethyl sul- 
fite] or low-toxicity flea powder (Dieterich, pers. observ.). 


Laboratory Management and Pathology 657 


Finally, all personnel regularly exposed to microtine breeding 
colonies should be required to wear lab coats and gloves for han- 
dling animals and washing cages. Standard tetanus-polio combi- 
nation and rabies inoculations should be given to reduce risk of 
infection. 


Pathology 


Although Microtus is the most widely studied genus of microtines 
in North America, there is a surprising paucity of information con- 
cerning pathogens associated with these rodents. Indeed, in Europe 
and the USSR, a much greater effort has been made to understand 
the etiology and epizootics of infectious diseases and the role mi- 
crotines play as vectors or reservoirs. Because most small mammals 
are studied by mammalogists lacking training in medical proce- 
dures, and because veterinarians and medical personnel tend to 
apply their energy and resources to more economically important 
species, the majority of specimens collected are discarded before a 
pathological examination is made, resulting in the loss of infor- 
mation in a potentially important area. 


Viral Infections 


Rabies.—Rabies is an acute and usually fatal infectious disease 
of the central nervous system caused by a virus which travels from 
the site of infection via the peripheral nervous system to the central 
nervous system; it appears to persist as a salivary gland infection 
in nature. All warm-blooded animals are susceptible (Sikes, 1970). 
The virus is usually transmitted by biting; however, infection through 
aerosol, nasal, and oral exposure also has been confirmed in both 
carnivores and rodents (Casals, 1940; Fischman and Ward, 1968; 
Ramsden and Johnston, 1975; Soave, 1966). 

The symptoms of the disease may take one of two forms. Animals 
exhibiting the furious form of rabies initially become anorexic, ap- 
prehensive, and nervous prior to an excitatory phase during which 
they become restless and vicious. They bite most objects in the 
immediate vicinity, although they have difficulty chewing and swal- 
lowing. During this time the saliva contains the greatest amount of 
virus, although it is usually present throughout the entire course of 
the disease. Subsequently, the strong furious actions slowly subside 


658 Mallory and Dieterich 


and incoordination and muscle tremors are often apparent. The 
final stage usually includes convulsions, followed by paralysis and 
death. Animals with the dumb form of rabies usually exhibit the 
later symptoms of the disease, incoordination, paralysis, and death. 

Post-mortum examination of the central nervous system usually 
identifies histopathologic lesions concentrated in the pons, medulla, 
brain stem, and thalamus (Sikes, 1970). Negri bodies, which are 
cytoplasmic inclusions in the neurons, are considered positive proof 
of rabies infection. Without these inclusions, a definite diagnosis 
cannot be made as lesions produced by other viral encephalitides 
are similar. 

Considerable attention has been given to epizootological studies 
of rabies in both domestic and large wild mammals, and current 
evidence suggests that the disease is largely transmitted by direct 
contact with, and wounds from, infected individuals, during high 
population densities (Sikes, 1970). However, very little research has 
been conducted on species that may be permanent asymptomatic 
hosts of the virus. Although our literature survey found no infor- 
mation associating rabies with Microtus in North America, signif- 
icant research has been done in Europe. Rabies virus has been 
isolated in small mammals in Czechoslovakia, from a region where 
fox epizootics occurred frequently, and from another area where 
rabies was not reported for a considerable time (Sodja et al., 1971). 
In this study, 103 of 556 M. arvalis and 14 of 29 M. agrestis were 
found to be rabies carriers, although symptoms were not apparent. 
In the enzootic and control areas, respectively, 22.5% and 12.8% of 
M. arvalis were diagnosed as positive; the incidence appeared to be 
higher in animals caught during the winter months. In a subsequent 
4-year study, Sodja et al. (1973) isolated 28 rabies virus strains 
from the brain, salivary glands, and brown fat of 2,162 small ro- 
dents (88% Microtus arvalis). The identity of the isolates with rabies 
virus was demonstrated by a positive direct immunofluorescence 
reaction, inhibition by specific serum, and a serum neutralization 
test. The various strains were both cerebrally and extraneurally 
pathogenic for the usual laboratory animals and for dogs and foxes. 
Ramsden and Johnston (1975) demonstrated that red foxes (Vulpes 
vulpes) and striped skunks (Mephitis mephitis), which feed largely 
on small mammals, died or developed serum neutralizing antibody 
when fed mice infected with rabies virus. In addition, tooth-marks 
from small mammals have been observed on dead fox carcasses later 


Laboratory Management and Pathology 659 


diagnosed as rabid (D. H. Johnston, pers. comm.). From these 
results it is reasonable to hypothesize that Microtus and other mi- 
crotines may be an asymptomatic reservoir for rabies, which can be 
transmitted to predators by ingestion, causing major outbreaks and 
epizootics to occur in these populations. 

Rabies has public-health as well as agricultural-economic sig- 
nificance. In 1966-1967, 1,336 rabies-caused human deaths were 
reported; 1,980,238 people received post-exposure antirabies pro- 
phylaxis, and 175 paralytic accidents were attributed to vaccine 
treatment (World Health Organization, 1967). In addition, hundreds 
of millions of dollars are lost annually owing to loss of livestock. 
For these reasons, researchers working with microtines should take 
appropriate precautions and a major effort should be made to assess 
the role of microtines in the epidemiology of this disease. 

Lymphocytic choriomeningitis (LCM) .—This disease appears to 
be worldwide in distribution and occurs naturally in mice and 
other wild rodents (Hotchin and Benson, 1970; Morris and Alex- 
ander, 1951). It is occasionally transmitted to man, causing a non- 
fatal meningitis. Susceptible animals infected with LCM virus often 
die from meningeal or visceral causes, although the carrier condition 
is often common and the virus may become disseminated throughout 
a breeding colony, with most infections being subclinical (Maurer, 
1964). 

Symptoms appear in susceptible Mus after 5—6 days of inocula- 
tion. The animal becomes hunched in posture, eyes half-closed, and 
often has convulsions. The rear limbs often become paralyzed and 
rigid prior to death. Naturally infected animals may show little or 
no illness or a temporary wasting syndrome as has been demon- 
strated in M. agrestis and Clethrionomys glareolus (Dalldorf, 1943; 
Findlay and Stern, 1936). The virus is distributed widely in the 
infected host and has been recovered from most tissues including 
brain, blood, spleen, lungs, blood marrow, adrenal glands, lymph 
nodes, kidney, liver, and testes. Wild rodents appear to be the pri- 
mary vertebrate host with ticks, mites, fleas, mosquitos, and other 
bloodsucking arthropods acting as vectors. LCM virus also has been 
transmitted to mice by direct contact with the conjunctiva, respi- 
ratory and digestive tracts, and intact skin (Maurer, 1964), and in 
man, handling of, or bites from, infected animals often produces 
infection. LCM is best controlled by sanitary measures in the colony 
and care taken in washing after handling animals. 


660 Mallory and Dieterich 


Eastern (equine) encephalitis (EEV).—This virus is known to 
infect a wide range of mammals, birds, and reptiles; several species 
of mosquitos are believed to be the main arthropod vectors. Karstad 
(1970) found neutralizing antibody to EEV in six species of wild 
rodents; experimental inoculation of eight species of rodents from 
Wisconsin demonstrated that infections were readily induced when 
small doses of virus were administered by routes simulating natural 
exposure (Karstad et al., 1961). Sign of illness was absent and 
viremia was rare but detectable. Karstad (1970) concluded that 
eastern equine-encephalitis virus should be considered a possible 
cause of encephalitis in wild rodents, which may act as reservoirs 
for the disease. 

Mice inoculated with equine encephalitis virus become paralytic 
and die between 2 and 6 days later. This disease is of significant 
socioeconomic importance because it can cause severe and often fatal 
encephalitis in man and horses, and epizootics in pheasants have 
been reported. Infants and children are most susceptible; symptoms 
include high fever, vomiting, drowsiness or coma, and severe con- 
vulsions (Feemster, 1938; Gittner and Shakan, 1933). In the most 
severe cases, death occurs within 3-5 days from onset; it also may 
occur later from complications. Survivors under 5 years of age often 
have mental retardation, periodic convulsions, and paralysis; sur- 
vivors over 40 generally recover completely (James and Harwood, 
1969). 

Western (equine) encephalitis (WEV).—WEV is similar to EEV 
in its epidemiology and transmission (Karstad, 1970); however, it 
generally is not fatal in man. High mortality occurs in equines. 
Initially thought to be limited to the western United States, it now 
has been shown to be present from eastern Canada to Brazil. Symp- 
toms of the disease are difficult to distinguish from other arbovirus- 
caused encephalitides. However, fever and drowsiness often accom- 
panied by convulsions are common (James and Harwood, 1969). 

St. Louis encephalitis (SLE) .—Similar to the two previous forms 
of encephalitis, SLE has an active bird-mosquito cycle; wild rodents 
are implicated as secondary hosts (Henderson et al., 1962). The 
largest epidemic occurred in St. Louis in 1933, with 1,100 cases 
and more than 200 deaths; however, other outbreaks have occurred 
in most regions of the United States. The symptoms are similar to 
other encephalitides and in the east, older age groups appear more 
susceptible (James and Harwood, 1969). 


Laboratory Management and Pathology 661 


Powassan virus.—This virus was first isolated in Ontario, Can- 
ada, from a fatal encephalitis case in 1958. Though widely distrib- 
uted foci are recognized in nature, no subsequent clinical cases have 
been verified. The virus has been isolated from ticks of the genera 
Dermacentor and Ixodes, which are common throughout North 
America (Timm, this volume). Isolates and serological sampling 
reinforce the conclusion that wild rodents and lagomorphs are a 
major reservoir of this pathogen (James and Harwood, 1969). 

Colorado tick fever virus (CT F).—CTF virus occurs in the Rocky 
Mountain states, the Black Hills of South Dakota, and in western 
Canada. It is transmitted by ticks of the genus Dermacentor, which 
are a common ectoparasite of mammals, including small rodents 
(James and Harwood, 1969; Timm, this volume). Clark et al. 
(1970) successfully isolated CTF virus from ticks collected on Cleth- 
rionomys gappert and Microtus longicaudus in southwestern Mon- 
tana, supporting the conclusion that small mammals may be res- 
ervoirs for the disease. Although no information was found describing 
the symptoms of this virus in microtines, humans experience fever, 
headache, and severe muscle pains 3-6 days after exposure to ticks. 
In children complications in the form of encephalitis and severe 
bleeding may occur. No lasting complications are reported (James 
and Harwood, 1969). 

Enterovirus.—Main et al. (1976) reported the isolation of six 
viruses from Clethrionomys gapperi trapped in Massachusetts in 
1969, two of which were similar to those identified from the same 
species by Whitney et al. (1970) from New York state. These iso- 
lates were related to an enterovirus isolated from Microtus montanus 
(Johnston, pers. comm.) trapped in Klamath County, Oregon, but 
were distinct from a strain found in M. pennsylvanicus in New York 
(Whitney et al., 1970). The pathology of these virions has not been 
described, however; generally, enteroviruses infect the gastro-intes- 
tinal tract and may cause diarrhea. 

Herpesvirus.—A herpesvirus has been isolated and characterized 
from the kidney of M. pennsylvanicus (Melendez et al., 1973) and 
may be associated with interstitial nephritis in this species (Dieter- 
ich and Preston, 19776). 

Ectromelia virus (mouse pox) .—Kaplan et al. (1980) reported the 
presence of this virus, which is highly contagious and often fatal in 
laboratory mice, in Microtus agrestis from Britain, where over half 
of the wild animals sampled had neutralizing antibodies. During 


662 Mallory and Dieterich 


the course of the disease in Mus, the virus multiplies in the cells of 
most organs. In the acute form, visceral lesions and hepatic necroses 
occur, with the animal dying within days, showing few external 
signs of illness. In susceptible colonies, 50-95% of the animals die. 


Sendai virus (parainfluenza type I).—Antibodies were present in 
a large proportion of animals examined from Britain, including M. 
agrestis (Kaplan et al., 1980). Sendai virus infections of the respi- 
ratory tract destroyed the ciliated epithelium and caused congestion 
(Fenner et al., 1974); in the gastro-intestinal system it may produce 
diarrhea. 


Theiler’s mouse encephalomyelitis virus (GDIII).—Antibodies re- 
acting to GDIII were detected in M. agrestis (Kaplan et al., 1980). 
In laboratory mice, infection usually causes unapparent intestinal 
infection. 


Pneumonia virus of mice (PVM).—PVM antibodies have been 
identified in M. agrestis in Britain (Kaplan et al., 1980) and may 
be responsible for producing this disease in voles. 


Reovirus III.—Antibodies which neutralize reovirus III have been 
identified in M. agrestis (Kaplan et al., 1980). 


Bacterial Infections 


Tularemia.—Tularemia is an acute, moderately severe infectious 
septicemia caused by the bacterium Francisella tularensis. It appears 
to be almost worldwide in distribution, affecting many species of 
mammals including man (Reilly, 1970). In the genus Microtus, it 
has been identified in M. pennsylvanicus, M. californicus, M. mon- 
tanus, M. oeconomus, and M. arvalis (Murray, 1965; Rausch et al., 
1969; Reilly, 1970). Clinical manifestations of tularemia are seldom 
evident and opportunities to observe the signs in nature are very 
limited, because infected animals are usually moribund or dead 
(Murray, 1965). In general, the gross and histopathological lesions 
from tularemia are tubercle-like nodules scattered in the liver, spleen, 
and lymph nodes, varying from pin-point size to large irregular 
foci, several mm in diameter. The liver may be dark bluish-red, 
enlarged; small white plaques may be evident in the lungs. ‘Throm- 
boses of small blood vessels are frequent. 

Transmission of tularemia usually occurs as a result of blood 


Laboratory Management and Pathology 663 


sucking ectoparasites, especially mites and ticks (James and Har- 
wood, 1969); however, flies, midges, fleas, mosquitoes, and lice also 
have been implicated (Reilly, 1970). Infection also has occurred 
owing to contact with infected vertebrates, inhalation of feces-con- 
taminated dust, and ingestion of infected carcasses and contami- 
nated water (Burroughs et al., 1945; Gorham, 1950; Maisky, 1945). 
In humans, the disease may take the form of a sudden fever, with 
severe pain affecting the lymph nodes. In susceptible individuals, 
septicemia may result in death from 4 to 14 days after exposure 
and pneumonic complications also may occur. Streptomycin is the 
usual antibiotic agent used to combat the disease (James and Har- 
wood, 1969). 

Sylvatic plague.—Plague is an acute infectious disease caused by 
the bacterium Pasteurella pestis; it primarily afflicts wild rodents. 
Few descriptions of the pathologic changes that occur in wild 
rodents have been published; however, it has been noted that a vari- 
ety of manifestations of the disease result from the interaction of 
different hosts, vectors, and environmental conditions. McCoy (1911) 
defined three categories in the California ground squirrel (Sper- 
mophilus beecheyi): 1) acute plague—the animal dies in 3-5 days 
with hemorrhagic buboes and an enlarged spleen, but no macro- 
scopic lesions develop on internal organs; 2) subacute plague—the 
animal dies at 6 or more days with caseous buboes, in the absence 
of hemorrhaging but in the presence of pinpoint nodular, necrotic 
foci in the spleen, liver, and lungs; and 3) residual plague—indi- 
viduals survive and have enlarged lymph glands containing yellow 
purulent foci. Since McCoy’s (1911) work, a latent form of plague 
has been described, which is characterized by an absence of gross 
lesions (Pollitzer, 1954); such asymptomatic infections are believed 
to be common especially among resistant genera like Microtus. 

Microtus californicus and M. montanus are both susceptible to 
invasions of the organism but usually do not succumb either to 
natural or experimental inoculation of large numbers of plague 
bacilli (Olsen, 1970). Bacilli persist in Microtus and may produce 
unapparent infections. They often are taken up by the lymph nodes 
and transported to the viscera where they multiply prior to ap- 
pearing in the blood and blood-filtering organs. Voles likely act as 
permanent reservoirs for this pathogen from which fleas become 
infected (Quan and Kartman, 1962). Studies of M. californicus have 
demonstrated that the proportion of individuals with positive sera 


664 Mallory and Dieterich 


can approach 100% in plague-prevalent regions (Hudson et al., 
1972). 

Sylvatic plague was first discovered in California; it now has been 
isolated from 57 rodent species in 15 western states as far east as 
Kansas, Oklahoma, and Texas, as well as Alberta, Saskatchewan, 
and northern Mexico (Olsen, 1970). Although plague is a disease 
of rodents and is transmitted by fleas, it has had a great influence 
on the course of history in the form of bubonic plague, characterized 
by epidemics that have decimated human populations of entire con- 
tinents (James and Harwood, 1969). For this reason, all microtines 
should be handled with this in mind. Both sulfonamides and strep- 
tomycin are effective for treating the disease once contracted. 

Pasteurellosis.—Pasteurellosis is an infectious disease of wild and 
domestic animals caused by the bacterium Pasteurella multocida. Its 
clinical manifestations vary, ranging from hemorrhagic septicemia 
to pneumonia, meningitis, mastitis, and arthritis (Rosen, 1970). 
Although it usually is associated with larger mammals, it was iso- 
lated from voles in the USSR (Ponomareva and Rodkevich, 1964), 
and epizootics were reported in M. montanus in Oregon (Murray, 
1965). Clinical symptoms in wild animals are rarely observed and 
most infected animals are found dead, with nasal and oral mucous 
discharges. It most often affects the respiratory system, producing 
pneumonia and hemorrhages in the lungs, trachea, and nasal mu- 
cosa. If the bacterium enters the circulatory system, septicemia oc- 
curs and, on occasion, meningitis. The mode of transmission is not 
understood; however, it may be transmitted by carriers, or be pres- 
ent generally and only become pathogenic when individuals become 
stressed. Human infections develop when individuals are bitten 
(Rosen, 1970). Pasteurellosis is worldwide in distribution and of 
great importance to poultry, livestock, and mink industries. Anti- 
biotics are used to treat individuals contracting this disease. 

Pseudotuberculosis.—Pseudotuberculosis is an infectious disease 
caused by the bacterium Pasteurella pseudotuberculosis, which affects 
many visceral organs, especially the spleen, liver, lungs, and small 
intestine. Although Holarctic in distribution and found in most 
species of Microtus, including M. mexicanus (Wetzler, 1970), very 
little is known about its symptoms. Few wild animals become ill, 
or they die without notice, and as a result most information comes 
from zoological gardens or research institutions. Outbreaks in chin- 
chillas were characterized by marked depression of activity, inap- 


Laboratory Management and Pathology 665 


petence, anorexia, diarrhea, and death within several days. Histo- 
pathogenic observations indicate that hypertrophy of the mesenteric 
lymphatics occurs, and visceral nodules develop in the spleen, liver, 
ileocecal junction, and occasionally the lungs. Serofibrinous peri- 
toneal fluid often is present. Diagnosis from clinical signs is vir- 
tually impossible; however, treatment is successful with a broad- 
spectrum antibiotic. Transmission appears to be via oral-fecal routes. 

Tuberculosis.—Tuberculosis is a chronic infection due to the ba- 
cillus Mycobacterium tuberculosis and related species. The organism 
has a broad host range, including man, domestic animals, poultry, 
and many wild species (Winkler and Gale, 1970). Geographic dis- 
tribution is essentially worldwide, although it is most predominant 
in temperate regions. Three varieties of Mycobacterium tuberculosis 
are recognized: M. t. hominis, M. t. bovis, and M. t. avium. There 
also is a vole bacillus, Mycobacterum mycroti, isolated from Muicrotus 
agrestis by Wells and Oxon (1937). The first description of tuber- 
culous lesions in a wild vole (M. arvalis) was by Koch (1884). 
Tuberculosis starting with pulmonary infection results in multiple 
lesions in lung parenchyma and is accompanied by respiratory dis- 
tress. Tuberculous bronchitis may progress to broncho-pneumonia 
and fatal respiratory collapse. Lymph glands often enlarge in the 
viscera and emaciation may be observed. Bacilli can be disseminated 
by infected animals via exhaled air, sputum, feces, urine, or milk. 
Jespersen (1975, 1976) has demonstrated that both Microtus arvalis 
and M. agrestis developed the disease when inoculated with M. t. 
hominis and M. t. bovis, although susceptibility was higher for M. 
t. bovis. Autopsy showed that infections of M. t. bovis caused lymph 
glands to be affected, and tubercles were frequently observed in the 
lungs but seldom the liver, spleen, or kidneys. Large numbers of 
bacilli were found in several organs, especially the lymph glands. 
M. t. hominis had little effect on lymph glands and the number of 
bacteria was few. Comparative experimental infection of voles with 
vole bacilli and the bovine tuberculosis organism produced similar 
generalized symptoms, except that bovine infections were of shorter 
duration and characterized by caseous lesions. Vole bacilli ran a 
longer course and produced non-caseated subcutaneous lesions 
(Winkler and Gale, 1970). 

Tuberculosis is of significant socioeconomic importance. For this 
reason proper administration of laboratory procedures should be 
followed. Authorities generally agree that elimination rather than 


666 Mallory and Dieterich 


treatment of tuberculin-positive animals is the proper procedure. 
Standard tuberculin tests can be used to identify tuberculin-positive 
animals. 

Erysipelas.—Erysipelas is a disease caused by the bacterium F7- 
ysipelothrix rhusiopathiae. ‘This organism infects a large number of 
animals, domestic and wild, causing septicemia. The disease is of 
socioeconomic importance because it affects domestic sheep, pigs, 
turkeys, ducks, and pheasants, and should be a concern of those 
responsible for maintaining captive animals (Shuman, 1970). There 
are no specific symptoms associated with the disease except signs of 
acute illness (prostration, a thick exudate around the eyes, and a 
history of sudden death). Cutaneous lesions sometimes occur in 
domestic and wild animals and diagnosis requires post-mortem ex- 
amination of infected tissue. 

An epizootic of erysipelas was reported in M. californicus (Way- 
son, 1927); it has since been found in other North American rodents 
(Connell, 1954). Old World reports indicate that it has been iden- 
tified in M. oeconomus (Khomyakov et al., 1970) and M. arvalis, in 
which it often reaches epizootic proportions (Shuman, 1970). It is 
not known specifically how the disease is transmitted; however, 
evidence suggests that direct ingestion may occur because it can 
persist free in nature. Ticks of the genera Dermacentor and Ixodes, 
mites, lice, house flies, and other insect vectors are implicated. Er- 
ysipelas appears to be worldwide in distribution and human infec- 
tion can occur. Penicillin has been used successfully in treating 
domestic animals and would probably be suitable for wild species 
(Shuman, 1970). 

Listeriosis.—As a zoonotic disease, listeriosis is becoming recog- 
nized as an important bacterial disease of man and domestic and 
wild animals. It is caused by the bacterium Listeria monocytogenes, 
which can produce a variety of pathologies, and is worldwide in 
distribution. The bacterium may cause encephalitis in domestic ru- 
minants, septicemia in monogastric animals and birds, meningitis 
in man, abortion in many mammalian species, and other lesser 
disorders. It is found in 42 different mammals, 22 species of birds, 
in addition to fish, crustaceans, ticks, house flies, sewage sludge, 
and soil (Eveland, 1970). Isolates have been identified in the voles 
M. montanus (Bacon and Miller, 1958), M. agrestis (Levy, 1948), 
M. arvalis (Kratokhvil, 1953), and the lemmings Lemmus trimu- 


Laboratory Management and Pathology 667 


cronatus and Dicrostonyx groenlandicus (Barrales, 1953; Magus, 
1955; Nordland, 1959; Plummer and Byrne, 1950). 

The characteristic lesions of the infection are well-defined, whit- 
ish-gray foci on the liver and spleen, lungs, and heart (Eveland, 
1970). However, these are not essentially different from those of 
tularemia or pseudotuberculosis. Evidence suggests that listeriosis 
may be carried by many organisms and may become pathogenic 
only under stressful conditions (Barker et al., 1978; Nordland, 1959). 
Thus, the disease may be asymptomatic in most wild populations, 
which act as carriers, and only appear when occasional epizootics 
are triggered by demographic or environmental factors. ‘Treatment 
is best accomplished by using broad-spectrum antibiotics. 

Bordetella.—Bordetella bronchiseptica 1s a common infectious agent 
in domestic and laboratory animals, sometimes as the primary dis- 
ease agent and other times as a secondary invader. The small ba- 
cillus can cause broncho-pneumonia and other respiratory infec- 
tions and often is reported to complicate other diseases such as 
chronic pneumonia, canine distemper, and atrophic rhinitis in swine. 
In man, it occasionally causes a syndrome similar to whooping 
cough. In 1973, it was isolated from M. montanus found dead or 
dying in northern Utah (Jensen and Duncan, 1980). At necropsy, 
gross pathologic changes were confined to the lungs, which were 
congested and edematous. Histopathologic examination disclosed a 
considerable degree of atelectasis, and alveoli contained fluid, fibrin, 
inflammatory cells, and in some cases erythrocytes. Bacteria isolated 
from the voles killed seven of eight laboratory mice when one drop 
of broth culture was given by intranasal instillation. Although the 
data support the conclusion that B. bronchiseptica was the primary 
etiological agent, the outbreak of pulmonary disease may have been 
associated with other pathogens. The distribution of this pathogen 
is unknown (Jensen and Duncan, 1980). 

Leptospirosis.—Leptospirosis is a group of infectious diseases of 
man and animals caused by small, coiled, actively motile spirochetes 
of the genus Leptospira. The disease can be unapparent or fatal, 
depending on the host and infecting serotypes. Wildlife may serve 
as sources of infection for domestic animals and man. 

Leptospira bullum has been isolated from M. pennsylvanicus but 
was infrequent in the population (Clark et al., 1961). L. icterohae- 
morrhagiae was found in M. montebelli from Japan (Kitaoka and 


668 Mallory and Dieterich 


Fujikura, 1975), and other serotypes were identified in M. agrestis 
and Clethrionomys glareolus in Britain (Twigg et al., 1968). The 
Japanese and European researchers considered the reservoir of lep- 
tospirosis in wildlife of considerable importance to the health and 
performance of domestic animals and man. 

Very little is known about the symptoms of this disease in wild 
mammals; but they include anorexia, anemia, hemoglobinuria, fe- 
ver, and death (Roth, 1970). The organism usually gains entrance 
through mucous membranes or broken skin and generally can be 
isolated from the blood from 4 to 9 days after infection. This con- 
dition precedes the febrile state by several days and by the time the 
fever subsides, the spirochetes no longer can be isolated from the 
blood. Antibodies normally appear about 10 days after infection 
and may persist for several months. Diagnosis usually requires se- 
rologic and bacteriologic methods (Roth, 1970). Treatment in hu- 
mans normally requires antibiotics. 

Relapsing fever.—Relapsing fever is a bacterial infection caused 
by spirochetes of the genus Borrelia; it is worldwide in distribution 
with the exception of Australia. It is transmitted mainly by ticks 
and lice and is an important infection of domestic animals and man. 
Experimental infection of B. hermsi in M. pennsylvanicus has been 
demonstrated (Burgdorfer and Mavros, 1970). Voles were shown 
to develop spirochetemias of various intensities and lengths. How- 
ever, they experienced no signs of illness. All animals exhibited 
three periods of spirochetemia which lasted from 1 to 7 days, with 
the longest periods occurring early in the infection. Human cases 
of relapsing fever from Spokane, Washington, revealed that the tick 
Ornithodoros hermsi was the vector, and that it commonly was as- 
sociated with a number of rodents, including M. pennsylvanicus 
(Burgdorfer and Mavros, 1970). In humans, an acute onset of fever 
occurs 3-10 days after infection and large numbers of spirochetes 
are present in the blood; they then disappear. Febrile attacks may 
recur three to 10 times and mortality rates of 50% have been re- 
ported. Penicillin and other antibiotics are an effective treatment 
(James and Harwood, 1969). 

Rocky mountain spotted fever.—This disease is caused by infection 
of Rickettsia ricketts1, which is one member of a group of rickettsial 
zoonoses. The common name is misleading as the disease is found 
in most states, with 25% of cases reported in Virginia (Bell, 1970). 


Laboratory Management and Pathology 669 


Indeed, members of this genus appear to be ubiquitous in temperate 
regions of the world (Asanuma et al., 1972; Burgdorfer et al., 1979; 
Tarasevich et al., 1976). 

Transmission regularly occurs because of bites from ticks of the 
genera Dermacentor, Amblyoma, Rhipicephalus, and Ixodes (Bell, 
1970). Ectoparasites other than ticks are not known to be vectors. 
The organism has been identified in a large number of rodents, 
including M. pennsylvanicus (Burgdorfer et al., 1975; Jellison, 1934), 
M. agrestis (Peter et al., 1981), M. arvalis, and C. glareolus (Rehacek 
et al., 1977), which may act as reservoirs of the disease. 

Symptoms in wild animals are virtually unknown. Experimental 
infections of M. pennsylvanicus have shown that the response to the 
infection varies between individuals. Burgdorfer et al. (1966) ob- 
served that voles were not severely affected but the pathogens pro- 
duced a microscopically detectable infection in the tunica vaginalis 
of the testes. Jellison (1934) found fever, swelling, and discoloration 
of the scrotum with adhesion formation, enlarged spleens, and mor- 
ibund conditions developing in some individuals. Proper diagnosis 
requires laboratory analysis. Human symptoms include rashes on 
the wrists and ankles, headaches, backaches, and marked malaise 
with fever. In fatal infections death usually occurs between days 9 
and 15. Broad-spectrum antibiotics are usually employed as treat- 
ment (James and Harwood, 1969). Other forms of rickettsieae, 
including coxiellosis, rickettsial pox, and eperythrozoonis, also may 
infect voles (Bell, 1970). 

Other bacterial diseases.—Salmonella and Streptococcus infections 
have been reported in many small mammals (James and Harwood, 
1969), transmitted by lice or other insect vectors. Murray (1965) 
reported the presence of these potential pathogens in M. montanus 
in Oregon and California during a population outbreak in 1957 
and 1958. Salmonella enteridis was found in live and dead voles and 
their associated fleas. One juvenile M. montanus was diagnosed as 
having “big foot,” a beta-hemolytic (Streptococcus) Group-A infec- 
tion and another individual, which exhibited paralysis, difficult 
breathing, and had an open wound, was found positive for non- 
typable, Group-A Streptococcus. Both these pathogens have been 
reported in small-mammal breeding colonies causing morbidity and 
death (Haleermann and Williams, 1958). Broad-spectrum anti- 
biotics have been used with some success. 


670 Mallory and Dieterich 


Protozoan Infections 


Babesiosis.—This is an infectious disease caused by protozoa of 
the genus Babesia, which are intraerythrocytic except during peaks 
in parasitemia, when they are liberated from ruptured red blood 
cells (Van Peenen and Healy, 1970). The life cycle and identity of 
these blood parasites still are not settled (James and Harwood, 
1969), and their distribution appears to be wide ranging. Piro- 
plasms of Babesia microti were found and observed in M. califor- 
nicus, M. ochrogaster, M. pennsylvanicus, M. oeconomus, M. arvalis, 
M. agrestis, and Lemmus lemmus (Fay and Rausch, 1969; Kram- 
pitz, 1979; Mahnert, 1972; Van Peenen and Healy, 1970; Wiger, 
1978a). The course of infection is extremely variable, with peak 
parasitemias occurring 7-20 days after inoculation in M. ochrogas- 
ter. Parasites usually could not be detected in the blood after 3-4 
weeks, but sub-patent infections were evident for up to 3 months. 
No deaths occurred among intact Microtus, but splenectomized, in- 
fected animals often died as did intact Lemmus lemmus (Wiger, 
19785). All infected animals developed anemia, hemoglobinuria, 
splenomegaly, and deposition of hematin in the reticuloendothelial 
system. In Germany, Krampitz (1979) found B. microti most fre- 
quently associated with M. agrestis, with prevalence being greatest 
in early summer when 71% of the voles were infected. Ticks of the 
genera Dermacentor and Ixodes appear to be the main vectors for 
this disease, and in eastern United States M. pennsylvanicus appears 
to be the primary reservoir (McEnroe, 1977). Recent human cases 
of babesiosis infection from Nantucket Island, off the southeastern 
Massachusetts coast (Healy et al., 1976), support the conclusion 
that babesiosis could become an important public health problem. 
Symptoms are malaria-like and are characterized by chills, fever, 
headache, lethargy, and myalgia. Diagnosis depends on recognition 
of trophozoites of Babesia in the blood. No information on treatment 
is available. Other piroplasms with similar effects associated with 
microtines include Hepatozoon and Grahamella (Wiger, 1979). 

Trypanosomes.—The term trypanosomiasis applies to all infec- 
tions with flagellate protozoal parasites of the genus 7rypanosoma. 
These parasites invade the blood, lymph, cerebrospinal fluid, and 
various organs in the body (liver and spleen) in many vertebrates 
from fish to man, in which they may produce sleeping sickness 
(James and Harwood, 1969). 

The first record of a trypanosome from a species of the genus 


Laboratory Management and Pathology 671 


Microtus was made by Laveran and Pettit (1909) when they de- 
scribed Trypanosoma microti from M. arvalis. Since that time, try- 
panosomes have been found to be almost worldwide in distribution, 
isolated from a large number of microtines including M. pennsyl- 
vanicus, M. ochrogaster, M. oeconomus, M. californicus, M. agrestis, 
M. nivalis, Lemmus lemmus, and Dicrostonyx torquatus (Fay and 
Rausch, 1969; Jolivet, 1970; McGeachin et al., 1970; Mahnert, 
1972; Molyneux, 1969; Quay, 1955; Wiger, 1978b; Woo et al., 
1980). Although symptoms may vary with species and individuals, 
and often are not apparent, trypanosome infections frequently cause 
anemia, hypoglycemia, and adrenal and splenic hypertrophy (Fay 
and Rausch, 1969; Wiger, 19784). Experimental infections with 7. 
lewisi in rats produced anemia, fetal resorption, abortion, and oc- 
casionally maternal death (Shaw and Dusanec, 1973), and Wiger 
(1977) suggested that these characteristics may apply to microtines. 
Transmission appears to occur from ticks and other blood-sucking 
insects (Liebisch, 1980); infestations tend to be highest at the end 
of the summer (Wiger, 1979). 

Chagas disease caused by the trypanosome, 7. cruzi, is common 
in the southern United States, Mexico, and South America. Symp- 
toms include fever, facial edema, adenitis, anemia, and often death, 
and many species of mammals in this region have been implicated 
as reservoirs (James and Harwood, 1969). 

Lyme disease.—Lyme disease is an epidemic inflammatory con- 
dition which starts with skin lesions and may be followed by neu- 
rologic and cardiac abnormalities and arthritis. Originally reported 
in Wisconsin, it is now known from throughout the northern states. 

A treponema-like spirochete that recently was isolated from the 
tick Ixodes dammini, a common associate of Microtus, strongly sug- 
gests that microtines may be a reservoir for this pathogen (Burg- 
dorfer et al., 1982). 


Fungal Diseases 


The single fungal-caused disease in Microtus, adiasperomyiosis, 
is caused by members of the genus Emmonsia, and is usually a 
benign, self-limiting, mycotic infection in the lungs of wild animals. 
Experimental infections can be established in any tissue and ani- 
mals given large enough doses succumb after weeks or months (Jel- 
lison, 1970). 

The fungus has been isolated from the lungs of rodents through- 


672 Mallory and Dieterich 


TABLE 2 


SPONTANEOUS NEOPLASMS IN COLONY-REARED MICROTINES 


Tumor Species References 
Gastric squamous papillomas Dicrostonyx Barker et al. (1982); 
groenlandicus Dieterich (pers. observ.) 


Mammary adenocarcinomas 


Pancreatic islet cell tumor 
Pancreatic adenocarcinoma 


Adrenal cortical adenoma 


Hardian gland adenocarcinoma 


Inguinal adnexal carcinoma 

Subcutaneous sarcoma 

Sarcoma 

Alveolar rhabdomyo sarcoma 

Retrobulbar squamous cell 
carcinoma 

Retrobulbar adenocarcinoma 

Uterus choriocarcinoma 

Sweat gland adenocarcinoma 

Mesothelioma 

Vaginal adnexal carcinoma 

Leiomyosarcoma 

Sebaceous adenoma 


Labial squamous cell carcinoma 
Perianal gland adenocarcinoma 


Pancreatic and bile duct adeno- 
carcinoma 


M. pinetorum 


Microtus spp. 
Lemmus 
trimucronatus 


D. groenlandicus 


Clethrionomys 
rutilus 

M. muurus 

Lemmus sp. 

D. groenlandicus 

D. groenlandicus 

M. abbreviatus 

D. groenlandicus 


D. groenlandicus 


Microtus spp. 

C. rutilus 

C. rutilus 

C. rutilus 

Not reported 
. rutilus 


C 
D. groenlandicus 


D. groenlandicus 

D. groenlandicus 

D. groenlandicus 

L. lemmus 

L. lemmus 

L. lemmus 

M. miurus X 
M. abbreviatus 

M. oeconomus 

M. pennsylvani- 
cus 

M. abbreviatus 


Cosgrove and O’Far- 
rell (1965) 
Lindsay (1976) 
Leininger et al. (1979); 
Raush and 
Rausch (1975) 
Barker et al. (1982); 
Lindsay (1976) 
Dieterich (pers. observ.); 
Lindsay (1976) 
Dieterich (pers. observ.) 
Lindsay (1976) 
Barker et al. (1982) 
Barker et al. (1982) 
Dieterich (pers. observ.) 
Barker et al. (1982); 
Dieterich (pers. 
observ. ) 
Barker et al. (1982); 
Lindsay (1976) 
Lindsay (1976) 
Lindsay (1976) 
Dieterich (pers. observ.) 
Dieterich (pers. observ.) 
Lindsay (1976) 
Dieterich (pers. observ.) 
Dieterich (pers. observ.) 


Dieterich (pers. observ.) 
Dieterich (pers. observ.) 
Dieterich (pers. observ.) 
Dieterich (pers. observ.) 
Dieterich (pers. observ.) 
Dieterich (pers. observ.) 
Dieterich (pers. observ.) 


Dieterich (pers. observ.) 
Dieterich (pers. observ.) 


Dieterich (pers. observ.) 


SS EE ES ee eee 


Laboratory Management and Pathology 673 


TABLE 2 
CONTINUED 


Tumor Species References 


Hepatic tumor Dicrostonyx sp. Lindsay (1976) 
C. rutilus 
M. miurus 
M. abbreviatus 
L. sibiricus 


L. lemmus 
Preputial gland carcinoma Microtus sp. Lindsay (1976) 
C. rutilus 
Dicrostonyx sp. 
Salivary gland carcinoma Microtines Lindsay (1976) 
Melanoma Microtines 
Chlolangiocarcinoma Microtines 
Seminoma Microtines 
Gastric squamous cell M. abbreviatus Rausch and Rausch 
carcinoma (1968) 


out North America and appears to be Holarctic in distribution. It 
is especially common in microtine rodents, including Microtus. In- 
halation is the only natural route of infection and histopathogenic 
examination should show the presence of numerous spherules in 
the lungs. McDiarmid and Austwick (1954) found evidence of 
pneumonia associated with this disease in dead and dying moles. 


Neoplasms 


Tumors are abnormal masses of tissue, whose growth exceeds, 
and is uncoordinated with, that of the normal parental stock, per- 
sisting after cessation of the stimuli that initiated their development. 
In most tumors, the neoplastic tissue consists of cells of a single 
type, which usually are classified histogenetically according to the 
tissues from which they arose. In addition, oncologists attempt to 
predict the behavior of tumors from their morphology, and classi- 
fication can range from benign to malignant (Willis, 1960). Tumors 
are classified further according to their stage of development. 

Viral, bacterial, nutritional, and other factors may act as etiologic 
agents, and genetic predisposition strongly influences the incidence 
and response to different carcinogens (Heston, 1963). 

Although published information on microtine neoplasms is 


674 Mallory and Dieterich 


sparse, they do occur, especially under laboratory conditions and 
should be a concern of those individuals managing breeding colonies 
(Table 2). 

The etiology of neoplasms in laboratory microtines is unknown; 
however, gastric parasites have been associated with hyperkeratosis 
in the stomach of M. ochrogaster (Dunaway et al., 1968) and with 
papillomas in muskrats (Cosgrove et al., 1968). Gastric squamous 
hyperplasia and dysplasia were found in Lemmus trimucronatus 
infected with the parasite Candida (Leininger et al., 1979), and 
Rausch and Rausch (1968) reported gastric papillomas and carci- 
nomas associated with these organisms. Lindsay (1976) found ham- 
ster type-H viruses and adenovirus associated with tumors in north- 
ern microtines, and Dieterich (pers. observ.) identified a type-R 
virus from mammary tumors. Although a number of possible etio- 
logic agents have been identified, no direct cause-effect relationship 
has been established in laboratory animals. 

Field data indicate that neoplasms occur rarely in natural pop- 
ulations, and are not an important factor in microtine demography. 
Rausch (1967), in a study of 9,376 wild arvicoline rodents from 
Alaska, found a single mammary tumor in M. oeconomus. This 
work was undertaken from 1949 to 1966, and included M. oecon- 
omus, M. miurus, M. longicaudus, M. xanthognathus, Clethrionomys 
rutilus, Dicrostonyx spp., Lemmus sibiricus, and Synaptomys borealis. 

Although neoplasms are relatively rare in wild populations, pos- 
sibly because of the short lifespan of most small mammals (Mallory 
et al., 1981), they are present in significant numbers in longer-lived 
laboratory populations and etiologic agents may be a threat to lab- 
oratory personnel (Barker et al., 1982). 


Constitutional and Other Diseases 


Constitutional diseases are generally defined as malfunctions or 
pathological lesions whose etiology depends to a significant degree 
upon the action of genetic factors. The problem of delineating these 
conditions is that most diseases are a result of environmental and 
genetic interactions, and it is very difficult to separate the two. In 
this section we attempt to describe those conditions that do not fall 
into the previous categories. 

Although information is not abundant, a number of pathologies 
have been mentioned in the literature (Table 3). Richmond and 
Conaway (1969) reported the occurrence of malocculusion of the 
incisors in M. ochrogaster which ultimately resulted in death. The 


Laboratory Management and Pathology 675 


TABLE 3 


PATHOLOGICAL FINDS OF A CONSTITUTIONAL NATURE FOUND IN MICROTINES FROM 


LABORATORY COLONIES 


Species 


Condition 


References 


M. oeconomus 


M. pennsyl- 


vanicus 


Clethrionomys 
rutilus 


Dicrostonyx 
stevensoni 


D. rubricatus 


Hepatic fatty infiltration, atherosclerosis, 


pulmonary congestion, pneumonia, pul- 
monary edema, renal lipidosis, hepati- 
tis, nephrotic syndrome, lipidosis, myo- 
carditis. 

Pulmonary hemorrhage, myocarditis, en- 
docarditis, anemia, hepatic necrosis, en- 
teritis, impacted stomach, impacted in- 
testine, metritus, nephritis, otitis media, 
malnutrition. 

Hepatic fatty infiltration, subacute inter- 
stitial pneumonia. 

Musculoskeletal inflammation, broncho- 
pneumonia, lobar pneumonia, pulmo- 
nary congestion and edema, enteritis, 
hypoplasia, endometritis, interstitial ne- 
phritis, glomerulonephritis, renal tubu- 
lar degeneration, malnutrition. 

Labyrinthitis. 


Pulmonary congestion, hepatic fatty infil- 
tration, atherosclerosis, nephritis, renal 
lepidosis, nephrotic syndrome, intersti- 
tial pneumonia. 

Atherosclerosis, hepatic fatty infiltration, 
pulmonary congestion, esophagitis, 
esophageal lipidosis, lipidosis of feet, 
pulmonary edema, nephrotic syndrome, 
cystitis, interstitial pneumonia, otitis 
media. 

Atherosclerosis, hepatic fatty infiltration, 
esophageal lipidosis, pulmonary conges- 
tion, interstitial pneumonia, fat infiltra- 
tion, cystitis, lipid pneumonitis, pneu- 
monia, pulmonary edema. 


Dieterich and 


Preston (1979) 


Dieterich and 
Preston (1977a) 


Dieterich et al. 
(1973) 

Dieterich and 
Preston 
(19776) 


Mallory (pers. 
observ.) 

Dieterich and 
Preston (1979) 


Dieterich and 
Preston (1979) 


prevalence of this condition was greater when they started their 
colony and were bringing voles in from the wild. Similar conditions 
were observed in M. pennsylvanicus and Dicrostonyx groenlandicus 
under laboratory conditions, and may be associated with problems 
of diet (pers. observ.). Gill and Bolles (1982), however, described 


676 Mallory and Dieterich 


elongate and distorted root development in the molars of M. cali- 
fornicus, which they believed was heritable. 

In a study of the effects of high cholesterol diets on microtines, 
Dieterich and Preston (1979) reported that the voles Clethrionomys 
rutilus and Microtus oeconomus, and the lemmings Dicrostonyx ste- 
vensoni and D. rubricatus, had marked increases in serum cholesterol 
causing lesions of atherosclerosis and hepatic fatty infiltration. D. 
rubricatus had the greatest increase in serum cholestrol (llx), sig- 
nificantly more lesions, and all animals that died spontaneously had 
pathologic lesions associated with hepatic fatty infiltration. Similar 
results were observed in M. pennsylvanicus and D. groenlandicus 
fed the same diet (Dieterich et al., 1973). 


Summary 


Although microtines of the genus Microtus are associated with a 
large number of diseases, personal experience and discussion with 
colleagues support the conclusion that pathogenic problems in lab- 
oratory colonies are relatively rare. Indeed, no instances of infection 
of laboratory personnel nor epidemics among animals have come to 
our attention. 

The many breeding colonies of microtines that have been main- 
tained successfully during the past 10 years (Table 1) have dem- 
onstrated that voles have many characteristics desirable of labora- 
tory mammals. Members of the genus Microtus are maintained 
easily and inexpensively, are relatively easy to handle, have high 
reproductive rates that can be sustained year-round, have good pre- 
and post-operative survival, are generally non-aggressive toward 
familiar conspecifics, appear to be relatively free from disease, and 
in most instances are obtained easily. In addition, compared to Mus, 
they are virtually odorless. These characteristics and others make 
Microtus ideal animals for the study of parameters influencing de- 
mography and other mammalian phenomena under controlled lab- 
oratory conditions. 


Acknowledgments 


We thank Drs. E. Kott and R. M. Simm for reviewing the 
manuscript and L. Spoltore for technical assistance. ‘This work was 


Laboratory Management and Pathology 677 


supported by a National Sciences and Engineering Research Coun- 
cil of Canada grant (No. A7241) to F. F. Mallory. 


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ENDOCRINOLOGY 
ROBERT W. SEABLOOM 


Abstract 


HE endocrinology of North American Microtus is not well 
AG known. Most studies have involved certain aspects of the fe- 
male reproductive system and the adrenopituitary system; limited 
data are available on the male reproductive system and on thyroid 
function. Comparative data are sparse; endocrine studies have been 
conducted on only six species. 

Annual reproduction in Microtus results from the interaction of 
an endogenous annual rhythm with several known exogenous fac- 
tors, including photoperiod, light intensity, temperature, nutrition, 
and social cues. Of special interest is the recent identification of 
plant substances that can stimulate or inhibit reproduction. 

Microtus exhibits a pheromonally induced estrus and coitus-in- 
duced ovulation. Successful ovulation can also be facilitated by 
pheromonal and other contact factors. A post-partum estrus occurs 
in all species. Extended copulatory stimulation or contact with the 
stud male enhances establishment of corpora lutea and the pre- 
implantation stages of pregnancy. The presence of a strange male 
can result in blockage of any stage of pregnancy (Bruce effect), or 
even impair litter survival. This phenomenon has been suggested 
as a side effect of induced estrus and ovulation. 

Estrogen and glucocorticoid-binding macromolecules have been 
demonstrated in the lactating mammary gland of Microtus. There 
is some indication of hypothalamic inhibition of prolactin secretion 
subsequent to exposure to a strange male, thus extending the Bruce 
effect to post-partum events. 

Adrenal weights of Microtus fall within the range of variation 
for other small mammals, but secretory activity is relatively high. 
A high level of 118-dehydrogenase activity occurs in the adrenal 
cortex of M. pennsylvanicus. This activity appears to vary season- 
ally, being highest in fall and winter. The level of corticosterone 
secretion exhibits a marked daily periodicity, normally reaching a 


685 


686 Seabloom 


peak during late afternoon, prior to the peak of motor activity. 
Secretory activity also varies seasonally, and is highest during the 
spring breeding season. 

Adrenal-gonadal interactions have been demonstrated in New 
World Microtus. At puberty, high testosterone levels in males in- 
hibit adrenal enlargement and corticosterone secretion, whereas es- 
trogens have the opposite effect on females. High progesterone levels 
during pregnancy appear to inhibit adrenal response. ACTH 
administration inhibits ovarian and uterine development, but the 
specific pathway of action is not known. 


Introduction 


Much of the research dealing with endocrine mechanisms in New 
World Microtus has emanated from widespread interest in the re- 
markable population phenomena exhibited by microtine rodents. 
Consequently, the status of our knowledge of Microtus endocrinol- 
ogy has been tempered by an ecological-behavioral perspective. Cer- 
tain aspects of adrenocortical function and female reproductive 
physiology have received significant attention in some species, while 
other endocrine systems have been relatively unstudied. Neverthe- 
less, work to date on the genus has made highly significant contri- 
butions to comparative endocrinology and indicates important di- 
rections for future research. 


Timing of Reproductive Function 


Sexual Maturation 


In an extensive review of reproduction in microtines, Hasler 
(1975) noted that most species, including North American Microtus, 
mature earlier than other rodents, with females frequently attaining 
puberty at about 30 days of age. However, along with adult repro- 
ductive development, the specific age of puberty appears to be re- 
lated to both endogenous and exogenous factors, including nutrition, 
social factors, and light. 


Endocrinology 687 


Seasonality 


With the exception of species living in warmer climates, North 
American Muicrotus exhibit variable breeding seasons that generally 
run from early spring until late summer or fall (Asdell, 1964). In 
some species, however, reproductive activity has been recorded dur- 
ing all months (Keller, this volume), with a variety of exogenous 
factors having the capability of maintaining an endocrinological 
balance favoring reproduction. Seasonal reproduction tends to occur 
in northern latitudes, whereas more southern species frequently 
breed throughout the year. 

Bailey (1924), along with numerous subsequent workers, ob- 
served M. pennsylvanicus females carrying embryos at all seasons. 
However, winter breeding in northern populations of this species 
is unusual, except under conditions of heavy snow (Beer and 
MacLeod, 1961) or during periods of cyclic population increase 
(Krebs et al., 1973). Sexual activity occurs throughout the year in 
M. ochrogaster (Fitch, 1957), but there is a seasonal incidence of 
enhanced reproduction in response to heavy precipitation and abun- 
dant new grass. M. californicus also breeds throughout the year 
(Greenwald, 1957). Early litters have the capability of mating in 
their first year, but late spring animals will not attain puberty until 
the following year. 

Adams et al. (1980) reported that initiation of spermatogenesis 
in Microtus breweri coincides with spring increases in daily photo- 
period and temperature. Plasma androgen levels were highest from 
April to June and lowest in October. Like other Microtus, early 
litters of M. brewert may become sexually mature during the season 
of their birth, but late litters delay puberty through the winter and 
become mature prior to the subsequent spring breeding season. 

The existence of an endogenous circannual rhythm of reproduc- 
tive development must be considered for the North American M:- 
crotus. These voles may undergo a refractory period after the breed- 
ing season in which the gonads regress while under the same light 
regimen providing the original stimulus (van Tienhoven, 1968). 
Grocock (1980) reported that the British vole, Microtus agrestis, 
undergoes spontaneous gonadal recrudescence after a 6-month pe- 
riod of inhibition following short daylengths. M. pennsylvanicus 
captured during the late summer or fall generally does not come 
into breeding condition in the laboratory until the following spring, 


688 Seabloom 


in spite of maintenance of favorable photoperiods (Seabloom, pers. 
observ.). 


Photic Cues 


In Microtus, as with many other rodents, light exerts a major 
influence over sexual maturation and gonadal recrudescence. Spe- 
cific components may include length of daily photoperiod, light in- 
tensity, and wavelength. Reproductive development of both New 
World and Old World microtines is positively correlated with in- 
creased photoperiods. Pinter and Negus (1965) reported that litter 
size in M. montanus is greater under 18-h versus 6-h photoperiods. 
However, optimal daylengths may exist, above or below which there 
are adverse effects on gonadal development and production of young. 
In M. pennsylvanicus, reproductive function is optimal under a 
16:8 light-dark cycle (Imel and Amann, 1979). Shorter (12:12) or 
longer (18:6) photoperiods have an adverse effect on female fertility. 

Despite behavioral preferences for low light intensities, there ap- 
pears to be a positive correlation between intensity of lighting and 
reproductive development in microtines. Geyer and Rogers (1979) 
compared litter production in M. pinetorum raised under high (75- 
200 lumens) and low (0-75 lumens) light intensities. Litter pro- 
duction and litter size were approximately doubled under the high 
intensities. Vaughan et al. (1973) reported that female M. montanus 
held in constant dark exhibited suppressed body size along with 
low ovarian, uterine, adrenal, and Harderian gland weights. ‘They 
further suggested that the influence of constant dark may be me- 
diated through the pineal gland. Darkness has been demonstrated 
to stimulate the pineal gland to produce the antigonadotrophin, 
melatonin, in laboratory rats. Both ovariectomy and constant dark 
inhibited thymic involution in M. montanus, suggesting that con- 
stant dark stimulates pineal production of melatonin which, in turn, 
inhibits the action of follicle-stimulating hormone (FSH) on ovarian 
secretion of thymolytic steroids. Earlier Vaughan et al. (1972) dem- 
onstrated the action of melatonin in blocking the effect of FSH on 
compensatory ovarian hypertrophy of unilaterally ovariectomized 
laboratory mice and M. montanus. 

There have been no studies of the effects of wavelength on re- 
productive development of New World Microtus, and reports in- 
volving other microtines are inconclusive. There is some indication 


Endocrinology 689 


that exposure to only the longer (red) wavelengths may result in 
delayed puberty, at least in females (Hasler, 1975). 


Nutritional Cues 


While the status of the food resource has long been recognized 
as having a major influence on reproductive performance, only in 
recent years have nutritional cues and their regulation of specific 
endocrine pathways been studied intensively. Much of the relevant 
work on wild species has dealt with North American Microtus (see 
Batzli, this volume). 

Initiation of breeding seasons has long been associated with fresh 
production of green plants, and many species experience reduced 
fertility during periods of drought. Some authors postulated that in 
certain rodents the timing of breeding seasons may be in response 
to the appearance of new vegetation rather than to photoperiodic 
cues, because the nutritional stimulus may be more appropriate in 
harsh environments (Labov, 1977). Greenwald (1957) observed a 
close association between breeding activity by M. californicus and 
the occurrence of new vegetative growth. Pinter and Negus (1965) 
discussed the interaction of diet and photoperiod in regulation of 
reproduction in M. montanus. They suspected the existence of a 
specific dietary cue rather than direct effects of changes in nutri- 
tional levels. 

A series of studies on M. montanus demonstrated that small di- 
etary supplements of plants and plant extracts have marked effects 
on rate of growth, endocrine development, and reproductive per- 
formance (Negus and Berger, 1977; Negus et al., 1977). Sprouted 
wheat supplied in the diet increased growth rates and reduced the 
time to onset of puberty (Pinter, 1968). Weight decreases of the 
pineal gland, and increases of uterus and adrenal gland followed 
dietary supplements of fresh lettuce, sprouted wheat, or spinach 
extract (Berger and Negus, 1974; Negus and Berger, 1971; Negus 
and Pinter, 1966). Supplements of spinach extracts resulted in in- 
creased numbers of ovarian follicles (Negus and Pinter, 1966). 
However, overall enhanced reproductive performance following such 
supplements appeared to be via increased frequency of post-partum 
matings and decreased rates of litter loss rather than through in- 
creased litter size (Negus and Pinter, 1966; Pinter and Negus, 1965). 

Recently, 6-methoxybenzoxazolinone (6-MBOA) was identified 


690 Seabloom 


as a stimulant of reproductive activity in M. montanus (Sanders et 
al., 1981). This naturally occurring plant-derived cyclic carbamate 
is a non-estrogenic compound, which, when added to a laboratory 
diet, resulted in significantly increased uterine and ovarian weights. 
Enlarged ovaries were due primarily to increased numbers of antral 
follicles. Although Sanders et al. (1981) noted that it is yet to be 
demonstrated whether this plant-derived cue is widespread among 
herbivorous mammals, equivalent response of laboratory mice (Mus 
musculus) indicates that at least it is not restricted to microtines. 

To test the capability of 6-MBOA in triggering reproduction of 
M. montanus, Berger et al. (1981) provided treated and untreated 
supplements of rolled oats to reproductively inactive populations 
during winter. After three weeks of treatment, males from the ex- 
perimental plots exhibited testicular hypertrophy and females a 
70% incidence of pregnancy. No pregnancies occurred on control 
plots. Consequently, they concluded that 6-MBOA provides an ul- 
timate cue for reproduction in this species, and suggested that it 
may play a more widespread role in other microtines. 

Berger et al. (1981) suggested that 6-MBOA operates at the 
neural or pituitary rather than gonadal level, and available evidence 
tends to support this hypothesis. Hinkley (1966) observed an in- 
crease in delta basophil cells in the pituitaries of Microtus montanus 
that received dietary supplements of extracts from wheat sprouts. 
Delta cells are known to secrete gonadotropins. Negus and Berger 
(1971) reported a significant decrease in pineal weight of M. mon- 
tanus following dietary supplements of fresh lettuce, and later Ber- 
ger and Negus (1974) added experimental evidence that the com- 
pound operates at the pineal-hypothalamic-pituitary level. It would 
appear, therefore, that the microtine pineal gland may utilize di- 
etary as well as photoperiodic cues in its regulation of pituitary 
secretion of gonadotropins. 

In addition to the utilization of dietary cues in initiation of its 
breeding season, Microtus montanus apparently relies on other nat- 
urally occurring compounds to signal termination of reproduction. 
Negus et al. (1977) provided data correlating initiation and cessa- 
tion of reproduction with seasonally varying chemical composition 
of vegetation. Furthermore, Berger et al. (1977) identified cinnamic 
acids and related vinylphenols as reproductive inhibitors in M. mon- 
tanus. Dietary supplements of these compounds resulted in de- 
creased uterine weight, inhibition of follicular development, and 


Endocrinology 691 


diminished reproductive activity. These compounds are most abun- 
dant in vegetation subsequent to flowering, senescence, and brown- 
ing. The physiological site of activity of these inhibitors has yet to 
be identified. 


Social Cues 


Population density.—High population densities apparently inhib- 
it sexual maturation and adult female reproduction in both North 
American and Old World microtines. Crowding was proposed by 
Christian (1961, 1963, 1971, 1975) to result in social pressures 
affecting natality as well as mortality. Pasley and McKinney (1973) 
reported that female M. pennsylvanicus that were housed in groups 
of eight from weaning until pairing exhibited lighter ovaries and 
uteri and fewer corpora lutea than those that were housed singly. 
They noted prior work by Christian et al. (1965) and Christian 
and Davis (1966), in which increased secretory activity of the pi- 
tuitary-adrenal axis was implicated as providing density-dependent 
negative feedback inhibiting reproduction. 

The pine vole (M. pinetorum), in contrast to M. pennsylvanicus, 
exhibits a relatively low reproductive rate and stable populations 
in nature. Schadler (1980) examined the histology of testes and 
ovaries of pine voles raised under varying conditions of crowding. 
Testes of crowded males weighed 41% less than uncrowded and 
exhibited low spermatogenic indices. None of the crowded females 
ovulated, in contrast to a 21% frequency of corpora lutea observed 
in uncrowded voles. Crowded voles exhibited premature formation 
of antra, a small proportion of mature preovulatory follicles, and 
increased atresia of undeveloped follicles. 

Pheromones and neuroendocrine response.—The total social envi- 
ronment, as well as density per se, functions as an external variable 
in regulation of rate of sexual maturation and development of 
breeding condition. There has been considerable work on the influ- 
ence of conspecifics and pheromonal factors influencing reproduc- 
tion in murids, but relatively little on microtines. 

Pheromonal inhibition of sexual maturation by littermates occurs 
in some species of Microtus. In M. ochrogaster, vaginal opening is 
earliest in weanling females paired with non-littermate adult males, 
intermediate with non-littermate weanling males, and slowest with 
littermate weanlings (Hasler and Nalbandov, 1974). Hasler and 
Nalbandov noted that age and degree of “strangeness” had two 


692 Seabloom 


distinct effects. Vaginal opening was influenced by both factors, but 
litter production was only affected by strangeness. Batzli et al. (1977) 
found that both sexual maturation and growth were suppressed by 
littermates in M. californicus and M. ochrogaster, but not in M. 
pennsylvanicus. A pheromone was implicated because suppression 
also occurred in voles isolated except for air supply. Normal devel- 
opment resumed when voles were housed with strangers of the 
opposite sex. McGuire and Getz (1981) obtained similar results 
with M. ochrogaster, but their data suggest that the activation pher- 
omone must be transmitted by naso-genital grooming rather than 
through the air. 

Age-related olfactory cues may change with the onset of testos- 
terone production and attainment of puberty in the male. Richmond 
and Stehn (1976) questioned, however, if early maturation merely 
involved early induction of estrus or might be “further regulated 
by prepuberal exposure to males or other conspecifics.” They noted 
that the stimulus provided by male exposure might have been pre- 
conditioned by a brief prepuberal exposure to another male. If so, 
then seasonal occurrence of delayed maturation characteristic of 
many microtines may be related to the seasonal absence of stimuli 
provided by sexually active males. 

Baddaloo and Clulow (1981) exposed laboratory-raised female 
meadow voles (M. pennsylvanicus) to mature males (with and with- 
out physical contact), virgin and multi-parous females, male urine, 
and empty cages. Exposure to males or male urine accelerated mat- 
uration, whereas female exposure had no effect. Consequently, 
Baddaloo and Clulow (1981) concluded that male mediation was 
pheromonal and that the active compound was in the urine. 

Recent studies have further documented the existence of a pher- 
omone in male urine having the capability of activating female 
reproduction. Carter et al. (1980) reported that virgin female M. 
ochrogaster over 20 days of age exhibited uterine growth and other 
indications of reproductive activity following exposure to male-re- 
lated stimuli. Exposure to an unfamiliar adult male for less than 1 
h induced uterine weight increases within 48 h and lasted at least 
10 days. Exposure to male urine induced similar reproductive de- 
velopment. In contrast to Baddaloo and Clulow’s (1981) study, 
Carter et al. (1980) reported that physical contact with an intact 
male or male urine was essential for reproductive activation, thus 
eliminating visual and airborne cues. Although sibling pairs nor- 


Endocrinology 693 


mally did not reproduce, estrus could be induced by direct appli- 
cation of a sibling male’s urine to the female’s upper lip, thus 
indicating a behavioral barrier to reproduction. 

In a related study elucidating the physiological pathways for 
reproduction in M. ochrogaster, Dluzen et al. (1981) exposed fe- 
males to a single drop of male urine on the upper lip. This produced 
a significant increase in serum luteinizing hormone (LH) in less 
than 1 min. The exposure also resulted in changes in luteinizing 
hormone-releasing hormone (LHRH) and norepinephrine (NE) in 
the tissue of the posterior olfactory bulb. They noted that most 
studies of LHRH release implicated the preoptic-hypothalamic 
areas, but that nerve terminals containing LHRH are found in the 
olfactory bulb. The catecholamines norepinephrine and dopamine 
are also reproductive regulators found in the olfactory bulb. Nor- 
epinephrine may be implicated in synthesis or release of LHRH, 
while dopamine is an inhibitor of reproductive processes. Dluzen 
et al. (1981) suggested that the observed increase in LHRH and 
its concentration in the posterior olfactory bulb of the prairie vole 
implicated a neuroendocrine link between the external environment 
and reproductive activation. 


Estrus and Ovulation 


The social cues discussed above appear to be instrumental in 
regulation of estrous cycles and ovulation in most microtines. Hasler 
(1975) discussed the problems associated with some of the early 
studies based upon females permanently paired with males or his- 
tological studies of wild-caught animals. Neither approach allowed 
examination of a recurrent cycle. Consequently, many reports in 
the literature yielded contradictory results. 

Older reports suggest that estrous cyles in New and Old World 
microtines are similar to those of laboratory mice and rats. Asdell 
(1964) cited unpublished data for M. pennsylvanicus indicating 
spontaneous changes in the vaginal smear typical of Rattus and 
Mus. Similar cycles were reported for M. oeconomus (Hoyte, 1955) 
and M. pinetorum (Kirkpatrick and Valentine, 1970). 

A preponderance of recent studies, however, indicate that exper- 
imentally isolated microtine females are capable of remaining in 
diestrus for extended periods. In contrast to the earlier report on 


694 Seabloom 


M. pinetorum (Kirkpatrick and Valentine, 1970), Schadler and 
Butterstein (1979) found no pattern of vaginal cyclicity. Female 
pine voles housed adjacent to males exhibited 1-22 days of contin- 
uous estrus followed by 1-9 days of diestrus. Similar patterns also 
have been described for M. pennsylvanicus, M. montanus, and M. 
ochrogaster. Clulow and Mallory (1970) could not demonstrate any 
regular cyles of vaginal smear patterns from wild-caught M. penn- 
sylvanicus. In addition, isolated females exhibited constant diestrus, 
whereas those housed with castrate males exhibited constant estrus. 
Similarly, isolated M. townsendw were found to delay maturation 
and extend diestrus prior to their first estrus (MacFarlane and 
Taylor, 1981). Both diestrus and estrus may be extended up to 18 
days, but isolated females do not ovulate or form corpora (Mac- 
Farlane and Taylor, 1982a). 

Regular estrous cycles do not occur in M. montanus that have 
been isolated or housed adjacent to males (Gray et al., 1974a). 
Isolated M. ochrogaster held under a 12-h photoperiod remain in 
continuous diestrus, but altering housing conditions can have vary- 
ing effects on reproductive activity and receptivity (Richmond and 
Conaway, 1969a). Richmond and Conaway found that 71-83% of 
the females attained estrus within a week if moved adjacent to males 
or allowed direct contact with males. 

Hasler and Conaway (1973) further studied the effect of males 
in inducing estrus in M. ochrogaster. In tests of the effect of the 
presence or absence of the male on the female reproductive state 
they found a 72-h exposure to be maximally effective in inducing 
estrus. Injections of low levels of estradiol cyclopentylpropionate in 
castrated females resulted in vaginal mucification, whereas higher 
levels resulted in cornification. Their data supported the hypothesis 
that among species exhibiting induced estrus and ovulation, it would 
be advantageous for development of the uterine epithelium or vagi- 
nal opening to occur only in the presence of a strong estrus inducer. 
Vaginal epithelial hyperplasia, vaginal opening, and uterine epi- 
thelial hyperplasia would represent successive stages with increas- 
ing levels or more prolonged exposure to estrogen stimulation. 

In addition to pheromonally induced estrus, ovulation induced 
by coitus further maximizes reproductive efficiency. This phenom- 
enon is widespread among mammalian orders, and microtine ro- 
dents are not exceptions. Indeed, Jéchle (1973) noted that “The 


Endocrinology 695 


TABLE 1 
TYPE OF OVULATION IN NORTH AMERICAN Maicrotus (IN PART, AFTER HASLER, 1975) 


Type of Time of 
Species ovulation ovulation References 
M. californicus Induced 15 h post-coitus Greenwald (1956) 
M. montanus Induced 8 h post-coitus Cross (1972) 
Induced 8 h post-HCG Gray et al. (19742) 
M. ochrogaster Induced 9-10 h post-coitus Richmond and Cona- 
way (19696) 
Induced — Gray et al. (19745) 
M. oeconomus Spontaneous — Hoyte (1955) 
Spontaneous _ Asdell (1964) 
M. pennsylvanicus Induced 12-18 h post-coitus Lee et al. (1970) 
Induced — Clulow and Mallory 
(1970) 
M. pinetorum Induced — Kirkpatrick and 


Valentine (1970) 


system is so effective in coordinating all necessary steps for the 
assurance of fertility, in so many species of different orders, families, 
and genera, that it makes one wonder why its principles, in toto or 
at least partially, have not found an even wider distribution in 
mammalian evolution.” 

Induced ovulation appears to be the rule in Microtus, and al- 
though there are reports to the contrary, Breed (1967) suggested 
that there is only circumstantial evidence for spontaneous ovulation 
in the genus. To date, induced ovulation has been demonstrated for 
six species of North American Microtus (Table 1). 

Post-copulatory ovarian changes have been reported for several 
species of Mnicrotus, but the associated requisite neurohormonal 
pathways involved must be inferred from studies of other species. 
Jochle (1973) summarized the known neurohormonal connections 
between the genital tract, hypothalamus, pituitary, and ovaries for 
a variety of spontaneous and induced ovulators. In rats and mice 
the pelvic nerves are involved, with the coital stimulus eventually 
reaching the preoptic region of the hypothalamus. The stimulus 
may activate the cyclic ovulatory center or descend to the median 


696 Seabloom 


TABLE 2 
MEAN (+SE) PLASMA LEVELS OF LH AND PROGESTERONE IN MONTANE VOLES, 
Microtus montanus (FROM GRAY ET AL., 1976) 


LH Progesterone 

Reproductive state (nanograms/ml) (nanograms/ml) 
Females 

Diestrus AOA ae yy) 9:0) = 019 

Estrus, unmated D3 leats D5 14.0 + 1.1 

Estrus, mated 896.1 + 136.7 22.0) 22 125 
Males 

Unmated 28.8 + 3.6 

Mated 123.0 + 40.5 


eminence, eventually resulting in triggering an ovulatory LH dis- 
charge from the adenohypophysis. 

Few data are available on precise hormonal changes in Microtus 
following copulation. Gray et al. (1976) reported plasma levels of 
LH and progesterone for different reproductive states of M. mon- 
tanus (Table 2). In females, mating resulted in a nearly 40-fold 
increase in LH, and a 57% increase in progesterone within 1 h. 
This response was similar to that observed for Old World M. agres- 
tis. In addition to the post-coital increase in progesterone, there is 
an accompanying decrease in serum estradiol. Estrous M. ochro- 
gaster have serum E, levels around 78 picograms/ml, which decline 
to 57 picograms/ml by 48 h post-coitum (Prentice and Shepherd, 
1973) 

Post-copulatory ovarian changes have been reported for several 
species of Microtus. Following copulation there is usually significant 
follicular enlargement. Follicular diameter of M. californicus en- 
larges from 500-600 um to 900 um, a 70-80% increase (Greenwald, 
1956). Post-copulatory follicles of M. ochrogaster average about 1,000 
um (Richmond, 1967). Cross (1972) observed follicular enlarge- 
ment in M. montanus of 623-722 um. However, Gray et al. (19742) 
did not observe any pre-ovulatory swelling in that species. 

In M. californicus, subsequent to pre-ovulatory swelling, there is 
a breakdown of the granulosa cells surrounding the ovum until it 
is free in the antrum, surrounded only by the corona radiata 


Endocrinology 697 


(Greenwald, 1956). Ova of all reported Microtus are of similar size, 
averaging about 60 um (Cross, 1971; Greenwald, 1956; Richmond, 
1967). By contrast, mature ova of Mus average 95 um (Rugh, 1968). 

Varying frequencies of copulatory activity can affect the proba- 
bility of ovulation and implantation. In M. ochrogaster, only one 
ejaculatory series is sufficient to induce ovulation and implantation, 
but the probability of ovulation increases with the number of in- 
tromissions and intravaginal thrusts (Gray et al., 19745). Similar 
results have been reported for M. montanus (Davis et al., 1974). 
Kenney et al. (19776) found that M. ochrogaster, like M. agrestis, 
ovulated in response to artificial vaginal-cervical stimulation, but 
only subsequent to one intromission from a male. However, unlike 
M. agrestis, less copulatory stimulation was required and there was 
no apparent dissociation between ovulation and subsequent for- 
mulation of a functional corpus luteum resulting from minimal 
mechanical stimulation. They also suggested that pheromonal or 
contact factors are a prerequisite to ovulation. This was supported 
recently by Dluzen et al. (1981), who found that exposure of fe- 
males to a single drop of male urine on the upper lip results in a 
rapid increase in LHRH in the olfactory bulb and LH in the 
serum. 


Formation and Duration of Corpus Luteum 


In Microtus, new corpora lutea are formed 15-18 h post-coitum, 
and are completely solid between 48 and 72 h (Greenwald, 1956; 
Lee et al., 1970). The corpus luteum forms from both thecal and 
granulosa cells but at the time it differentiates into luteal cells the 
distribution of the two components cannot be determined. 

The life of the corpus luteum in those New World Microtus in 
which it has been studied is similar to that described for Mus (Rugh, 
1968). Lee et al. (1970) mated mature female M. pennsylvanicus 
with vasectomized males, and observed persistent corpora lutea up 
to 9 days post-coitum. These corpora lutea had well-defined, func- 
tional luteal cells with small fat particles. Regression began on days 
10-11, as evidenced by the presence of vacuolization, connective 
tissue cells, and large fat particles. 

Corpora lutea are functional throughout pregnancy, reaching 
maximum size near the end of gestation (Greenwald, 1956; Lee et 


698 Seabloom 


al., 1970; Richmond, 1967). Some females possess large numbers 
of corpora (up to 29), most of which are regarded as accessory 
corpora (Greenwald, 1956). 

Limited copulatory stimuli, while sufficient to induce ovulation 
(Gray et al., 19746), may result in short-lived corpora lutea. Ken- 
ney and Dewsbury (1977) subjected M. montanus females to only 
one ejaculatory series prior to examination for CL on days 3 and 
8 after mating. Seven of 10 females had well developed CL on day 
3, while only one of 10 had CL and implanted embryos by day 8. 
This rapid degeneration of CL following limited mating is similar 
to reports for the Old World M. agrestis (Milligan, 1974, 1975), 
and may represent an additional type of reproductive cycle for the 
non-pregnant female mammal. 


Gestation 


Most small microtines have gestation periods averaging 20-25 
days (Hasler, 1975). However, various endocrine mechanisms can 
influence gestation, up to and including its termination. 

Although lactational delay of gestation has been reported for a 
variety of microtines (Hasler, 1975), it has not been found in New 
World Microtus. Reports for M. montanus (Pinter and Negus, 1965) 
and M. ochrogaster (Richmond and Conaway, 1969a) specifically 
indicated no lactational delay of gestation. Data on litter intervals 
for M. pennsylvanicus, M. oeconomus, M. miurus, and M. abbreviatus 
also tend to support this conclusion (Morrison et al., 1976). 

Subsequent to fertilization, continued tactile and olfactory stim- 
ulation by the stud male can be important in reinforcing the neu- 
roendocrine pathways requisite to the pre-implantation stages of 
pregnancy. Richmond and Stehn (1976) reported that in M. och- 
rogaster, between 1 and 4 days of cohabitation were required to 
achieve a maximum (over 90%) incidence of successful pregnancies. 
In M. montanus, removal of the stud male within 24 h of mating 
caused a significant incidence of pregnancy terminations (Berger 
and Negus, 1982). However, continued mating activity for up to 
48 h enhanced the maintenance of pregnancy. Similar results were 
reported for Old World M. agrestis by Milligan (1975) who indi- 
cated that, although limited mating can induce ovulation, the re- 


Endocrinology 699 


sulting corpora lutea degenerate rapidly and cannot maintain a 
decidual reaction. 

The termination of pregnancy by pheromonal influence of a 
strange male (Bruce effect) has been demonstrated for both Old 
World and New World Microtus. Male-induced abortion has been 
reported for M. pennsyluvanicus, M. ochrogaster, M. montanus, and 
M. pinetorum. Clulow and Langford (1971) demonstrated a de- 
pressed pregnancy rate of 20% in female M. pennsylvanicus exposed 
to strange males 3 days or less after coitus with an original stud. 
Clulow and Mallory (1974) further demonstrated that the preg- 
nancies of M. pennsylvanicus can be terminated repeatedly when 
exposed to a series of strange males, each subsequently inducing 
ovulation and initiating a further pregnancy. Mallory and Clulow 
(1977) studied normal and blocked pregnancy in M. pennsylvanicus 
in the laboratory, and compared blockage with the incidence of 
pregnancy failure in the wild. Females were susceptible to blockage 
on days 2 and 5 post-coitum. Occurrence of a second set of corpora 
lutea apparently did not accelerate involution of the first set. Lac- 
tating females were not susceptible to male-induced blockage. The 
latter observation was consistent with Bruce’s (1966) conclusion 
that blockage is dependent on hypothalamic inhibition of prolactin 
secretion. Apparently, the neural stimulus provided by nursing young 
overrides the pheromonally-induced blocking action provided by the 
strange male. 

Pre-implantation pregnancy blockage can apparently be induced 
by heterospecific as well as conspecific strange males. In M. mon- 
tanus, blockage was induced by male Lagurus curtatus (Jannett, 
1979). 

Male-induced pregnancy blockage has now been demonstrated 
for post-implantation as well as pre-implantation stages of preg- 
nancy. Blockage was induced in M. ochrogaster during most stages 
of pregnancy with no reduction in incidence until after day 15 
(Stehn and Richmond, 1975). Kenney et al. (1977a) reported preg- 
nancy blockage by day 14 in M. ochrogaster and M. pennsylvanicus, 
as well as in the cricetid, Peromyscus maniculatus. The incidence of 
blockage was lower than that reported for M. ochrogaster by Stehn 
and Richmond, but may have been due to higher levels of prolactin 
in recently lactating females of the latter study. Stehn and Jannett 
(1981) further reported on the incidence of pregnancy blockage in 
M. ochrogaster, M. montanus, M. pinetorum, and Lagurus curtatus. 


700 Seabloom 


Abortions occurred in all species tested except L. curtatus. Concur- 
rent lactation did not reduce abortion in M. ochrogaster or M. mon- 
tanus in contrast to that reported for M. pennsylvanicus (Mallory 
and Clulow, 1977) and to the earlier suggestion that the low inci- 
dence of blockage in M. ochrogaster was associated with recent lac- 
tation (Kenney et al., 1977a). 

Schadler (1981) reported an incidence of 87-88% blocked preg- 
nancies in M. pinetorum when females were exposed to a strange 
male on day 10 or 15. A high incidence of post-implantation abor- 
tion also occurred when females were only exposed to cage litter 
soiled by strange males. Consequently, these data support the con- 
clusion that odor alone is sufficient to induce blockage at any stage 
of pregnancy in Muicrotus. 

Male-induced pregnancy blockage in microtines may be a side 
effect of induced estrus and ovulation (Stehn and Richmond, 1975). 
Stehn and Jannett (1981) further suggested that strong selection 
for acceleration of puberty and estrus may exist in microtines, and 
that the occasional loss of a litter through male-induced estrus may 
be a relatively unimportant consequence. However, Kenney et al. 
(1977a) detected no significant differences in the incidence of preg- 
nancy blockage between spontaneous and induced ovulators. ‘They 
concluded that the data did not suggest an association between in- 
creased male-induced pregnancy blockage and induced ovulation. 
Nevertheless, there appears to be a definite association of the inci- 
dence of pregnancy blockage with a variety of species in which the 
induction of estrus and ovulation plays an overriding role. 


Post-partum Events 


Post-partum Estrus 


All microtines apparently experience a post-partum estrus, be- 
coming receptive shortly after giving birth (Hasler, 1975). North 
American Microtus for which post-partum estrus has been described 
or implied include M. abbreviatus (Morrison et al., 1976), M. cal- 
ifornicus (Greenwald, 1956), M. miurus (Morrison et al., 1976), M. 
montanus (Gray et al., 1974a; Pinter and Negus, 1965), M. ochro- 
gaster (Richmond and Conaway, 1969a, 19696), M. pennsylvanicus 
(Lee et al., 1970; Morrison et al., 1976), M. pinetorum (Kirkpatrick 


Endocrinology 701 


and Valentine, 1970; Schadler and Butterstein, 1979), and M. town- 
sendu (MacFarlane and Taylor, 19826). 

In M. pennsylvanicus, estrus occurs on the day of parturition, 
with copulation inducing ovulation on the same day (Lee et al., 
1970). Richmond and Conaway (1969a) observed M. ochrogaster 
females copulating before completion of all births of a litter. M. 
ochrogaster females may remain in continuous estrus throughout 
lactation, or if separated from a male, for about 4 days following 
parturition. 


Lactation 


There has been very little research on lactation per se in micro- 
tine rodents. What little has been done indicates that mammary 
physiology may be comparable to that described for laboratory rats 
and mice. However, some neuroendocrine pathways controlling lac- 
tation may be somewhat distinct. 

Hormone receptor proteins have been identified and partially 
characterized in the lactating mammary gland of M. montanus. Spe- 
cific estrogen receptor proteins were demonstrated by Beers and 
Wittliff (1973) in mammary and uterine cytosol. Hydrocortisone 
had no effect on the binding of *H-estradiol-176 to mammary or 
uterine receptors, but later work (Turnell et al., 1974) reported the 
presence of distinct glucocorticoid-binding macromolecules in the 
lactating mammary gland. These protein receptors have similar 
characteristics to those identified in the lactating mammary gland 
of Rattus and Mus. Estrogens and progesterone function in prolif- 
eration of mammary cells, whereas glucocorticoids, along with in- 
sulin and prolactin, are required for cell differentiation (Bentley, 
1976), 

There is some indication that the neuroendocrine influences as- 
sociated with male-induced pregnancy blockage now may be ex- 
tended into the period of lactation. Schadler (1982) recently re- 
ported that removal of a stud M. pinetorum which was paired to a 
nursing female, and replacement with a strange male, resulted in 
high litter mortality and poor weight gain in surviving young. This 
implies an extension of the Bruce effect into post-partum events via 
hypothalamic inhibition of prolactin secretion resulting in failure 
or impairment of lactation. Under this scheme, the olfactory stim- 
ulus provided by a strange male would result in hypothalamic pro- 
duction of FSH-RH and subsequently high estrogen levels associ- 


702 Seabloom 


ated with estrus. In addition, the same olfactory stimulus would 
provide for hypothalamic production of prolactin release-inhibiting 
hormone (P-R-IH), with resulting diminished mammary cell dif- 
ferentiation and secretion. 


Testicular Activity 


In contrast to the bulk of research on reproductive physiology of 
female Microtus, relatively little has been done on the male. The 
morphology of the male reproductive tract of M. ochrogaster was 
described by Janes (1963). The testis is comparable to that of other 
mammals, and is very similar to Old World M. arvalis. Secretory 
interstitial cells are of variable shape and occur in groups of 1-10 
in angular spaces between the seminiferous tubules. Other mor- 
phological features of the testes (seminiferous tubules, rete testis, 
efferent ducts) are all characteristic of other small rodents. Relative 
testicular size in microtines appears to be high compared to other 
rodents. In M. pennsylvanicus, relative weight of the testis is about 
double that of the laboratory mouse (Dieterich and Preston, 1977). 

Although testicular morphology is similar to other species, tes- 
ticular activity in Microtus is relatively high. Microtus ochrogaster 
exhibited the shortest known spermatogenic cycle (7.2 days) of sem- 
iniferous epithelium (Schuler and Gier, 1976). The entire process 
of spermatogenesis in M. ochrogaster, including meiotic stages, en- 
compassed 28.7 days. The durations of spermatogenic cycles for 
other microtines have not been reported to date. 

Data on circulating androgens are limited to two species of North 
American Microtus, the beach vole (M. breweri) and Townsend’s 
vole (M. townsendi). Plasma androgens of M. brewer: were highest 
(>2 nanograms/ml) during April-June, the period of greatest tes- 
ticular weight (1,300—1,600 mg) and spermatogenic activity (Adams 
et al., 1980). Androgen levels were minimal (<1 nanogram/ml) 
during October when testes were smallest (43 mg) and spermato- 
genic activity was nil. Intraperitoneal administration of 10 ug of 
either ovine or murine LH resulted in a two- to three-fold increase 
in plasma androgens. 

Total androgens of male M. townsendi during a spring popula- 
tion decline were reported by McDonald and Taitt (1982). Andro- 
gen levels of larger (>80 gm) voles averaged about 2.6 nanograms/ 
ml. Smaller males had levels averaging 1.25 nanograms/ml. An- 


Endocrinology 703 


drogen levels reported for other rodents were highly variable (Gus- 
tafson and Shemesh, 1976), but those indicated for M. breweri and 
M. townsendu appear to be in the low range. However, those values 
should not necessarily be regarded as representative of microtines 
until data are available involving seasonal and diurnal variation in 
other more widely distributed species. 


Thyroid 


Thyroid activity has not been extensively studied in Microtus. 
Those studies which have been conducted indicate similar responses 
to various stressors, photoperiod, and temperature to those observed 
for laboratory rodents. 

In M. californicus, thyroid activity can be inhibited by various 
stressors, including high population density, food depletion, and 
harassment (Houlihan, 1963). In a penned experiment, voles in the 
control group (low density) accumulated 20.7% of administered 
1 after 24 h. Thyroidal '*'I uptake by voles in the experimental 
(high density) pen was 14.4%. The observed diminished thyroidal 
activity is consistent with results of experiments by other workers 
using a variety of stresses on laboratory rats. 

Circulating levels of thyroxine have been reported for M. mon- 
tanus and M. ochrogaster. In M. montanus maintained under a 16- 
h photoperiod, T, levels averaged from 4.4 to 4.6 ug/dl (Petterborg, 
1978). These levels were suppressed under short (8-h) photoperi- 
ods, concomitant with loss of body weight. Similar photoperiodic 
effects on growth and thyroid activity in M. pennsylvanicus were 
reported by Pistole and Cranford (1982). Subadult voles gained 
weight more rapidly under 18-h than 6-h photoperiods, and adults 
lost weight under the shorter photoperiods. Relative thyroid weights 
were similar under the two light regimes, but thyroid activity was 
significantly higher in voles held under the 18-h photoperiods. Thy- 
roid uptake of '°I and circulating thyroxine were both significantly 
higher than in voles held under 6 h of light. These data, along with 
those of Petterborg (1978) have been interpreted as indicative of a 
metabolic adjustment resulting in reduced body size and lowered 
energy demands in preparation for winter. 

Serum T, in M. ochrogaster averaged 4.8 ug/dl (Hudson, 1980), 
a level comparable to that in M. montanus. Thyroid secretion was 
inhibited by Tapazole but there was no effect on standard metab- 


704 Seabloom 


olism. Tapazole blockage of thyroxine resulted in a 3°C increase in 
the highest air temperature tolerated without stress. In subsequent 
experiments, there were no significant differences in Serum T, in 
voles exposed to a variety of air temperatures from 5 to 35°C. 
However, there was a high correlation between '*°I clearance and 
air temperature. The half-life of '*I labeled T, was 20.2 days at 
35°C, but this decreased to 4.3 days at 5°C. The conflicting data 
between thyroxine levels and rate of radioiodine release caused 
Hudson (1980) to question the reliability of using circulating thy- 
roxine as an indicator of thyroid secretory activity. 


Adrenal Cortex 


Adrenal Morphology 


Adrenal weight has long been utilized as a convenient indicator 
of the functional state of cortical activity. In the absence of other 
differential influences, there is a positive logarithmic relationship 
between adrenal weight and body size which holds for a variety of 
mammals, including Muicrotus (Christian, 1953). Adrenal weight 
relationships have been published for a variety of species of New 
World Microtus, including M. brewer: (To and Tamarin, 1977), 
M. californicus (Mullen, 1960), M. montanus (McKeever, 1959; 
Pinter, 1968), M. oeconomus (Dieterich et al., 1973), M. pennsyl- 
vanicus (Christian, 1953; Christian and Davis, 1966; Dieterich et 
al., 1973; Quiring, 1951; Seabloom et al., 1978; ‘To and Tamarin, 
1977), and M. pinetorum (Christian, 1953). Dieterich et al. (1973) 
compared adrenal and other organ weights of M. pennsylvanicus, 
M. oeconomus, and seven other species of myomorph rodents in- 
cluding laboratory mice (Mus musculus). Adrenal weights averaged 
from 0.05 to 0.09% of body weight and were greater than values 
for Mus or most of the other species examined. Although the values 
were within the published range of averages for various species of 
Microtus, they do not reflect the known range of variation due to 
age, sex, reproductive condition, and response to external stimuli. 

Significant changes in adrenal size occur with sexual maturation. 
In M. montanus and M. pennsylvanicus, adrenal size is not signifi- 
cantly different in juvenile males and females (McKeever, 1959; 
Seabloom et al., 1978). With sexual maturity, however, there is a 
decrease in relative adrenal size in males, but in females relative 


Endocrinology 705 


TABLE 3 
ANNUAL VARIATION IN ADRENAL WEIGHT [MG/100 G Bopy WEIGHT + SE (N)] OF 
Microtus pennsylvanicus FROM PINAWA, MANITOBA (FROM SEABLOOM ET AL., 1978) 


Males Females 

Age Age 
Season class Adrenal weight class Adrenal weight 
Late summer 1971 J 65.0 + 5.1 (4) J 7O%Gs= 31,8 (2) 
A 28.3 22:17) A OP 4 e977 (5) 
P 71.4 + 0.0 (2) 
Fall 1971 J 47.3 + 4.8 (11) J 43.6 + 4.8 (6) 
A 29.3 (1) A Se.2. 15.7 (2) 
Winter 1971-72 I 33.8 + 3.4 (5) I 46.4 + 5.7 (2) 
Spring 1972 A S59 2255 (Gli/)) A 76.0 6,0 (5) 
le 0875s 76 1011) 

Early summer 1972 SA 41.3 + 5.4 (6) 

A 35.3 + 4.7 (20) A 107.4 + 6.7 (4) 
P 115.2 + 8.5 (15) 


Abbreviations of age classes are: J, juvenile; SA, subadult; A, adult; P, pregnant; 
I, inactive. 


weight may be doubled (Table 3). Christian (1975) reviewed re- 
ported causal factors for the observed shifts in relative size, and 
noted that immature male Microtus along with many other species 
have an X-zone which is involuted by increased testosterone levels 
at puberty. Delost (1952) reported that the X-zone of Old World 
M. arvalis regenerates during periods of sexual inactivity. However, 
Seabloom et al. (1978) did not observe any adrenal enlargement of 
M. pennsylvanicus during winter, the only period when sexually 
inactive adult voles occurred. 

Females of many species of small mammals have heavier adrenals 
than males (Chester Jones, 1957), but in Microtus the differences 
are especially pronounced (Christian and Davis, 1964, 1966). In 
the laboratory rat (Rattus norvegicus) the female adrenal may av- 
erage 20-50 percent larger than that of the male (Chester Jones, 
1957); sexually mature female M. pennsylvanicus may have adre- 
nals two to four times as heavy as those of mature males (‘Table 3). 
This sexual dimorphism was attributed by Christian (1975) to: 1) 
different configurations of social stimuli between sexes; 2) estrogen- 
ic stimulation resulting in higher levels of corticosteroid binding 


706 Seabloom 


proteins in mature females; and 3) greater rates of hepatic metab- 
olism and clearance of corticosteroids in females. Christian sug- 
gested that the lowering of free corticosteroids resulted in decreased 
inhibition of pituitary secretion of ACTH causing adrenal enlarge- 
ment and increased secretion rate. 

There has been some disagreement as to the nature of the 
X-zone in female Microtus and its contribution to adrenal size. In 
contrast to the situation in the male, the X-zone of female Microtus 
apparently persists until involution during the first pregnancy 
(Christian, 1956; Christian and Davis, 1964; Delost and Chirvan- 
Nia, 1956). However, Chitty and Clarke (1963) reported a persis- 
tent X-zone in females of the British vole, M. agrestis, which en- 
larges during pregnancy, thus accounting for the marked sexual 
dimorphism in adrenal size. This contention was refuted by Chris- 
tian and Davis (1964), who cited evidence indicating that the inner 
juxtamedullary zone of the adrenal cortex of female M. pennsyl- 
vanicus is an “‘inner-fasciculata-reticularis” rather than an X-zone. 
Christian (1975) further suggested that X-zone involution in the 
female may be brought about by ovarian secretion of testosterone 
during pregnancy. 


Secretory Products 


The fluorometric characteristics of adrenocortical secretory prod- 
ucts from Microtus have indicated corticosterone to be the major 
hormone produced (Olsen and Seabloom, 1973; Seabloom, 1965). 
Chromatographic evidence subsequently verified corticosterone as 
the major endogenous steroid produced from in vitro incubation of 
adrenals from M. pennsylvanicus and the British vole, M. agrestis 
(Ogunsua et al., 1971; Ungar et al., 1973, 1978). In addition to 
corticosterone, six other steroids have been identified in small 
amounts from in vitro metabolism of progesterone-4"*C or pregnen- 
olone-4-"*C by Microtus adrenals (Table 4). 

Ungar et al. (1973) initially identified 11-dehydrocorticosterone 
(Compound A) and other 11-keto rather than 118-hydroxysteroids 
as the major products of incubation of adrenals from M. pennsyl- 
vanicus. This finding was not reported for other species and con- 
flicted with fluorometric and other data implicating corticosterone 
(Compound B) as the major steroid produced. The presence of the 
11-keto forms is indicative of a high level of 116-hydroxysteroid 
dehydrogenase activity in the Microtus adrenal. Under the condi- 


Endocrinology 707 


TABLE 4 
STEROID PRODUCTS FROM METABOLISM OF RADIOACTIVE PRECURSORS BY Microtus 
ADRENALS (FROM OGUNSUA ET AL., 1971; UNGAR ET AL., 1973, 1978) 


Microtus Microtus 
Product agrestis pennsylvanicus 

Corticosterone x x 
11-Dehydrocorticosterone xX x 
11-Deoxycorticosterone x 
18-Hydroxycorticosterone x 
18-Hydroxy-11-dehydrocor- 

ticosterone x 
Tetrahydro-11-dehydrocor- 

ticosterone x 
Aldosterone x 


tions of in vitro incubation in a closed system, Ungar et al. (1973) 
concluded that Compound B and other 116-hydroxysteroids were 
formed and oxidized to the 11-keto form. They also noted that, 
whereas low levels of Compound A were detected in many species, 
significant levels were only found in incubations of rabbit adrenal. 

In a subsequent study, Ungar et al. (1978) established Com- 
pound B as the major conversion product from steroid precursors 
incubated with homogenates of Microtus adrenals, and that Com- 
pound A formed a secondary conversion product via action of 118- 
OHD (116-hydroxysteroid dehydrogenase). They further noted a 
significant seasonal variation in 118-OHD activity in M. pennsyl- 
vanicus and M. ochrogaster. Peak activity occurred during fall and 
winter and dropped markedly during spring and summer. They 
suggested that, in light of prior association of other components of 
adrenal function with reproductive activity, there may be a signif- 
icant negative correlation between 118-OHD activity and seasonal 
reproductive development. 


Level of Secretion 


Serum corticosterone levels averaged 50.4 (34.0 to 69.7) ug/100 
ml in lab-raised male M. pennsylvanicus and 71.4 (58.5 to 83.9) 
ug/100 ml in females (Seabloom, 1965). Plasma levels reported for 
M. townsendu averaged 27 wg/100 ml in males and 234 wg/100 ml 
in females (McDonald and Taitt, 1982). Corticosterone concentra- 


708 Seabloom 


tions in Microtus were three to six times greater than those reported 
for laboratory mice and rats. However, studies of steroid levels in 
Rattus and Mus have been confined essentially to inbred domestic 
strains. The wild Norway rat (Rattus norvegicus) has adrenal glands 
several times larger than those of its domestic counterpart. While 
severity of daily living can be a factor in determination of adrenal 
size and secretion rate, Seabloom and Seabloom (1974) suggested 
that “if smaller size is related to reduced adrenal function, it is 
possible that in the process of selection for ‘tameness’ and in the 
absence of natural selective pressures certain genetic shifts, includ- 
ing those affecting adrenocortical function, may occur.” Superfused 
adrenals of wild and domestic house mice exhibited significantly 
different levels of response to ACTH stimulation. Adrenals of wild 
house mice (Mus musculus) reared from birth by domestic mothers 
responded in the same manner as their wild-caught counterparts, 
indicating genetic differences between wild and domestic stocks 
rather than response to the stimuli of capture and handling. 

Corticosterone levels in wild-caught M. pennsyluvanicus were 
markedly higher than in laboratory-reared voles (Seabloom, 1965). 
Certainly, the captive environment does not provide the configu- 
rations of stimuli for adrenal response comparable to that occurring 
in the wild. However, the data also indicate that in the process of 
selection for domestication the responsiveness of the adrenal cortex 
in a wild species may be greatly diminished. 

The initial exposure to the captive environment provides a sig- 
nificant stimulus for prolonged, elevated secretion of corticosterone 
in M. pennsylvanicus (Olsen and Seabloom, 1973). Both adrenal 
and serum corticosterone were highest on day 1 of captivity, de- 
clined rapidly until day 30, and then went into a more gradual 
decline until they appeared to stabilize around day 70 (Table 5). 
Regression coefficients of logs of adrenal and serum corticosterone 
levels on time were significantly different from zero in both males 
and females. Furthermore, the slopes of the regressions were sig- 
nificantly steeper in males than females. Consequently, wild M:- 
crotus must make profound physiologic adjustments during the first 
few weeks of captivity. The alteration in level of adrenocortical 
secretion subsequent to capture appears to provide an indicator of 
acclimation, and is also indicative of the difficulty in obtaining valid 
estimates of secretion in wild voles. Estimates of levels of secretion 
in captive colonies are subject to question because of selection for 


709 


Endocrinology 


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710 Seabloom 


tameness, while determination of normal secretion rates in wild- 
caught stocks appear to require extensive periods of acclimation. 


Periodicity 


The adrenal-cortical function of M. pennsylvanicus exhibits a 
marked daily periodicity, and can fluctuate as much as 157% around 
the 24-h mean (Fig. 1). Peaks of both serum and adrenal corticoste- 
rone occur in mid-afternoon and lows during hours of darkness. 
The daily rhythm is similar to that demonstrated for laboratory 
mice (Mus musculus), where the adrenal peak precedes the motor- 
activity peak by about 4 h. However, unlike Mus, M. pennsylvanicus 
does not exhibit a well-defined rhythm of daily motor activity (Sea- 
bloom, 1965). Under controlled conditions, there are successive short 
bursts of motor activity throughout the 24-h period. However, these 
bursts are more numerous and of longer duration during hours of 
darkness. Consequently, as with more distinctive nocturnal species, 
the Microtus adrenal cortex appears to be activated in anticipation 
of the onset of increased motor activity. Meier (1975) reviewed 
work on the functions of corticoid rhythms in a variety of vertebrates 
and concluded that the daily light-dark cycle is the principal en- 
trainer of the daily adrenal cycle. The daily adrenal cycle in turn 
functions in entraining many metabolic and behavioral rhythms, 
including that of motor activity. 

The superfused adrenal of M. pennsylvanicus exhibits an annual 
periodicity in response to ACTH stimulation which can be corre- 
lated with the animal’s behavioral and reproductive state (Seabloom 
et al., 1978). Although there are no significant changes in adult 
male adrenal weight throughout the year, there is a gradual increase 
in magnitude of response to ACTH which peaks in spring, followed 
by a sharp drop during early summer (Table 6). A high level of 
secretory responsiveness occurs in pre-pubescent subadults during 
early summer. This peak, along with that exhibited by spring adults 
occurs in animals that have recently entered or are reaching breed- 
ing condition. Spring adults are in the process of establishing ter- 
ritories during a period of high aggression, whereas summer sub- 
adults represent inexperienced young interacting with a population 
of established intolerant adults. Consequently, the adrenal response 
in these cohorts of the population may be attributed to their behav- 
ioral state. 


Endocrinology 711 


MALES ADRENAL ——— 


200 


150 


100 


(% OF 24-HR MEAN) 
a 
fo} 


FEMALES 


150 


RELATIVE CHANGE 


100 


50 


"Woo 
1500 
1900 
2300 
0300 
0700 


Fic. 1. Daily change in serum and adrenal corticosterone in Microtus pennsyl- 
vanicus (from Seabloom, 1965, with permission). 


Seabloom 


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Endocrinology 713 


In adult and pregnant females, there is a marked peak adrenal 
response to ACTH which occurs in spring, but the increase in 
weight of the gland appears to lag, reaching maximum size during 
summer and fall (Tables 3 and 6). Estradiol enhances ACTH se- 
cretion (Coyne and Kitay, 1969), and estrogen dependent increases 
in corticoid binding during the breeding season result in compen- 
satory adrenal growth and secretion (Christian, 1975). In Microtus, 
the time-lag between the peaks of adrenal responsiveness and glan- 
dular size increase appears to be significant, however, and complete 
dependence on adrenal weight as an index of seasonal changes in 
secretion may result in considerable timing error. 


Response to Stimuli 


Secretions of the adrenal cortex are involved in metabolic regu- 
lation and play a significant role in acclimation to environmental 
change. There is a plethora of reports involving adrenocortical re- 
sponse of laboratory species, especially mice and rats, to a variety 
of stimuli. However, in-depth studies involving wild species, in- 
cluding Microtus, are uncommon. 

The duration of daily illumination appears to have an indirect 
effect on development and secretion of the adrenal cortex. In M. 
montanus, typical sexual dimorphism in adrenal size (see Adrenal 
Morphology) was masked in animals kept under short photoperiods 
(Pinter, 1968). Normal development of the adrenal, however, is 
probably more a direct function of reproductive status than photo- 
period, whereas the daily light-dark cycle functions in entraining 
the 24-h corticoid rhythm (Meier, 1975). 

The stimulus of captivity results in significant increases in serum 
and adrenal corticosterone in M. pennsylvanicus (see Level of Se- 
cretion). The relative response of males to captivity appears to be 
greater than that of females, but the total period of acclimation is 
about the same. After at least 70 days of confinement, corticosterone 
levels were considered to represent “complete” acclimation to the 
captive environment. However, it is not known if these levels were 
representative of those exhibited by free-living meadow voles in the 
wild. 

There is a considerable body of evidence correlating adrenocor- 
tical activity with social or behavioral stimuli. The spring peak 
adrenal response to ACTH in adult male M. pennsylvanicus re- 
ported by Seabloom et al. (1978) (see Periodicity) is associated with 


714 Seabloom 


the season of elevated levels of male aggression (Turner and Iver- 
son, 1973). Interactions between different behavioral components 
and the functioning of the adrenal-pituitary axis have been re- 
viewed by Brain (1972), Bronson and Desjardins (1971), and Da- 
vidson and Levine (1972). Brain (1972) noted the difficulty in sep- 
arating behavioral and physiological (gonadal) influences on adrenal 
function, but it generally is agreed that routine activity, fighting, 
sexual activity, and fear-motivated responses all cause elevated se- 
cretion of corticosteroids. These behaviors are at their peak during 
spring and are associated with territorial establishment and other 
events of the early breeding season. In like manner, the elevated 
adrenal response of subadult males during early summer may result 
from the stresses involved in recruitment of inexperienced pubescent 
animals into an established territorial population. 

Population density may, in conjunction with other social factors, 
elicit increased rates of corticosteroid secretion. However, documen- 
tation of the effect of such factors on adrenocortical function has 
been extremely difficult because of the rapid and stereotyped re- 
sponse of the cortex to many different stimuli, and the consequent 
problem of distinguishing the response to the density-dependent 
stimulus from that to trapping and handling. Even though much 
has been written on correlation of adrenal function with fluctuations 
in population density in Microtus, there have been very few in- 
depth studies dealing with confined or wild populations of this or 
any other genus of small mammal. 

Studies of confined and free-living New World Microtus to date 
have correlated high population density with decreased eosinophil 
counts, an indicator of increased cortical activity (Louch, 1956, 
1958), and increased adrenal weight (Christian, 1959; Christian 
and Davis, 1966). Subsequently, Christian (1975) presented data 
indicating significant positive correlations between adrenal weight 
and population size for female M. pennsylvanicus, but not for males. 
However, adrenal size in males was significantly correlated with 
degree of scarring (presumably from fighting). Using data from a 
variety of sources, Christian (1975) proposed that endocrine behav- 
ioral feedback mechanisms can operate in mammalian populations 
through aggressive encounters, resulting in increased pituitary-ad- 
renal activity and diminished pituitary-gonadal activity “by periph- 
eral feedbacks in the form of adrenal androgens and possibly pro- 


Endocrinology TAS 


gesterone, or by a short loop feedback in the form of ACTH 
inhibition of gonadotrophin secretion.” 


Adrenocortical-Gonadal Interaction 


Adrenals of adult female Microtus may be two to four times larger 
than those of adult males, while levels of circulating corticosterone 
and adrenal response to ACTH can average 150-200% of observed 
values for adult males (see Adrenal Morphology, Levels of Secre- 
tion, Periodicity). Furthermore, response to ACTH by adrenals of 
pregnant female meadow voles is suppressed when compared to 
nonpregnant adults (Table 6; Seabloom et al., 1978). 

Although the female-male and pregnant-nonpregnant cohorts are 
certainly exposed to differing configurations of social stimuli, there 
is overwhelming evidence based largely on work with other species 
for significant negative feedback between the pituitary-adrenal and 
pituitary-gonadal axes. Testosterone inhibits ACTH secretion, 
whereas estradiol is a known stimulus (Coyne and Kitay, 1969, 
1971). Furthermore, progesterone inhibits corticosterone secretion 
(Rodier and Kitay, 1974). Consequently, adrenal enlargement and 
secretion in the male are inhibited with sexual maturation; secretory 
activity in the female is modulated by the relative levels of the 
principal gonadal hormones present at various stages of estrus and 
pregnancy. Hunter and Hunter (1972) noted that adrenal function 
may shift with stage of pregnancy, again a correlation with estro- 
gen-progesterone balance. Therefore, the differing levels of ACTH 
responsiveness in non-pregnant and pregnant meadow voles can be 
interpreted in terms of estrogen and progesterone domination. 

Conversely, a high level of adrenocortical activity can affect re- 
productive function. Christian (1975) noted that increased secretion 
of adrenal corticoids, androgens, progesterone, and other steroids is 
associated with inhibition of reproductive activity. Increased levels 
of adrenal androgens and progesterone may inhibit secretion of 
gonadotrophins. Christian also suggested that ACTH per se can 
act as a short-loop feedback inhibiting gonadotrophin releasers at 
the hypothalamic level. Pasley and Christian (1971) found that 
exogenous ACTH administration inhibited ovarian development, 
uterine development, and spermatogenesis in M. pennsylvanicus, 
effects similar to those observed in Mus and Peromyscus. In a sub- 


716 Seabloom 


sequent study, Pasley (1974) stimulated endogenous production of 
ACTH in M. pennsylvanicus through administration of metyra- 
pone, an 116-hydroxylase inhibitor. Following daily metyrapone 
injections, compensatory increase in ACTH production occurred, 
resulting in depressed body, uterine, and ovarian weights of females, 
and decreased seminal-vesicle weights of males. Pasley further not- 
ed that, in the absence of 118-hydroxylation, ACTH stimulation 
enhances secretion of adrenal androgens, thus providing additional 
inhibition of gonadotrophin secretion. 


Summary and Conclusions 


Detailed knowledge to date of the endocrinology of the North 
American Microtus is limited to certain aspects of the reproductive 
and adrenopituitary systems, involving six species. Comparative data 
are sparse; indeed, the literature indicates that values and mecha- 
nisms described for one species have been extrapolated readily to 
the entire genus and beyond. 

North American representatives of the genus generally exhibit 
an annual periodicity of reproductive activity that results from a 
balance between an endogenus circannual rhythm and several known 
exogenous factors, including daily photoperiod, light intensity, tem- 
perature, nutritional cues, and social factors. The recent identifi- 
cation of naturally occurring plant compounds that can stimulate 
or inhibit reproduction in M. montanus has major significance in 
comparative physiology and ecology. If their effects can be dem- 
onstrated in other species, a new chapter will have been written in 
our understanding of the regulation of breeding cycles. 

Olfactory cues involving pheromones contained in male urine 
have important regulatory effects on female maturation and induc- 
tion of estrus. Recent studies have implicated the posterior olfactory 
bulb as providing a neuroendocrine link between the external en- 
vironment and secretion of the reproductive regulators LHRH and 
norepinephrine. 

Coitus-induced ovulation appears to be well established in both 
New World and Old World Microtus as an important phenomenon 
maximizing reproductive efficiency. Vaginal-cervical stimulation 
alone may be sufficient to induce ovulation, but there is also indi- 
cation that pheromonal or other contact factors may play a role. 
Limited copulatory stimulation may result in formation of abnor- 
mally short-lived corpora lutea. 


Endocrinology 717 


Male-induced pregnancy blockage in Microtus has been docu- 
mented for pre-implantation and post-implantation stages, and there 
has been recent evidence for the “strange male” or Bruce effect 
resulting in poor litter survival following parturition. Odor alone 
is sufficient to effect blockage, and there is evidence that the phe- 
nomenon may be a side effect of induced estrus and ovulation. 

All microtines studied go through a post-partum estrus, which 
occurs between one and four days following parturition. In some 
cases, estrus and ovulation may occur on the day of parturition. 

Little work has been done on the control of lactation in Microtus, 
but estrogen and glucocorticoid-binding macromolecules have been 
demonstrated in the lactating mammary gland. There is some in- 
dication that the “‘strange male” or Bruce effect can apply to post- 
partum events, such as lactation, via hypothalamic inhibition of 
prolactin secretion. 

In contrast to female Microtus, there has been little attention paid 
to male reproductive physiology. The morphology of the male re- 
productive tract has been described. The spermatogenic cycle has 
been described for M. ochrogaster, and circulating androgen levels 
are reported for M. brewert and M. townsendit. 

Thyroid activity has been studied in four species of North Amer- 
ican Microtus. Generally, activity is suppressed by high population 
density, food depletion, harassment, and shortened photoperiods. 
Serum thyroxine and rates of radioiodine release have been studied 
in M. montanus, M. ochrogaster, and M. pennsylvanicus. Blockage 
of thyroid secretion results in a 3°C increase in the highest air 
temperature tolerated without stress in M. ochrogaster. Serum thy- 
roxine does not change with alteration of air temperature, but rate 
of radioiodine uptake is reciprocally related to air temperature. 

Adrenal-weight relations have been recorded for six species of 
North American Microtus, and generally fall within the range of 
variation for other small mammals. With maturation, there is a 
significant sexual dimorphism in adrenal size. Relative adrenal 
weight in females is doubled; a decrease occurs in males that is 
associated with involution of the X-zone. In females, adrenal en- 
largement is associated with increase in inner cortical mass in re- 
sponse to greater rates of binding in plasma and hepatic clearance 
of corticosteroids. 

Corticosterone is the major steroid secreted by the Microtus ad- 
renal, but small amounts of other steroids also have been recorded. 
The occurrence of Compound A (11-dehydrocorticosterone) in M:- 


718 Seabloom 


crotus adrenal-incubates indicates a very high level of 116-hydrox- 
ysteroid dehydrogenase activity. There is indication that the level 
of dehydrogenase activity varies seasonally, being highest during 
fall and winter. 

Levels of corticosterone secretion are significantly higher than 
those recorded for laboratory rats and mice, in spite of comparable 
relative adrenal size. These secretion rates may be attributed to the 
stimulus of capture and confinement, and to genetic adaptation of 
a wild species to its natural environment. 

The adrenal cortex exhibits both daily and seasonal periodicity 
in secretion rate. The daily rhythm can fluctuate as much as 157% 
around the 24-h mean, with a peak in the afternoon and a low 
during hours of darkness. Seasonal adrenal response to ACTH 
stimulation is highest during spring (the early breeding season). 

As with other species, Mzcrotus adrenal function is influenced by 
many exogenous stimuli, including light, captivity, aggression, and 
population density. However, specific documentation of each re- 
sponse has been very difficult because of the sterotyped, high-mag- 
nitude response of the gland to all stimuli. 

Adrenal-gonadal interactions have been demonstrated in New 
World Microtus. Adrenal enlargement and secretion in males is 
inhibited by high testosterone levels at puberty. Secretory activity 
in females is modulated by increased levels of gonadal hormones 
during estrus and pregnancy. At puberty and estrus, there is adrenal 
enlargement and a high secretion rate in the estrogen-dominated 
female, whereas high progesterone levels during pregnancy appear 
to inhibit adrenal response. 

Conversely, ACTH administration has been shown to inhibit 
spermatogenesis and ovarian and uterine development in M. penn- 
sylvuanicus. The effect can be direct or via ACTH stimulation of 
adrenal androgen secretion, which in turn inhibits secretion of go- 
nadotrophins. 


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STEHN, R. A., AND F. J. JANNETT, JR. 1981. Male-induced abortion in various 
microtine rodents. J. Mamm., 62:369-372. 

STEHN, R. A., AND M. E. RICHMOND. 1975. Male-induced pregnancy termination 
in the prairie vole, Microtus ochrogaster. Science, 187:1211-1213. 

To, L. P., AND R. H. TAaMarRin. 1977. The relation of population density and 
adrenal gland weight in cycling and non-cycling voles (Microtus). Ecology, 
58:928-934. 

TURNELL, R. W., P. C. BEERS, AND J. L. WITTLIFF. 1974. Glucocorticoid-binding 
macromolecules in the lactating mammary gland of the vole. Endocrinol- 
ogy, 95:1770-1773. 

TURNER, B. N., AND S. L. Iverson. 1973. The annual cycle of aggression in male 
Microtus pennsylvanicus, and its relation to population parameters. Ecol- 
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Unaar, F., R. GUNVILLE, AND R. W. SEABLOOM. 1973. 11-dehydrocorticosterone 

(Compd. A) formation by the Microtus adrenal. Steroids, 22:503-514. 

1978. Seasonal variation in adrenal 11f6-hydroxysteroid dehydrogenase 

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docrinol., 36:111-118. 

VAN TIENHOVEN, A. 1968. Reproductive physiology of vertebrates. Saunders, 
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VAUGHAN, M. K., G. M. VAUGHAN, AND R. J. REITER. 1973. Effect of ovariectomy 
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VAUGHAN, M. K., R. J. REITER, G. M. VAUGHAN, L. BIGELOW, AND M. D. 
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REPRODUCTIVE PATTERNS 
BARRY L. KELLER 


Abstract 


ARIATION in breeding duration, breeding intensity, and litter 
V size of New World voles is reviewed. Most species appear to 
follow a facultative strategy with regard to environmental cues that 
mediate onset and duration of breeding. Eight species (Muicrotus 
californicus, M. oregoni, M. townsendi, M. montanus, M. ochrogaster, 
M. oeconomus, M. pennsylvanicus, and M. pinetorum) show consid- 
erable variation in their breeding periods, whereas six (M. brewer, 
M. chrotorrhinus, M. longicaudus, M. mexicanus, M. richardsoni, and 
M. xanthognathus) appear to have restricted breeding seasons. Early 
termination or late initiation of breeding are found in species dis- 
playing either annual or multi-annual cycles, and it is still not clear 
why such breeding variations occur. Pregnancy rate does not appear 
to vary in predictable patterns among species or years, but seasonal 
variations are apparent. It is unclear whether success of copulation 
and capacity of a strange male to block pregnancy are important in 
natural populations, as contrasted to effects documented for labo- 
ratory populations. Age at maturation may directly affect breeding 
intensity, whereas minor variations in sex ratio appear unimpor- 
tant. Significant changes in breeding intensity can be affected by 
major disruption of the sex ratio such that the social structure of 
populations is affected. Age at sexual maturation and length of 
breeding season may change with such perturbations, but it is not 
clear whether such effects occur in all species. Small differences in 
litter size appear to be a phenotypic rather than a genotypic re- 
sponse to environmental variation. M. pinetorum has the smallest 
litter size, M. xanthognathus the largest; but it is not clear why litter 
sizes differ between species. Contrasts within and among species 
are encumbered because of differences in seasons of collection of 
specimens, sampling intensity, and inappropriate use of statistical 
techniques. Age and parity of the female and a variety of other 
factors may affect litter size. Pre- and post-implantation losses do 
not appear to significantly affect the reproductive output for the 

725 


726 Keller 


few species studied, but temporal or geographic differences in litter 
size may contribute to the capacity of a population to cycle. 

A plea is made for development of corroborative experiments that 
critically test the importance of reproductive patterns detailed in 
descriptive studies. Some experiments are suggested that would in- 
crease our understanding of the importance of seasonal and annual 
differences in reproductive patterns among species. 


Introduction 


Reproductive attributes of microtine rodents have been investi- 
gated widely, but the genus Microtus has been studied most exten- 
sively (Hasler, 1975). Laboratory or field studies have been re- 
ported for 18 species, although reproductive data are available for 
M. abbreviatus, M. canicaudus, and M. miurus, largely as a result 
of studies associated with laboratory colonies. No field studies are 
published for M. coronarius, M. guatemalensis, M. nesophilus, M. 
oaxecensis, M. umbrosus, M. quasiater, and M. abbreviatus. Microtus 
californicus, M. longicaudus, M. montanus, M. ochrogaster, M. penn- 
sylvanicus, and M. pinetorum have been studied at widely separated 
geographical locations, whereas geographical variation in repro- 
ductive patterns of Microtus agrestis have received the most attention 
in Europe. I include, for contrast, some information on winter 
breeding for the field vole (M. agrestis), because Ellerman and Mor- 
rison-Scott (1951:702) suggested and Klimkiewicz (1970) presented 
morphometric evidence that Microtus agrestis is conspecific with M. 
pennsylvanicus. By contrast, Matthey (1952) noted chromosomal 
differences and Johnson (1968) showed that serological differences 
exist between M. agrestis and M. pennsylvanicus. Thus, I treat M. 
pennsylvanicus as a distinct species. Additionally, I include winter- 
breeding information from the Old World literature for M. oecon- 
omus (European root vole), although the North American tundra 
vole (M. ratticeps?) may not be conspecific with the root vole (Hall, 
1951). 

This chapter is limited to a consideration of factors known or 
suspected, on the basis of field and laboratory evidence, to affect 
reproductive performance of voles in natural populations. I avoid 
review of evolutionary implications and anatomical and endocrin- 
ological aspects of reproduction, as they are considered elsewhere 
(see Carleton, this volume; Phillips, this volume; Seabloom, this 


Reproductive Patterns dQ. 


volume). I have considered environmental factors known to influ- 
ence the breeding effort. 

Laboratory studies of endogenous factors known to affect repro- 
ductive performance of voles suggest many predictions that could 
be field-tested. Unfortunately, definitive evidence is lacking as to 
whether these processes, particularly pheromonally mediated events, 
are important controls of reproductive tactics for natural popula- 
tions. I have assumed reproductive, aggressive, and recognition be- 
havior of individual voles is mediated at least partially by phero- 
mones distributed from specialized glands (Quay, 1962, 1965, 1968). 
Certain olfactory cues can moderate behavior (Beard, 1978; Jan- 
nett, 1981a; Lyons, 1979) and these substances may be found to be 
important for integration of breeding. 

Only recently have we begun to recognize that the social fabric 
of vole populations may be important in the integration of repro- 
ductive processes (Anderson, 1980; Getz, 1978; Jannett, 1980; Lid- 
icker, 1980; Madison, 1980; Wolff, 1980). This adds confusion to 
the literature because many field studies have described reproduc- 
tive patterns without regard for reproductive mechanisms disrupted 
through data collection procedures or experimental manipulation. 
For example, we do not know if post-partum breeding in a pair- 
bonding species such as M. ochrogaster (Getz et al., 1981) is per- 
manently disrupted by removing females to determine litter size in 
conjunction with experiments (see Cole and Batzli, 1978). Can 
reproductive estimates be compared in populations subjected to dis- 
ruption of incest taboos (McGuire and Getz, 1981) or maturation 
controls (Hasler and Nalbandov, 1974)? Clearly, removal of a sam- 
ple of individuals to assess reproductive parameters by autopsy 
(Keller and Krebs, 1970; Rose and Gaines, 1978) may significantly 
affect the remaining social structure and reproductive pattern owing 
to action through the Whitten effect (Whitten, 1956) or the Bruce 
effect (Bruce, 1959) on breeding performance. Rose and Gaines 
(1978) certainly altered the breeding intensity of their selectively 
trapped populations by removing only animals weighing >20 g, 
and their subsequent samples, taken at approximately 2-month in- 
tervals, probably reflected enhanced reproductive effort, lowered 
ages at sexual maturity, and altered reproductive fitness of individ- 
uals. 

Infrequent disruptions of social or age structure of voles may be 
unimportant. However, we presently lack carefully graded and rep- 


728 Keller 


licated experiments that would separate effects disruptive to repro- 
ductive processes, as observed in the laboratory, from processes that 
occur naturally under field conditions. The extent to which varia- 
tion in reproductive patterns of voles is due to investigator-induced 
changes in field populations and to artifacts caused by modifications 
of social structure in the laboratory must be clarified. 

This chapter is subsectioned in accord with the early studies of 
Hamilton (1937, 1941), who suggested that changes in density for 
M. pennsylvanicus were fostered by: 1) increased duration of the 
reproductive season such that females produced more litters; 2) an 
acceleration of the rate of breeding; and 3) an increase in the num- 
ber of young produced by pregnant females. These initial premises 
have been used as focal points in many field studies of voles. Only 
now are variations in reproductive performance among individual 
voles and heritability of litter size, age at sexual maturity, and 
ability to breed during winter beginning to be investigated under 
field conditions. More research needs to be concentrated on this 
aspect of microtine reproductive biology. 


Length of Breeding Season 


Seasonal rhythms in reproduction in New World voles may result 
from a variety of factors, including temperature, dehydration, pho- 
toperiod, nutrition (see Batzli, this volume), and chemical cues. 
Additionally, both phenotypic (Christian, 1971) and genotypic 
(Clarke, 1977; Keller and Krebs, 1970) differences among individ- 
uals may affect reproductive capabilities of voles. Further, spacing 
behavior, which may be mediated partially by pheromones, may 
alter reproductive performance. It remains to be discovered, how- 
ever, which pheromones are released in response to exogenous or 
endogenous factors in natural populations. In the laboratory, their 
release has been related to endogenous hormone production (Mil- 
ligan, 1976), but endocrine responses leading to initiation of breed- 
ing appear to be intimately related to environmental cues (Sea- 
bloom, this volume). Thus, environmental cues may control the 
onset and perhaps the duration of the breeding effort, but a network 
of intrinsic cues may integrate breeding processes. This network 
may very well be tied to behavioral systems. 


Reproductive Patterns 129 


Environmental Cues 


Baker and Ranson (1932) suggested that photoperiod was a syn- 
chronizing agent in voles. During their studies on M. oregoni, Cow- 
an and Arsenault (1954) suggested that both temperature and pho- 
toperiod operated in combination to initiate breeding. Greenwald 
(1957) and Hoffmann (1958) noted a correspondence between green 
vegetation and reproduction in Microtus californicus, a relationship 
also suggested by Batzli and Pitelka (1971) on the basis of extensive 
analysis of the diet of this species. Subsequently, Lidicker (1976) 
studied M. californicus in artificially watered enclosures during the 
California dry season and concluded that water and vegetation de- 
termined the length of the breeding season. Pinter and Negus (1965), 
studying the effect of photoperiod and a supplement of sprouted 
wheat, concluded that reproduction in M. montanus was enhanced 
by a combined action of diet, photoperiod, and other environmental 
variables. Negus and Pinter (1966) subsequently suggested that 
“phytoestrogens” constituted an important environmental stimulus 
for reproduction in montane voles, but Berger and Negus (1974) 
demonstrated that the stimulatory plant substances were not estro- 
genic. Rather, they appear to act through the pineal-hypothalamic- 
pituitary axis, increasing the production of substances that elicit 
steroid production by the ovaries and testes (Seabloom, this volume). 
The induction of reproductive activity by a “start cue” has been 
demonstrated in field populations of M. montanus during two win- 
ters (Negus and Berger, 1977). Conversely, Sanders (1976) extract- 
ed cinnamic acids and their related vinylphenols, which are natu- 
rally occurring plant compounds, and concluded that they inhibited 
reproduction in montane voles but that the physiological response 
times were longer for males than for females. Berger et al. (1977) 
suggested that these compounds serve as stop cues, indicating the 
termination of a food supply conducive to breeding activity. Most 
recently, Sanders et al. (1981) identified a compound (6-MBOA) 
that can trigger reproduction in Muicrotus montanus; Berger et al. 
(1981) suggested that this compound may be generally important 
in cueing reproduction in other species. 

It seems doubtful that all New World species have adopted a 
strategy of using vegetation as an ultimate Zeitgeber, because a 
varied diet is known to exist for different species (Batzli, this vol- 
ume). Negus et al. (1977) proposed that voles in highly predictable 


730 Keller 


environments may be selected for stereotyped breeding seasons. In 
such environments, the central cue might consist of a fixed param- 
eter such as photoperiod. By contrast, species requiring a facultative 
reproductive strategy may be selected to cue, although not neces- 
sarily completely, on substances available during periods favorable 
for breeding. 

It seems to me, because environments tend to vary in plant com- 
position on a temporal basis, that mid-continental populations of 
vole species with broad distributions might possess differing cue 
sensitivities based upon the predictability of the environment in 
which they live. Studies are needed to quantify variations in re- 
sponse to a variety of environmental cues among individuals of 
single species collected along geographical and altitudinal gradients. 
Perhaps the quantities of plant cues or the nutritional value of 
vegetation mediate the integrity of the breeding process by altering 
sensitivities to other cues, but we lack quantitative information on 
response to cues for any geographic area. 


Breeding Duration 


New World voles possess considerable variation in their periods 
of reproduction. This variation may result in differences in ampli- 
tude displayed by populations that undergo either annual or multi- 
annual cycles, although other influences could be important as well. 
Birney et al. (1976) suggested that cover, especially because it af- 
fects a variety of factors that impinge upon voles, may affect am- 
plitude, and Krebs et al. (1969) noted that frustration of dispersal 
also affected amplitude. 

Two patterns of variation in the duration of the reproductive 
period are commonly reported for New World voles. First, peak 
density populations often appear to terminate breeding early in the 
summer of peak numbers and initiate breeding late the following 
spring. Secondly, at least nine species are known to occasionally 
extend reproduction into the dry or winter season. Keller and Krebs 
(1970) suggested that the progeny of winter breeders might be at a 
selective advantage. However, only a limited amount of information 
has been developed on the extent, success, and causes of extended 
reproduction. Early investigators often attributed winter breeding 
to the quantity (Bailey, 1924; Fitch, 1957; Hamilton, 1937) or 
quality (Fuller, 1967) of the food supply. Unfortunately, only An- 


Reproductive Patterns 731 


derson (1975) has attempted to determine whether individual asea- 
sonal breeders (winter breeders in her study) are genetically dis- 
tinct. Her results for Mucrotus townsend indicate a lack of 
heritability for this trait. Similarly, Clarke (1977) speculated that 
sexual development in winter-breeding M. agrestis may be due to 
the prevalence of genetically distinct individuals that have a greater 
tendency to breed under short photoperiods. 

Our knowledge of the importance of winter breeding is fragmen- 
tary for a number of reasons. The preponderance of studies com- 
pleted in areas of snowfall have been conducted during summers. 
Further, repeatability has rarely been measured where winter 
breeding has been documented, and the causes for breeding often 
have been evaluated post hoc (but see Getz et al., 1979). Some of 
the difficulty in obtaining such information results from a lack of 
employment of sampling systems now available or recently devel- 
oped (Fay, 1960; Iverson and Turner, 1969; Keller et al., 1982; 
Larsson and Hansson, 1977; Merritt and Merritt, 1978; Pruitt, 
1959), but the winter ecology of small mammals is now receiving 
increased attention. 


Species with Restricted Breeding Periods 


Recognizing that further study may demonstrate substantial shifts 
in the breeding seasons of all species, I would presently list five 
species (M. brewert, M. longicaudus, M. mexicanus, M. richardsont, 
and M. xanthognathus) as seasonally restricted breeders. The breed- 
ing season of M. brewer: generally extends from April through 
October. Tamarin (1977a) suggested that the duration of the breed- 
ing effort for this species was consistent during his 3-year study 
and that a delay of breeding during one spring was followed by an 
extension of breeding the following fall. Goldberg et al. (1980) 
noted significant dietary shifts in the beach vole (M. brewerz) that 
appeared to correspond with the non-breeding period, but a cause— 
effect relationship has not been demonstrated. 

Some data are available on the breeding habits of M. longicaudus 
and M. mexicanus. As a result of his 61-week study in New Mexico, 
Conley (1976) suggested that the breeding season for the long-tailed 
vole ceased in October and was resumed during spring. M. mexi- 
canus trapped in the same area were breeding from May through 
November. Based upon lack of recruitment the following year, Con- 


732 Keller 


ley (1976) suggested that the Mexican vole did not breed during 
winter, but he did not sample his area from mid-November to May. 
He suggested M. longicaudus populations were completing a peak- 
decline phase and M. mexicanus a low phase during his study, but 
his data from M. mexicanus actually suggest that the Mexican vole 
is an annual cyclic species. Baker (1956), by contrast, found preg- 
nant Mexican voles during January in Coahuila, Mexico. Thus, 
without further data, the characterization of this species as a sea- 
sonally restricted breeder should be considered tentative. Farris 
(1971) found Microtus longicaudus breeding from March through 
October in Washington and cited 17 years of snap-trapping samples 
collected between October 12 and November 9 in which only two 
of 93 adult females were pregnant. It is of interest to note that he 
suggested long-tailed voles on his study area were seed (Rosa) and 
bark (Symphoricarpos albus) feeders during fall and winter (Farris 
1971:74). Van Horn (1982) observed breeding from mid-May 
through mid-September in long-tailed voles found in coniferous 
forest in southeast Alaska. Microtus longicaudus did not appear to 
exhibit a multi-annual cycle during the combined 3-year study of 
Farris (1971) and Wright (1971), or during Van Horn’s (1982) 
3-year study. 

Subdivision of populations of the water vole, M. richardson1, into 
small isolated groups (Anderson et al., 1976) and the sociobiology 
of the yellow-cheeked vole, Microtus xanthognathus (Douglass, 1977; 
Wolff and Lidicker, 1980), would appear to preclude extension of 
their respective breeding seasons. In Alberta, the water vole bred 
from June through August, but only the first litters matured in 
their season of birth. No winter breeding was evident in summer 
samples of overwintered individuals during a 1-year study by An- 
derson et al. (1976). The yellow-cheeked vole bred from early May 
to July and young did not breed during their season of birth (Wolff 
and Lidicker, 1980; Youngman, 1975). Males initiated breeding 
approximately 1 month before females (Wolff and Lidicker, 1980), 
a condition also observed by Douglass (1977) during a 3-year live- 
trapping study. Douglass (1977), however, found females breeding 
in August, but none in September. Wolff and Lidicker (1980) also 
noted that males achieved maximum seminal-vesicle length 2 weeks 
to 1 month after the testis size declined in this species, a condition 
that may be important to social integration of non-breeding indi- 
viduals that form midden groups (Wolff and Lidicker, 1981) during 


Reproductive Patterns 733 


winter. We do not know how the duration of breeding would be 
affected during periods of irruption in either the yellow-cheeked or 
water vole; however, Youngman (1975) suggested such irruptions 
occur about every 20 years in M. xanthognathus. The intervals be- 
tween irruptions are unknown in M. richardsoni (Anderson et al., 
1976). 

In summary, significant variations in length of breeding season 
appear to be largely absent in five species of New World voles 
studied over periods of one to several years. I would tentatively add 
that, although annual or multi-annual live-trapping studies are not 
available for rock voles (M. chrotorrhinus), museum and field-col- 
lection data suggest that this species has a restricted breeding season 
extending from March to mid-October (Kirkland, 1977; Martin, 
1971; Timm et al., 1977). It remains to be established if rock voles 
undergo cycles in optimal habitat (species review: Kirkland and 
Jannett, 1982). 


Species with Variable Breeding Periods 


Considerable variation occurs in length of the breeding season of 
voles found in both snow-free areas and areas covered by moderate 
or limited snow. Extension of the breeding season has been found 
under both conditions and at least one species that does not usually 
demonstrate multi-annual cycles, M. townsendii, occasionally 
undergoes extension of the breeding season into winter (Krebs, 1979; 
‘Taitt and Krebs, this volume). 

In snow-free areas, M. californicus displays both annual (Krohne, 
1982; Lidicker, 1973) and multi-annual cycles (Krebs, 1966). Lid- 
icker (1973) suggested that this species usually shows a monotonous 
pattern of breeding that begins several months after autumn rains 
(September to December) and terminates with the desiccation of 
vegetation (usually June). Batzli and Pitelka (1971), Bowen (1982), 
Greenwald (1957), Hoffmann (1958), Lidicker and Anderson 
(1962), Pearson (1963), and others have also proposed that breed- 
ing closely corresponds to wet seasons for the California vole. How- 
ever, Lidicker (1973) noted one multi-annual cycle that was asso- 
ciated with a continued breeding effort during the dry season, which 
he attributed to high-quality habitat and an unusual early rainfall 
in September. Krohne (1982), who studied a northern coastal pop- 
ulation for several years, found that breeding extended well into 


734 Keller 


summer in a population that did not cycle, and Batzli and Pitelka 
(1971), Greenwald (1957), Krebs (1966), and Krebs and DeLong 
(1965) found that breeding can be extended during dry seasons in 
populations displaying multi-annual fluctuations. Krebs (1966) also 
failed to find breeding females for over 2 months following an Oc- 
tober rain that produced green vegetation. Lidicker (1976) subse- 
quently analyzed breeding variation by artificially watering enclo- 
sures containing voles during dry periods. He suggested that ade- 
quate food was required for reproduction; available moisture, in- 
cluding dew, was the most important factor controlling length of 
the breeding season, and individuals subjected to dehydration de- 
layed reproduction in spite of adequate food. 

Microtus oregoni appears to vary its breeding habits with the 
quality of the habitat it occupies. Gashwiler (1972) suggested that 
creeping voles breed from mid-February to mid-September in clear- 
cut and virgin Douglas fir forests in western Oregon. By contrast, 
Sullivan (1980) suggested that these voles breed from April to Au- 
gust on both burned and unburned cutover areas in British Colum- 
bia. Redfield et al. (1978a) showed that experimental disruption of 
the sex ratio affects the duration of breeding (see below). In a study 
of five populations of M. oregoni, Sullivan and Krebs (1981) failed 
to find a consistent pattern of breeding in four different types of 
habitat. It is noteworthy that the highest vole densities achieved 
during their study (Sullivan and Krebs, 1981:Fig. 5) occurred on 
an area suggested to be optimal habitat, and that a short burst of 
breeding following a mild winter occurred on this area. Breeding 
rapidly terminated, but resumed earlier than that observed on a 
similar old-field grid where M. townsend was present and may 
have been a competitor. 

Microtus townsend populations in coastal British Columbia have 
been studied very thoroughly by experimentation. Perhaps with one 
or two exceptions, they did not display multi-annual cycles (Krebs, 
1979; Taitt and Krebs, this volume). Breeding duration, although 
not reported by a long-term autopsy study, usually began early in 
spring and terminated in fall, but a number of exceptions were 
documented. Winter breeding (December to February), as assessed 
by the presence of lactating females, was documented for three 
populations (two control, one experimental) at a reduced level (18- 
22%), whereas seven populations displayed limited breeding (1- 
10%), and three others none at all (Krebs, 1979). No commonality 


Reproductive Patterns 125 


was found among populations breeding during winter, but two of 
the three populations displaying limited winter breeding achieved 
higher peak densities the following year. The third population (ex- 
perimental) was subjected to a pulse-removal experiment that may 
have affected the speed of growth; enumeration was not carried out 
beyond May (Krebs, 1979:Fig. 5). Thus, we do not know the ul- 
timate density that this population might have achieved. Anderson 
(1975) showed that the tendency of breeding in winter is not in- 
herited to any extent in Townsend’s voles. 

Besides extensions of the breeding season, early cessation and late 
initiation of breeding periods also have been noted (Anderson and 
Boonstra, 1979; Beacham, 1980; LeDuc and Krebs, 1975). Beach- 
am (1980) suggested that dispersal and death of fast-growing, early- 
maturing Townsend’s voles may result in a shortened breeding sea- 
son during summers of peak density. Other variations also have 
been documented. Boonstra and Krebs (1977) noted reduction to 
near zero in mid-summer breeding in an enclosed population at 
peak density, and Taitt and Krebs (1981) were able to shorten non- 
breeding periods with extra food. Taitt et al. (1981) achieved the 
same effect with extra cover. Neither female nor male enrichment 
of the sex ratio (see below) significantly altered length of the breed- 
ing season (Redfield et al. 19785). 

In areas that usually receive snowfall, inconsistent patterns of 
winter breeding occur. In their review of winter breeding in M:- 
crotus, Keller and Krebs (1970) suggested that individuals of high 
body weight continue to breed during the winter months of popu- 
lation increase and that this breeding appeared to lead to population 
peaks. Subsequent studies suggest that winter breeding is not al- 
ways associated with periods of population expansion in at least six 
species. 

Muicrotus montanus was found to undergo multi-annual fluctua- 
tions in three cycles monitored over a 10-year period by Negus in 
Wyoming (7m Jannett, 1977) and one cycle monitored by Hoffmann 
(1958) in California. Pattie (1967) and Hoffmann (1974) both sug- 
gested that alpine populations do not cycle, however. Hoffmann 
(1958) concluded after a 3-year summer study in mountain mead- 
ows that montane voles showed a reasonably consistent pattern of 
breeding from June to August. Reproduction, as assessed by back- 
dating pregnancies, was initiated earlier during the year of peak 
numbers and terminated earlier in the summer preceding a decline. 


736 Keller 


Farris (1971) found pregnant females in every month except De- 
cember, but suggested the main breeding season occurred from mid- 
February through November. The limited winter breeding he ob- 
served appears to have occurred during a Type-H decline. Working 
in the same area in Washington, Wright (1971) found individuals 
breeding from early February through December during his 18- 
month study, but his data cannot be separated for individual years 
and his samples for January and February were limited to a total 
of two adults. I documented (pers. observ.) winter breeding in en- 
closed, expanding populations of M. montanus near Pocatello, Ida- 
ho, during experiments conducted over several years, and Groves 
and Keller (1983) found that montane voles continued breeding 
during a period of winter population expansion at the Idaho Na- 
tional Engineering Laboratory. Negus et al. (1977) noted natural 
late-winter breeding in saltgrass marshes bordering the Great Salt 
Lake during February for 1 of 6 years; they attributed this breeding 
to the presence of fresh green vegetation. As noted above, Negus 
and Berger (1977) were able to trigger reproduction in sexually 
quiescent montane voles by use of sprouted wheatgrass and 6-MBOA 
(Berger et al., 1981). 

Prairie voles (M. ochrogaster) breed throughout the year in some 
areas, although the intensity of the effort varies seasonally and may 
be reduced during winters or summers. Fitch (1957), Gaines and 
Rose (1976), Jameson (1947), Martin (1956), and Rose and Gaines 
(1978) have documented varied patterns in populations near Law- 
rence, Kansas, but these studies largely suggest that winter breed- 
ing, if it occurs, is most pronounced prior to peak years and is 
highly unpredictable. By contrast, Rolan and Gier (1967) did not 
obtain pregnant females during December, January, or February 
in their sample of 198 female prairie voles trapped on native Kansas 
prairies over an 11-year period. Abdellatif et al. (1982) were able 
to cause more intensive mid-summer breeding in females residing 
in an artificially watered, enclosed population, but despite this 
breeding increase, the population continued to decline. 

In Indiana, Corthum (1967) and Keller and Krebs (1970) found 
that winter breeding in prairie voles occurred prior to peak densi- 
ties, but Quick (1970) found winter breeding following a period of 
population decline in Kentucky. Fisher (1945) suggested that win- 
ter breeding can occur during mild but prolonged winters, and 
Richmond (1967) also noted winter breeding during studies in Mis- 


Reproductive Patterns 737 


souri; however, neither author documented the breeding durations 
of populations that were sampled. DeCoursey (1957) noted a very 
reduced level of winter breeding during what appears to have been 
a period of population expansion in Ohio. Meserve (1971) noted 
perforate females in Nebraska during winter. Cole and Batzli (1978) 
were able to extend the breeding period for an Illinois population 
of prairie voles all months of one winter by supplemental feedings 
with rabbit pellets. They suggested that food availability affected 
both the length of breeding and its intensity (see below) which, in 
turn, affected the amplitude of cycles. 

Abramsky and Tracy (1979) studied the effects of various com- 
binations of water and soil-mineral nitrogen treatments on Colo- 
rado prairie-vole populations and suggested that unusually high 
reproductive activity during winter, prior to peak densities, was not 
necessary to produce high numbers. During an extensive analysis 
of live-trapped prairie vole populations in Illinois, Getz et al. (1979), 
concluded that a gradient for habitat qualities was responsible for 
significant variations in the length of breeding periods they encoun- 
tered. Reproduction continued during two winters of decline in two 
independent cycles but failed to occur during a winter of heavy 
snow prior to a spring where breeding was delayed. M. ochrogaster 
populations expanded following this delay, but failed to achieve 
peak amplitudes equivalent to those reached during a previous cycle. 

Microtus oeconomus (=M. ratticeps?) breeds from approximately 
April to September during a period of cyclic peak, but in one study 
showed a delay in the initiation of breeding until early May and 
ceased breeding in mid-August during a period of low numbers 
(Whitney 1976). Whitney (1976) suggested that the tundra vole 
displayed a multi-annual cycle during his studies. The weight dis- 
tributions (Whitney 1976:Fig. 10) provided for this species suggest 
that these voles were breeding during the winter of increase when 
snow depth prevented Whitney from sampling. Tast and Kaikusalo 
(1976) suggested that the European root vole normally breeds from 
May to late September, but recorded winter reproduction following 
an exceptionally warm summer in Finland that induced fall rather 
than spring shoot development of some plants. 

Winter breeding in Microtus pennsylvanicus occurs in a variety 
of distinctly different habitats and widely separated geographical 
areas. Hamilton (1937), Beer and MacLeod (1961), Krebs et al. 
(1969), and Keller and Krebs (1970) found winter breeding to be 


738 Keller 


associated with periods of population expansion in M. pennsylvan- 
icus in New York, Minnesota, and Indiana. Subjective evaluation 
of Linduska’s (1942, 1950) statements about densities of meadow 
voles also suggests that this pattern occurs in Michigan. Christian 
(1971) suggested that winter breeding occurred in Pennsylvania 
whenever mature individuals were available to breed. From 4 years 
of necropsy data for meadow voles collected in Manitoba, Iverson 
and Turner (1976) found a 4-month spread in the occurrence of 
positive epididymal sperm smears during winter for males initiating 
breeding. The last pregnancy recorded over a 6-year period oc- 
curred in August or September, but during one winter, males with 
abdominal testes had positive sperm smears and pregnancy was 
noted in females from November through February. This unusual 
period of winter reproduction occurred in animals of lower weight 
than that observed for individuals during summers, as contrasted to 
the results of Keller and Krebs (1970). From live-trapping studies, 
Iverson and Turner (1974) suggested that lower weights were a 
result of winter weight loss experienced by individuals until snow 
cover was established. Peak densities were achieved following the 
period of winter breeding, but breeding occurred when this popu- 
lation was at low density (Mihok, pers. comm.). More recently, 
Tamarin (1977a) found a limited amount of winter breeding in M. 
pennsylvanicus in Massachusetts among populations interpreted to 
have reached peak densities, and Getz et al. (1979) found few mead- 
ow voles breeding during a winter of population expansion in Il- 
linois. 

Microtus agrestis also breeds during winter months (for example, 
see Raynaud, 1951; Thibault et al., 1966). Tast and Kaikusalo 
(1976) and Larsson and Hansson (1977) called special attention to 
this condition in Finland and Sweden, but Chitty (zn Krebs and 
Myers, 1974) reported complete cycles in England in which winter 
breeding was absent. 

Hamilton (1938) initially proposed that Microtus pinetorum was 
a cyclic species, but Horsfall (1963) suggested that pine voles main- 
tained relatively stable densities. No subsequent studies indicate 
that pine voles display multi-annual fluctuations. During a 3-year 
study of pine voles in New York orchards, Benton (1955) found 
that reproduction occurred from late December or January through 
October. During a 3-year live-trapping study in Connecticut, Mil- 


Reproductive Patterns 739 


ler and Getz (1969) found breeding individuals from May through 
September, but their trapping was not conducted during all months 
each year. Paul (1966:73) found pregnant females during all months 
on one study area in North Carolina. During an 18-month study 
in Oklahoma, Goertz (1971) detected no pregnant female pine voles 
during May to August in the first summer of his study, but caught 
pregnant females the following summer in June and July. He sug- 
gested reproduction was curtailed during summer. 

Pine voles appear to breed year-round in Virginia (Horsfall, 
1963), although Cengel et al. (1978) failed to obtain pregnant fe- 
males in samples taken in November and January for a maintained 
and abandoned orchard, respectively. Valentine and Kirkpatrick 
(1970) concluded that reproduction occurred from March through 
October. However, the results from the latter 1-year study may 
have been confounded by a change in sampling sites (Valentine and 
Kirkpatrick, 1970). 

In summary, for the 15 species examined above, neither snow 
cover nor periods of prolonged breeding effort are necessary and 
sufficient to produce rapid population expansion. Amplitudes 
achieved by individual species, however, may be affected by dura- 
tion of breeding, but not invariably so (Abramsky and Tracy, 1979). 
Food quality or cues in food may be sufficient to explain periods of 
extended breeding, but prolonged periods of high food quality have 
not been established as causative agents under natural conditions. 
Alternately, breeding can be re-initiated or extended, at least in 
Microtus montanus, by experimentally supplying a population with 
6-MBOA, or in M. ochrogaster with food; but we do not know 
whether the quantity consumed produces effects similar to those 
achieved through consumption of natural vegetation. 

Early terminations or late initiations of breeding may be associ- 
ated with earlier dispersal of individuals capable of breeding, ge- 
notypic or phenotypic differences among individuals in ability to 
respond to environmental cues, phenotypic effects that regulate so- 
cial structure, or physiological mechanisms. It is not clear which of 
these factors, either singly or in consort, are necessary and sufficient 
to stop breeding efforts in natural populations of any species, but 
we cannot eliminate the possibility that cessations and late initia- 
tions of breeding efforts are regulated by one mechanism, especially 
since both patterns are common in different species. 


740 Keller 


Breeding Intensity 


Since Hamilton (1937, 1941) first suggested that population ex- 
pansion in meadow voles (M. pennsylvanicus) was caused partially 
by an increased rate of breeding, numerous investigators have sought 
to document pregnancy rates and their seasonal, temporal, and geo- 
graphic variation. Three observations can be drawn from these data 
for New World voles: 1) pregnancy rates vary seasonally but are 
generally greatest at the midpoint of the breeding season and are 
generally lower if extensions (winter breeding) occur; 2) pregnancy 
rates vary geographically among conspecific populations; and 3) 
pregnancy rates lack a consistent pattern of change during the gen- 
eralized breeding periods among years. In short, pregnancy rates 
are as likely to be high in a summer of low density as they are in 
a summer of high density, and population declines are not neces- 
sarily associated with low pregnancy rates (but see Getz et al., 
1979). Unfortunately, these observations are probably confounded 
by shifts in age at sexual maturity, which affects calculation of the 
rate of breeding. 

Operationally, four parameters interact and can potentially affect 
the observed variation: 1) the frequency of consecutive pregnancies; 
2) the ratio of pregnant to non-pregnant females; 3) the age at 
sexual maturity; and 4) the sex ratio. Each of these factors is im- 
portant, but data on consecutive interbirth intervals have not been 
separated from the ratio of pregnant to non-pregnant females such 
that we can deduce the importance of any single parameter on the 
variation observed in field populations (Keller and Krebs, 1970). 
Thus, in this section I look at the implications of the variability in 
the first two parameters combined. 


Pregnancy 


Changes in the interval between consecutive pregnancies (inter- 
birth interval) are a function of variation in post-partum receptivity 
of females and the probability that coitus will produce a conception 
that ends in parturition. Greenwald (1956) concluded that Mrcrotus 
californicus underwent induced ovulation and Breed (1967, 1969, 
1972) subsequently suggested that M. agrestis was an induced ovu- 
lator. The pattern has now been confirmed for M. canicaudus (Tyser, 
1975), M. ochrogaster (Richmond and Conaway, 1969), M. penn- 


Reproductive Patterns 741 


sylvanicus (Clulow and Mallory, 1970; Lee et al., 1970), M. pine- 
torum (Kirkpatrick and Valentine, 1970), M. montanus (Cross, 
1972), M. richardsoni (Jannett, 1979), and M. townsendi (Mac- 
Farlane and Taylor, 1982a). Breed (1967) suggested that induced 
ovulation is probably prevalent in all species for the genus Microtus. 
Because estrus appears to be induced within several days by contact 
with males or their urine (for example, see Carter et al., 1980; 
Clulow and Mallory, 1970; Gray et al., 1974; and others), it is also 
reasonable to assume that male-induced estrus (Whitten effect), 
given that it is the pattern for the genus, should prevent prolonged 
periods of anestrus if infertile matings occur. Further, all members 
of the genus appear to undergo a post-partum estrus (Hasler, 1975). 
Thus, extended intervals between consecutive pregnancies in nat- 
ural populations should constitute an unusual condition and preg- 
nancy rates of females should approach maximal limits. If true, 
these conditions differ markedly from laboratory litter intervals dur- 
ing which some permanently paired females fail to conceive after 
parturition and enter temporary periods of anestrus or pseudopreg- 
nancy. I know of no field evidence that suggests this occurs for long 
intervals during normal breeding periods, except in M. richardsoni 
(Anderson et al., 1976). 

Pregnancy can be determined at approximately 6 days post-coi- 
tum in necropsy samples (Hoffmann, 1958) or at about 9 days by 
abdominal palpation of living voles (Innes, 1978a), although some 
authors suggest longer periods (for example, see Cole and Batzli, 
1978; Stehn and Jannett, 1981). Thus, pregnancy rates (fraction of 
females pregnant) should approach 0.71 (15/21) in necropsy and 
0.57 (12/21) in field samples of voles that have gestation periods 
of approximately 21 days. Only Microtus oregoni (23.5 to 25 days; 
Cowan and Arsenault, 1954), M. pinetorum (24 to 25 days; Schad- 
ler and Butterstein, 1979), and M. townsendii (21 to 24 days; 
MacFarlane and Taylor, 19825) have slightly longer gestation pe- 
riods, which raises overall values to a maximum of 0.76 (19/25, 
laboratory) and 0.64 (16/25, field). Sufficient data exist from both 
necropsy and palpation to suggest that often not all adult females 
are pregnant even if they are reproductively mature and environ- 
mental conditions are conducive for reproduction. Additionally, 
pregnancy rates occasionally exceed these upper limits, perhaps 
owing to sampling error or as a result of synchronous breeding. 
Consequently, we need to ask why this variation exists. 


742 Keller 


Success of copulation.—Successful initiation of pregnancy in voles, 
based upon laboratory evidence, may be related to whether copu- 
lation occurs during male-induced estrus or post-partum estrus and 
the duration of the normal mating sequence (to satiety). Pregnancy 
in Microtus ochrogaster and M. montanus occurring during post- 
partum estrus is significantly less successful when numbers of cop- 
ulations are restricted than when they are unrestricted (Dewsbury 
et al., 1979). Additionally, the presence of two male prairie voles 
(M. ochrogaster) caused a decrease in the number of mounts, in- 
tromissions, and thrusts prior to the first ejaculation (Evans and 
Dewsbury, 1978). In species where pair-bonding occurs, such as in 
M. ochrogaster (Getz et al., 1981), successful post-partum breeding 
seemingly should be maintained and pregnancy assured. Perhaps 
this explains why more complex mating sequences are required to 
maximize pregnancy in M. montanus, which is polygamous. Fur- 
ther, Gavish et al. (1981) noted that forced non-sib monogamous 
pairings of M. ochrogaster resulted in production of more pups than 
forced polygamous pairings. However, these laboratory data may 
be of limited value for ascertaining conditions in natural situations 
where more complex social interactions may occur. If disruptions 
to the mating sequence are an important factor, then pregnancy 
rate might be expected to be lowest during initiation and cessation 
of the breeding season when territorial boundaries are not fully 
established. Additionally, early reduction or termination of breeding 
during periods of peak density may be related partially to reduced 
mating success in multiparous females. Sterile breeding cycles may 
be rare in M. townsend (MacFarlane and Taylor, 1981), but West- 
lin (1982) and Westlin and Nyholm (1982) suggested sterile mat- 
ings may be a general feature in overwintered females caught at 
the beginning of the breeding season. Additionally, they might be 
more common in autumn populations containing largely subadult 
individuals. M. californicus (Greenwald, 1956), M. oeconomus 
(Hoyte, 1955), and M. pinetorum (Kirkpatrick and Valentine, 1970) 
are known to have sterile matings. It would be of interest to learn 
if the success of copulatory acts varies in relation to seasonal changes 
in density or social groupings and to the degree of successful insem- 
ination based upon the estrous condition of the female in field sit- 
uations. Few data are available on these aspects and more labora- 
tory information is needed for many species. 


Reproductive Patterns 743 


Pregnancy failure.—Pregnancy rate in natural populations could 
also be affected by inhibition of implantation or premature termi- 
nations of gestation. For voles, in which the lifespan is typically 
short, both types of failure only slightly affect field assessments of 
pregnancy rates in populations, but they potentially lower the re- 
productive fitness of females through reduction in the potential 
number of young that could be delivered and weaned. However, 
terminations occurring in late stages of pregnancy, as described for 
M. ochrogaster (Stehn and Richmond, 1975), would be especially 
significant if they occurred toward the end of conditions favorable 
to breeding. 

The capacity of a conspecific strange male to block pregnancy of 
a female mated with a stud of proven fertility (Bruce effect) has 
been reported from laboratory experiments with M. agrestis (Clu- 
low and Clarke, 1968), M. montanus (Berger and Negus, 1982; 
Jannett, 1980), M. ochrogaster (Stehn, 1978; Stehn and Richmond, 
1975), M. pennsylvanicus (Clulow and Langford, 1971; Mallory 
and Clulow, 1977), and M. pinetorum (Schadler, 1981; Stehn, 1978). 
The Bruce effect is known to be mediated via olfaction of urine, 
although other environmental factors, such as disturbance, can pro- 
duce blockage (Stehn and Jannett, 1981). Additionally, both parity 
and the continued presence of the male appear to be important 
(Milligan, 1976). Lastly, blockage may be related to the social sta- 
tus of an individual. Labov (1981) presents data that refute this 
possibility in Mus, but comparative and contrasting studies that 
consider the status of the female have not been undertaken on voles. 

Mallory and Clulow (1977) suspected that pregnancy blockage 
occurred in eight females from field populations of M. pennsylvan- 
icus and suggested that incidence of blockage was related to density. 
Subsequently, Mallory (in litt.) concluded from studies of Milligan 
(1975) that three of those females developed corpora lutea as a 
result of an insufficient number of copulations with males. Re- 
evaluation of the importance of Mallory and Clulow’s (1977) re- 
maining five animals is necessary because it may be impossible to 
distinguish sets of luteinized corpora lutea produced during the 
Bruce effect from those developed from a penultimate sterile mating 
(Westlin and Nyholm, 1982). Thus, further studies are needed to 
establish if the Bruce effect occurs in wild populations of Microtus. 
Milligan (1976) suggested that, in general, short-lived corpora lutea 


744 Keller 


represent limited matings rather than pregnancy blockage. Further, 
pregnancy failures of M. californicus, described by Greenwald (1956) 
and thought to be due to blockage by Mallory and Clulow (1977), 
may have resulted from males completing an insufficient number 
of mounts and copulations. 

Based upon laboratory studies of the Bruce effect, several pos- 
tulates can be suggested for assessment in field studies where preg- 
nancy rates appear variable. 


1) The duration of contact with strange males in the absence 
of the original stud appears to be related to the probability 
that disruption will occur. Therefore, populations that are 
subjected to frustrated dispersal or increasing immigration 
should be more prone to display the Bruce effect. Addition- 
ally, populations seeded with conspecific strange males 
should display proportionally more blocked individuals. 

2) Lactation, parity, or age appears to somewhat reduce the 
probability of a Bruce effect for some species (Kenney et 
al., 1977). Therefore, nulliparous mature females will be 
more prone to disruption of their first pregnancy when the 
social fabric of the population is changing or becoming es- 
tablished during the autumn of peak density and the spring 
of decline, respectively. Thus, the Bruce effect may account, 
at least in part, for ineffective breeding following a popu- 
lation peak. (Other hypotheses exist; for example, see Bea- 
cham, 1980; Christian, 1971; Lidicker, 1976). 

3) The presence of a group of females with a female exposed 
to a strange male inhibits blockage. Therefore, communally 
grouping species, especially those in which previous pair- 
bonding has been present, will be less prone to undergo the 
Bruce effect. Thus, blockage may be more common in species 
in which family groups do not form. 


Other hypotheses are also possible for field populations. But until 
further evidence is accumulated on the occurrence of the Bruce 
effect for field populations in species known to display it under 
laboratory conditions, and pending further elaboration of the social 
structure for natural populations, field studies may prove of limited 
value. Non-histological methods to assess disrupted pregnancies need 
to be developed and used for field studies. 

Aside from the fact that pregnancy disruption may play a role in 
affecting changes in the interbirth interval, it may be important as 


Reproductive Patterns 745 


a mechanism to effect genetic changes in populations. Unfortu- 
nately, few studies have attempted to consider the reproductive con- 
tribution of individual pairs (Krebs, 1979); techniques developed to 
trace parentage (Tamarin et al., 1983) may be of value. Contri- 
butions of individual parents may prove difficult to document if 
multiple paternity, such as observed for laboratory M. ochrogaster 
(Dewsbury and Baumgardner, 1981), occur in field situations. Fur- 
ther research on this aspect is clearly warranted. Finally, the evo- 
lution of the Bruce effect, especially as it relates to reproductive 
strategies for voles, is of considerable interest. Schwagmeyer (1979) 
and Labov (1981) reviewed the purported advantages to species 
that exhibit the Bruce effect. Dawkins’ (1976) hypothesis that there 
is a mutual advantage to both sexes appears most probable for 
members of the genus Microtus. Boonstra (1980) presented com- 
pelling evidence that nestling mortality is not related to density in 
four species of voles, and he suggested disruption of pregnancies 
was unimportant on the basis of limited evidence from studies of 
reproduction by necropsy. Based upon laboratory evidence, the Bruce 
effect clearly is important in the reproductive tactics of at least five 
species of Microtus, but it remains to be established why this is so 
and whether or not this factor significantly affects pregnancy rates 
in field populations. 


Sexual Maturity 


Undoubtedly, much of the variation in pregnancy rates is a result 
of difficulties in measuring attainment of puberty (Leslie et al., 
1952) in young females, except by autopsy. In live-trapping studies, 
investigators commonly have employed fixed-weight criteria or have 
used external reproductive characteristics that may or may not iden- 
tify breeding individuals. In females, mid-winter nipple size sug- 
gests active reproduction by a limited number of females, whereas 
autopsy samples indicate reproductive quiescence (compare ‘Tam- 
arin, 1977a and Tamarin, 19776). Further development of criteria 
to assess which portion of a necropsy sample is mature can involve 
circular reasoning (Keller and Krebs, 1970), and juvenile mice that 
are capable of induced ovulation may be excluded because of lack 
of appropriate signs of maturity (Hasler, 1975). Further, if females 
undergo sterile breeding cycles at the termination of the breeding 
season, necropsy may suggest they were mature. Thus, it is not 
clear how much of the variation in pregnancy rates can be attributed 
to pregnancy failure in females as contrasted to inappropriate as- 
sessment of the number of mature breeding females. 


746 Keller 


In general, it appears that field criteria used in identifying ma- 
turity in female voles may be more accurate than criteria used for 
males, because several measures such as weight change, known 
pregnancy, suspected lactation, condition of the pubic symphysis 
(open), perforation of the vaginal orifice, and the presence of a litter 
in a trap can be combined for assessment. Although a series of 
combined criteria can be used to establish fecundity in female voles, 
external reproductive characteristics of males may be poor indica- 
tors of fecundity (for example, see Batzli and Pitelka, 1971; Iverson 
and Turner, 1976). Thus, determination of temporal changes in 
the age at maturity and identification of individual males remaining 
reproductively active during “quiescent” periods may require esti- 
mation of plasma androgen levels. Although these data are available 
for M. brewer: (Adams et al., 1980), continuous assessments on 
individuals remaining alive in natural populations have not been 
sought because adequate techniques have not been available. 

Assessment of temporal changes in age of sexual maturity are 
important factors affecting the rate of population growth (Cole, 
1954; Schaffer and Tamarin, 1973; Stearns, 1976). Many factors 
are known to affect sexual maturation in voles, (see reviews by 
Hasler, 1975; Nadeau, this volume) as ascertained from laboratory 
studies. In natural populations, the social structure and condition 
of the food supply are known to affect age at puberty; both factors 
are subject to change as a result of changes in population density. 
Laboratory studies suggest that estrous suppression of grouped fe- 
males (Lee and Boot, 1955) and male-induced estrus (Whitten ef- 
fect), which may simply be expression of the Bruce effect, leads to 
seasonal changes in age (weight) at which sexual maturity is achieved 
in field populations of voles. Batzli et al. (1977) examined attain- 
ment of sexual maturity in M. californicus, M. ochrogaster, and M. 
pennsylvanicus, and concluded that suppression, which they ob- 
served for sib-held M. californicus and M. ochrogaster but not for 
M. pennsylvanicus or M. oeconomus (Facemire and Batzli, 1983), 
was probably related to behavioral strategies initially proposed by 
Christian (1970). But, it remains to be established whether or not 
suppression operates as a result of urine-behavioral interactions for 
field populations. M. xanthognathus (Wolff and Lidicker, 1980), 
M. ochrogaster (Getz, 1978; Getz et al., 1981), M. montanus (Jan- 
nett, 1978), and M. miurus (Murie, 1961; Quay, 1951) have family 
groups where suppression might occur. 


Reproductive Patterns 747 


Seasonal and temporal shifts in the age at sexual maturity have 
been assessed for several species of voles, both on live-trapped sam- 
ples and by necropsy. Since the age of individuals is difficult to 
determine, body weight or length has been substituted as an index 
for age, but both of these measures must be viewed with caution 
because of variations in growth rates known to occur among indi- 
viduals born at different times (Krebs and Myers, 1974). Compar- 
isons have been sought by computing a median weight at sexual 
maturity (Leslie et al., 1945) for four species. 

From necropsy samples of M. ochrogaster, Keller and Krebs (1970) 
found that both males and females matured at approximately equal 
weights, but that maturity was achieved at higher weights during 
years of peak density than during years of increasing or low density. 
Further, weights at sexual maturity were found to vary seasonally. 
By contrast, Rose and Gaines (1978) found a trend toward reduc- 
tion in weight during peak density and greater weights in females 
present in declining populations of Kansas prairie voles. Addition- 
ally, Rose and Gaines (1978) found lower weights at sexual ma- 
turity for Kansas prairie voles than those documented in Indiana 
by Keller and Krebs (1970). In M. pennsylvanicus, Keller and Krebs 
(1970) found seasonal increases in weight at sexual maturity and 
slightly higher median weights at sexual maturity during periods 
of peak density. Tamarin (1977a) computed median weights at 
sexual maturity for M. breweri. Maturity in Brewer’s vole was 
achieved at much greater weights than in M. ochrogaster and M. 
pennsylvanicus, seasonal trends were apparent, and females ma- 
tured at lighter weights than males during the early portion of the 
breeding season. M. brewer: populations did not cycle during Tam- 
arin’s (1977a) 4-year study; thus, seasonal trends could not be con- 
trasted to different densities during different years of a cycle. 

Although assessment of temporal changes in age at sexual ma- 
turity may be encumbered by assumptions about the reproductive 
competency of individuals during quiescent reproductive periods, 
estimates have been developed for shifts in weight at sexual matu- 
rity in M. townsend during the usual breeding seasons. Beacham 
(1980) and Krebs et al. (1976) found a spring-to-fall increase in 
weight at sexual maturity in M. townsendi, which Boonstra (1980) 
suggested was density dependent. Boonstra and Krebs (1977) doc- 
umented a significant autumn decrease in weight at sexual matu- 
rity for each sex in both an enclosed and control peak population 


748 Keller 


exposed to a large flush of green vegetation. Based on studies of 
families of M. townsendii in small pens, Anderson (1975) suggested 
that some component common to the environment of individual 
pups prior to weaning influenced sexual maturation such that size 
at maturation was more similar among sibs than among unrelated 
individuals. However, Anderson’s (1975) studies were not com- 
pleted in the normal complex social situation in which individuals 
freely mix. Under these circumstances, alterations of sex ratios (see 
below) of voles appear to affect social structure, and maturity occurs 
earlier. Both the immediate family environment and the social 
structure of populations appear to affect maturation in this species. 

In summary, variations in pregnancy rate appear to be common. 
Although Krebs and Myers (1974) treated pregnancy rate as an 
unimportant factor in cyclic fluctuations in voles, changes in social 
structure that in turn influence age at sexual maturation affect our 
ability to determine how much variation in this parameter is nec- 
essary to significantly alter reproductive output. Thus, until we 
understand the social structure of New World voles, attempts to 
generalize about the importance of pregnancy to production levels 
may be counterproductive. 


Sex Ratio 


Variations in sex ratio may have important demographic and 
genetic consequences if the operational adult sex ratio does not 
approach unity. Such a condition may result from disparate sex 
ratios at birth that are subsequently maintained in breeding adults, 
or may develop through differential survival, movement, trappa- 
bility, or growth. As an initial premise, a population with an adult 
sex ratio favoring females will have a potentially higher reproduc- 
tive output; populations having more breeding females should reach 
peak densities more frequently (Stenseth, 1977). 

Myers and Krebs (1971) have modeled the demographic conse- 
quences of variations in sex ratio of populations of M. ochrogaster 
and M. pennsylvanicus live-trapped in Indiana. They found that a 
significant excess of males was recruited into populations, but at- 
tributed this excess to increased trappability of males because of 
their more rapid growth. By contrast, the live-trapping data, at any 
instant in time, usually showed a slight deficiency in males except 
during a period of decline (Myers and Krebs, 1971:Figs. 1, 2). 


Reproductive Patterns 749 


From their simulations, increased male recruitment was found to 
lower population growth, and they concluded that populations 
maintained approximately equal numbers of males and females. 

Some New World voles have sex ratios that deviate significantly 
from unity, but the reproductive consequences of these deviations 
are poorly understood. Further, it is difficult to ascertain whether 
these variations are a result of sampling error owing to different 
factors affecting susceptibility of males and females to being cap- 
tured, or to differences related to production or survival. Two stud- 
les suggest that unusually large disparities can exist in adult vole 
sex ratios without significant demographic consequences. Anderson 
et al. (1976) found that the first litter of M. richardsoni was com- 
posed only of females, but this observation needs further evaluation 
because they did not provide information on whether or not males 
were actually produced. Redfield et al. (1978a) studied a non- 
manipulated population of M. oregoni where the sex ratio was 21% 
males, a significant deviation from the sex ratio reported elsewhere 
(for example, see Gashwiler, 1972). 

Alternatively, Jannett (19815) argued that sampled sex ratios 
and operational sex ratios may differ. He found that, in M. mon- 
tanus, the ratio of older males to older females in high-density pop- 
ulations significantly favored females as a result of territoriality by 
breeding males. Further, territorial males remained in breeding 
condition. Therefore, the total number of males, which includes 
non-territorial males, becomes irrelevant to the breeding pattern for 
this species. 

Deliberate manipulation of the sex ratio has important conse- 
quences to the breeding structure of voles. Redfield et al. (19786) 
artificially manipulated the sex ratio of M. townsendiu on unenclosed 
grids to determine if the demographic performance of these popu- 
lations was altered by a greatly disparate sex ratio. Their results 
suggested that an enrichment of the proportion of males produced 
no significant differences in the percentage of adult or subadult 
males with scrotal testes. Further, no significant difference was 
detected in lactation between the female-enriched and control grids. 
However, weight at sexual maturity for the rarer sex on both en- 
riched grids was lower than the value for the same sex on the 
control. 

Muicrotus oregoni also was subjected to manipulation (Redfield et 
al., 1978a) during the above studies on M. townsend, and a sum- 


750 Keller 


TABLE 1 
SUMMARY OF CHANGES IN THE BREEDING PATTERN OF Microtus oregoni ON 0.64-HA 
UNENCLOSED STUDY AREAS WHERE THE SEX RATIO OF THE EXPERIMENTAL POPULA- 
TION Was MANIPULATED (REDFIELD ET AL., 19782) 


Experimental populations 


Main breeding 
season 


Winter breeding 
season 


Sexual 
maturity 


Recruitment of 
sexes 


Control population 


Adult 6é enter breeding 
condition 6 weeks 
before 92, 1973; not 
clear for 1972 


Adult 86 enter breeding 
condition 6 weeks 
before ¢? (February 
vs March) but no 
winter breeding in 
adults 

Subadult 6¢ mature be- 
fore subadult 22 but 
are not mature in 
winter 


Male- 
enriched 


More scrotal 66 
than control 


Higher percent 
46 breeding; 
breed longer, 
and in winter 


Subadult 66 ma- 
ture during 
winter 


More ¢6¢ and 22 
recruited 
than control 


Female- 
enriched 


92 breed more in- 
tensively and 
longer than 
control 


Higher percent 
9¢ lactating; 
breed longer 
(October), but 


not in winter 


Subadult ¢¢ do 
not mature 
during winter 


More 4é and 22 
recruited than 
control 


mary of the changes that occurred in the creeping vole is presented 
in Table 1. Although the initial populations were found to be dis- 
torted (21% males), further distortion of the sex ratio produced a 
profound change in the demographic pattern of the enriched pop- 
ulations. With regard to reproduction, no winter breeding occurred 
in the control population. However, breeding continued in the male- 
enriched population (at a reduced level by both adults and sub- 
adults). Females also continued to breed for a longer period during 
the first winter. Although Redfield et al. (1978a) did not comment 
on age at sexual maturation, their data suggests that males on the 
male-enriched grid initiated breeding at lighter body weights. Ad- 
ditionally, other components in the reproductive process were sub- 
jected to alteration (fine-tuning changes), but the potential effects 
of these changes in relation to subsequent changes in density are 
not clear. 


Reproductive Patterns 751 


In summary, sex ratios for many species of New World voles 
have been documented over extended periods, but only two studies 
have dealt with the potential effects on reproductive processes if 
these ratios are significantly altered experimentally. From these 
studies, it appears that changes in the breeding potential can be 
induced, but it is neither clear what range of disruption is required 
to significantly alter this potential nor how disruption affects the 
social structure of populations. Krebs (1964) proposed that the sex 
ratio only affected the number of breeding animals in polyestrous 
mammals, but a significant disruption of this ratio also appears to 
alter the social structure of populations such that age at sexual 
maturity and length of the breeding season may be affected. 


Litter Size 


A comparison of interspecific and intraspecific variation in litter 
size for New World voles is difficult for several reasons. Presently 
it is not possible to assess the amount of variation that is genetically 
determined in each species. Where phenotypic differences have been 
noted, either geographically or temporally, the statistical treatments 
are often inadequate, largely as a result of small samples. Addi- 
tionally, because parity, season of collection, weight, age, and phys- 
iological condition of females are all subject to variation, assessment 
of geographical variation among conspecific populations may be of 
limited value. Presently, we lack adequate estimates for the pro- 
portion of variation in litter size produced by each of these factors. 

Table 2 gives the mean litter size and pertinent data on sampling 
durations and locations for 18 species of New World Microtus. 
Except as noted, I excluded studies in which counts of placental 
scars were included with counts of embryos because placental scar 
counts are not always reliable (Corthum, 1967; Martin et al., 1976; 
Rolan and Gier, 1967). In some cases, I computed grand mean 
values by pooling data for individual periods. Additionally, I ex- 
cluded data for individual species in which sample size was <10 
unless the data base was found limited or the locality distinct. Thus, 
more data are available, especially for M. californicus, M. ochrogas- 
ter, M. pennsylvanicus, and M. pinetorum, but they are largely an- 
ecdotal or are presented in regional works in which samples were 
pooled from broad geographical areas. 


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The smallest mean litter sizes shown are for M. pinetorum (Cen- 
gel et al., 1978), M. quasiater (Hall and Kelson, 1959), and M. 
mexicanus (Brown, 1968), whereas the largest is reported for M. 
xanthognathus (Wolff and Lidicker, 1980). Values provided in the 
table for laboratory colonies are lower than the highest values ob- 
served under field conditions, excepting those in M. oregoni and M. 
pinetorum. 


Genotypic and Phenotypic Variation 


Innes (19786) reviewed the relation between embryo counts and 
latitude and elevation for 42 independent literature samples of M:- 
crotus species. Although he found a significant correlation (r = 0.77, 
P < 0.01) between litter size and these variables when values for 
several species were pooled, no correlation could be demonstrated 
for each of four species with sufficient sample sizes for contrasts. 
Thus, Innes (19786) concluded that the relationship of latitude and 
altitude, or both, were of questionable importance for explaining 
litter size in voles. Kenney et al. (1979) suggested litter size in voles 
is related to persistence of copulatory behavior. However, subse- 
quent consideration of several untested species failed to support this 
hypothesis (Dewsbury and Hartung, 1982). Lord (1960) suggested 
large litter size compensated for presumed higher winter mortality 
in northern areas. Spencer and Steinhoff (1968) suggested that larg- 
er litters were favored as a result of short breeding seasons. But the 
two latter studies failed to differentiate litter size at birth and re- 
cruitment. Thus, voles with larger litters would only be at repro- 
ductive advantage if their young have larger litters and are recruited 
in at least proportionate numbers of if they breed for longer dura- 
tions. The relative contribution of young by individual females re- 
mains largely unknown for any species of Microtus, but Anderson 
(1975) documented high repeatability for litter size in female M. 
townsendi studied in breeding enclosures. Unfortunately, the degree 
of similarity of litter sizes between breeding adults and recruited 
young could not be measured in her experimental enclosures. An- 
derson and Boonstra (1979) also were unable to demonstrate a 
relationship between maternal body size or parity and litter size at 
recruitment. Thus, it is not clear how selection for litter size op- 
erates on voles under natural conditions, and its role within and 
between different species of voles remains an enigma. 


Reproductive Patterns 761 


Statistical Considerations 


In voles, phenotypic rather than genotypic responses to environ- 
mental variation probably produce the intraspecific differences in 
litter size observed geographically, altitudinally, and temporally 
(Krohne, 1980). Unfortunately, appropriate statistical treatments 
are difficult to make for a number of reasons. Pelikan (1979) noted 
that many of the comparisons made for litter size in small mammals 
are derived from sample sizes that do not provide reliable mean 
estimates and that increasing litter size is correlated with increasing 
standard deviations. Thus, in species with large embryo counts, 
greater sample sizes are required to distinguish between alternative 
hypotheses. For example, in M. pinetorum, which has a litter size 
approximately equivalent to Pitymys subterranus, between 30 and 
40 pregnant females were required to obtain a reliable mean for 
contrast (Pelikan, 1979). For species with mean litter sizes of 4.91 
to 6.20, 90 to 120 pregnant females were needed to estimate a mean 
with the same reliability (Pelikan, 1979). 

The above observations are important in assessing differences 
among species, such as the contrast provided by Innes (19785), 
because assumptions of ANOVA procedures are violated when cross- 
species comparisons are sought with samples that are heteroscedas- 
tic. Additionally, Pelikan’s (1979) analyses clearly indicate that con- 
specific contrasts require complete monthly seasonal data sets for 
comparisons, because mid-season means differ statistically from 
whole-season means owing to greater variability in embryo counts 
at the beginning and end of breeding periods. Because relatively 
few studies have separated peak seasonal data into blocks for com- 
parisons among years of treatments, and because data blocks are 
often developed with limited samples, most of the litter-size values 
that now exist are not commensurable. In order to improve future 
commensurability, data should be displayed by week for individual 
months. 

Pelikan (1979) did not address the question of the effect of parity 
and weight on mean values of litter size, but this variation also 
affects comparability. A number of studies for voles indicate that 
litter size varies with the age (weight) of females and their parity. 


Age (Weight) and Parity 


Leslie and Ranson (1940) first noted an association between in- 
creased litter size and age in Microtus agrestis; Hasler (1975) re- 


762 Keller 


viewed the literature on the effect of parity. A relationship between 
parity and litter size has not been found for M. chrotorrhinus (Mar- 
tin, 1971), M. canicaudus (Tyser, 1975), M. townsendi (Anderson 
and Boonstra, 1979), or M. xanthognathus (Wolff and Lidicker, 
1980). Exceptions have been noted in M. longicaudus (Wright, 1971), 
M. ochrogaster (Rose and Gaines, 1978), and M. brewer: (Tamarin, 
LOTTO). 

When the weight of females, which may or may not relate to 
parity, affects litter size, and breeding is not synchronized like that 
observed in M. xanthognathus, significant differences in litter size 
among years or between areas being sampled may be distinguished 
only on the basis of covariance analyses (Keller and Krebs, 1970). 
Thus, the different contributions of weight (age) and parity, be- 
cause they are rarely detailed, renders many estimates of embryo 
counts difficult to compare on a geographical basis. 

Some investigators have made contrasts of embryo counts after 
adjusting for parity and weight differences among samples. Keller 
and Krebs (1970) and Tamarin (1977a) were unable to demon- 
strate significant differences in embryo counts for primiparae and 
multiparae female M. pennsylvanicus in Indiana and Massachu- 
setts. No significant depression in embryo counts among years for 
cycling meadow voles was found by these authors. 

Keller and Krebs (1970) found that multiparous and primipa- 
rous female M. ochrogaster differed in their embryo counts; the 
former contained embryo counts depressed by 25% during periods 
of peak density. By contrast, Rose and Gaines (1978) were unable 
to demonstrate significant weight-embryo regressions for prairie 
voles in Kansas, but the absence of light females may have influ- 
enced their results as females <20 g were not collected. Marked 
seasonal effects on living embryo counts were observed, but a re- 
duction in litter size was not found at the peak density (Rose and 
Gaines, 1978). 

No significant differences in embryo counts among years have 
been found for non-cyclic species. Tamarin (1977a) was unable to 
demonstrate a significant relationship between parity or weight and 
embryo count in Microtus brewert, but Anderson and Boonstra (1979) 
found that litter size for M. townsendi is influenced by weight and 
not parity and that embryo counts were significantly larger in spring 
than summer or fall. 


Reproductive Patterns 763 


Other Factors 


Many authors attribute differences in litter size to nutritional 
deficiencies (Batzli, this volume), endocrine responses related to 
density (Seabloom, this volume), or physiological responses related 
to the presence of chemical substances that stimulate reproduction 
(Negus et al., 1977). Given that substances such as 6-MBOA (Ber- 
ger et al., 1981; Sanders et al., 1981) stimulate rapid reproductive 
development of reproductively quiescent voles other than M. mon- 
tanus, we would expect populations exposed to greater quantities 
of stimulatory chemicals to display larger litters at the height of the 
breeding season. Although this supposition awaits a critical evalu- 
ation, studies exist which demonstrate that litter size differs signif- 
icantly in qualitatively different habitats for other species. Cengel 
et al. (1978) suggested that food quality affected litter size in M. 
pinetorum. Krohne (1981) was able to eliminate effects of parity 
and age on embryo counts in M. californicus populations trapped 
in annual and perennial grasslands. In a series of replicated studies 
in enclosures, he was able to establish that embryo-count differences 
in voles occupying the two habitats were the result of responses to 
vegetation (Krohne, 1980). Since these populations were established 
with a pair of sibs, a genetic basis for these differences seems un- 
likely, although Krohne (1981) noted that genetically based dissim- 
ilarities in embryo production occurred among conspecifics raised 
under laboratory conditions. Additionally, replicated experiments 
all demonstrated similar patterns. Krohne (1982) suggested that 
reduced litter size in California voles in perennial grasslands was 
partially responsible for the lack of a multi-annual cycle in his 
population. 

Cole and Batzli (1978) observed greater production of young M. 
ochrogaster fed rabbit pellets under field conditions. Although sam- 
ple sizes used for comparison were small and the parity-weight 
relationships of these samples were not reported, the results are 
suggestive; concurrent studies in dissimilar habitats suggested dis- 
similar embryo counts (Cole and Batzli, 1979). 


Prenatal Mortality 


The potential litter size in voles, as contrasted to the number of 
embryos that develop, can only be determined by autopsy. Rela- 


Keller 


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Reproductive Patterns 765 


tively few studies have been undertaken on New World voles to 
assess the degree of prenatal mortality associated with changes in 
density, although some seasonal assessments are available. Table 3 
shows the pooled values of pre- and post-implantation loss for four 
species of voles. I included the results of Beer et al. (1957) for 
contrast, although the data were produced from a variety of lo- 
cations and from unknown population densities. The data from 
Tamarin (1977a) are restricted to peak periods of density for M. 
pennsylvanicus. Data for M. californicus were excluded, because 
accessory corpora lutea develop in this species (Greenwald, 1956; 
Hoffmann, 1958; Lidicker, 1973), a condition that prevents assess- 
ment of total loss because pre-implantation mortality cannot be 
determined. Post-implantation mortalities (percent resorbing em- 
bryos) for M. californicus in the three studies were 7.2, 3.9, and 4.7, 
respectively. Post-implantation resorptions in laboratory M. ochro- 
gaster exceeded field resorptions (32/278 = 11.5%; Stehn, 1978). 
On the basis of these studies, levels of prenatal mortality do not 
appear related to changes in density. Total losses appear highest in 
M. brewer: (Table 3), but comparative data are lacking for most 
species. 

In voles, pre-implantation losses can be determined by computing 
the difference between implantations (living and resorbing) and the 
number of corpora lutea (except in M. californicus). Cases of pre- 
sumed polyovuly or polyembryony (twinning) range from approx- 
imately 2% to 13% and the values appear to be relatively consistent 
within two species where independent determinations have been 
made. The lowest values, 1.2% (2/170) and 1.6% (3/185), were 
reported for Microtus ochrogaster by Keller and Krebs (1970) and 
Rose and Gaines (1978). Beer et al. (1957) reported 6.8% (17/ 
251), Keller and Krebs (1970) 4.3% (7/162), and Tamarin (in litt.; 
1977a) 5.3% (3/57) for M. pennsylvanicus. The value for M. brew- 
ert (Tamarin, 1977a) was 3.9% (4/102) (Tamarin, in litt.). Hoff- 
mann (1958) found the largest value (13.0%; 14/108) in Microtus 
montanus. ‘Tamarin (in litt.) did not find twinning in either M. 
brewer or M. pennsylvanicus, but Beer et al. (1957) noted that 
approximately 30% (5/17) of their results could be attributed to 
twinning. 

In cases in which the number of implants exceeds the number of 
corpora lutea, and twinning is excluded, corpora lutea may be 
counted incorrectly. Snyder (1969) sectioned ovaries of M. penn- 
sylvanicus and found that one corpus luteum in a sample of 24 


766 Keller 


ovaries was overlooked. Values for polyovuly or polyembryony 
should be viewed as conservative estimates because they are under- 
estimated if corpora lutea and implant counts are identical and early 
resorption of one or more embryos is missed. Additionally, total 
pre-implantation losses (already noted in conjunction with potential 
changes in the interbirth interval) are missed frequently because 
corpora lutea rapidly undergo involution following blockage by 
strange males (Bruce effect). 

Post-implantation losses result from failure of one or more em- 
bryos, but we are unable to separate genetic failure of individual 
implants from failures due to exogenous or endogenous factors that 
affect the physiology of female voles. Total losses are rarely en- 
countered in necropsy samples. The loss may be total where stress 
(Seabloom, this volume) or the Bruce effect occur, but the oppor- 
tunity to observe male-induced abortion, because of its rapid com- 
pletion, is unlikely in kill-trap samples. Stehn and Richmond (1975) 
documented the sequence of events for male-induced abortion in M. 
ochrogaster. ‘They noted that termination was accompanied by a 
mucilaginous bloody discharge that contained amorphic pieces of 
debris. Although we cannot determine whether live-trapped popu- 
lations display these symptoms because of handling or the Bruce 
effect, I have observed female discharges composed of debris similar 
in composition to the placental sign described by Venable (1939), 
in M. montanus, M. ochrogaster, and M. pennsylvanicus. 

In summary, it is not presently possible to separate the factors 
that have led to variation in litter size for New World voles. Phe- 
notypic plasticity appears to account for much of the variation ob- 
served for conspecific populations living in qualitatively dissimilar 
habitats. The number of living embryos shows seasonal peaks that 
may be related to the size, age, weight, or parity of females. Many 
statistical treatments can be faulted where these relationships are 
not considered. No compelling evidence suggests embryo production 
is lower during periods of population decline, but the number of 
embryos is generally lower in females pregnant early or late in the 
breeding season. 


Discussion 


Since Hasler’s (1975) excellent review of the literature on repro- 
duction in the subfamily Microtinae was published, most field stud- 


Reproductive Patterns 767 


ies have continued to assess variation in breeding patterns without 
corroborative experiments. More emphasis needs to be placed on 
reproductive analyses in which suspected variables are manipulated 
experimentally. Describing relationships between breeding inten- 
sity and environmental parameters in contrast to testing necessary 
and sufficient agents responsible for breeding patterns seems to me 
to be a self-defeating task; further description may add little to our 
knowledge of how reproductive parameters affect population 
changes. Years ago, Chitty (1952) tried to convince us that social 
factors affect reproductive status and fertility of individuals. It ap- 
pears that in our haste to describe why populations decline, cycle, 
and disperse, we often ignored the reproductive success of individ- 
uals and remained content to consider only the average of the masses. 
If we find that some species adjust their breeding seasons as a result 
of chemicals in vegetation, then we must immediately ask about 
individual variation in responsiveness to limited cues. Pheromones 
and social learning seem to play a synergistic role in behavior of 
voles. Do all individuals respond to these cues in a similar manner? 
I stress the importance of individual variation in reproductive ad- 
aptations in voles, but it is evident that we also are unable to directly 
relate reproductive variation, as measured in field populations, to 
subsequent population patterns. Much remains to be learned. In 
summary, the following list illustrates some experimental manip- 
ulations that should increase our understanding of intraspecific re- 
productive processes for populations of New World voles: 1) chem- 
ical identification and field experimental studies of pheromones that 
may serve to integrate environmental cues with the social organi- 
zation required for breeding in voles; 2) field experiments with voles 
unable to smell their conspecifics (see Horton and Shepherd, 1979; 
Richmond and Stehn, 1976); 3) application of graded doses of 6- 
MBOA in a variety of species over an entire winter non-breeding 
period; 4) 6-MBOA enhancement of breeding in early-stop peak 
and late-start declining populations; 5) quantification of seasonal 
and altitudinal variation in 6-MBOA content of vegetation; 6) sex- 
ratio enrichment experiments for species other than M. townsendii 
and M. oregon1, especially in single-species populations; 7) extensive 
heritability analyses for age at sexual maturity, growth potentials, 
and winter breeding in species known to cycle; 8) analyses of re- 
productive success in marginal habitats for colonizing individuals; 
9) assessment of the degree of reliability between necropsy and field 


768 Keller 


assessment of fecundity, especially for “‘winter’’ breeders; 10) delib- 
erate introduction of unknown conspecifics into known populations 
in large enclosures where breeding can be carefully assessed prior 
to introduction and can be followed subsequently for Bruce-Whitten 
effects; 11) initiation of large, enclosed field populations with fe- 
males having small litters versus females having large litters pre- 
viously housed in laboratory situations. Age, weight, and pairs must 
be equalized. 


Acknowledgments 


This chapter was made possible through a grant to the Idaho 
State University Foundation provided through the offices of Kirk- 
land Ellis, Chicago, Illinois. I especially want to thank Mrs. Joan 
Downing, Assistant Librarian, Idaho State University, and the staff 
of the libraries of Idaho State University and the University of Utah 
who went to great lengths to be helpful and provide space during 
development of this chapter. I thank Bonnie Bowen for offering 
comment on the final manuscript and the reviewers who offered 
comment on the initial draft. 


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NUTRITION 
GEORGE O. BATZLI 


Abstract 


EVERAL characteristics of the gastro-intestinal tracts of microtine 
S rodents appear to be adaptations for use of high-fiber, low- 
protein, and low-mineral diets, which are consistent with the ob- 
servation that most microtine species eat primarily the vegetative 
parts of plants. The exact compositions of diets are a function of 
the availability of food items and the nutritional adaptations of 
individual species; the same species in different habitats and differ- 
ent species in the same habitat eat different food items. Food-item 
preference seems to depend upon a combination of the positive 
(water and nutrient content) and negative (fiber content and plant 
secondary compounds) characteristics of the item, and different mi- 
crotine species have different tolerances for specific secondary com- 
pounds. Performances of microtines on particular food items, as 
measured by food intake and body growth, parallel their food pref- 
erences. 

Although little is known about nutrient requirements of micro- 
tine rodents, they seem to require lower concentrations of digestible 
energy and protein in their diets than do laboratory rodents. Min- 
eral requirements are similar to those of laboratory rodents, but 
concentrations in natural diets may often be low. Increased intake 
can compensate for low-quality food (low digestibility or low-nu- 
trient content) so that requirements for energy and nutrients are 
met. But this compensation is not always sufficient, and mounting 
evidence indicates that the quality of available forage can help to 
explain differences in the densities of microtine populations among 
habitats, among seasons, and among years. 


Introduction 


Because all the life processes of organisms depend upon the ac- 
quisition of energy and nutrients, the topic of nutrition can be 


779 


780 Batzli 


expanded to include much of biology. However, the scope of this 
chapter is restricted to the more traditional topics of nutrition— 
food habits, food quality, nutritional physiology, and nutritional 
ecology. My approach is functional and comparative; my goals are 
to understand the mechanisms behind and the implications of the 
patterns that we see. The chapter treats microtine rodents as a 
group because our understanding of Muicrotus can be greatly en- 
hanced by considering additional information from closely related 
genera. 

Microtine rodents have evolved morphological characteristics that 
can be interpreted as adaptations to high-fiber, low-nutrient diets. 
In general, they possess high-crowned molars with enamel loops 
that provide prismatic grinding surfaces (Guthrie, 1965; Hinton, 
1926). This allows reduction of vegetative material to fine particles 
without wearing teeth down to the gums. As a further adaptation, 
genera that take large amounts of fibrous and siliceous material 
(Lemmus and Microtus) have rootless molars that continue to grow 
through life. 

The morphology of microtine stomachs is extremely variable and 
overlaps broadly with other muroid rodents. Vorontsov (1962, 1967) 
argued that the tendency to a chambered stomach and a reduced 
glandular zone is analogous to stomach development in ruminants, 
but Carleton (1973, 1981) pointed out the varied nature of micro- 
tine stomachs and diets and challenged this view. 

The cecum and large intestine of microtines are among the largest 
and most elaborate of all muroid rodents (Vorontsov, 1962, 1967). 
Cecal size and the post-cecal spiral are particularly well developed 
in the most herbivorous species (Lange and Staaland, 1970). The 
enlarged cecum seems to function as a chamber for digestion of fiber 
and for production of protein and B-vitamins (McBee, 1970, 1971), 
and the post-cecal spiral may be a mechanism for mineral retention, 
particularly sodium (Staaland, 1975). Because the cecum occurs at 
the juncture of the small and large intestines, feces must be rein- 
gested if the microbial protein and vitamins are to be absorbed. At 
least one microtine (Microtus pennsylvanicus) is known to practice 
coprophagy in a manner similar to rats and rabbits (Ouellette and 
Heisinger, 1980). Thus, although the functional significance of 
morphological peculiarities of the gastro-intestinal tract of micro- 
tines cannot be specified with certainty, most evidence points to 
adaptation for handling high-fiber (and silica), low-protein, and 
low-mineral diets. 


Nutrition 781 


In the discussion that follows, it becomes clear that the diet and 
nutritional adaptations of microtines vary considerably among 
species, although most species are primarily herbivorous. Because 
the nutrition of microtines per se is poorly understood, many of the 
principles developed from studies of domesticated animals (May- 
nard et al., 1979) and wildlife (Robbins, 1983) must be applied to 
them. But this should be done with caution, for we must expect 
nutritional systems of ruminants (cattle, sheep, and deer) or om- 
nivorous rodents (laboratory rats and mice) to be somewhat differ- 
ent from those of herbivorous rodents such as microtines. Lago- 
morphs (rabbits and hares) seem to be the group whose nutritional 
characteristics are most similar to those of microtine rodents; both 
groups are small, monogastric herbivores with enlarged cecae. 


The Diets of Microtines 


Food Habits 


Although it is common knowledge among mammalogists that 
microtine rodents are herbivores, there have been relatively few 
reliable, quantitative studies of food habits. The most accurate es- 
timates of diet composition for microtine rodents seem to be volu- 
metric estimates based upon microscopic examination of stomach 
contents (Batzh and Pitelka, 1971; Hansson, 1970; Neal et al., 
1973; Williams, 1962). Estimates based on frequency overestimate 
the importance of items taken regularly in small amounts. Differ- 
ential digestibility of epidermal cells, which bear the distinctive 
characteristics that allow identification, causes errors in estimates 
based upon fecal samples. Items with relatively thin cell walls (di- 
cotyledons) tend to be underestimated, and items with thick cell 
walls (monocotyledons and mosses) tend to be overestimated. Cor- 
rection factors can be calculated for a particular population by com- 
paring the abundance of items in stomachs with the abundance of 
the same items in fecal pellets from the colon of the same animals 
(Batzli and Pitelka, 1971, 1983), but this is seldom done. Another 
source of error may be the underestimation of seeds and arthropods 
in the diet because much of the material in these items lacks dis- 
tinctive characteristics (Fish, 1974); only the seed coat and chitinous 
exoskeletons are easily detected. Finally, there is substantial vari- 
ability in the relative abundance of items in individual stomachs, 


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786 Batzli 


so population estimates for a particular time and place should be 
based upon at least 10, and preferably 20, samples (Batzli and 
Pitelka, 1983). 

To reduce potential error the dietary information reviewed here 
is restricted to studies based upon adequate numbers of stomachs 
(or corrected fecal samples) for which volumetric estimates were 
made of all types of food items. In general, these data support the 
notion that microtine rodents are primarily herbivorous; all species 
take <10% animal material (Table 1). However, if we distinguish 
true herbivores (those that consume vegetative parts of plants) from 
granivores (seed eaters) and frugivores (fruit eaters), then clear 
differences between species and populations can be seen. Microtus 
ochrogaster takes variable amounts of seeds (up to 35% of its diet) 
depending upon location, and M. californicus switches to a predom- 
inantly seed diet (73%) during summer (Table 1). Clethrionomys 
rutilis in Alaskan taiga takes mostly fruit throughout the year, sup- 
plemented by substantial amounts of fungi or moss at different 
seasons. 

Although the two lemmings (Lemmus and Dicrostonyx) and all 
Microtus species consume mostly vegetative plant parts, the types of 
plants taken vary within and between species. Thus M. pennsyl- 
vanicus takes mostly monocotyledons or mostly dicotyledons de- 
pending on location and season; fungi and seeds make up about 20 
to 40% of their diet in prairie habitats during autumn and winter. 
In non-prairie habitats both M. pennsylvanicus and M. ochrogaster 
shift from favoring dicotyledons in summer to monocotyledons in 
winter. Both M. xanthognathus and M. oeconomus (when not in 
tundra) eat substantial amounts of horsetails (Equisetum spp.), and 
both favor rhizomes in winter. In arctic tundra, Lemmus strongly 
and consistently favors monocotyledons, Dicrostonyx strongly and 
consistently favors dicotyledons (particularly willow), and M. oe- 
conomus takes large amounts of both, although it takes more mono- 
cotyledons. All three microtines also eat mosses; both Lemmus and 
Dicrostonyx increase their consumption of mosses in winter, but 
Lemmus eats more moss year-round. 

Given that all these species are plant eaters, why this bewildering 
variety of dietary patterns? Three main factors are probably in- 
volved: 1) the relative abundance of some items in the diet of mi- 
crotines simply reflects the availability of those items in the local 
habitat; 2) the nutritional adaptations of microtine species differ 


Nutrition 787 


owing to their different evolutionary histories; 3) microtines show 
strong preferences for different items depending on the quality of 
that item in relation to the nutritional adaptations of the species. 
The last point is particularly important; the quality of plant ma- 
terial as food is not only a function of the plant’s physical and 
chemical characteristics but also a function of the herbivore’s re- 
quirements, abilities, and tolerances. The most certain assay of the 
quality of a food item is the performance of the herbivore in ques- 
tion when fed that food item, and even then some results may be 
artifacts of experimental conditions that affect feeding behavior. 


Food Selection 


Clear differences in food habits occur between pairs of species 
living in the same habitat, such as Lemmus and Dicrostonyx in arctic 
tundra, Clethrionomys and Microtus in taiga, and M. ochrogaster 
and M. pennsylvanicus in central Illinois prairie and old bluegrass 
pasture (Table 1). These differences between species confronted 
with the same array of vegetation indicate that the species have 
specialized preferences, even though all still take a wide variety of 
food items and all show strong shifts in their diet with location and 
season. Narrow specialization on very few species of plants has been 
reported only for two microtine populations: M. brewert on Mus- 
keget Island, Massachusetts, eat almost only beach grass (Ammoph- 
ila breviligulata) and bayberry (Myrica pennsylvanica) (Rothstein 
and ‘Tamarin, 1977), and M. montanus at Tempe Springs, Utah 
eat primarily (>90% of diet) Distichlis stricta (Berger et al., 1977). 
Both species live in habitats with very low vegetational diversity, 
and both show seasonal shifts in the parts of plant taken. 

If an animal shows a consistent response to a particular food 
item, then diet composition will be related to availability of that 
item. Although there are several ways to make this comparison 
(Lechowicz, 1983) a simple preference index (PI = proportion of 
diet/proportion of forage) allows one to assess a variety of patterns 
(Batzli, 1983). If the herbivore responds to availability of the food 
item, there will be a positive correlation between percent of diet 
and percent of forage accounted for by that item; PI > 1 if consis- 
tently preferred, PI < 1 if consistently avoided, or PI = 1 if taken 
in the same amount as available. Alternatively, an item may be 
taken erratically or in relatively constant amounts no matter what 


788 Batzli 


its availability (no consistent preference or PI decreases with in- 
creased availability, respectively). This type of analysis requires 
multiple samples from a variety of sites with different availability 
of food items, and given the paucity of quantitative analyses of diets, 
it is not surprising that there have been few such studies. Analyses 
that have been done show three general types of responses of her- 
bivorous microtines to food items: consistent preference, consistent 
avoidance, or relatively constant intake (Batzli and Jung, 1980; 
Batzli and Pitelka, 1983). 

Preferences shown by analyses of diets in the field generally, but 
not always, agree with palatability measured by intake in the lab- 
oratory. Thus Batzli and Jung (1980) reported that Lemmus and 
Microtus strongly preferred cotton grasses (Eriophorum spp., PI ~ 
5) in their diet near Atkasook, Alaska, and these were among the 
most palatable foods in the laboratory. Dicrostonyx and Mhicrotus 
strongly preferred willows (Salix spp., PI ~ 5) and forbs (PI ~ 10) 
and found them palatable in the laboratory; Lemmus avoided wil- 
lows (PI ~ %4) and forbs (PI ~ 4) in the field, and both had low 
palatability ratings for Lemmus. Certain evergreen shrubs (Ledum, 
Cassiope, and Empetrum) were avoided by all microtines in the field 
(PI < ¥,) and were generally unpalatable in the lab. On the other 
hand, no microtines showed any consistent preference for the most 
common plants, sedges in the genus Carex. Whatever the avail- 
ability of Carex, Lemmus consistently took large amounts (30 to 
60% of diet), Microtus took substantial amounts (about 20% of diet), 
and Dicrostonyx took small amounts (<10% of diet). Although pal- 
atability was highest for Lemmus, it was also high for the other 
microtines. Apparently, Carex was a staple food item for Lemmus 
no matter what its availability (it was relatively common in all 
habitats), and other palatable foods (Eriophorum, some grasses, and 
some mosses) filled in the diet in relation to their availability. Dr- 
crostonyx had a strong preference for other foods that were usually 
available (Eriophorum, Salix, and forbs), and Carex simply acted as 
a filler. The pattern for Microtus fell between the other two species. 
Clearly, these microtine species responded very differently to the 
same food items, presumably because these items affected them dif- 
ferently; that is, the quality of each food item varied with the species 
consuming it. 

What aspects of forage do rodents respond to when selecting their 
diet? Probably they respond to the same factors that humans do: 


Nutrition 789 


aroma, texture, and flavor. But these are merely cues that indicate 
to the vole that the food is good or of poor quality. The value of 
cues lies in their correlation with underlying determinants of qual- 
ity, such as digestibility, nutrient content, and plant secondary com- 
pounds. 

Three studies looked at forage palatability to voles in relation to 
nutrient concentrations. Hansson (1971) compared the rank order 
of palatability for seven species of monocotyledons at three seasons 
to results from a proximate chemical analysis (organic matter, crude 
protein, ether extract [total lipid], crude fiber, N-free extract, ash, 
and kcal/g). He found positive correlations between ranks for pal- 
atability and those for protein and ether extract and a negative 
correlation between palatability and fiber, but none was significant. 
Nevertheless, it was probably no coincidence that the most utilized 
species under natural conditions, Agrostis tennuis, had high-protein 
and low-fiber content. Meade (1975) compared intake of 27 plant 
species by M. pennsylvanicus under laboratory conditions with their 
water, nitrogen, phosphorus, and potassium contents. Using only 
species that were acceptable forage, he found significant positive 
correlations between intake and all of the nutrients, but the strong- 
est relationship by far was for water (A? = 0.75). Multiple regres- 
sion techniques revealed that only the relationships with water and 
nitrogen content remained significant when effects of other nutrients 
were removed. Finally, Goldberg et al. (1980) reported on variation 
in nutrients (proximate chemical analysis and calcium, magnesium, 
and phosphorus) in relation to seasonal shifts in preference for parts 
of beach grass (A. breviligulata). In spring and summer voles chose 
leaf blades, which had the highest concentrations of all nutrients 
and the lowest fiber concentrations; in late summer and early au- 
tumn voles chose roots, which had the lowest fiber at that time; in 
winter voles chose stems, which then had the lowest fiber content 
and the highest phosphorus content. Water content was generally 
similar in all plant parts in all seasons except winter when water 
in leaf blades was half that (34%) of the other parts. 

Thus, it seems that voles use fiber content (poorly digestible and 
tough), water, and nutrient content (particularly protein and phos- 
phorus) when selecting among palatable plant parts or species, but 
some other factor(s) is involved in determining palatability as well. 
As suggested by numerous authors, one such factor is likely to be 
plant secondary compounds (see Harborne, 1982 for review). In 


790 Batzli 


the last 10 years a variety of secondary plant compounds has been 
implicated as factors affecting food intake by microtine rodents (Ta- 
ble 2). Apparently intake is depressed as a result of strong odor 
(terpenes; Batzli and Jung, 1980), bitter taste (alkaloids; Kendall 
and Sherwood, 1975), or astringency (quebracho; Lindroth and 
Batzli, 19845). Effects of these compounds on performance are con- 
sidered below. 

In general then, both availability and quality of individual food 
items affect the diet composition of herbivores. For example, Lin- 
droth and Batzli (19845) show that important food items of M. 
pennsylvanicus may be either poor in quality but highly available 
(taken in large amounts even though they are selected against) or 
high in quality but poorly available (taken in large amounts because 
they are strongly selected). 


Intake, Forage Quality, and 
Individual Performance 


General Considerations 


Forage quality can affect three basic aspects of microtine perfor- 
mance: growth, reproduction, and survival. These effects may occur 
because of low concentrations of digestible nutrients in the forage, 
because of physical or chemical characteristics of the forage that 
reduce intake or digestibility, because of toxins in the forage, or 
because of a combination of these factors. 

Whatever its diet, an organism must consume enough to meet its 
long-term metabolic requirements, including both energy and nu- 
trients. Energetic considerations have usually been emphasized by 
biologists, perhaps because energy is relatively easy to measure and 
bears a clear relationship to performance for all organisms. Nu- 
trient requirements vary widely among species and general patterns 
are more difficult to discern. Nevertheless, nutrient requirements 
for any herbivore are closely linked to energy requirements and 
digestibility of the forage. This is because nutrient turnover is di- 
rectly related to metabolic rate and the amount of material passing 
through the gut (Barkley et al., 1980). In the discussion that follows 
I sometimes adjusted body mass in relation to metabolic rates to 
facilitate comparisons among animals of different sizes; however, I 


SECONDARY 


Species of 
microtine 


Microtus penn- 


sylvanicus 


M. montanus 


M. ochrogaste 


M. oeconomus 


Lemmus sibiricus 


PLANT COMPOUNDS 


TABLE 2 


LIKELY 


To 


RODENTS 


Compound and 


plant species 


B-nitroproprionic 


acid in crown 
vetch (Coronilla 


varia) 


Saponins in alfal- 
fa (Medicago sa- 


tiva) 


Alkaloids in reed 


canary grass 


(Phalaris arun- 


dinacea) 


Cinnamic acids 
and related vi- 
nyl phenols in 
wheat and salt 
grass (Distichlis 


stricta) 


r Flavonoid (quer- 
cetin) and tan- 


nins (tannic 


acid and que- 
bracho) in arti- 


ficial diet 


Ethanol extracts 


of Laborador 
tea (Ledum pal- 


ustre) 


Ethanol extracts 


of willow (Salix 


pulchra) and 


Labrador tea 


Effect 


Depressed intake, 
growth, and 
survival 


Depressed intake 
and growth 


Depressed intake, 
increased reti- 
culocytes, and 
kidney lesions 


Depressed repro- 
duction 


Depressed growth 
by quercetin 
and tannic acid, 
depressed in- 
take by que- 
bracho 


Terpenes depress 
intake and un- 
identified com- 
pounds depress 
growth and 
survival 


Terpenes depress 
intake and un- 
identified com- 
pounds depress 
growth and 
survival 


Nutrition 791 


BE DELETERIOUS TO MICROTINE 


References 


Barnes et al. 
(1974); Gustine 
et al. (1974); 
Kendall et al. 
(1979); Shenk 
(1976); Shenk et 
al. (1970, 1974) 


Kendall and Leath 
(1976); Marcar- 
ian (1972) 

Goelz et al. (1980); 
Kendall and 
Sherwood 
(1975); Kendall 
et al. (1979) 


Berger et al. 
(1977) 


Lindroth and Bat- 
zli (19842) 


Batzli and 
Jung (1980); 
Jung and Batzli 
(1981) 


Batzli and Jung 
(1980); Jung 
and Batzli 
(1981) 


792 Batzl 


TABLE 2 
CONTINUED 
Species of Compound and 
microtine plant species Effect References 
Dicrostonyx tor- Ethanol extracts Terpenes depress Batzli and Jung 
quatus of sedge (Carex intake and un- (1980); Jung 
aquatilus) and identified com- and Batzli 
Labrador tea pounds depress (1981) 
growth 


do not review the bioenergetics of microtine rodents because that is 
done elsewhere in this book (Wunder, this volume). 


Digestibility and Intake 


Intake of food and output of feces and urine can be measured by 
placing animals in metabolic cages. Intake and apparent digestibil- 
ity of forage can then be compared to weight change of the animal. 
Animals do not always respond well to confined conditions, and 
there are often great individual differences in their performance. 
Nevertheless, some reassuring patterns emerge. First, as expected, 
change in body mass is directly related to intake of digestible dry 
matter (or energy) on a given diet (Fig. 1; Shenk, 1976). The better 
performance of M. ochrogaster in Fig. 1 occurred because the arti- 
ficial diet was of higher quality for them (greater growth on the 
same intake as the other species). The generally low intake by 
Lemmus compared to Microtus indicates lower palatability of the 
diet to them. Second, intake of palatable food decreases as digest- 
ibility of the food increases (Fig. 2). This trend results from com- 
pensation for low digestible energy and nutrient content by in- 
creased intake so that nutritional requirements are met, a 
phenomenon that will be discussed in more detail below. ‘Third, the 
digestibility of food items is related to the general type of food over 
a wide variety of plant and microtine species. A review by Batzli 
and Cole (1979) showed that, on average, microtines digested 89% 
of the energy in seeds and garden vegetables, 74% of dicotyledon 
stems (non-woody) and leaves, and 54% of monocotyledon stems 
and leaves. Digestible dry matter (DDM) followed a similar trend, 
but fewer data were available. 

Digestibility of forage for herbivores is generally negatively cor- 


Growth (9g: d~°) 


] 
oO 


nN 
oO 


=o. 0) 


Nutrition 793 


4 M. ochrogaster 
O M. oeconomus 
® /. sfbiricus 


Pes 
ra\ 


O2 (9) 0.4 0.5 06 Oy 0.8 
Intake (g:g BW °°-d7') 


Fic. 1. Relation of growth rate of animals to relative rate of intake of digestible 
dry matter on an artificial diet. Data for Microtus oeconomus and Lemmus sibiricus 
are combined because regressions were not significantly different. Regression equa- 
tions with 95% C.L.: Y = 2.61 + 1.21 X — 1.70 + 0.70 (R? = 0.70) for M. ochro- 
gaster, and Y = 3.05 + 1.21 X — 2.70 + 0.67 (R? = 0.68) for M. oeconomus and L. 
sibiricus. See Lindroth et al. (1984) for methods. 


related with fiber content (hemicellulose, cellulose, and lignin), and 
weight gain of voles on grass diets may also be negatively correlated 
with fiber content (Russo et al., 1981). Nevertheless, intake and 
weight gain improved when weanling meadow voles ate cereal diets 
with 18% cellulose (alphacel) compared to the same diets without 
cellulose. Chemically isolated cellulose (alphacel) is essentially un- 
digested by voles (Shenk et al., 1970) and the improved performance 
with alphacel in the diet may simply reflect a need for bulk. Ap- 
parently 10 to 30% of natural fiber can be digested by voles (Keys 
and Van Soest, 1970). Most of this digestion is probably done by 
microbes in the cecum, but cellulolytic bacteria and fermentation 
products have also been found in the stomach (Kudo et al., 1979; 
McBee, 1970). Toughness and texture of the diet also are related 
to the amount and arrangement of fiber, and too much fiber may 
inhibit intake of forage (Ulyatt, 1973). 


0.9 


794 Batzli 


Bion’ 


Intake (kcal/g :day/) 


fe) 
aoe ora a Os 


20 40 60 80 
Digestibility (%) 


Fic. 2. Comparison of total intake of energy (solid points and solid line) to intake 
of digestible energy (open points and dashed line) in relation to digestibility of forage 
by Microtus ochrogaster, M. californicus, and Lemmus sibiricus. Circled points represent 
unpalatable food; vertical lines give 95% confidence intervals (after Batzli and Cole, 
1979). 


The compensatory increase of intake for less digestible food is 
well known for ruminants (Ulyatt, 1973), laboratory rats (Adolf, 
1947), and laboratory mice (Dalton, 1963). Of course, lower di- 
gestibility of forage must be compensated by greater intake if the 
animal is to survive. Although the size of a single meal for voles 
may be limited by gastro-intestinal fill (Kendall et al., 1978), total 
daily intake appears to be adjusted depending upon digestible en- 
ergy or nutrients. For many foods intake may compensate com- 
pletely so that the consumption of digestible energy and dry matter 
remains relatively constant (Fig. 2). But some foods, usually those 
of low quality, simply are not palatable enough to be taken in large 
amounts. Thus, although mosses may form up to 40% of the diet 
of L. stbiricus, they are poorly digested compared to monocotyledons 
(23% DDM and 33-37% DDM, respectively), and voluntary 
intake of mosses alone is not sufficient to maintain the animals. 
Similarly, M. ochrogaster does not consume enough bluegrass to 


Nutrition 795 


O 


@ Early summer 1976 + lab 
O Late summer 1976 
4 Late summer |977 


Relative foraging rate (mg/gBW-?.min) 


O 40 80 120 160 200 240 280 
Monocot biomass (g/m*) 


Fic. 3. Relative foraging rates for brown lemmings (Lemmus sibiricus) in relation 
to forage availability (from Batzli et al., 1981). 


maintain its body weight, and bluegrass is relatively poorly digested 
(51% DDM) compared to more palatable dicotyledons (61 to 69% 
DDM). 

It is difficult to assess how herbivores would perform on food 
they will not eat, but it is clear that different species of microtines 
show different physiological responses to the same food. Whereas 
Lemmus only digested 33-37% of the dry matter in tundra mono- 
cotyledons, M. ochrogaster digested 52% of the same plants (Batzli 
and Cole, 1979). Similar differences can be seen on laboratory diets. 
Two microtines that prefer monocotyledons (L. sibiricus and M. 
californicus) digested only 53-54% of the dry matter in commercial 
rabbit chow (largely alfalfa meal), whereas a dicotyledon eater (M. 
ochrogaster) digested 68% (Batzli and Cole, 1979). On an artificial 
diet made with chemically defined materials, Lemmus and M. oe- 
conomus digested 54%, whereas M. ochrogaster digested 61% of the 
dry matter (Lindroth et al., 1984). 


796 Batzli 


In nature, of course, it takes time to select and harvest food, and 
it is not surprising that foraging rate (rate of intake) varies with 
availability of palatable food (Fig. 3). Stage of growth and year-to- 
year variability in growth form also affect foraging rates; older, 
larger plants are consumed more slowly (Batzli et al., 1981). Thus, 
as quality and availability of food items change, herbivores must 
change their diet in order to maintain high rates of intake. If they 
cannot switch diets, they must spend more time foraging, and this 
means greater exposure to the physical environment and to preda- 
tion. Hence, seasonal changes in food selection can be viewed as the 
expected response to seasonal changes in availability and quality of 
food items. In order to track this changing quality a herbivore must 
continually sample available forage, which accounts for the wide 
variety of food items taken in small amounts by most generalist 
herbivores (Westoby, 1978). 

Flexible turnover times of gut contents exist in most species so 
that less digestible forage is processed more rapidly (Batzli and 
Cole, 1979), but whatever the demand for nutrients, intake of food 
can be no faster than the gut can process it. Traditional wisdom 
says that smaller ruminants must eat a more highly digestible diet 
to survive—the Jarman-Bell principle (Geist, 1974; Janis, 1975; 
Jarman, 1974; Parra, 1978). The argument goes as follows: 1) 
smaller animals have similar relative gut size but larger relative 
metabolic rates and more rapid turnover of gut contents than do 
larger animals; 2) for a given diet, a decrease in turnover time is 
also associated with a decrease in digestibility; 3) mathematical 
relationships are such that for a given diet smaller animals get less 
energy relative to their metabolic requirements than do larger an- 
imals; and 4) therefore smaller animals must eat more digestible 
food. 

When fed similar forage, the gut turnover time for a wide variety 
of herbivores decreases in a regular way with body size (Fig. 4). 
Monogastric animals have a shorter turnover time than ruminants, 
but the rate of decline with body size (slope of the line) is the same. 
Given the same general relationship (even with different parameter 
values) for monogastric herbivores as for ruminants, the same ar- 
guments should apply to ruminant and monogastric herbivores. 
However, it is clear that many small herbivores, including some 
microtine rodents, eat large amounts of poorly digestible food (Bat- 
zli and Cole, 1979). Furthermore, some microtines can digest hay 
almost as well as horses, even though they are several orders of 


Nutrition 797 


O 


TO= .33W:-26 
r2=.77 


Turnover Time 
(days) 


O| .! | lO lOO !000 
Body Weight (kg) 


Fic. 4. Turnover time of gut contents in relation to body size for ruminant 
(triangles) and non-ruminant (circles) animals (from Batzli, unpubl. observ.). 


magnitude smaller (Batzli, pers. observ.). How can this be? The 
traditional analysis assumes that digestion proceeds as a simple 
exponential function of time in the gut, a model proposed by Blaxter 
et al. (1956). In fact, it is more likely that small molecules in cell 
contents are absorbed very quickly by the gut, non-fibrous polymers 
(proteins, glucans, and pectin) require moderate processing, and 
fibrous polymers (cellulose and lignin) require much longer pro- 
cessing (Hungate, 1966). Thus, digestibility is a mixed function of 
time; small animals that chew forage very finely, thereby rupturing 
the cells and releasing cell contents, can reduce turnover time with- 
out suffering the full consequences expected based upon a simple 
continuous function (Batzli, pers. observ.). 


Nutrients and Performance 


The exact nutrient requirements of organisms are difficult to 
specify because of the large number of required nutrients, interac- 
tions among nutrients, and substantial individual differences within 
a species. As a result only the nutritional requirements of domes- 
ticated rodents are very well known. Because of the increasing use 
of voles for bioassays in agricultural research, they have now been 
included in the group of laboratory animals covered by the National 
Research Council’s publication on nutrient requirements of domes- 


798 Batzli 


TABLE 3 
RECOMMENDED NUTRIENT CONTENT OF DIETS FOR GROWTH AND REPRODUCTION OF 
RODENTS AND RABBITS 


Guinea Ham- 


Rabbit? Rat? Mouse? pig? ster? Vole 

Digestible 2,500 3,800 3,700 3,000 4,200 3,750 
energy 2,000-3,000° 
(kcal/kg) 

Protein 16.0-17.0 15-1 18.0 18.0 15.0 13.0 
(%) 8.0" 

Calcium 0.4-0.7 0.5 0.4 0.8-1.0 0.6 0.3-0.5» 
(%) 

Phosphorus 0.2-0.5 0.4 0.4 0.4-0.7 0.3 0.2-0.4° 
(%) 

Sodium 0.20 0.05 0.08 ? 0.15 >0.02° 


(%) 


* Based upon National Research Council publication on nutrient requirements for 
domestic animals and references cited therein (National Research Council, 1977, 
1978). 

» Based upon data for voles and lemmings (Batzli, unpubl. observ.; Batzli and Cole, 
1979; Lindroth et al., 1984). 


tic animals (National Research Council, 1978). As can be seen in 
Table 3, requirements of microtines appear to be similar to labo- 
ratory rodents and rabbits, but many nutrient requirements have 
not been studied. Recent work indicates that digestible energy re- 
quirements of voles are more similar to rabbits than to laboratory 
rodents (Table 3) and that Lemmus sibiricus may only require 70% 
as much digestible energy in its diet as does M. ochrogaster (Batzli 
and Cole, 1979). Data for an artificial diet (Lindroth et al., 1984) 
suggest that the protein requirement for maximal growth of young 
M. ochrogaster is only 8% or less of dry matter (Lindroth and Batzli, 
1984a), rather than the 13% suggested by data for M. pennsyl- 
vanicus (Shenk et al., 1970). Other requirements of different species 
of microtines also may differ. Species with the same intake of digest- 
ible dry matter on the same diet may show significantly different 
growth rates (Fig. 1). 

The nutrients that appear to be most critical for microtine rodents 
in their natural food are digestible energy, protein (organic N), 
calcium (Ca), phosphorus (P), and sodium (Na), but this may be 


Nutrition 799 


an artifact of the paucity of studies involving other nutrients. Re- 
quirements for nutrients are greatest for lactating females; in mi- 
crotine rodents the mass of the litter at weaning is often greater 
than that of the female (Batzli and Jung, 1980; Batzli et al., 1974). 
Thus, it is not surprising that the breeding season for most herbiv- 
orous microtines coincides with the growing season, the period when 
the quality of available food is usually highest (Fleming, 1973; 
Goldberg et al., 1980). For most temperate species this means spring, 
summer, and fall (M. montanus, M. ochrogaster, M. pennsylvanicus), 
although in a Mediterranean climate the growing season is reversed 
and breeding stops during the dry summer (M. californicus). As 
plants age, their quality as forage for microtines declines (Hansson, 
1970; Martinet and Daketse, 1976; Martinet and Meunier, 1969; 
Myllym4ki, 1977). Thus, during the breeding season the diets of 
these herbivores are mostly fresh stems and leaves, whereas they 
gradually shift to seeds, stem bases, and roots as the above-ground 
parts of the plants age and die back. After a breeding pause, when 
quality of available food is low (Batzli, in press), reproduction re- 
commences with the first appearance of high-quality green shoots 
(Batzli and Pitelka, 1971; Negus et al., 1977). Apparently the an- 
imals respond to a chemical cue (6-M BOA) in the developing plants 
(Berger et al., 1981; Sanders et al., 1981). Provision of high-quality 
food can maintain breeding during the cold winter (Cole and Batzli, 
1978) or dry summer (Ford, 1978). 

Length of reproductive season, litter size, body growth, and sur- 
vival rates all correlate with nutrient content of natural forage (Cole 
and Batzli, 1979; Hoffmann, 1958), and laboratory feeding trials 
indicate that growth and reproduction are direct responses to nu- 
trient content of the diet. Cole and Batzli (1979) reported that M. 
ochrogaster grew more rapidly on natural diets with higher nutrient 
concentration, and Batzli (in press) found that summer diets for 
M. californicus (grass seeds) are deficient in Ca and Na, both of 
which affect reproductive success. 

The role of sodium in microtine nutrition has been of particular 
interest. Aumann and Emlen (1965) found that reproductive output 
(number of young) of M. pennsylvanicus in small pens increased 
when a sodium supplement was added to their water, and that 
animals increased their sodium intake as conditions became more 
crowded. Normal sodium levels in urine of voles (MV. arvalis) and 
lemmings (L. lemmus), and sodium levels in the feces of lemmings 


800 Batzli 


(L. lemmus), are extremely low (DeKock and Robinson, 1968; Lange 
and Staaland, 1970). Apparently these patterns of sodium conser- 
vation occur because of the low sodium content in the diet of these 
herbivores and the evolution of efficient mechanisms for absorption 
of sodium in the colon of microtines, but social stress upsets endo- 
crine balance and can result in unusually high loss of sodium in 
urine. 

The nutrients that are most important for microtines probably 
vary with season and location. A simulation model of N, Ca, and 
P nutrition for L. sibiricus indicated that for lactating females N 
was in short supply in winter, P was limiting in early summer, and 
a high Ca/P ratio caused difficulties in late summer (Barkley et 
al., 1980). But nutrient content of the major food type, monocoty- 
ledon stems and leaves, varied by a factor of 2 from year to year, 
and nutritional difficulties only occurred in low-nutrient years. As 
already mentioned, Ca and Na availability seem to limit summer 
breeding by M. californicus, and no doubt other nutrients are im- 
portant in other places. 


Secondary Plant Compounds and Performance 


For microtines, negative nutritional factors other than high fiber 
appear to consist largely of secondary plant compounds. The same 
compounds that reduce intake of particular plant species also reduce 
growth, survival, and reproduction if given in amounts equivalent 
to expected dietary levels (Table 2). Thus, saponins, alkaloids, and 
phenolic compounds have all been shown to be detrimental to voles 
when ingested, and no doubt other classes of compounds, such as 
terpenes, also will prove to be detrimental. Terpenes do disrupt 
digestive processes in ruminants (Oh et al., 1970). 

Not all secondary compounds affect microtines in the same way, 
nor does the same compound affect different species of microtines 
in the same way. Evaporation of ethanol extracts of plant tissue on 
laboratory diets produced a variety of effects on growth, body com- 
position, and organ weight of arctic microtines (Jung and Batzli, 
1981). Performance on diets containing extracts of three foods—a 
sedge (Carex aquatilis) that was highly palatable to L. sibsricus and 
M. oeconomus, a willow (Salix pulchra) that was highly palatable 
to D. torquatus and M. oeconomus, and Labrador tea (Ledum pal- 
ustre) that was palatable to none of the microtines—were entirely 
consistent with results of palatability trials. Willow extract con- 


Nutrition 801 


tained compounds that reduced growth and body fat of Lemmus but 
not Microtus or Dicrostonyx; sedge extract reduced growth and body 
fat of Dicrostonyx, but only body fat of Lemmus and Muicrotus; and 
Ledum extract reduced growth and body fat of all three microtines 
(and caused the death of Lemmus even though food intake was 
normal). 

Some secondary compounds act as toxins ($-nitroproprionic acid, 
alkaloids) when absorbed, but others may act by reducing the di- 
gestibility of important dietary components, for instance complexing 
of protein by some phenolics (Rhoades and Cates, 1976). Thus, 
voles (M. ochrogaster) fed artificial diets containing two kinds of 
phenolics had poorer growth on low-protein diets than on high- 
protein diets (Lindroth and Batzli, 1984a). Protein digestibility 
was also lower for voles on low-protein diets with high levels of 
tannic acid, but these voles also had higher intake so that they 
digested equivalent total amounts of protein on low- and high- 
phenolic diets. The level of detoxication products (glucuronides) in 
urine also suggested that the depression of growth by phenolics was 
the result of a toxic effect and not because of lowered protein di- 
gestibility. High levels of protein may have protected the voles from 
the toxic effect by binding with the tannic acid. This interaction 
between protein levels and phenolic levels is probably not unique, 
and it seems likely that the quality of forage is a product of multiple 
interactions between positive and negative chemical factors. 


Optimal Foraging 


Given a complex array of forage that varies in availability and 
quality through time and space, herbivores must somehow decide 
what to eat. If we assume that animals eat so as to maximize their 
performance under a given set of conditions, and if we understand 
how these conditions influence performance, then we should be able 
to predict how an animal will forage and what it will eat. This is 
the basis for optimal foraging theory, most of which has been de- 
veloped for predators (Krebs, 1978). Much of this theory requires 
that food items be ranked according to their net value, which usually 
is couched in terms of net energy yield and does not seem directly 
applicable to herbivores. 

One optimization model that has been applied to microtine her- 
bivores is the graphical model developed by Stenseth and Hansson 
(1979), which predicts the net fitness gain from food in relation to 


802 Batzli 


its value (digestible energy content). Net gain for each food type is 
a function of the direct cost of foraging activities (which increases 
with decreasing availability of an item), maintenance cost (which 
increases with the time spent foraging), and the distribution of 
values for the food type (not all items of the same type have the 
same value). Thus, the net gain from a food type increases as the 
values and densities for items in a type increase. If the distributions 
of net gains (items with different values within a type have different 
net gains) for different food types overlap substantially, the animal 
maximizes its net gain by taking a mixed diet. Unlike most of the 
optimization models developed for predators, this model predicts 
that relative densities of food items (not just absolute densities) 
influence diet choice and that partial preferences (not all or none 
responses) for food items will occur. However, like other models, 
Stenseth and Hansson’s (1979) model requires a currency. The 
currency they favor is energy, although they acknowledge that oth- 
ers might be used. 

Stenseth et al. (1977) used the graphical model outlined above to 
predict diets of M. agrestris in Sweden and Finland. They included 
four food types (grass, forbs, seeds, and bark) and assigned the value 
of items by digestible energy content. They successfully predicted 
nearly equal use of grass and forbs in spring in northern Sweden, 
but predictions for other seasons and for two communities in Fin- 
land depended upon somewhat arbitrary evaluations. In addition, 
they needed to invoke “‘search images” and polymorphic behavior, 
for which they presented no evidence, to reconcile predictions and 
observed diets. 

A different approach to optimal foraging, the use of linear pro- 
gramming, was suggested by Westoby (1974) and Pulliam (1975). 
In this technique constraints (such as minimal nutrient intake) are 
established; the combination of food items that satisfies those con- 
straints and maximizes or minimizes some other factor (for instance 
energy or foraging time) is sought. The most successful use of this 
technique to date has been that of Belovsky (1978) with moose. He 
used constraints of 1) minimal energy and sodium requirements for 
maintenance and reproduction, 2) maximal times allowed to spend 
foraging in water (because of heat loss) and on land (owing to time 
needed for rumination), and 3) maximal amount of bulk in the diet 
(rumen capacity is more quickly filled by aquatic plants with high 
water content). Then he predicted the amount of aquatic plants, 


Nutrition 803 


forbs, and leaves of shrubs in the diet if energy intake were maxi- 
mized or foraging time were minimized. Actual diets almost exactly 
matched those predicted by the strategy of energy maximization. Of 
course, not all plant species within these general food categories 
were taken, and predicting which species would be taken was more 
difficult (Belovsky, 1981). Selection of aquatic plants seemed clearly 
related to their sodium content, but use of terrestrial plants did not 
depend simply on their nutrient content or availability. 

It seems likely that positive and negative nutritional factors (such 
as secondary compounds) need to be balanced by herbivores when 
selecting their diet (Lindroth, 1979). Certainly, the information 
available to date for microtine rodents suggests that this is so (see 
above). Thus, a model that predicts the diet of microtine rodents 
probably will need to include multiple constraints within which 
there is very little room to maximize nutrient or energy intake. 
Indeed this may explain why the performance of animals and pop- 
ulations varies so with habitat type and, therefore, quality of avail- 
able food. 


Forage Quality and Population 
Characteristics 


Habitat Differences 


That population densities and demography differ in different 
habitats is well known, but the causes of these differences generally 
are not. Most microtines require a minimal amount of cover, pre- 
sumably as protection against predation, and Birney et al. (1976) 
have suggested that response to cover explains many of the differ- 
ences in density among habitats. Addition of water and fertilizer to 
shortgrass prairie markedly increased the density of M. ochrogaster, 
but it is not clear how much of the response was due to increased 
cover and how much was due to improved nutrition (Grant et al., 
On): 

Two studies have shown that the quality of diet differs in differ- 
ent habitats, and because of the effects of diet quality on growth, 
reproduction, and survival, the population dynamics in the habitats 
varied. Cole and Batzli (1979) found low, moderate, and high den- 
sities of M. ochrogaster in tallgrass prairie, abandoned bluegrass 


804 Batzl 


pasture, and abandoned alfalfa fields. Growth of young, litter size, 
length of breeding season, and survival were all clearly related to 
the quality of different diets in three study areas, and these differ- 
ences accounted for the different densities reached in the popula- 
tions. Krohne (1980, 1982) found that litter sizes of M. californicus 
were greater and that penned populations had greater reproductive 
output and rates of growth when fed annual grasses compared to 
perennial grasses. These results corresponded to different popula- 
tion dynamics found in the field: seasonal fluctuations at low den- 
sities in perennial grassland and multi-annual fluctuations reaching 
high densities in annual grasslands. In neither of these studies could 
the differences between habitats be explained by availability of cover. 

It is not clear how often differences in populations between hab- 
itats can be related to available food because most studies do not 
examine nutrition adequately. Collared lemmings and brown lem- 
mings in arctic Alaska have strong habitat preferences that are 
associated with concentration of preferred foods (Batzli and Jung, 
1980; Batzli et al., 1983), and Batzli (1983) suggested that the wide 
variability in the population densities of lemmings in different geo- 
graphical regions of tundra is a function of the quality of available 
food. Because cover and food often are contributed by the same 
plants, the two are not always separable, but it seems clear that 
given a minimal amount of cover (and therefore food), the quality 
of available food accounts for many of the observed differences in 
microtine rodent populations in different habitats. 


Population Dynamics 


Because the reproductive season of microtines is often linked to 
available food, it follows that seasonal changes in density (increases 
during the reproductive season and declines during the non-breed- 
ing season) are also a function of nutrition. Thus, every summer 
when vegetation dries, the voles shift to grass seeds that are deficient 
in Ca and Na, reproduction ceases and population densities of M. 
californicus decline (Batzli, in press; Batzli and Pitelka, 1970, 1971). 
Most temperate species show a similar pattern of shifting food 
habits and a reproductive pause during winter, although the pop- 
ulation of trappable animals does not always decline immediately 
(Gaines and Rose, 1976; Getz et al., 1979; Krebs et al., 1969; Negus 
et al., 1977; Tamarin, 1977; Whitney, 1976; Wolff and Lidicker, 


Nutrition 805 


1980). Winter breeding may occur in some species if high-quality 
forage is accessible under the snow (Batzli et al., 1980), and winter 
breeding can be maintained if supplemental food is given (Cole and 
Batzli, 1978). 

In addition to seasonal changes, many microtine species go through 
extreme multi-annual fluctuations in density (cycles). Because these 
fluctuations are analyzed in another chapter of this book (Taitt and 
Krebs, this volume), and because I recently reviewed the role of 
nutrition in these cycles (Batzli, in press), I only make a few com- 
ments here. 

First, the data on habitat effects summarized above indicate that 
only when high-quality forage is available can microtine rodents 
reach the high densities associated with cyclic peak populations. 
Second, theoretical analyses and empirical data (Batzli, in press; 
Batzli et al., 1980) indicate that neither the food-shortage hypoth- 
esis of Lack (1954) nor the nutrient-recovery hypothesis of Pitelka 
(1964) and Schultz (1964) are likely to account for cycles. The 
plant-production hypothesis of Kalela (1962) recently was both 
supported (Laine and Henttonen, 1983) and rejected (Andersson 
and Jonasson, in litt.) for two areas in northern Fennoscandia. 
Third, manipulations of natural populations by providing fertilizer 
or supplementary food all indicate improved reproduction, growth, 
and survival during the population increase (Cole and Batzli, 1978; 
Desy and ‘Thompson, 1983; Krebs and DeLong, 1965; Schultz, 
1969; Taitt and Krebs, 1981), but none prevented the population 
decline. However, these experiments were flawed because they did 
not monitor or prevent an influx of predators to the small experi- 
mental sites when all other nearby populations declined. One ex- 
periment on penned populations that included predator control did 
prevent a population crash by provision of food and water (Ford, 
1978). Fourth, a theoretical analysis of the implications of positive 
nutrient feedback versus negative nutrient feedback (secondary plant 
compounds) suggested that, whereas strong positive nutrient feed- 
back leads to instability or stability of a soil-plant-herbivore-pred- 
ator trophic system, inducible secondary compounds acting as pro- 
posed by Haukioja (1980) may lead to oscillatory instability (Batzli, 
in press). Thus, if changes in nutrition are sufficient to produce 
population cycles, it is most likely because food plants respond to 
damage with lowered quality, probably because of production of 
secondary plant compounds. 


806 Batzli 


On the whole I doubt that any single factor, including nutrition, 
will be sufficient to explain population cycling. Environmental fac- 
tors, such as nutrition and weather, and responses of organisms, 
such as aggressive behavior and dispersal, interact in complex ways, 
and it is those interactions that need to be examined. 


Conclusions 


It seems clear that nutrition plays a large role in the well-being, 
habitat preference, and successful reproduction by microtine ro- 
dents. Thus, much of the morphology, physiology, and behavior of 
these animals should be interpretable in relation to the availability, 
quality, and processing of forage. A thorough analysis of such pat- 
terns awaits the development of much better information on diet, 
gut morphology, and nutritional physiology for a wider variety of 
species. Only then will the relationships among these variables, and 
the evolutionary response of microtine species to the variable nu- 
tritional conditions found in their habitats, become clear. 


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Nutrition 811 


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Microtus. J. Mamm., 46:605-612. 


ENERGETICS AND 
THERMOREGULATION 


BRUCE A. WUNDER 


Abstract 


N general, Microtus species live in cool environments, are thought 
I to have a boreal origin, and are small. They feed primarily upon 
vegetative plant parts which have relatively high fiber and low 
digestibility. Thus, voles should have high energy needs while feed- 
ing on an energetically dilute, but abundant, food; yet none shows 
any form of torpor. This review covers the manner in which voles 
accumulate and allocate energy and the environmental and social 
factors which affect those processes. 

Digestibility of food by voles varies between species and is af- 
fected by season and plant or plant part, but it does not seem to be 
affected by increased energy flow drains from cold stress or repro- 
duction. Microtus species regulate body temperature (T) well but 
generally have not been tested at extremely low ambient tempera- 
tures. The data available make it difficult to conclude whether they 
regulate at high T, or not. Microtus species can vary insulation 
relative to habitat and season but do not show high insulation as a 
group. Basal metabolism (BMR) of Microtus species is about 20— 
40% greater than expected from allometry (but not the 70-80% 
greater that is now given in the literature). The effects of food, 
photoperiod, and temperature on BMR and non-shivering ther- 
mogenesis are discussed. 

When expressed as exponential growth constants, but not when 
summed as growth during lactation, growth rates of Microtus species 
are high. However, many environmental factors affect these rates 
and the energy required for them. Gestation and lactation necessi- 
tate about 35% and 100-120% increases in energy flow, respective- 
ly, although values for M. pinetorum are low. Population energy 
considerations are briefly discussed. 


812 


Energetics and Thermoregulation 813 


Introduction 


To exist as homeotherms and continue as populations or as species, 
mammals must acquire and expend energy. There are several re- 
views of the general concepts of how and what avenues are used by 
animals in general, and mammals in particular, to do this (Calow, 
1977; Slobodkin, 1962; Townsend and Calow, 1981). There are 
also several reviews of energetics in small mammals in particular 
(Ferns, 1980; Gessaman, 1973; Grodzinski and Wunder, 1975). 

To exist and to maintain body mass and body temperature a vole 
must balance energy gain with energy expenditures. We can envi- 
sion such balance and the avenues for exchange in Fig. 1. I dis- 
cussed these balance factors before as representing a cascade of 
priorities for energy use (Wunder, 1978a). First, a vole initially 
must allocate enough energy for thermoregulation to maintain body 
temperature; otherwise it will become hypothermic and can do 
nothing else. Second, because foraging is the only feedback for en- 
ergy acquisition, that need must be met, and will vary depending 
upon the animal’s total energy needs. Once these two functions are 
met, excess energy can be stored (fat) or used for other activities. 
One important aspect of this view, and implied in the model, is that 
energy allocated to one function generally cannot be used for another. 
In order to reproduce, a vole must accumulate enough energy to 
thermoregulate, feed, and then meet all the physiological and be- 
havioral requirements for reproduction. Another assumption made 
in considering the importance of energetics for organisms is that 
energy may be limiting at certain times for certain activities during 
an animal’s life (for example, during winter there may not be enough 
energy for both thermoregulation and reproduction). 

There are several ways of looking at energy limitations. I pre- 
viously discussed some of these such as total needs and turnover 
needs (Wunder, 1978a). In addition, energy availability in the en- 
vironment (food density) may limit an animal’s capacity to acquire 
and use energy. Another limiting factor that is seldom considered 
by ecologists is the limitation imposed by the morphology and phys- 
iology of the gut. An animal’s acquisition of energy is limited by 
the volume of food it can process per unit time and the efficiency 
of energy extraction from that volume. Thus, even though energy 
may be available in the environment, it can only become chemically 


814 Wunder 


Physical 


Environmental 


ize, Factors 
PSsiM ENERGY 
IN 


EVGp 


a an - eked 
Thermoregulation 
2 BMR. NST, Shivering,Torpor 
oO Behavior 
So 
oO 
> 
S) 
Feeding 
= oe ee 
J Growth 
Behavior Young 
Breeding EGetauion 
Socidl 
Play 


Dispersion 
Investigative 


Fic. 1. A conceptual model of energy balance for a small mammal, indicating a 
priority cascade for energy allocation. Lines represent both total energy flow and 
rate functions (from Wunder (1978a), with permission). Abbreviations are: BMR, 
basal metabolism; NST, non-shivering thermogenesis; Evap, evaporation; assim, as- 
similation. 


available for an organism within certain limits. White (1978) dis- 
cussed this as a relative shortage of food. 

Energy limitation is significant in the life histories of Muzcrotus. 
In general, Microtus species live in cool environments, are thought 
to have a boreal origin (Hooper, 1949; Zakrzewski, this volume; 
Hoffmann and Koeppl, this volume), and they are small. They feed 
primarily on vegetative plant parts, which have high fiber and low 


Energetics and Thermoregulation 815 


digestibility (Grodzinski and Wunder, 1975). They are the only 
small mammals that do not regularly feed on a calorically dense 
food (flesh, seeds, or fruits) and that do not show any form of torpor. 
Most cricetines or other small mammals, by contrast, hibernate (for 
example, Zapus) or at least show daily torpor (for example, Pero- 
myscus). Thus, voles have high energy needs yet feed on an ener- 
getically inferior but abundant food type. Most of this review con- 
siders energy balance at the individual level and how Microtus species 
solve these problems. In this discussion I emphasize New World 
Microtus; however, reference to Old World forms is necessary be- 
cause much work has been done with them. 

From studies of ecosystem function ecologists have developed an 
interest in the concept of ecosystem energy flow (from Lindemann, 
1942, to recent IBP studies). ‘Thus, there is an interest in how small 
mammals like Microtus may be involved. Because there have not 
been many detailed studies of this type (but see Ferns, 1980; French 
et al., 1976; Golley, 1960; Whitney, 1977), I only cover this subject 
lightly. 


Methods 


A variety of techniques has been used to investigate the bioen- 
ergetics of small mammals (Grodzinski and Wunder, 1975; Grod- 
zinski et al., 1975; Petrusewicz and MacFadyen, 1970). Basically 
they consist of respirometry trials, which give information about 
maintenance costs or food consumption trials that include both 
maintenance and production costs. Respiration trials cannot give 
information about energy tied up in production because they only 
measure consumption or production of gases associated with res- 
piration (oxygen, carbon dioxide) as an index to heat production. 

There is a certain terminology used in bioenergetics and since I 
use it throughout the chapter, I discuss it here. Food energy that is 
ingested is called ingestion (1) or consumption. Energy that is not 
absorbed through the gut is lost in the feces and called egested energy 
(F). Food absorbed into the blood may be stored or utilized. When 
utilized, most carbon is ultimately lost as CO,. When protein is 
catabolized, nitrogen is released and forms urea. This is voided in 
urine and the energy lost in these chemical bonds 1s excretory energy 
(U). Since it is now used throughout the ecological literature, I use 


816 Wunder 


EXCRETA, Urine (U) 


(Energy of Urine) 


DIGESTED ENERGY (D) 
(Digested Energy) RESPIRATION (M) 


(Respiration, cost 
of maintenance) 


ASSIMILATION (A) 


(Metabolizable Energy) 


INGESTION (1) 


(Gross Energy) 


PRODUCTION (P) 


(Energy of Production 


ECESTA, Feces (F) 


(Fecal Energy) 


Fic. 2. Conceptual relation of energy compartmentalization in mammals. Ter- 
minology is from Petrusewicz (1967). 


the terminology of Petrusewicz (1967). In his terminology the por- 
tion of consumption remaining after deducting egestion and excre- 
tion is called assimilation (A). This definition differs from that nor- 
mally used by physiologists and animal nutritionists who define 
assimilation as consumption minus egestion (Brody, 1945). This 
latter quantity is called digestion (D) by Petrusewicz. Fig. 2 outlines 
the relation between these parameters. 

Energy balance of an individual can be represented by the fol- 
lowing equation: 


A=I-(F+U)=M+P (1) 


where A equals energy assimilated into the body for use by an 
animal, I is total energy ingested, and F and U are energy lost in 
feces and urine, respectively. M is energy used for maintenance 
functions and P is energy expended and stored due to production 
(this may include growth of an individual and development of em- 
bryos and young). Digestibility refers to the amount of energy (or 
any nutrient under consideration) digested relative to that ingested 
and is usually referred to as a percent, which can be represented 
by the equation: 


Energetics and Thermoregulation 817 


D 
Percent digestibility = T x 100 (2) 


where D = (I — F). This is a useful concept because it gives an 
index to how much of the energy in a volume of food can be ex- 
tracted. For Microtus, such an index can be important because many 
voles eat vegetative plant parts which are not as highly digestible 
as fruit or seeds (Grodzinski and Wunder, 1975). When reading 
the literature one must be careful to note whether digestibility in- 
cludes or excludes urinary energy loss. Not all authors use the term 
the same way; however, urinary energy loss is usually no more than 
2-—4% of total ingestion (Grodzinski and Wunder, 1975). 

For estimating maintenance costs several approaches are used. 
In some energetics models standard metabolic rate (SM R—resting 
metabolic rate in thermoneutrality; see Bartholomew, 1977) mul- 
tiplied by some constant (usually 2 or 3) is used as an index to total 
energy costs (see Gessaman, 1973). Another approach devised by 
Grodzinski (see Grodzinski and Wunder, 1975) is to use the Av- 
erage Daily Metabolic Rate (ADMR). This is determined by mea- 
suring metabolic rate (usually oxygen consumption) for 24 h from 
an animal in a cage with food, water, nesting material, and occa- 
sionally an exercise wheel. ‘The idea is that this better approximates 
field conditions because the animal can be active and feeding (Grod- 
zinski and Wunder, 1975) and different temperatures can be used 
to simulate different seasons. The use of radioisotopes or other 
tracers has been used to estimate metabolism of mammals in the 
field (Mullen, 1973), but they have not been used with Microtus. A 
last approach is to combine field-time budget data with a metabolic 
model, which allows estimates of instantaneous rates of metabolism 
(Wunder, 1975). The first two methods give an integrated single 
value for metabolism over some time period (usually 24 h). Thus, 
there is no easy way to test the effects of environmental change or 
animal activity. By using a mechanistic model (Wunder, 1975), sen- 
sitivity analyses can be made to test for effects of changes in activity 
level or period and changes in nest or air temperature for various 
periods over a 24-h day. 


Energy Acquisition 


Mammals may use solar energy as a means of increasing their 
surface temperature and hence effectively increase insulation, thus 


818 Wunder 


sparing energy needed for thermoregulation (Campbell, 1977); but 
they cannot gain useful energy (for biochemical processes) from the 
sun or other sources of radiant energy (houses, barns, etc.). Given 
that they inhabit environments with grasses or other types of 
closed microcanopies, Microtus species probably use the sun little, 
if at all, for behavioral thermoregulation. Thus, accumulating food 
energy is the primary mode of energy acquisition for Microtus. This 
involves two general processes. Voles must find, handle, and chew 
food, and they need to digest and assimilate this food. 


Gathering Food 


Gathering food involves a variety of activities and the associated 
costs are not simply energetics, but include risks (ecological costs 
such as predation and social interaction). ‘There are numerous re- 
views on foraging strategies (Charnov, 1976; Pyke et al., 1977; 
Schoener, 1971); most theories consider the time and energy costs 
involved in finding and handling food. For Microtus, these may not 
be significant because most voles feed on grasses or dicot leaves; 
hence, finding food may not be a major energetic challenge for them 
(but see Batzli, this volume; Madison, this volume; Wolff, this 
volume). 

Furthermore, there are few references to species of Microtus stor- 
ing food as is frequently the case with cricetines and other small 
granivores (Barry, 1976). However, Wunder (1978a) suggested that 
clipped vegetation left by Mzcrotus may be used as a nutrient (es- 
pecially protein) source in winter. Wolff and Lidicker (1980) re- 
ported that yellow-cheeked voles (M. xanthognathus) store rhizomes 
for winter. 


Digestibility and Processing 


Although Microtus feed primarily upon vegetative plant parts, 
which are relatively easy to find, this does not necessarily mean that 
acquiring energy is not a problem for them because there is another 
step involved in “‘gaining” energy: digestion and processing. Micro- 
tus species may be food limited in how well and how fast they can 
digest and assimilate energy from a food source (White, 1978; Wun- 
der, 1978a). In this regard, energy acquisition entails three func- 
tions: 1) how well food can be processed (what is the digestibility), 
2) how fast a unit volume can be processed, and 3) how much 
volume can be processed per unit time. For Microtus, there is in- 


Energetics and Thermoregulation 819 


TABLE 1 


DIGESTIBILITY OF DIFFERENT Foops By Microtus 


Species 


M. californicus 


M. mexicanus 


M. ochrogaster 


M. oeconomus 
(European 
populations) 


M. pennsylvanicus 


M. pinetorum 


M. richardsoni 


Season and food 


Rabbit chow 


Bromegrass 
Ryegrass 
Lab chow 
Lab chow 


Summer; rat chow 


Winter; rat chow 
Rabbit chow 


Alfalfa 

Rabbit chow and alfalfa 

Bluegrass 

Tundra monocots 

Rat chow 

Spring; mixed grasses 
and herbs 

Summer; mixed grasses 
and herbs 

Autumn; mixed grasses 
and herbs 

Autumn; as above plus 
beets and roots of 
parsnip and carrots 

Oatmeal, lettuce, 
carrots 

Alfalfa 

Bluegrass, white clover 

Rat chow 


Bluegrass 


Red top (Agrostis 
stolonifera) 

Rat chow 

Lab chow 

Lab chow 


Lab chow 


Reference 


Batzli and Cole 
(1979) 


Bradley (1976) 
Bradley (1976) 


Cherry and Verner 
(1975) 


Batzli and Cole 
(1979) 


Bradley (1976) 
Gebczynska (1970) 


Golley (1960) 


Cowan et al. (1968) 

Johnson and Groepper 
(1970) 

Johanningsmeier and 
Goodnight (1969) 


Bradley (1976) 


Bradley (1976) 
Lochmiller et al. 
(1982) 


Bradley (1976) 


820 Wunder 


formation available on digestibility, but relatively little information 
is available on the latter two components. They are areas in need 
of much more study. 

The ability of small mammals to extract energy from food varies 
as a function of food type (animal matter, fruits, and seeds are more 
digestible than vegetative plant parts such as leaves and stems); it 
has been discussed by Grodzinski and Wunder (1975). Since most 
Microtus species are grazing herbivores (but see Batzli, this volume), 
in contrast to other small mammals, they should have lower di- 
gestibility, and must process more food to gain similar amounts of 
energy. Therefore one might predict that in times of energy stress 
microtines should change digestive efficiency, food type (to one more 
digestible), food volume processed per unit time, or some combi- 
nation. 

Unfortunately, most studies on digestibility have been performed 
with artificial diets (for example, lab chows), which don’t really tell 
us much about how much energy wild Muicrotus species may be 
getting from natural diets. What information there is in the liter- 
ature suggests that digestibilities for grazing herbivores range from 
60 to 70% (Grodzinski and Wunder, 1975); however, recently Bat- 
zli and Cole (1979) cautioned that these values actually range from 
30 to 90% depending upon species of herbivore and the plant ma- 
terial consumed. Table 1 compares some of the data from the lit- 
erature for digestibility in New World Microtus (Old World forms 
show similar values; Batzli and Cole, 1979; Grodzinski and Wun- 
der, 1975). As an example of this variability, Cole and Batzli (1979) 
found that the digestibilities of alfalfa and bluegrass, which have 
similar energy densities, were quite different (67% and 50%, re- 
spectively) in M. ochrogaster. Thus, we really need more careful 
studies of digestibility for natural diets of species of Microtus. 

Seasonal changes in plant composition can affect digestibility. 
Keys and Van Soest (1970) showed that digestibility decreased as 
the amount of cell-wall (fiber) content in the diet increased for M. 
pennsylvanicus. Thus, it is interesting to note that, although beach 
voles (M. breweri) eat primarily beach grass, they eat different parts 
at different seasons (Goldberg et al., 1980). In their study, Goldberg 
et al. (1980) noted that voles did not always choose those portions 
of the plant with the highest energy content. However, they did 
note that voles usually chose those plant parts which had the lowest 
cell-wall content (determined by neutral detergent fiber analysis) 


Energetics and Thermoregulation 821 


and speculated that beach voles “*. . . probably realize the advantage 
of increased assimilation of energy and nutrients... .” by selecting 
such foods. Energy content was not studied in that investigation but 
it poses the interesting possibility that energy levels (through di- 
gestibility) may have varied. More studies of a similar sort are 
needed to see whether Microtus species can select more digestible 
food at energetically stressful times of year. 

Certain chemicals in food affect digestibility. Kendall et al. (1979) 
found that certain allelochemicals in forage plants can inhibit forage 
intake by meadow voles (M. pennsylvanicus). Negus (pers. comm.) 
also found that the compound 6-MBOA in green vegetation in- 
creases growth in M. montanus (Sanders et al., 1981) without ne- 
cessitating significant increases in food intake over controls, imply- 
ing that some digestive or processing changes are occurring. And 
energy density in food itself may influence intake. Although Batzli 
and Cole (1979) suggested that microtines do not regulate food 
intake on the basis of energetic considerations alone, Kendall et al. 
(1978) and Shenk et al. (1970) showed that individual meal size in 
M. pennsylvanicus is regulated by energy content when energy con- 
centration in the food is high and by gastrointestinal fill when it is 
low. This suggests that energy density in food can be an important 
factor limiting energy accumulation and should be investigated more 
critically in Microtus, especially because there may be species dif- 
ferences in food digestibility. 

The only data relating to seasonal changes in digestibility inde- 
pendent of food type are those of Cherry and Verner (1975) for M. 
ochrogaster eating lab chow. Digestibility was 73% in summer and 
65% in winter. For Old World M. agrestis, Hansson (1971) also 
found digestibility of a mixed grass diet to be slightly lower in 
winter than in summer. 


Energy Allocation 


Maintenance 


Temperature regulation.—Since there are no reports of any species 
of Microtus (or any microtine) showing torpor either on a seasonal 
basis (hibernating) or for a shorter term (daily), they must always 
expend energy for thermoregulation. In contrast, many cricetines 
and other small mammals in similar habitats are capable of daily 


822 Wunder 


torpor, if not hibernation, when thermal stress is high (cold) or 
energy difficult to find (Wunder, 1978a). ‘Thus, thermoregulation 
is a major maintenance cost for species of Microtus, but one which 
allows them to be active throughout the year. 

Microtus species studied to date are able to regulate body tem- 
perature (T,) well. Their patterns of regulation relative to ambient 
temperature (T,) exposures are similar to other small placental 
mammals. In most studies, voles were not exposed to T, much 
below 0°C and all species studied were able to maintain T’, at that 
exposure (Beck and Anthony, 1971; Bradley, 1976; Hart, 1971; 
Packard, 1968; Wunder et al., 1977). In a study of microtine ro- 
dents, Bradley (1976) found that six species of Microtus (pennsyl- 
vanicus, ochrogaster, mexicanus, californicus, pinetorum, richardsont 
[=Arvicola richardsoni]|) were able to maintain T’, constant between 
T, exposures of 2-34°C. Above 34°C some species showed loss of 
T, regulatory ability. Beck and Anthony (1971) noted that at high 
T, (34 to 36°C) M. longicaudus showed obvious heat stress, but 
unlike some other small mammals (for example, Peromyscus), it did 
not show saliva-spreading to increase heat dissipation. ‘They sug- 
gested that Microtus may not handle heat stress as well as other 
forms. However, this needs to be investigated more closely because 
results of Bradley (1976) and Wunder et al. (1977) suggest that 
many species of Microtus, as well as other small mammals, regulate 
at these high T,s. 

There are no data suggesting that the level at which T, is reg- 
ulated changes seasonally; Wunder et al. (1977) showed that it 
definitely does not change in M. ochrogaster. 

Bradley (1976) concluded that Microtus species regulate T at a 
high level. Using a review table from Hudson and Brower (1971), 
he calculated the mean T, for 36 species of non-microtine rodents 
to be 37.3°C, whereas the mean T for six species of Microtus that 
he studied was 38.4°C. However, Wunder et al. (1977) did not find 
that M. ochrogaster regulated at such high levels. Prairie voles 
brought in from the field regulated at 37.8°C both in summer and 
winter. Perhaps this difference was due to technique. Our animals 
were fresh from the field and Bradley’s M. ochrogaster were from 
a lab colony at Cornell University. Interestingly, our animals, which 
were held for warm (30°C) or cold (5°C) acclimation in the lab for 
2 weeks, maintained higher T, (38.3°C) following acclimation (sim- 
ilar to Bradley’s voles in the lab). However, following lab accli- 


Energetics and Thermoregulation 823 


mation and exposure to various T,s, M. montanus showed a T, of 
37.8°C (Packard, 1968), and M. longicaudus showed a T, of 37.7°C 
(Beck and Anthony, 1971). Obviously, more studies need to inves- 
tigate the level of ‘I; regulation more rigorously. 

Thus, species of Microtus regulate T well, and none appear to 
resort to torpor. Considering that many species live in relatively 
cool regions or areas with cold winters, they have three methods to 
assist in maintaining T. They can 1) select warmer microclimates 
to reduce cold stress (for example, they can confine most activities 
to subnivean areas; Wolff, this volume); 2) increase insulation to 
reduce heat loss; and 3) increase thermogenic capacity. 

Insulation is the inverse of thermal conductance (TC); hence, the 
values of TC can be used as an index to insulation (Bartholomew, 
1977). Thermal conductances in New World Microtus are slightly 
less than those predicted by the allometric equation of Herreid and 
Kessel (1967; Table 2). However, they are generally not different 
from values for other similar sized cricetid rodents (Bradley, 1976). 
New world Muicrotus appear to show insulation values that are 
generally as expected for their body sizes, or slightly lower. In any 
case, they are not insulated extraordinarily for their size. 

There have not been many studies which investigated factors 
affecting insulation in species of Microtus. However, Bradley (1976) 
found that habitat influences insulative values. M. richardsoni had 
the lowest thermal conductance; it occurs in a cold, aquatic envi- 
ronment. M. pinetorum had the value closest to that predicted by 
allometry; it has somewhat semi-fossorial habits in a potentially 
more stable microhabitat. Wunder et al. (1977) found that thermal 
conductance varied seasonally in M. ochrogaster (Table 2)—it was 
higher in winter than in summer—and it was not affected by heat 
or cold acclimation in either season. Much of the change was due 
to body-size changes. Interestingly, Cherry and Verner (1975), us- 
ing different techniques, did not find significant seasonal changes 
in thermal conductance of M. ochrogaster in Illinois. 

In summary, there appears to be some capacity for modification 
of thermal conductance in relation to habitat and season, but, in 
general, New World Microtus do not show any strong adaptive 
trends in insulation as might be expected for a small, boreal, non- 
hibernating mammal. 

Insulation can also effectively be modified by nest behavior. M. 
xanthognathus (Wolff and Lidicker, 1980) and M. pinetorum are 


824 Wunder 


TABLE 2 
THERMAL CONDUCTANCE IN NEW Wor.Lpb Micro7us. SPECIES ARE LISTED 
APPROXIMATELY IN ASCENDING ORDER OF BODY Mass 


Thermal conductance! 


Deviation 
Body from 
mass Mea- Pre- prediction 
Species (g) sured dicted? (%) Reference 
M. longicaudus 25 0.87 0.97 — 0) Beck and Anthony 
(1971) 
M. pinetorum 26 0.92 0.95 = Bradley (1976) 
M. mexicanus 27 0.81 0.93 =13 Bradley (1976) 
M. montanus 31 0.82 0.87 =6 Packard (1968) 
M. ochrogaster 3i/ 0.75 0.79 = Cherry and Verner 
(summer) (1975) 
M. ochrogaster 39 0.73 0.77 =) Cherry and Verner 
(winter) (1975) 
M. ochrogaster 48 0.56 0.70 =2() Wunder et al. (1977) 
(summer) 
M. ochrogaster 38 0.71 0.78 =) Wunder et al. (1977) 
(winter) 
M. ochrogaster 50 0.61 0.68 —10 Bradley (1976) 
M. pennsylvanicus 37 0.72 0.79 = 9} Bradley (1976) 
M. pennsylvanicus 51 0.67 0.67 0 Morrison and Ryser 
ae (1951) 
M. californicus 43 0.66 0.73 0) Bradley (1976) 
M. richardsoni 51 0.56 0.67 —16 Bradley (1976) 


' Units of thermal conductance are cal g™' h7! °C™'. 
> Predicted values were calculated using the allometric relation of Herreid and 
Kessel (1967): thermal conductance = 4.91(g)~°”. 


social species which nest in groups during winter; thus, they may 
reduce their maintenance costs. 

Thermogenesis.—The other principal means Microtus species have 
to combat winter cold is to increase metabolism. ‘There are two 
metabolic components. One is minimal energy turnover, basal me- 
tabolism. In small mammals minimal energy needs are more ap- 
propriately described by standard metabolism (SMR; see Bartholo- 
mew, 1977) because the conditions necessary for defining basal 
metabolism are seldom met; yet the values reported are usually 
called basal as often as standard (see Grodzinski and Wunder, 
1975). The second component is the increase in metabolism above 
standard in response to low T, (thermoregulatory response), which 


Energetics and Thermoregulation 825 


involves shivering and non-shivering thermogenesis (Jansky, 1973; 
Wunder, 1979, 1984). 

The pioneering studies of Kleiber (1932) and Brody (1945) es- 
tablished that metabolism in mammals is related to body size. In 
their classic paper, Scholander et al. (1950) suggested that basal 
metabolism (BMR) is not adaptive and the major means of adap- 
tation to harsh environments is through thermal conductance (or 
insulation). More recently, however, several studies have shown 
that basal metabolism may be more adaptive than Scholander and 
his colleagues concluded. Many desert species show reduced BMRs 
(see Bartholomew, 1977; Hudson and Brower, 1971; Hudson et 
al., 1972) and some mammals have high BMRs (insectivores: Mor- 
rison et al. [1959], Neal and Lustick [1973]; Lepus americanus: Hart 
et al. [1965]; Tamiasciurus hudsonicus: Irving et al. [1955]; some 
pinnipeds and cetaceans: Hart and Irving [1959], Kanwisher and 
Sundes [1965]). 

It is frequently stated that microtines have high BMRs (Grod- 
zinski and Wunder, 1975; Hart, 1971). This conclusion is based 
primarily upon the paper by Packard (1968) in which he reported 
a BMR (SMR) for M. montanus of 75% greater than that predicted 
by the allometric equation of Kleiber (1961). He also reviewed the 
literature available at that time and reported high BMR from other 
studies of microtines. Subsequently Beck and Anthony (1971), fol- 
lowing Packard’s methods, reported the SMR of M. longicaudus to 
be 75% greater than predicted. However, these values are all arti- 
ficially high (Wunder et al., 1977). Most of the earlier reports dealt 
with animals that were not tested in thermoneutrality and hence 
had high responses because of added thermoregulatory costs (values 
can be found in Bradley, 1976, or Hart, 1971). Further, it is now 
well known that cold acclimation will cause an increase in SMR 
of many small mammals (Hart, 1971; Wunder, 1979). In attempt- 
ing to maintain M. montanus and M. longicaudus on “natural” 
environmental conditions in the lab both species were actually cold 
acclimated, which probably accounts for the higher value (75%) 
than predicted. Wunder et al. (1977) found that the SMR of M. 
ochrogaster freshly captured from the field varied with season; 
the effects of cold or heat acclimation also varied with season (‘Table 
3). Interestingly, when prairie voles (Wunder et al., 1977) were 
cold acclimated in winter (as in Packard’s [1968] study), they too 
showed SMRs 80% greater than predicted. Nevertheless SMR val- 


826 Wunder 


TABLE 3 
METABOLISM OF PRAIRIE VOLES DURING SUMMER AND WINTER. DATA ARE FROM 
WUNDER ET AL. (1977), WITH METABOLISM MEASURED AT 27.5°C. VALUES GIVEN 
ARE MEans +1 SD. NUMBERS IN PARENTHESES ARE SAMPLE SIZES 


Deviation 
from 

Metabolism predicted? 
Treatment! Body mass (g) O, g' h"! (ml) (%) 
Winter, field 38.5 + 4.5 (15) 2.16 + 0.34 (15) +41 
Winter, 5° 41.0 + 5.6 (8) 2.72 + 0.40 (8) +81 
Winter, 30° 48.4 + 8.9 (10) 2.19 + 0.25 (10) +52 
Summer, field 47.4 + 8.9 (9) 1.74 + 0.20 (9) +20 
Summer, 5° 50.0 + 4.7 (11) 1.76 + 0.12 (11) +23 
Summer, 30° 48.5 + 8.7 (10) 1.40 + 0.15 (10) 0 


' Treatments are voles fresh from the field or temperature acclimated at 5°C or 
30°C during winter or summer. 

> The following equation was used to estimate predicted metabolism: O, g™' h™' = 
3.8 W-°*, in ml (modified from Morrison et al., 1959) for calculation of percent 
deviation. 


ues for field animals were still higher than predicted by the Kleiber 
equation (20% in summer and 41% in winter). In addition, Bradley 
(1976) found that SMRs of the six Microtus species he studied (all 
under identical lab conditions) never deviated by more than 37% 
from the Kleiber prediction (Table 4), and M. ochrogaster was right 
on the predicted value. Thus, I conclude that SMRs of New World 
Microtus are higher than allometric predictions but only by 20- 
40%, not the 70-80% now given in the literature. 

Packard (1968) argued that since the subfamily Microtinae ap- 
parently evolved in boreal regions, it is reasonable to postulate that 
high metabolic rates are adaptive to allow for increased thermogene- 
sis during acute low-temperature stress. Jansky (1966) and Lechner 
(1978) independently showed that maximal metabolism in mam- 
mals is generally not greater than 7-10 times the basal rate. If such 
is the case then increases in SMR may allow for a higher maximal 
thermogenesis and hence tolerance to lower 'T, exposures. 

The ambient temperature at which a mammal maintains Ts, 
given a particular metabolic rate, can be calculated by rearranging 
the following equation (Bartholomew, 1977): 


MR = 1C(1;, = T,) (3) 


Energetics and Thermoregulation 827 


TABLE 4 
STANDARD METABOLIC RATES (SMRs) OF NEW WorRLD Microtus STUDIED IN THE 
SAME LABORATORY (DATA FROM BRADLEY, 1976). SPECIES ARE LISTED IN DES- 
CENDING ORDER OF SMR 


Deviation 
SMR from 

Body mass O,g 7! h"! Predicted predicted 
Species (g) (ml) SMR (%) 
M. pinetorum 25 1.98 1.60 +24 
M. pennsylvanicus 39 1.93 1.41 +37 
M. richardsoni 51 1.74 1.31 +33 
M. mexicanus 29 1.63 RDS +6 
M. californicus 44 1e55 1.37 rile) 
M. ochrogaster* 54 1.18 129 =e) 

* See: Rable:3: 
MR 
oi 4 


where IT’, is ambient temperature, I, is body temperature, TC is 
minimal thermal conductance, and MR is mass-specific metabolic 
rate. Using the allometric equations of Kleiber (1961) for SMR 
and Herreid and Kessel (1967) for TC, we can calculate the above 
values for any given body mass. If we assume maximal metabolism 
is seven times SMR (Lechner, 1978) and T, is 38°C, then we can 
use equation (4) to calculate the minimal T, which could be tol- 
erated without a drop in Ty. For a 40-g mammal this would be 
—37.4°C. If SMR were increased by 30% and maximal metabolism 
is seven times that value, then the lower temperature at which the 
mammal could maintain T, would be reduced to —60°C. 

Thus, increasing SMR could be an effective means of lowering 
the lower lethal temperature. However, energetically it is rather 
expensive because there is the increased metabolic cost in ther- 
moneutrality; that may be manifest all year although cold stress 
may only occur in winter. In fact, King and Farner (1961) argued 
that increased SMR for birds would not be adaptive because of the 
increased energy cost in thermoneutrality. Wunder et al. (1977) 
argued much the same for mammals (in that paper we incorrectly 
referred to seasonal changes in SMR as non-shivering thermoge- 
nesis; see below). It may well be that during their evolution, mi- 
crotines moved from a calorically dense, hard-to-find food (seeds) 


828 Wunder 


to a calorically more dilute but easy-to-find food (vegetative plant 
parts). Thus, if the processing capacity of the gut existed (see be- 
low), readily available food could be used, allowing for high me- 
tabolism. But, of course, the argument does not provide an expla- 
nation for why high metabolic rates exist. There may be several 
reasons why Muicrotus species have slightly high rates of metabolism, 
and adaptation to cold may be only one. McNab (1980) recently 
argued that mammals with high metabolic turnover rates (see Klei- 
ber [1975] for discussion of terminology) also show high potential 
for reproduction and hence population growth. Obviously this area 
needs more attention. 

An important factor involved in acclimatization to winter cold is 
the increased capacity for thermoregulatory non-shivering thermo- 
genesis (Jansky, 1973; Wunder, 1979, 1984). As discussed in Jan- 
sky (1973), a mammal metabolizes at the level of SMR in ther- 
moneutrality, but when exposed to lower ambient temperatures, it 
must increase thermogenesis. In small forms (<5 to 10 kg) the first 
mechanism used is non-shivering thermogenesis (NST); they then 
turn to shivering when NST capacity is nearly exhausted. ‘The 
advantage of NST over increases in SMR for increasing metabolic 
capacity is that it is only used at low T, and hence does not increase 
energetic costs when not in use (for example, in thermoneutrality). 
The capacity for NST in small mammals can be enhanced following 
cold exposure or in response to photoperiod changes so that total 
metabolic capacity can be increased during colder times of year and 
as needed. I (Wunder, 1981, 1984) found that M. ochrogaster 
changed capacity for NST from essentially no capacity to 17.1 cal 
g-' h-! following cold (5°C) acclimation in the lab. When tested 
fresh from the field in July prairie voles had no significant NST. 
The capacity increased during fall and animals caught in December 
showed 10.5 cal g-! h™'. This represented an increase of 136% over 
SMR, a significantly greater addition to thermogenesis than in- 
creased SMR following cold exposure. These winter NST values 
varied from year to year and probably depend upon the T’, to which 
the voles were exposed before capture (Wunder, 19786, 1984). 

Since most Microtus species are seasonally exposed to cold it 
would seem adaptive to stimulate NST capacity prior to cold ex- 
posure. It is now well established (Heldmaier et al., 1982) that 
short photoperiods can stimulate NST capacity in dwarf hamsters 
(Phodopus sungorus) and Peromyscus leucopus (Lynch and Gendler, 


Energetics and Thermoregulation 829 


NST 
mlO> (gh)! 


MONTH 


Fic. 3. Seasonal changes in non-shivering thermogenesis (NST) of M. ochrogas- 
ter. Symbols designate means; numbers are sample sizes; vertical lines represent +2 
SE. Unshaded triangles are voles held outside, and shaded triangles voles held at a 
constant lab temperature (23°C) but with a seasonally changing photoperiod. The 
shaded circle indicates animals fresh from the field in September; unshaded and 
shaded squares are animals held on long-day (15L:9D) or short-day (9L:15D) pho- 
toperiods, respectively, captured in September and tested in November and January. 


1980; Lynch et al., 1978). Initial experiments suggested that M. 
ochrogaster also was sensitive to photoperiod (Wunder, 1984). How- 
ever, voles were studied throughout the year only on natural pho- 
toperiods at a constant lab temperature of 23°C. Subsequent studies 
with voles exposed to long (15L:9D) and short (9L:15D) photo- 
periods throughout fall and winter suggested that they did not cue 
on photoperiod but had an endogenous rhythm for changes in NST 
(Wunder, pers. observ.; Fig. 3). Voles held on either photoperiod 
increased NST into winter just like the animals on natural photo- 
periods, with no statistically significant differences among the groups. 

Thus, NST is a powerful means whereby Microtus species en- 
hance their capacity for thermogenesis at low T, exposures without 
increasing energetic costs in thermoneutrality. The capacity can be 


830 Wunder 


enhanced by low T, exposure either chronically (Wunder, pers. 
observ.) or by short daily exposure to low T, (Wunder, 1981, pers. 
observ.). Although Phodopus sungorus and Peromyscus leucopus 
change NST capacity in response to short-day photoperiods in fall, 
it is still unclear whether M. ochrogaster does so or whether it has 
an endogenous rhythm for seasonal changes in NST. 

Activity.—The energetic costs of activity in species of Muzcrotus 
are largely unknown. To estimate such costs we need to know the 
cost of locomotion per unit time or speed and the amount of time 
spent in such activity each day (or year, depending upon the time 
frame). There are many studies of activity patterns and time spent 
active by Muicrotus for laboratory, enclosures, and field circum- 
stances (Wolff, this volume; Madison, this volume). The energetic 
costs of locomotion can be estimated from the allometric relations 
published by Taylor et al. (1982), but no Muicrotus species have 
been studied in this manner. Given that species of Muicrotus are 
active so often throughout a 24-h period, they should be good ex- 
perimental subjects for studies of activity costs. 


Production 


Growth.—The energetic consequences and costs of growth in New 
World Microtus have received some attention. Growth ties up en- 
ergy in tissue and includes the energetic cost of building such tissue. 
The cost for energy in tissue is relatively easy to measure and cal- 
culate; it is the product of the mass of tissue accumulated multiplied 
by its caloric density: 

Energy accumulated in increase 


| =. x caloric density. 
tissue during growth in mass 


In mature animals this tissue is usually fat; in young animals it 
reflects a combination of body components. But these potential dif- 
ferences have not been well studied. The costs for growth were 
reviewed by Grodzinski and Wunder (1975) and their conclusions 
remain unaltered. Energy content of tissue in Microtus species is 
1.03 kceal/g (Gorecki, 1965), so growth, at a minimum, costs that 
much per gram to produce. 

The other cost of growth is the metabolic cost of building addi- 
tional tissue. This topic has been addressed critically in the animal 
production literature but has not been pursued by ecologists, per- 
haps because it is not easy to measure. Theoretical considerations 


Energetics and Thermoregulation 831 


of the energy contained in, and biochemical processes associated 
with, fat disposition suggest that deposition of fat should cost little 
more than a 2% increase over normal metabolic costs (Baldwin and 
Smith, 1974). However, Jagosz et al. (1979) estimated empirically 
that tissue deposition costs are 8.57 kcal g"' in Muicrotus agrestis, 
and that overall cost of depositing and subsequently using energy 
stored in tissue (versus catabolizing the original foodstuffs) is 35% 
greater. Rock and Williams (1979) proposed that fat levels may 
serve as an index to the “condition” of an animal. They stressed 
M. montanus with low-food rations, low temperature, or both, and 
showed that fat reserves seem to serve as an energy store used in 
response to environmental stress. 

Rapid growth rates have been suggested as important features of 
animal life histories because they allow animals to reach maturity 
faster (see Case, 1978, for discussion). In addition, McNab (1980) 
argued that increased metabolic turnover rate (Kleiber, 1975) al- 
lows for faster individual growth which, in turn, allows for faster 
population growth. ‘Thus, it seems important to ask whether species 
of Microtus have increased growth rates compared to other similar- 
sized small mammals, because they can attain high population den- 
sities rapidly. Table 5 summarizes growth data for different species 
of Microtus during lactation; this is usually the period of fastest 
growth. Using this index, most species are comparable to other 
similar-sized small mammals (Table 5; Morrison et al., 1977). 
However, using a logistic growth constant (Ricklefs, 1967), McNab 
(1980) argued that microtines have higher growth rates than sim- 
ilar-sized cricetines. 

There are several factors which affect growth rates. They can be 
categorized as physical factors in the environment and social factors. 
There are numerous reports in the literature that many small mam- 
mals from boreal regions show lower body masses in winter than 
in summer (Brown, 1973, and references therein; Dehnel, 1949; 
Fuller et al., 1969; Schwarz et al., 1964). A number of species of 
Microtus are included in these studies. For a long while it was 
proposed that the reason lower average body mass was found in 
winter was because older, heavier individuals died, leaving only 
younger cohort animals. We now know that individual animals 
actually lose mass in winter or change growth rates. This was 
shown clearly in field studies with marked individuals of M. penn- 
sylvanicus (Brown, 1973; Iverson and Turner, 1974). Season ap- 
pears to affect growth in this species. Several factors could be im- 


832 Wunder 


TABLE 5 
GROWTH IN MALE AND FEMALE Mucrotus 


Growth rate! 


Adult % 


body Adult Lab or Season 
mass body field of 
Species (g) (g/d) mass study birth Reference 
M. abbreviatus 56 0.82 1.5 L — 
M. californicus 53 0.83 1.6 L — Hatfield (1935) 
62 0.98 1.6 L — Selle (1928) 
M. miurus 36 0.56 1.6 L — Morrison et al. (1977) 
M. montanus 40 0.63 1.6 — Seidal and Booth, in 
Innes and Millar 
(1979) 
M. oregoni 22 0.61 2.8 L — Cowan and Arsenault 
(1954) 
M. ochro- — 0.61 — L — Fitch (1957) 
gaster — 0.81 — L _— Richmond and Cona- 
way (1969) 
45 0.83 1.8 ? — Cooksey, in Innes and 
Millar (1979) 
_ 0.73 —- L _ Kruckenberg et al. 
(1973) 
M. oeconomus 45 0.79 1.8 IL; — Morrison et al. (1954) 
32 0.67 2A L — Morrison et al. (1977) 
M. pennsyl- 35 0.40 1.1 F June- Barbehenn (1955) 
vanicus Aug 
35 0.20 0.6 F July- 
Sept 
48 0.80 1.7 L — Hamilton (1937) 
29 0.67 pip) L — Innes and Millar (1979) 
40 0.65 1.6 L — Morrison et al. (1977) 
M. pinetorum? 28 Or 2 1.8 L _ Hamilton (1938) 
29 0.35% 1.2 L — Lochmiller et al. (1982) 


' Growth rates were usually calculated to 20 days of age. 

> Value of growth calculated to weaning at age of 17 days. 

>Growth rates were calculated as the average, for the average litter size (2.2), 
because growth varied with litter size. 


portant in causing (ultimate factors) or cueing (proximate factors) 
such changes. Two obvious factors that affect growth (and hence 
the energy costs of it) during winter are decreased quality of food 
and an increased proportion of energy intake necessary for ther- 


Energetics and Thermoregulation 833 


moregulation. These suppositions have not been tested directly; 
however, some component parts have. There have been no careful 
studies of the effects of temperature on growth in New World M:- 
crotus; however, Daketse and Martinet (1977) studied its effects on 
young M. arvalis and found (contrary to the suppositions above) 
that the young grow faster and larger when raised at lower tem- 
peratures (5°C) rather than at higher temperatures (22 or 33°C). 
We also know that lab animals (rats, pigs, etc.) grow larger when 
raised at low T, with plenty of food available. Thus, this growth 
may be due to high food availability (and high-quality food) while 
at low T,. 

It is also known that food quality or some factor in food may 
affect growth rates of Microtus species. Daketse and Martinet (1977) 
found that voles fed alfalfa harvested in spring grew faster and 
heavier than those exposed to the same conditions except fed alfalfa 
harvested in summer. In field and enclosure studies, Cole and Batzli 
(1979) demonstrated that M. ochrogaster grew faster and attained 
higher body mass when fed alfalfa than when sustained on blue- 
grass or prairie habitats. It is not known whether such effects are 
due to some special nutrient, to a caloric deficiency, or to some 
digestive difference. However, Batzli and Cole (1979) showed that 
M. ochrogaster does not do as well on monocots as do other Microtus 
species, but does grow better on dicots. It also may be that these 
forage effects are due to chemicals in the food acting as cueing 
agents to affect the animals’ physiology. Negus and his colleagues 
showed that specific chemicals in plants eaten by M. montanus can 
affect reproduction and growth (Berger et al. 1981; Negus, pers. 
comm.). 

One other physical environmental factor that may affect growth 
is photoperiod. Although growth of certain Muicrotus species varies 
with season (see above), the factors affecting such growth are not 
known. Pinter (1968) showed that photoperiod affected growth of 
M. montanus, and Petterborg (1978) showed that photoperiod may 
be the most important factor that affects differential growth (and 
hence maturation) in different seasonal cohorts for this species. More 
recently, Pistole and Cranford (1982) found that photoperiod affects 
growth in M. pennsylvanicus. In both species, young animals on 
long-day photoperiods grew faster than those on short-day photo- 
periods, and adult animals on long days maintained a higher body 
mass than those on short days. Further, adults on short days lost 
body mass, whereas long days stimulated growth to, or maintenance 


834 Wunder 


of, high mass. When animals in any treatment were switched to 
the alternate photic conditions they reversed their mass dynamics 
to reflect their photic environment. The energetic consequences of 
such changes are that animals on short days have less body mass to 
maintain, or with lower growth rates they have a lower energetic 
commitment to growth. 

Several studies suggest that social factors affect growth in species 
of Microtus. Batzli et al. (1977) found that when M. ochrogaster 
were raised in the laboratory in the same cage as littermates, they 
showed suppressed growth and maturation compared to controls 
raised alone in cages or when raised with strangers of the opposite 
sex. The pattern was not clear with M. pennsylvanicus, which the 
authors attributed to differences in habitat type and use. Baddaloo 
and Clulow (1981) subsequently showed that female M. pennsyl- 
vanicus grew faster (compared to controls) when exposed to males 
or male urine, even if separated by a wire barrier. They proposed 
that growth may be controlled by a pheromone in male urine. 

Beacham (1980) also reported that growth may be influenced by 
population density in M. townsendw and that this effect may be 
influenced by differential growth rate of “behavioral types” in the 
population. In this field study he showed that voles born in spring 
had higher growth rates than those born in any other season and 
that growth rates decreased in summer and autumn (a photoperiod 
effect ?). He also found that heavy males present in peak populations 
gained mass throughout the previous winter, whereas all other males 
lost body mass. Beacham and Krebs (1980) categorized voles as 
docile or aggressive and found that “docile” M. townsendu under 
50 g had faster growth rates than similar-sized aggressive ones. ‘The 
energetics of these changes in growth have not been investigated so 
we do not know whether the changes are simply the consequence 
of changes in food consumption, changes in relative efficiencies, or 
due to differential hormone levels. These studies clearly indicate 
that once voles are weaned and exposed to the physical and biolog- 
ical environment many factors may affect their growth rates. 

Reproduction.—A convenient way to envision the costs of repro- 
duction is to divide them into those occurring during gestation and 
those during lactation. Such a division allows one to separate better 
the adaptive responses shown in mammals. Costs incurred during 
each phase of reproduction are quite different, both in magnitude 
and mechanism. 


Energetics and Thermoregulation 835 


TABLE 6 
INCREASE IN ENERGY CONSUMPTION FOR REPRODUCTION IN SPECIES OF Muicrotus 


Increase 
over non- 
reproductives 
(%) 


Body EE 
size Litter Gesta-  Lacta- 

Species (g) size tion tion Reference 
Mnicrotus arvalis 25.3' 4.25 S2 133 Migula (1969) 
Microtus pennsylvanicus 29.42 5.05 36 122 Innes and Millar 

(1981) 
Microtus pinetorum 28.9? 2.20 — 47.5 Lochmiller et al. 


(1982) 


' Body mass of non-pregnant female. 
? Post-partum body mass. 
‘Mean mass throughout lactation. 


In both cases energy needs can be divided into two categories: 1) 
increased energy needed to gather more energy from the environ- 
ment; and 2) increased energy to digest food and form the com- 
pounds used by the embryo or young for growth and maintenance. 
During gestation the embryo essentially uses the same foodstuffs as 
the mother because transfer is via the vascular system, and since 
the embryo is inside the female, she need not produce extra heat to 
keep it warm. Once the embryo is born there should be increased 
costs for maintenance because the young is outside the female and 
must be brooded for thermoregulation. Also, as the embryo becomes 
larger, its total energy needs for continued growth will be greater. 

To my knowledge there have been only two studies of the direct 
energetic costs for reproduction in New World Microtus (Innes and 
Millar, 1981; Lochmiller et al., 1982) and three for one species of 
Old World Microtus (Kacmarski, 1966; Migula, 1969; Trojan and 
Wojciechowska, 1967). In all cases the actual costs can’t be frac- 
tionated further than increased costs due to gestation and those due 
to lactation. In these studies food consumption of pregnant or lac- 
tating females was simply compared to similar-sized non-reproduc- 
tive females in the laboratory. Thus, we really have no estimates of 
the increased cost for gathering food during reproduction and in no 
studies were the animals on natural diets. 


836 Wunder 


Both gestation and lactation are energetically expensive. Al- 
though there are few data for Microtus, energy needs during ges- 
tation increase with larger litter sizes (Grodzinski and Wunder, 
1975), and the same is true for lactation in many species, including 
Microtus pinetorum (Lochmiller et al., 1982). Table 6 summarizes 
the increased energy requirements from reproduction in voles. Ges- 
tation increases costs 30% or more and lactation usually entails 
increases of more than 100-—120% over non-lactation. This appears 
true not only for M. arvalis and M. pennsylvanicus, but also many 
other small mammals (Mattingly and McClure, 1982; Millar, 1979; 
Randolph et al., 1977). However, Lochmiller et al. (1982) reported 
a somewhat low value for M. pinetorum, which characteristically 
has small litter sizes; that may be the reason for the low increase 
in total energy needs. Lochmiller et al. (1982) suggested that this 
trait, along with efficiency of energy conversion to young, may allow 
pine voles to breed throughout winter in some years. However, voles 
and lemmings with larger litter sizes and masses also occasionally 
breed in winter (Taitt and Krebs, this volume). 

Many incidental observations and studies suggest that species of 
Microtus may be near their limits for food gathering and processing 
during reproduction. Although not rigorously tested, modelling of 
energy flow for M. arvalis suggests this (Stenseth et al., 1980). 
Molt-pattern changes in reproductive and non-reproductive M. 
brewer. also suggest that reproduction cannot be maintained at the 
same time as certain molts (Rowsemitt et al., 1975). And the ob- 
servation that many species do not breed in winter when thermo- 
regulatory costs are high suggests that added costs during repro- 
duction cannot be met (Millar, 1978; Wunder, 1978a). 

Given those constraints, it is interesting that, although small 
mammals in general, and Muicrotus species in particular, increase 
energy intake during reproduction, there are no indications that 
process time is decreased (energy cannot be gained more quickly 
from a unit of food). And there is good evidence that percent diges- 
tion and assimilation do not increase in Microtus during reproduc- 
tion (Innes and Millar, 1979; Johnson and Groepper, 1970; Loch- 
miller et al., 1982; Migula, 1969). Thus, the only means species of 
Microtus appear to use to increase energy accumulation for repro- 
duction is increased food intake. 


Energetics and Thermoregulation 837 


Energy-Flow Models: 
Individuals and Populations 


To describe energy flow through an individual mammal, one 
simply integrates the metabolic costs discussed in this chapter over 
some unit of time. This can be done using an Average Daily Met- 
abolic Rate model or some combination of models to integrate met- 
abolic costs (Wunder, 1975) with a time budget (see Methods). For 
mammals in general this approach is well described in Grodzinski 
and Wunder (1975) and Ferns (1980). 

To discuss the effects of small mammal populations on commu- 
nity function and the role of energetics in such functions, investi- 
gators occasionally have generated energy flow models for popula- 
tions. These models give some insight into: 1) how much of the 
energy flowing through a community is channeled through small 
mammals (voles for our purposes), and hence how voles may influ- 
ence production or community processes; 2) how seasonal bottle- 
necks in energy availability or need may influence population pro- 
cesses; and 3) how patterns of community function vary in different 
ecotypes. The models are essentially population integrations of the 
energy costs associated with individuals. Although these models are 
discussed in Grodzinski and Wunder (1975), a more complete and 
lucid discussion is given by Ferns (1980) using M. agrestis as an 
example. 

There have been very few studies of the population energetics of 
New World Microtus. Golley (1960) published the earliest study 
on population energetics in M. pennsylvanicus. Grodzinski (1971) 
undertook studies on population energetics of M. oeconomus in Alas- 
ka. Studying the energetics of small mammals in grassland ecosys- 
tems, French et al. (1976) found highest energy turnover (172 x 
10° kcal/ha) in tallgrass prairie systems dominated by M. ochro- 
gaster. However, the efficiency of biomass supported was not as 
great as in northern shortgrass prairie systems that did not have 
any species of Microtus. Using Clethrionomys rutilus and Microtus 
oeconomus, Whitney (1977) tested the hypothesis that arctic and 
subarctic communities have low production, and found the hypoth- 
esis unsupported. He also found that maintenance energy costs for 
both species during winter were double summer costs (despite re- 


838 Wunder 


production only in summer), in contrast to findings of Gebcezynska 
(1970). Using population energetics, Stenseth et al. (1980) sug- 
gested that energy considerations limit reproduction in M. agrestis. 
In analyzing a number of small mammal energy models including 
some for M. oeconomus, M. pennsylvanicus, and several Old World 
species, Ferns (1980) suggested that populations inhabiting open 
habitats (such as species of Microtus) have higher annual energy 
flow than those in more mature habitats. Production efficiency and 
ecological efficiency of his M. agrestis population were about 1%. 

Englemann (1966) suggested that there is a linear relationship 
between annual production and respiration per unit area in animal 
populations. McNeill and Lawton (1970) and Humphreys (1980) 
re-examined that suggestion and found that it is apparently true. 
Based on these relations, Humphreys (1980) separated homeo- 
therms into four groups, one of which is “small mammal commu- 
nities.” Muicrotus are not notably different from other small mam- 
mals in this relationship. 


Future Studies 


I have indicated throughout the text where knowledge is lacking; 
I only highlight certain questions here. Microtus species provide 
excellent models for studies of small mammal energetics because 
they are the smallest mammals that eat relatively high-fiber (en- 
ergetically dilute) food and yet live in cool environments. So why, 
and by what mechanism, do they have BMRs 20-40% greater than 
expected? Is it related to thyroxine and high cellular metabolism, 
or do voles simply carry more gut (a metabolically active tissue) to 
digest their food than similar-sized mammals? McNab (1980) ob- 
served that populations of mammals with high BMRs have high 
rates of natural increase. Perhaps these mammals have more gut to 
process more food for allocation to production, and increased BMR 
relates to more gut tissue. Or is BMR simply related to thermo- 
regulatory needs? We need detailed, long-term studies on the bal- 
ance of energy gain and loss. Are voles limited, temporarily or 
seasonally, in their capacity to find and process enough food for 
several simultaneous energy-demanding functions (for example, molt 
and reproduction, cold-induced thermogenesis and reproduction) ? 
More data are needed on reproductive costs of populations with high 


Energetics and Thermoregulation 839 


and low litter sizes. The phenomenon of seasonal body-mass change 
needs long-term study because changes do not always occur (Wun- 
der, 19785). Such studies would allow better documentation of year- 
ly patterns; then questions about the mechanism and significance 
of such changes could be better formulated. These studies should 
consider not only climatic factors but also fiber content of food and 
6-MBOA levels (Sanders et al., 1981). Lastly, more detailed studies 
of limits to energy gain are needed. How important are behavioral- 
physiological factors in allowing voles to select low-fiber food (as 
in Goldberg et al., 1980) relative to their physiological ability to 
digest these foods (Batzli and Cole, 1979)? We know nothing at all 
about food passage rates or gut-size variation in voles and their 
effects on energy gain, although we are pursuing the latter. 


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RICKLEFS, R. E. 1967. A graphical method of fitting equations to growth curves. 
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Rock, P., AND O. WILLIAMS. 1979. Changes in lipid content of the montane vole. 
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RowseMITT, C., T. H. Kunz, AND R. H. TAMARIN. 1975. The timing and patterns 
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SANDERS, E. H., P. D. GARDNER, P. J. BERGER, AND N. C. NecGus. 1981. 
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GENETICS 
MICHAEL S. GAINES 


Abstract 


IFFERENT kinds of genetic variation in New World Microtus 
D are reviewed. This variation ranges from traits controlled by 
single genes such as coat color and allozymes to those that are 
polygenic such as body weight and agonistic behavior. Coat color 
polymorphisms reported in the literature are unsatisfactory from a 
genetic standpoint because the mechanism of inheritance of most 
polymorphisms is unknown. At the karyotypic level, there is little 
variation in diploid chromosomal number or fundamental number. 
Karyotypic analyses have been used primarily as tools in elucidating 
systematic relationships within the genus. The frequency distribu- 
tions of genic diversity values based on allozymic variation for M:- 
crotus and other mammal species indicate similar levels of genetic 
variation. There is some evidence from physiological components of 
fitness and perturbation experiments that natural selection main- 
tains polymorphisms at a few electrophoretic loci. However, non- 
selective forces also play a significant role in gene-frequency change 
over short time periods. I conclude that changes in gene frequency 
at electrophoretic loci are effects of demographic changes and are 
not causally related to population cycles. There is a dearth of studies 
on the inheritance of quantitative traits in the genus. Heritabilities 
for dispersal behavior, aggressive behavior, growth rates, and age 
at sexual maturity have been estimated from full-sib analysis in M. 
townsend populations. Three areas are profitable for future re- 
search: 1) the effect of social dynamics on genetic structure of pop- 
ulations; 2) inheritance and evolution of quantitative traits; and 3) 
the application of new molecular techniques to assess genetic vari- 
ation. 


Introduction 


In a review of this scope an obvious starting point is to extoll the 
virtues of Microtus as a suitable organism for genetic investigations. 


845 


846 Gaines 


Because there is detailed information on the ecology of microtine 
rodents, it affords investigators the opportunity of combining ge- 
netics and ecology in the study of natural populations. This syn- 
thetic approach taken by ecological geneticists will enhance our 
understanding of evolutionary processes in natural populations. ‘The 
periodic fluctuations in population density exhibited to some degree 
by most microtine species enable the ecological geneticist to measure 
the direction and intensity of natural selection during different phases 
of a population cycle that consists of an increase, peak, and decline 
phase. The synchrony in microtine fluctuations reported over large 
geographic areas (see Taitt and Krebs, this volume) also allows for 
spatial replication. 

The major theme of this chapter is the kinds of genetic variation 
found in Microtus. The variation discussed spans the spectrum from 
traits controlled by single genes, such as coat color and electro- 
morphs, to those that are polygenic, such as body weight and ago- 
nistic behavior. Wherever possible, I examine the evolutionary sig- 
nificance of the variation. I conclude with a section on areas of 
genetic research that may prove to be fruitful in the future. 


Pelage Coloration 


The pelage of Microtus varies from pale yellow to dark brown 
or black. Variation in coat color is due to differences in the number 
of completely black hairs and the width of a subapical band of 
yellow pigment on black hairs. A summary of coat-color variants 
reported in six species of Microtus is given in Table 1. The list is 
unsatisfactory from a genetic standpoint for several reasons. First, 
there may be problems with the nomenclature because few attempts 
have been made to cross-check new color morphs with actual spec- 
imens of similar phenotypes reported in the literature. Thus, either 
the same morph may be renamed by different investigators or dif- 
ferent morphs may be given the same name. A case in point is the 
grey-eared morph in M. ochrogaster (Semeonoff, 1973), which is 
similar in overall appearance to a smoky morph in the same species 
reported by Pinter and Negus (1971). However, after direct com- 
parison, Semeonoff concluded that the two morphs had very differ- 
ent phenotypes. Second, in only a few cases have investigators per- 
formed the appropriate breeding studies to determine the genetic 
basis of the color polymorphism. 


847 


Genetics 


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Genetics 849 


Finally, there is little information on the adaptive significance of 
coat color polymorphisms in natural populations of Microtus. A 
notable exception is the buffy coat color in Muicrotus californicus. 
Lidicker (1963) found that buffy coat color is due to a single-locus 
recessive mutation. The wild type agouti allele (+ ) is completely 
dominant over the buffy allele (4/) so that the +/+ homozygote 
and bf/+ heterozygote are phenotypically indistinguishable. Lid- 
icker (as reported by Gill, 1977) monitored the frequency of buffy 
in a population of M. californicus over a 7-year period on Brooks 
Island off the coast of California. Gill (1977) reported that the 
frequency of buffy individuals in the population fluctuated season- 
ally and was highest after the breeding season. Changes in the 
frequency of buffy individuals lagged behind changes in population 
density. In laboratory crosses, heterozygous females (b//+ ) had a 
higher mean number of offspring born per month and mean num- 
ber of offspring weaned than both homozygotes, and heterozygous 
males were more fertile than other males. Gill (1976) proposed that 
the seasonal decrease in the frequency of buffy homozygotes resulted 
from differential predation and that the subsequent increase during 
the breeding season resulted from the high fertility of heterozygotes. 
If Gill’s proposition is correct, this form of overdominance could 
maintain the coat color polymorphism in this island population. In 
support of her hypothesis she noted that on the mainland where 
predation is high, the buffy phenotype is almost absent. Clearly, 
more studies of this type are necessary before we can begin to 
understand the mechanisms for maintenance of coat color polymor- 
phisms in natural populations of Microtus. 


Cytogenetics 


Karyotypic analyses of new world Microtus have been used pri- 
marily as tools in elucidating systematic relationships within the 
genus. Many species of Microtus differ in both diploid chromosome 
number and fundamental number (Table 2). The latter is deter- 
mined from the total number of autosomal chromosome arms, 
counting one for each telocentric or acrocentric chromosome and 
two for each metacentric chromosome. There is little variation in 
diploid chromosomal number and fundamental number within 
species because discoveries of this sort usually lead to new species 
assignations. For example, there was some disagreement whether 


850 Gaines 


TABLE 2 
DIPLOID AND FUNDAMENTAL CHROMOSOME NUMBERS OF NEW WORLD SPECIES OF 
Microtus. SOURCES ARE HSU AND BENIRSCHKE (1967-1975) AND MATTHEY (1973) 
UNLESS OTHERWISE NOTED 


Species Diploid number Fundamental number 
Microtus brewert' 46 50 
Microtus californicus* D2, 99, 24. 60, 61, 62 
Microtus canicaudus 24 48 
Microtus longicaudus 56 84 
Microtus mexicanus 44 54 
Muicrotus montanus? 22, 24 40, 44 
Microtus ochrogaster 54 64 
Microtus oeconomus 30 52 
Microtus oregoni 179;186 a2 
Microtus pennsylvanicus 46 50 
Microtus pinetorum* 62 62 
Muicrotus townsend 50 48 
Microtus xanthognathus> 54 62 


' Fivush et al. (1975); ? Gill (1982); > Judd et al. (1980); * Beck and Mahan (1978); 
> Rausch and Rausch (1974). 


the species M. canicaudus and M. montanus should be considered 
as conspecific (Johnson, 1968). The former has a limited range in 
Oregon and Washington, whereas the latter is widely distributed 
throughout much of the western United States. The diploid number 
of both species is 24 and all the autosomes are metacentric. How- 
ever, the X-chromosomes differ; they are acrocentric in M. montan- 
us but metacentric in M. canicaudus. In addition, there are subtle 
differences in the structure of the autosomes: three pairs of smaller 
autosomes are similar in size in M. canicaudus but dissimilar in M. 
montanus. On the basis of these differences in karyotype, Hsu and 
Johnson (1970) supported the view that M. canicaudus should be 
given full species status. 

There are a few exceptions to the rule of constant chromosomal 
number within species of North American Microtus. Geographic 
variation in diploid chromosomal number has been reported for M. 
longicaudus (Judd and Cross, 1980). Specimens examined from Ar- 
izona, Colorado, and New Mexico all have a diploid number of 56 
with 10 pairs of medium- to large-sized biarmed chromosomes, 12 
pairs of small to large acrocentric, and five pairs of small metacen- 
tric chromosomes. Six other chromosomal forms (2n = 57, 58, 59, 


Genetics 851 


62, 66, and 70) were observed from southern Oregon and northern 
California. The major differences in the California and Oregon 
races compared with the 2n = 56 race were six pairs of metacen- 
trics, only 11 pairs of acrocentrics, and variations in number of 
supernumerary or minute chromosomes. The absence of a pair of 
acrocentrics and an extra pair of metacentrics suggests that this was 
a result of a pericentric inversion. Although supernumerary chro- 
mosomes have been found in other rodent species (for instance, 
Reithrodontomys [Shellhammer, 1969] and Perognathus [Patton, 
1977]), this is the only case reported to date for a Microtus species. 

Gill (1982) found a polymorphism in chromosomal number in 
M. californicus populations. Individuals have diploid numbers of 
52, 53, or 54 chromosomes with fundamental numbers ranging 
from 60 to 62. Furthermore, based on breeding data, Gill (1980) 
suggested that M. californicus is undergoing speciation. Finally, 
Fredga and Bergstr6ém (1970) reported a chromosomal polymor- 
phism in M. oeconomus caused by a centric fission of one chromo- 
some pair. In an isolated population in northern Europe, animals 
with 2n = 31 and 2n = 32 were captured. Although this is not a 
New World microtine, it is nominally the same species as that 
which occurs in North America. 

The differential staining of specific regions of chromosomes also 
has been useful in determining differences and similarities between 
populations. In a thorough analysis of chromosomal variation in 
M. montanus, Judd et al. (1980) compared populations from Ari- 
zona and New Mexico (2n = 24) to a population from Oregon 
(2n = 22). One conspicuous difference between the two karyotypes 
was the absence of the smallest pair of metacentrics (pair 8) in the 
22-chromosome form. The following differences were observed be- 
tween the two forms with respect to constitutive heterochromatin 
(C-bands): 1) the 22-chromosome form had smaller C-bands com- 
pared to the 24-chromosome form; 2) in the 22-chromosome form, 
pair 5 had much less centromeric heterochromatin; and 3) in both 
forms, pairs 9, 10, and 11 had little or no heterochromatin, the 
C-banded X-chromosomes were identical, and the Y-chromosome 
was totally heterochromatic. The G-banding patterns of the two 
forms were almost identical; the only difference was in the short 
arms of chromosome 2. The location of nucleolar organizing regions 
(NORs), identified by the silver staining method of Hubbell and 
Hsu (1977), were invariable in both karyotypes; chromosomal pair 


852 Gaines 


10 had NORs on the long arm and pair 11 had them on the short 
arm. On the basis of their karyotypic analysis, Judd et al. (1980) 
suggested that the two forms of M. montanus might be specifically 
distinct. Nadler et al. (1976) also used G-banding techniques to 
investigate interpopulational variation of Holarctic microtine species; 
they found similar patterns in Alaskan and Siberian populations of 
M. oeconomus and Clethrionomys rutilus. 

Recently, there has been a considerable amount of interest in the 
rates of karyotypic change and direction of evolution. Maruyama 
and Imai (1981) estimated the evolutionary rates of change of mam- 
malian karyotypes by making pairwise comparisons of chromo- 
somal number and arm number of species belonging to each genus. 
They calculated probabilities, which decrease exponentially with 
time, that two randomly chosen species from a given genus would 
have the same karyotype. Assuming that the average divergence 
time of a mammalian species from a common ancestor is 2.5 x 10° 
years, they estimated the rate at which a karyotype changes in unit 
time for different genera. The genus Microtus had the highest rate 
of karyotypic change (8.18 x 10~-’ chromosomal or arm number 
changes per year) of the 18 rodent genera included in the study. 

Three hypotheses have been proposed for the mode and direction 
of chromosomal evolution in mammals: fusion hypothesis (Ohno, 
1969), fission hypothesis (Todd, 1967), and the modal hypothesis 
(Matthey, 1973). The fusion hypothesis assumes that the ancestral 
karyotype consisted of a large number of acrocentric chromosomes 
which were reduced in number through a series of pericentric in- 
versions and centric fusions. Fedyk (1970) proposed that in the 
gregalis-group of Microtus the primary mechanism of karyotypic 
evolution in the subarctic species involved centric fusions, whereas 
in the Nearctic species of the group, pericentric inversions were 
predominant. Conversely, the fission hypothesis assumes that an- 
cestral mammals had a low diploid number which generally in- 
creased under the influence of centric fissions. The modal hypoth- 
esis assumes that ancestral mammals had a diploid number near 
the present mode and that chromosome numbers moved upward or 
downward. 

Matthey (1973) suggested that the modal hypothesis best ex- 
plains chromosomal evolution in the subfamily Microtinae because 
32 of the 78 species examined have 54 or 56 chromosomes. Matthey 
(1973) stated that this subset is “exclusively found in the genera 


Genetics 853 


regarded by taxonomists as the most primitive on the basis of their 
morphology.” Considering that only five species of microtines have 
diploid numbers greater than 56, most of the Robertsonian rear- 
rangements occurring over evolutionary time had to be centric fu- 
sions. Matthey’s hypothesis for chromosomal evolution in Microtus 
is reasonable only if fusions are the predominant Robertsonian rear- 
rangement over evolutionary time. However, in a recent study, Imai 
and Crozier (1980) presented evidence from a statistical analysis of 
mammalian karyotypes which strongly supports fission rather than 
fusion as the predominant Robertsonian rearrangement. Needless 
to say, the directionality of karyotypic evolution in New World 
Microtus is still open to interpretation. 

Karyotypic analyses promise to be useful tools for elucidating 
systematic relationships within the genus Microtus and assessing 
the amount of chromosomal variation within species. In many stud- 
ies to date karyotypic analysis was performed on only a few indi- 
viduals. Moreover, as one progresses to finer levels of karyotypic 
analysis (for example, C- and G-banding), sample sizes decrease, 
and in fact, some banding studies are based on only one individual 
from each species. As both the number of species studied and the 
sample sizes increase, karyotypic analysis, especially using differ- 
ential staining techniques, will undoubtedly increase our under- 
standing of the organization of the genetic material. 


Allozymic Variation 


With the widespread application of protein electrophoresis, es- 
timates of genic variation have now been determined for hundreds 
of organisms (Nevo, 1978; Selander, 1976). Surprisingly, Microtus 
has been relatively neglected in surveys of allozymic variation. I 
have summarized the available data in Table 3. ‘The most thor- 
oughly studied Microtus species to date is M. californicus (Bowen 
and Yang, 1978) in which 28 proteins were examined. Fewer pro- 
teins are represented in the remaining studies in Table 3, primarily 
because allozymes were used as genetic markers in live-trapping 
programs that prohibited sacrificing animals. ‘Thus, investigators 
relied exclusively on plasma or hemolysate, obtained from blood 
samples, for electrophoresis. More protein polymorphisms were re- 
vealed when a wider range of tissues was included in the analysis. 


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Fic. 1. The frequency distribution of genic diversity (1) for species of Microtus 
(see Table 3) compared to other mammals (from Smith et al., 1975). Abbreviation: 
N, number of loci. 


For instance, Bowen and Yang (1978) found nine polymorphic 
proteins in kidney tissue alone (Table 3). However, the genus in- 
herently may have low levels of variation because of periodic bot- 
tlenecks that occur during low phases of density cycles. 

Frequency distributions of genic diversity values for Microtus and 
other mammal species (Smith et al., 1978) are presented in Fig. 1. 
The distributions are similar but there is a slight excess of loci with 
relatively high genic diversity (for example, 0.4-0.5) in Microtus 
species. Certain loci tend to appear in this range. In particular, 
leucine aminopeptidase has a genic diversity of about 0.45 in four 
of the seven species of Microtus included in Table 3. Several other 
loci have relatively high genic diversities, including the esterases, 
transferrin, and 6-phosphogluconate dehydrogenase. These geneti- 
cally diverse polymorphisms have been studied more extensively to 
investigate the roles of different evolutionary forces in maintaining 
protein polymorphisms in Microtus populations. 

Recently, some doubts have been raised about the reliability of 


Genetics 857 


certain electromorphs as genetic markers in Microtus populations. 
McGovern and Tracy (1981) exposed field caught M. ochrogaster 
in Colorado to different temperature regimes in the laboratory and 
found changes in the mobility of electromorphs at the TF and LAP 
locus. Although there is extensive mating data for both the LAP 
and TF systems (Gaines and Krebs, 1971), the results are incon- 
clusive because animals were housed at a constant temperature. 
Mihok and Ewing (in press) found complete reliability in TF and 
LAP electromorphs in M. pennsylvanicus. Because McGovern and 
Tracy’s results have serious implications on the interpretation at 
genic variation in the genus, their experiments need to be repeated 
further. 

Several different approaches have been taken to measure the di- 
rection and intensity of selection on structural proteins in Microtus 
populations. Kohn and Tamarin (1978) plotted Ap, (=p,,, — p,) 
against p, from successive trapping periods at the TF and LAP loci 
in populations of M. brewer: and M. pennsylvanicus. They argued 
that a significant negative regression around the point where Ap, = 
O would be evidence for a stable polymorphism. They calculated 
regressions for M. brewer (for 7f*) and for M. pennsylvanicus (for 
7f* and Lap‘) in four areas and by sex within each area. All 24 
regression lines had negative slopes and ten were significantly dif- 
ferent from 0. Thus, Kohn and Tamarin (1978) concluded that the 
polymorphisms were maintained by selection. 

However, the method of regressing Ap on p has been shown to 
be inadequate for estimating selection pressures in populations. Kir- 
by (1974) showed that the regression coefficient, calculated from 
data obtained from a sequential census of one population, does not 
provide an unbiased estimate of the amount of immigration or se- 
lection maintaining an equilibrium gene frequency. Furthermore, 
Whittam (1981) demonstrated that a negative regression coefficient 
is expected when sequential gene frequencies are simply random 
numbers from the interval [0, 1] of a uniform probability distri- 
bution. Using computer simulations, Whittam (1981) randomly 
sampled gene frequencies from a uniform probability distribution, 
plotted Ap versus p, and obtained a significant negative regression 
coefficient with the regression line explaining about 60% of the 
variance in Ap. A comparison of Kohn and Tamarin’s (1978) re- 
sults and the confidence limits for the regression coefficients indi- 
cated that about half of the slopes obtained from natural popula- 
tions did not differ from the negative slopes obtained by the 


858 Gaines 


TABLE 4 
ESTIMATES OF THE DEVIATION OF PROPORTIONS OF HOMOZYGOTES FROM 
HarRDY-WEINBERG PROPORTIONS (H) DURING DENSITY FLUCTUATIONS OF Microtus 
pennsylvanicus. DATA ARE COMBINED FROM THREE LIVE-TRAPPING GRIDS. NUMBERS 
IN PARENTHESES ARE ESTIMATES OF THE STANDARD ERROR OF H (FROM BIRDSALL, 


1974) 
Diag Or TF locus LAP locus 
cycle Males Females Males Females 
Increase .007 (.014) —.009 (.015) =,037* (016): =.021:G018) 
Peak 005 (.013) 004 (.014) —.025 (.014) —.002 (.016) 
Decline 10652 :(0 24) .050F (0.29) 025 (.027) 011 (.031) 


* Significant deviation from Hardy-Weinberg proportions (P < 0.05). 
+ Significant difference in heterozygosity between males and females (P < 0.05). 


simulation. A second analysis of genetic drift with a small amount 
of migration and different population sizes revealed many signifi- 
cant regression coefficients were negative and many were significant 
(357 out of 1,000 simulations) in the absence of selection. Thus, 
the interpretation of a negative slope as evidence for selection main- 
taining a polymorphism is questionable. 

Birdsall (1974) used deviation of genotypic frequencies from 
Hardy-Weinberg equilibrium as evidence for selection acting on 
the TF and LAP loci in fluctuating populations of M. pennsylvan- 
icus. He estimated the excess proportions of each homozygote, H, 
following the method of Smith (1970). Estimates of the deviation 
of the proportions of homozygotes from Hardy-Weinberg equilib- 
rium during different phases of the density fluctuation for three 
trapping grids combined, treating sexes separately, are given in 
Table 4. Birdsall (1974) interpreted the deviations in the proportion 
of genotypes at the two loci as evidence for natural selection and 
not a consequence of non-selective forces because the two loci ex- 
hibited different patterns of deviation during the density cycle (Ta- 
ble 4). There was a significant excess of male TF heterozygotes in 
the decline phase, whereas there was a significant excess of male 
LAP heterozygotes in the increase phase. Furthermore, the signif- 
icant difference between male and female heterozygosity at the TF 
locus during the decline phase is difficult to explain by non-selective 
forces because they should affect both sexes similarly. 


Genetics 859 


TABLE 5 
MINIMUM SURVIVAL RATES/14 Days OF TF AND LAP GENOTYPES IN Microtus och- 
rogaster POPULATIONS DURING PHASES OF INCREASING AND DECLINING DENSITY RE- 
PORTED IN Two STUDIES IN SOUTHERN INDIANA AND ONE STUDY IN EASTERN KANSAS 
(FROM GAINES, 1981) 


Locality 
Indiana Indiana Kansas 
(1965-1967) (1967-1969) (1970-1973) 
Locus and phase ee ee ae ee 
of cycle Male Female Male Female Male’ Female 
Transferrin* 
Increase 
Fast homozygote 84 92 .78 .87 .82 83 
Heterozygote .76 .76 49) 85 ie 85 
Slow homozygote ~~ _— = a .86 .87 
Decline 
Fast homozygote 259 .68 70 .69 .65 65 
Heterozygote AD 33 ee 74 .66 .69 
Slow homozygote — — — — ath 82 
Leucine aminopeptidase* 
Increase 
Fast homozygote — — .60 84 .80 85 
Heterozygote a — a) O91 88 EO 
Slow homozygote — 85 .86 .80 .86 
Decline 
Fast homozygote — — .70 .62 51 58 
Heterozygote — — 5) 58 59 58 
Slow homozygote — — 5 fl .63 .63 


* Genotypes for the TF locus were 7f*/7f*, Tf*/Tf*, and Tf*/Tf*, and for the LAP 
locus were Lap*/Lap*, Lap’/Lap*, and Lap*’/Lap‘, respectively. 


Another approach used in live-trapping studies is to measure 
physiological components of fitness (Gaines and Krebs, 1971; Gaines 
et al., 1978; Kohn and Tamarin, 1978; LeDuc and Krebs, 1975; 
Tamarin and Krebs, 1969). Because animals are marked in the 
field and their genotypes are known, one can estimate survival rates, 
growth rates, and breeding activity for each genotypic class. Min- 
imum survival rates for TF and LAP genotypes during density 
fluctuations of M. ochrogaster are presented in Table 5. In spite of 
variation in survival rates over different studies, certain trends are 


860 Gaines 


apparent. At the TF locus, the 7?/7f homozygote was extremely 
rare in Indiana populations. The 7//7f heterozygote generally 
had higher survival rates than 7/7 homozygotes during the de- 
cline phase in both Indiana studies, the only exception being females 
in the study of Tamarin and Krebs (1969). In declining Kansas 
populations, individuals with at least one 7f allele had higher 
survival rates than 7 /7Tf homozygotes. 7/*/7/ homozygotes had 
the highest survivorship of any genotype. In Indiana and Kansas, 
Lap’/Lap’ homozygotes had the highest survival rates for males 
and females during population declines. In addition to survival rates, 
Gaines et al. (1978) found differences in the breeding activity and 
growth rates among TF and LAP genotypes in Kansas prairie-vole 
populations. 

Perturbation experiments provide the strongest evidence for se- 
lection acting on electrophoretic loci. Gaines et al. (1971) introduced 
laboratory voles into a fenced enclosure so as to found the popula- 
tion with a 7f gene frequency of 0.50. 7 gene frequencies in 
natural populations in the area ranged from 0.80 to 0.90. Gene 
frequences of the enclosed and control populations were monitored 
every 14 days over a 16-week period. The experiment was repli- 
cated over three seasons. At the conclusion of each experiment all 
animals were removed from the enclosure and the new introduction 
was made. In all three replicates the 7 gene frequencies increased 
and approached values observed in open field populations. 

Although natural selection may play a role in maintaining poly- 
morphisms, not all observed gene-frequency changes necessarily re- 
sult from the action of selection. Demographic changes also affect 
local population sizes and rates of migration, which in turn can 
lead to random fluctuations in allele frequencies. To assess the roles 
of selective and non-selective forces in gene-frequency change, Le- 
wontin and Krakauer (1973) developed a statistical test that relies 
on a comparison of gene-frequency distributions for different loci. 
Their rationale is that alleles at all loci will be similarly affected 
by the breeding structure of the population and, thus, the effects of 
non-selective forces, such as genetic drift and migration, should be 
uniform over loci. However, natural selection, operating through 
differential fitness of genotypes, affects gene frequency only at spe- 
cific loci. Therefore, a measure of genetic variation at each poly- 
morphic locus over an ensemble of populations should be similar if 
only non-selective forces are operating but dissimilar when selection 


Genetics 861 


is acting upon alleles at specific subsets of loci. The measure chosen 
by Lewontin and Krakauer is a standardized variance of gene fre- 
quencies called the effective inbreeding coefficient, F.. 

For a locus with two alleles, F, is calculated as the ratio of the 
observed variance in allele frequency, s’,, to the maximum variance 
possible for the average allele frequency, p, as follows: 


A s 


| ee = 
“BU — p) 

Note that F, is the same as Wright’s (1965) F,,. For neutral alleles, 
the F, values calculated for each of many loci over an ensemble of 
populations will be statistically homogeneous, whereas if selection 
is occurring there will be heterogeneity in F. values. 

Heterogeneity in F, values among loci can be tested from the 
ratio of the observed variance in F.’s over all loci to the theoretical 
variance. Lewontin and Krakauer (1973) found the theoretical vari- 
ance of F, over n subpopulations in the absence of selection to be a 
function of the average F, as follows: 


ke 
(a — 1) 


Through computer simulation, the limiting value of k = 2 was found 
for various underlying distributions of gene frequencies. The ratio 
of s,?/o,” is compared with an F(n — 1, 00) distribution. If the sam- 
pling variance is significantly greater than the theoretical variance, 
one can infer heterogeneity in F,’s among loci. 

The Lewontin-Krakauer test (L-K test) has been criticized in its 
application to spatial distribution of gene frequencies. Ewens and 
Feldman (1976), Nei and Maruyama (1975), and Robertson (1975a, 
19756) contended that heterogeneity of F. could result from factors 
other than selection (for example, different initial gene frequencies 
in each population). However, this problem is unlikely in tests of 
temporal distributions of gene frequencies within populations where 
the initial gene frequencies are known. 

Gaines and Whittam (1980) used the L-K test to assess changes 
in gene frequencies at five polymorphic loci in fluctuating popula- 
tions of M. ochrogaster in eastern Kansas. Although gene frequency 
data were available for 2-week samples (Gaines et al., 1978), they 
chose a 14-week interval to avoid confounding effects of the same 
individual being sampled more than once. Each of seven time pe- 


Ge 


862 Gaines 


TABLE 6 
ESTIMATES (TOP) OF EFFECTIVE INBREEDING COEFFICIENTS (F.) CORRECTED FOR 
SAMPLING VARIANCE AT FIVE LOCI AMONG SUBPOPULATIONS DURING SEVEN TIME PE- 
RIODS ON EACH GRID, AND (BOTTOM) A SUMMARY OF HETEROGENEITY TESTS OF F, 
VALUES. THE VARIANCE RATIO, 5,?/o,’, IS COMPARED WITH AN F,... DISTRIBUTION 
(FROM GAINES AND WHITTAM, 1980). ALL RATIOS ARE NON-SIGNIFICANT 


Locus/ Cue 

statistic A B C D 
TF 0.026 0.021 0.044 0.050 
LAP 0.010 0.007 0.037 0.050 
EST-1 0.034 0.072 0.036 0.104 
EST-4 0.042 0.026 0.010 0.007 
6-PGD 0.000 0.063 0.004 0.005 
F. 0.023 0.038 0.027 0.042 
Se 0.0002 0.0006 0.0003 0.0006 
O,? 0.0002 0.0005 0.0002 0.0006 
5p2/o," 1.000 1.200 1.500 1.000 


Abbreviations are: F., mean estimate of effective inbreeding coefficient; s,’, ob- 
served variance; o,’, theoretical variance. For identities of proteins, see Table 3. 


riods sampled was considered a subpopulation for calculations of 
the F.’s. They corrected for both sampling variance within time 
periods and correlations in alleles over sampling periods. 

The F, values, using the mean and variance in gene frequency 
over the seven time periods, for the five polymorphic loci on four 
live-trapped grids, are given in Table 6. The homogeneity of F, 
values indicates that non-selective forces are primarily responsible 
for the changes in gene frequency through time. 

The results of the L-K test conflicted with those of Gaines et al. 
(1978) who concluded from an analysis of the same data set that 
changes in gene frequency at the TF and LAP loci were probably 
due to selection. Their conclusion was based on differences in phys- 
iological components of fitness (see Table 5) among genotypes. 
Gaines and Whittam (1980) attributed these conflicting interpre- 
tations to a reductionist versus holistic approach. Physiological com- 
ponents of fitness were measured during each phase of the density 
fluctuation without considering the historical events that preceded 
them. On a micro-scale, Gaines et al. (1978) found statistically 
significant differences in fitness components among genotypes dur- 


Genetics 863 


0.2 

u” 0,1 

0 
Time periods: 1 2 3 4 5 
Density phase: increase increase peak decline low 


(early) (low) 


Fic. 2. F,, values for resident M. californicus from four subpopulations averaged 
over four loci (from Bowen, 1982). 


ing phases of increasing density. However, assuming that the L-K 
test is valid for temporal variation in vole populations, the intensity 
of selection was not strong enough to counteract the effects of non- 
selective evolutionary forces, such as random genetic drift, which 
most likely predominate during the periodic bottlenecks of the low- 
density phase and lead to random changes in allelic frequencies 
observed over short time periods. 

Bowen (1982) used F-statistics to measure genetic differentiation 
in a population of M. californicus. The population was subdivided 
into four 0.15-ha grids spaced 50 m apart. F,, values for four elec- 
trophoretic loci (PGD, GPI, GOT-1, and LAP) were calculated 
for five time periods during a 2-year density cycle. The average F,, 
values for the four loci over the cycle are presented in Fig. 2. The 
greatest genetic differentiation occurred during phases of the pop- 
ulation cycle when density was low, whereas the population became 
relatively more homogeneous as density increased during the breed- 
ing season. Bowen interpreted the U-shaped distribution of F,, val- 
ues in Fig. 2 as evidence for increased dispersal at the onset of the 
breeding season. Once migrants established themselves in existing 
patches of habitat, the genetic heterogeneity among patches would 
decrease as a result of gene flow. After the population density re- 
turns to a low phase, genetic heterogeneity would be reestablished 
as a result of genetic drift within isolated patches. Thus, Bowen 
(1982) related changes in the genetic structure of a population of 
M. californicus to changes in its population dynamics. 


864 Gaines 


In summary, there is evidence that natural selection maintains 
polymorphisms at the TF and LAP locus in natural populations of 
Microtus. Significant differences were observed between genotypes 
in certain physiological components of fitness, and these observa- 
tions were repeatable both in time and space. The most convincing 
evidence for selection comes from perturbation experiments in which 
enclosed field populations started with different initial frequencies 
converged to the frequencies found in natural populations. How- 
ever, non-selective forces also play a significant role in gene-fre- 
quency change over short time periods as revealed by the L-K test 
on five polymorphic loci in M. ochrogaster populations, and by F,, 
values calculated for M. californicus. 


Quantitative Genetics 


There has been a dearth of studies on quantitative traits in M- 
crotus. Guthrie (1965) related intrapopulational variation in den- 
tition of the extinct M. paroperarius and the recent M. pennsylvan- 
icus to the rapid evolution of microtine rodents in the late Pliocene 
and Pleistocene. Guthrie (1965) suggested that rapid evolution of 
the molars may have been a response to a major change in diet 
from fruit and seeds to grass and bark. Gill and Bolles (1982) found 
variation in the root length of teeth in two populations of M. cali- 
fornicus. Although the trait had some genetic component, its mode 
of inheritance was unclear. Hilborn (1974) studied the inheritance 
of three non-continuous skeletal variants (preorbital foramina, 
maxillary foramina, and sphenoid foramina) from a captive colony 
of M. californicus. Breeding data indicated some association between 
phenotype of parent and offspring for the preorbital foramina. 

In all these studies it is difficult to assess the environmental and 
genetic components of each trait. Only a few attempts have been 
made to estimate the heritability of polygenic traits in Mrcrotus 
populations. Heritability (h?) in the narrow sense is defined as 
(Falconer, 1981): 


where V, is the additive genetic variance, and V> is the phenotypic 
variance. The V, term is the sum of the environmental variance 


Genetics 865 


(V;) and the total genetic variance (V,). The total genetic variance 
can be partitioned into the additive genetic variance (V,), the vari- 
ance due to dominance effects (V,), and the variance resulting from 
epistatic interactions (V,). The evolutionary response to natural 
selection depends primarily on the additive genetic variance. 

Most methods used to estimate heritability rely upon phenotypic 
resemblances among relatives. If we know the expected phenotypic 
correlation between relatives based entirely on the additive effects 
of genes, then any deviation from the expected correlation is due 
to environmental effects. For example, since offspring share 2 their 
genes with their parents, the phenotypic covariance between off- 
spring and one parent or offspring and the mean of both parents is 
Y%. The slope of the regression line of offspring phenotypic values 
against phenotype values of a single parent is 2V,/V> or % h’. In 
the case of midparent values the slope of the regression line would 
be %2V,/%V> or h’®. Estimation of heritability from sib analysis is 
more complicated (Falconer, 1981). The phenotypic covariance be- 
tween half sibs is 4, based on the additive effects of the genes they 
have in common. Full sibs share % their genes but are phenotypi- 
cally similar due to effects of dominance and a common environ- 
ment. Heritability of siblings can be estimated by the intrafamily 
correlation (t), which is defined as: 


= 2B) 
s°(T) 


where s°(B) is the between-family component of variance and s?(T) 
is the total populational variance (the sum of between- and within- 
family components). 


Dispersal Behavior 


Howard (1965) codified dispersal behavior of rodents into two 
categories: innate dispersal and environmental dispersal. He sug- 
gested that the former is instinctive behavior governed by laws of 
heredity, whereas the latter is a behavioral response to overcrowd- 
ing, food supply, mate selection, homing ability, and other environ- 
mental factors. The results from several electrophoretic studies of 
Microtus populations have indicated that dispersers are genetically 
different from residents at some loci, supporting Howard’s innate 
dispersal hypothesis. Myers and Krebs (1971) found differences in 


866 Gaines 


genotypic frequencies between dispersers and residents in two species 
of Microtus in southern Indiana. In M. pennsylvanicus, Tf*/Tf* 
homozygotes were more common among dispersing males, com- 
pared to resident males, during the late population peak and decline 
phase of the density cycle. During periods of population increase, 
Tf°/Tf heterozygotes were more common among dispersing fe- 
males than in resident females. There was also increased dispersal 
of Lap’/Lap® males during the peak phase. In M. ochrogaster pop- 
ulations, the rare 7f*/7f’ homozygote was found only among dis- 
persing males. Pickering et al. (1974) found differential dispersal 
of individuals with different esterase phenotypes in M. ochrogaster 
populations in Illinois. Dispersing M. townsendu individuals were 
not a genetically random subsample from a resident population at 
the LAP locus (Krebs et al., 1976). Keith and Tamarin (1981) 
found an excess of the 7f° allele in dispersing individuals in M. 
pennsylvanicus and M. brewert populations. However, there was no 
evidence for differential dispersal of LAP and TF genotypes in M. 
pennsylvanicus and M. ochrogaster populations in [Illinois (Verner, 
1979), nor did the genetic composition of dispersers and residents 
differ at seven electrophoretic loci in M. californicus populations 
(Riggs, 1979). Although genetic differences at electrophoretic loci 
between dispersers and residents are consistent with an innate dis- 
persal hypothesis, this result is not sufficient to conclude that dis- 
persal behavior has a large genetic component because a causal 
relationship cannot be demonstrated. 

There have been three attempts to estimate the heritability of 
dispersal tendency in Microtus. The most exciting work to date is 
from a Ph.D. thesis on M. townsendii by Judith Anderson (1975), 
which represents the first attempt to examine the inheritance of 
ecologically relevant traits. Anderson (1975) housed individual 
breeding pairs of M. townsendii in 16 small field enclosures (6 m x 
6 m) surrounded by rodent-proof fences. After litters were weaned, 
siblings were tagged, removed from the small enclosure and released 
either in a larger 0.8-ha enclosure or in an unfenced grid. If dis- 
persal tendency has a genetic component, there should be a higher 
within-family correlation for length of residence in the population 
on the unfenced grid where dispersal can occur than on the fenced 
grid where no dispersal is possible. Siblings resembled one another 
closely in duration of life on both unfenced (t = 0.62) and fenced 


Genetics 867 


grids (t = 0.37). Furthermore, the intrafamily correlation on the 
unfenced grid was significantly higher than on the fenced grid. 

Hilborn (1975) analyzed differences in dispersal tendency within 
and between sibships in M. californicus, M. ochrogaster, M. penn- 
sylvanicus, and M. townsendu. If dispersal tendency has a large 
genetic component, then members of a single sibship should be more 
similar in their dispersal behavior than individuals from different 
sibships. An analysis of variance indicated that within-litter vari- 
ance for disappearance rates was significantly lower than between- 
litter variance. Because disappearance could be due to either dis- 
persal or death in situ, the results were ambiguous. Beacham (1979) 
was able experimentally to separate disappearance into survivor- 
ship and dispersal components in enclosed populations of M. town- 
sendu, and compare within- and between-litter variability for both 
parameters using an analysis of variance. Dispersers were identified 
as those individuals that crossed an 18.3-m mowed area and were 
captured in pitfall traps. An analysis of variance indicated that in 
increasing and peak populations, identifiable families tended to sur- 
vive or disperse as a unit. 

The results from these three studies suggest that sibs resemble 
one another in their tendency to disperse. However, estimates of 
heritability from full-sib analysis should be viewed as upper limits 
of the true heritability values because it includes both common 
environment and dominance effects. Another problem is the large 
standard errors associated with these heritability estimates. Finally, 
in the latter two studies, sibs were determined by their similarity 
in weight and proximity of their trapping locations. This indirect 
method may have led to incorrect assignations of some individuals 
to family units. 


Aggressive Behavior 


Anderson (1975) also estimated heritability of agonistic behavior 
in M. townsendi. Adult voles were brought into the laboratory from 
the field and each test animal was matched against an opponent of 
the same sex. All tests were performed in a neutral arena (61 cm xX 
30 cm). The two opponents were separated for five minutes by 
a partition. After this time period the barrier was lifted and for 10 
min the number of different types of behavior was recorded. ‘The 


868 Gaines 


following behavioral variables were scored in each bout: active threat, 
approach latency, initiate investigation, fight initiator, defensive 
posture, mutual upright, retaliation, submissive posture, and activ- 
ity. Voles were returned to the field after testing. Heritability was 
measured from the regression of offspring scores on midparent scores 
for each behavioral variable separately. The slopes of all regression 
lines were not significantly different from 0. Correlation coefficients 
were then calculated between offspring and sire scores, and off- 
spring and dam scores, for each behavioral variable. There was 
only one association that was statistically significant: offspring at- 
tacks versus dam’s attacks (r = 0.36, P < 0.05). When stepwise 
multiple regression of offspring behavioral variables on all maternal 
variables was performed, four of the nine offspring variables could 
be predicted at a statistically significant level by varying combina- 
tions of the dam’s variables. Conversely, the sire’s behavior could 
not predict any of the offspring’s behavioral variables. Thus, there 
is a large maternal effect contributing to offspring behavior. 


Growth Rates 


Anderson (1975) used changes in skull width to measure growth 
rates of juvenile M. townsend. Growth rates of skull width were 
measured for juveniles captured at least twice within a 4-week 
period. After correcting for seasonal effects by regression analysis, 
adjusted growth rates were compared among sibs. The intrafamily 
correlation, t, among full sibs resulted in an estimate of h* = 0.46. 

Estimating the heritability of maximum body size presents a spe- 
cial problem because voles in natural populations usually disappear 
before they reach an asymptote in size. Anderson (1975) arbitrarily 
used skull width at last capture as a measure of maximum size. 
Parents whose skull widths were still changing rapidly were ex- 
cluded from the analysis. She was able to correct for age by re- 
gressing maximum size on age and obtaining an adjusted maximum 
size for different age classes. These standardized sizes were used in 
estimates of heritability. Neither slopes of the regressions of off- 
spring’s maximum size on midparent’s maximal size, or on sire’s 
maximum size, were significantly different from 0. However, there 
was a positive correlation between offspring’s maximum size and 
the dam’s size, suggesting a maternal influence. 


Genetics 869 


TABLE 7 
ESTIMATES OF HERITABILITY FROM INTRAFAMILY CORRELATIONS OF FULL SIBS FOR 
SIX QUANTITATIVE TRAITS IN Microtus townsendit (FROM ANDERSON, 1975) 


Trait Heritability Standard error 
Dispersal tendency (unfenced grid) 0.62 0.11 
Duration of life (fenced grid) 0.37 0.08 
Adult agonistic behavior 0.00 — 
Juvenile growth rate 0.46 0.24 
Maximum body weight 0.00 a 
Age at sexual maturity 0.55 0.20 


Age at Sexual Maturity 


Because the time of birth of litters born in breeding enclosures 
was known, Anderson (1975) was able to estimate the age at pu- 
berty for most of them. After adjusting for seasonal effects, the 
estimate of the intrafamily correlation for age at puberty was 0.55. 
This estimate of heritability was based on data from 41 litters and 
89 offspring. 


General Evaluation 


Anderson’s (1975) attempt to elucidate the genetic control of 
quantitative traits in M. townsend is a trailblazing effort in several 
respects. It represents the first attempt to measure heritability in 
natural populations of Microtus. By raising litters in small breeding 
enclosures and later releasing littermates in natural populations, 
she provided a realistic environment for estimating heritability. 
Furthermore, the traits she examined were all ecologically relevant 
in the context of population cycles. The heritabilities of these traits 
are summarized in Table 7. Because the estimates were based on 
full-sib analysis, phenotypic resemblance may have been due in part 
to a common environment and dominance effects. Separate analyses 
of sib’s phenotype on dam’s phenotype and on sire’s phenotype 
indicated that most traits were influenced by a maternal effect. In 
spite of difficulties in interpretation of the results of studies of this 
kind, similar attempts need to be made in other microtine species. 
In the future, problems associated with maternal effects could be 
circumvented by the use of paternal half-siblings and cross-fostering 


870 Gaines 


experiments. At the very least, we should be able to obtain a range 
of estimates of heritabilities for traits in populations of the same 
species in different localities as well as across species. 


Relationship between Genetics and 
Population Regulation 


Chitty (1967) formulated a genetic-behavioral hypothesis to ex- 
plain multiannual density cycles in microtine rodents. His hypoth- 
esis was originally based on an r- and a-selection argument (Sten- 
seth, 1978) but was later modified by Krebs (1978) to include 
dispersal. The model assumes: 1) a trade off between reproductive 
capabilities and survivorship, and 2) that space becomes limiting at 
high population densities. When densities are low, mutual inter- 
ference is minimal, and natural selection favors those genotypes 
with a high reproductive output. As density increases and resources 
and space become limited, genotypes that are aggressive and exhibit 
spacing behavior have a selective advantage. The agonistic inter- 
actions resulting from spacing behavior by aggressive individuals 
promote the dispersal of subordinates. Dominant individuals of both 
sexes may pay for their aggressiveness by sacrificing other compo- 
nents of fitness such as reproduction, which sets the stage for the 
population decline. The major tenet of Chitty’s (1967) hypothesis 
is that demographic changes are mediated by natural selection op- 
erating on the genetic composition of the population. 

Historically, the first step in testing Chitty’s (1967) hypothesis 
was to determine whether genetic changes occurred in the popula- 
tion and if these changes were closely associated with density. In 
several studies changes in gene frequency at electrophoretic loci 
were correlated with changes in density. Changes in gene frequen- 
cies at the TF locus (Tamarin and Krebs, 1969) and the TF and 
LAP loci (Gaines and Krebs, 1971) were correlated with popula- 
tion density in M. ochrogaster and M. pennsylvanicus in southern 
Indiana. LeDuc and Krebs (1975), monitoring gene frequency at 
the LAP locus in a population of M. townsendiu, found a positive 
association between changes in the Lap* allele and changes in pop- 
ulation density. Kohn and Tamarin (1978) reported that changes 
in gene frequency at the TF locus were correlated with changes in 
density in M. pennsylvanicus and M. brewer: populations in Mas- 
sachusetts. 


Genetics 871 


TABLE 8 
CORRELATION COEFFICIENTS FOR CHANGES IN GENE FREQUENCY AT TRANSFERRIN AND 
LEUCINE AMINOPEPTIDASE LOCI IN RELATION TO POPULATION DENSITY FOR Microtus 
ochrogaster IN KANSAS ON FOUR GRIDS DURING DIFFERENT PHASES OF THE POPULA- 
TION CYCLE, 1970-1973 (FROM GAINES, 1981) 


Number of : 
> allel Lap* allel 
Location and _ trapping eee Be ae ee 
phase periods Male Female Male Female 
Grid A 
Increase 27 OWwss= 0.56* —0.37 0.17 
Decline 9 —0.42 —0.56 0.89** 0.10 
Grid B 
Increase 28 O95 = 0.67** 0.20 0.51* 
Decline 14 —0.90** —0.08 0.77** 0.71** 
Grid C 
Increase 14 —0.14 0.06 —0.26 —(0:38** 
Decline Dif 0.18 0.16 0.48* 0.16 
Grid D 
Increase 13 0.61* 0.10 0.32 0.20 
Decline 14 0.02 —0.04 O72** 0.22 
*P< 0.05. 
** P< 0.01. 


One shortcoming of the above studies is that only one or at most 
two loci were monitored. Gaines et al. (1978) expanded the scope 
of earlier studies by monitoring changes in gene frequency at five 
loci: TF, LAP, 6-PGD, EST-1, and EST-4. Four live-trapped 
grids of M. ochrogaster were monitored over a 3-year period in 
eastern Kansas. Densities and gene frequencies are presented in 
Gaines et al. (1978:Figs. 1-6). Three general patterns of changes 
in gene frequency emerged from the Kansas data. 1) One locus 
(6-PGD) had relatively stable gene frequencies over the population 
cycle. The common allele, 6-Pgd’, went to fixation during some 
trapping periods with the polymorphism being restored by immi- 
gration. 2) Two loci (EST-1 and EST-4) had changes in gene 
frequencies unrelated to density. The largest temporal changes in 
gene frequencies occurred at the two esterase loci and were quan- 
tified by calculating averages of absolute changes in gene frequency 
(Ap) over time (Gaines et al., 1978:Table 3). 3) Two loci (IF 
and LAP) had gene frequency changes correlated with density. 
Correlation coefficients for 7f* and Lap” gene frequencies versus 


872 Gaines 


density during different phases of the population cycle are given in 
Table 8. 

I found a somewhat different pattern of temporal variation at the 
TF and LAP loci in southern Indiana populations. In Indiana, 7f* 
frequencies in both sexes were positively correlated with density 
over the entire population cycle. In Kansas, except for grid C, 
changes in gene frequency in both sexes were positively correlated 
with density during the increase phase. Changes in Lap” frequency 
in Indiana populations were negatively correlated with density of 
males over the entire cycle, whereas these two variables were pos- 
itively correlated in males during the decline phase in Kansas pop- 
ulations. Thus, only changes in gene frequency at the TF locus are 
repeatable over time and space. 

Correlations between changes in gene frequency and density are 
consistent with Chitty’s (1967) hypothesis, but it is difficult to dis- 
entangle cause and effect. Genetic changes may cause demographic 
changes or may be an effect of density changes. Charlesworth and 
Giesel (1972) demonstrated with computer simulations that a cor- 
relation between gene frequency and density could be produced by 
a change in the rate of population growth. They define the Wrighti- 
an fitness w,, of the genotype carrying alleles 7 and j in an equilib- 
rium population as: 


Ww; = > e~ "1, (x)m, (x) 
x=1 


where 7 is the rate of population growth of an equilibrium popu- 
lation in its stable age distribution, /,,(x) is the probability of the 
ith genotype living to age x, and m,,(x) is the number of offspring 
produced by the zjth genotype per unit time at age x. It follows 
from the above equation that as r becomes increasingly positive, 
younger age classes make a proportionately greater contribution to 
fitness, and gene frequencies change in favor of the genotype that 
reproduces earliest. Conversely, as r becomes increasingly negative, 
older age classes will be weighted more heavily and gene frequencies 
will change in favor of late reproducing genotypes. Thus, fluctua- 
tions in population age structure can alter relative contributions of 
early and late reproducing genotypes to the gene pool. Charlesworth 
and Giesel (1972) assigned m(x) functions to three genotypes, each 
having three age classes, such that one homozygote started repro- 
ducing earlier than the other. In each case the heterozygote started 


Genetics 873 


reproducing at the same age as the earlier homozygote. Fluctuations 
in population density were accomplished by changing the m(x) 
schedules of all genotypes uniformly to produce the desired change 
in population growth-rate. This procedure is equivalent to an ex- 
trinsic factor that has an identical effect on fecundity of all geno- 
types and age classes. In simulations consisting of 400 time inter- 
vals, gene-frequency changes were closely associated with changes 
in density (Charlesworth and Giesel, 1972: Fig. 2). These results 
suggest that fluctuations in gene frequency could be a side effect of 
population cycles (also see Charlesworth, 1980). 

There are several lines of evidence supporting Charlesworth and 
Giesel’s (1972) contention that changes in gene frequency are effects 
of density changes. First, a number of protein polymorphisms have 
been shown to be correlated with population density in a variety of 
New World and Old World microtine species (Bowen, 1982; Gaines 
and Krebs; 1971; Gaines et al., 1978; Kohn and ‘Tamarin, 1978; 
Mihok et al., 1983; Nygren, 1980; Semeonoff and Robertson, 1968; 
Tamarin and Krebs, 1969). It is exceedingly unlikely that all these 
loci chosen at random are causally related to population cycles. 
Second, a comparative study of changes in gene frequency at the 
TF locus revealed similar patterns of temporal variation in a non- 
cycling island population of M. brewer: and a cycling mainland 
population of M. pennsylvanicus (Kohn and ‘Tamarin, 1978). Fi- 
nally, the best evidence comes from two perturbation experiments. 
Gaines et al. (1971) introduced “‘pure stands” of three different TF 
genotypes of M. ochrogaster into three separate fenced enclosures. 
There was no significant effect of genotype on population growth 
rate, percentage of breeding females, recruitment index, or survival 
rate of voles. LeDuc and Krebs (1975) maintained divergent allelic 
frequencies at an LAP locus by selective removal and addition of 
genotypes in two field populations of M. townsendi. The altered 
allelic frequencies in the two populations did not have any consis- 
tent effects on demography. 

Perturbation experiments suggest that genetic changes at a single 
locus are effects of demographic changes, but they were not designed 
to test whether changes in average heterozygosity over many loci 
were causing density changes. Smith et al. (1975) related average 
heterozygosity to fluctuations in rodent numbers. They suggested 
that at low density inbreeding decreases heterozygosity, whereas at 
high density there is increased dispersal and the population becomes 


874 Gaines 


relatively more outbred, leading to increased heterozygosity. Be- 
cause Garten (1976) found an increase in aggressive behavior with 
increased heterozygosity in Peromyscus polionotus populations, it 
could be argued that an increase in heterozygosity owing to out- 
breeding, as the population increases, results in increased aggressive 
behavior, which in turn is followed by increased mortality, de- 
creased reproduction, and a population decline. This scenario is 
consistent with Chitty’s (1967) hypothesis. However, Gaines et al. 
(1978) found a greater deficiency of heterozygotes averaged over 
five electrophoretic loci, compared to the expected number based on 
Hardy-Weinberg equilibrium in prairie-vole populations, as density 
increased. 

I suggested previously (Gaines, 1981) that if density and the 
genetic structure of a population are in a closed feedback loop as 
implied by Chitty’s (1967) hypothesis, the cause and effect dilemma 
becomes a moot issue. In this self-regulatory model, genotypic fit- 
ness is a function of density and a change in density will change 
the fitness of genotypes, which in turn will act back on density. If 
the genetic structure of the population and its demography are 
intimately associated with one another, we would like to know 
whether there is a set of simultaneous equations that describes the 
interaction between these two variables. The challenging task is to 
determine the form and relevant parameters of these equations. 

Stenseth (1981) modeled a self-regulatory system in accordance 
with assumptions implicit in Chitty’s (1967) genetic-behavioral hy- 
pothesis. He used two behavioral morphs, a docile phenotype and 
an aggressive phenotype, which were under simple Mendelian con- 
trol. The two morphs were assigned fitnesses such that the docile 
phenotype had a selective advantage at low population density be- 
cause of its higher reproduction, whereas selection favored the ag- 
gressive phenotype as density increased because of its higher sur- 
vivorship and its depressing effect on the reproduction of the docile 
form. Stenseth (1981) demonstrated formally, using several mating 
schemes, that one morph eliminated the other. The outcome of 
which form persisted was dependent upon the dominance relation- 
ship between the docile and aggressive allele. Stenseth (1981) con- 
cluded that stable limit cycles could be generated only by the inter- 
vention of extrinsic environmental factors. The major weakness of 
Stenseth’s model is its over-simplification of the real world. A com- 
plex behavioral trait is assumed to be controlled by two alleles; time 


Genetics 875 


lags and age structure are ignored. Nevertheless, it does represent 
one of the first direct tests of Chitty’s hypothesis from a purely 
theoretical standpoint. 

We can increase the complexity of the genetic feedback model by 
incorporating extrinsic factors such as weather. For example, 
changes in climate may cause changes in density and concomitantly 
cause changes in the genetic structure of the population. The prob- 
lem of distinguishing between cause and effect is now compounded 
even further; not only must we consider the interaction of genetics 
and density, but also how demographic and genetic changes covary 
with different combinations of extrinsic factors. Lidicker (1973) is 
the leading proponent of this multi-factorial approach to the study 
of population regulation (see Taitt and Krebs, this volume). 

In summary, there is convincing evidence from a number of stud- 
ies that genetic changes at electrophoretic loci are closely associated 
with density changes in Microtus populations. It is an error to 
interpret these associations as support for Chitty’s (1967) hypoth- 
esis. Theoretical and field studies suggest that genetic changes at a 
single locus were effects of demographic changes rather than vice- 
versa. In the future, attempts to relate genetic structure to popu- 
lation regulation must focus on those traits deemed ecologically 
relevant. The first steps in this direction have been taken by An- 
derson (1975). Finally, Smith et al.’s (1975) hypothesis about the 
relationship between average genic heterozygosity over many loci 
and density needs to be explored in natural populations of Microtus. 
If there is a consistent association between the two variables, per- 
turbation experiments should be done. 


Conclusions 


In this concluding section I identify areas for future research in 
the genetics of Microtus. Of course these selections reflect my per- 
sonal bias. Three research areas that may prove to be profitable in 
the future are: 1) the effect of social dynamics on the genetic struc- 
ture of populations; 2) inheritance and evolution of quantitative 
traits; and 3) the application of new molecular techniques to assess 
genetic variation in natural populations. 

Mating systems can have profound effects on the genetic structure 
of populations. If a population is subdivided into small inbreeding 


876 Gaines 


units or demes, genotypic frequencies will deviate from the expected 
proportions based on Hardy-Weinberg equilibrium; there will be 
an excess of homozygotes and a deficiency of heterozygotes. Fur- 
thermore, a cohesive family unit will restrict gene flow between 
populations. Microtines present real difficulties in studying social 
behavior because individuals are nocturnal or crepuscular and oc- 
cupy habitats which preclude direct observation (see Getz, this vol- 
ume; Wolff, this volume). As a result of these difficulties most of 
the genetic studies referenced in this review have treated microtine 
populations as one large panmictic unit. However, Wolffs review 
(this volume) of social behavior in microtines indicates that mating 
systems can vary from monogamy to promiscuity. From a genetic 
interest, we need to know how social behavior changes as a function 
of different demographic parameters such as density and reproduc- 
tive activity, and how the social dynamics relate to the temporal 
and spatial distribution of gene frequencies. Hopefully, we will be 
able to answer these questions as the technology for studying social 
behavior becomes better developed. 

Future work in genetics should be directed towards the inheri- 
tance of quantitative traits. We now have estimates of heritability 
from full-sib analysis for several traits in M. townsend (Anderson, 
1975). Krebs (1979) has arranged microtine populations on a de- 
mographic continuum from strongly cyclic, exhibiting 3—4 year cycles 
at one end, to stable, exhibiting annual cycles at the other end. 
Krebs (1979) hypothesizes that this demographic continuum can be 
mapped directly on a genetic continuum of the heritability of spac- 
ing behavior, from high heritability in strongly cyclical populations 
to low heritability in stable populations. This hypothesis can be 
tested by estimating the heritability of behavioral traits in a variety 
of microtine species. The major obstacle is devising techniques to 
determine parentage in the field. Anderson (1975) housed breeding 
pairs in small field enclosures and subsequently released littermates 
in open field populations where traits were quantified. Because 
rates of disappearance of these young voles from open field popu- 
lations were high, sample sizes were greatly reduced. Tamarin et 
al. (1983) developed a new technique for determining matrilineal 
kinship in natural populations of microtines that should be useful 
in estimating heritability. Pregnant females trapped in the field 
were injected with different gamma-emitting radionuclides and re- 
leased. Young animals subsequently captured were subjected to 


Genetics 877 


whole-body gamma spectroscopy and identified by the spectral 
characteristics of the nuclides used to tag the mother. By combining 
this technique with electrophoresis of mothers, young, and potential 
fathers, the maternity and paternity of offspring may be determined 
in the field. 

After obtaining estimates of heritability, it would be interesting 
to estimate genetic correlations between pairs of traits. For example, 
we could determine whether there is a genetic correlation between 
agonistic behavior and dispersal tendency. Genetic correlations can 
be calculated from the following formula: 


COV xy 
iN = ae 
Oxo y>y 
where COV,, is the among family component of covariance between 
the two traits and o’, and o’, are the among-family components of 
variance for the two traits. Generally, data from paternal half-sib 
families are used in this formula but full-sib data can be used 
assuming no dominance effects. Genetic correlations between phe- 
notypic variables could be due to pleiotropy or linkage. If selection 
is weak, pleiotropy will be the predominant cause of genetic co- 
variance (Falconer, 1981). 

As we accumulate more information on heritability and genetic 
correlation of phenotypic characters, it will eventually lead us to a 
point where we can make meaningful conclusions about multivari- 
ate phenotypic evolution. Lande (1979) provided a theoretical 
framework for the evolution of quantitative traits by examining the 
effects of natural selection on correlated characters within popula- 
tions. Some progress is being made in this area by Atchley and his 
coworkers (Atchley and Rutledge, 1980; Atchley et al., 1981) on 
size and shape variation in the laboratory rat. In the future, quan- 
titative genetic analysis of traits in microtine populations also may 
be a useful data base to test some of the predictions generated by 
Lande’s (1979) theory. 

After electrophoresis was first applied to natural populations of 
organisms by Lewontin and Hubby (1966), investigators relied ex- 
clusively on this technique to estimate levels of genetic variation in 
a multitude of species ranging from bacteria to humans. Recently, 
new techniques have become available from the field of molecular 
biology that are more sensitive in detecting genetic variation. One 
such method compares sequences of DNA segments obtained with 


878 Gaines 


the use of restriction endonucleases. These enzymes recognize spe- 
cific nucleotide sequences and cleave the DNA at these sequences. 
Fragments can then be compared with electrophoresis. Avise et al. 
(1979) used six restriction endonucleases to measure mitochondrial 
(mtDNA) sequence relatedness in natural populations of Peromys- 
cus. They found heterogeneity in mtDNA among individuals in the 
same population and among individuals from different populations. 
Individuals from the same population showed less than 0.5% se- 
quence divergence, whereas those from different populations sepa- 
rated by 50-500 miles differ by 1.5%. Similar types of analyses 
could be done on microtine populations to get more reliable esti- 
mates of genetic variation. In addition, these new techniques will 
be extremely useful in determining phylogenetic relationships in 
the genus Microtus (see Anderson, this volume). 


Acknowledgments 


I am indebted to Thomas S. Whittam for the extraordinary 
amount of work that he did in improving the first draft of the 
manuscript. Also, I am grateful to Ayesha Gill who made many 
constructive comments and directed me to source material for this 
chapter. The following individuals read selected sections of the 
manuscript and made many helpful suggestions: W. Bloom, K. 
Hamrick, R. Lande, L. McClenaghan, Jr., and R. Tamarin. My 
own work on the genetics of Microtus has been supported by grants 
from the General Research Grant Fund of the University of Kansas 
and the National Science Foundation. 


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Murig, O. J. 1934. Melanism in an Alaskan vole. J. Mamm., 15:323. 

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NADLER, C. F., V. R. RauscH, E. A. LYAPUNOVA, R. S. HOFFMANN, AND N. N. 
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882 Gaines 


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Nel, M., AND T. MaruyAMA. 1975. Lewontin-Krakauer test for neutral genes. 
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Nevo, E. 1978. Genetic variation in natural populations: patterns and theory. 
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OHNO, S. 1969. The mammalian genome in evolution and conservation of the 
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OwEN, R. D., AND R. M. SHACKELFORD. 1942. Color aberrations in Microtus and 
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PaTTON, J. L. 1977. B-chromosome systems in the pocket mouse, Perognathus 
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Genetics 883 


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INDEX* 


Activity rhythms, 374-389, 412 
circadian, 381-382 
climate, 387-389 
competition, 386-387 
energetics, 384, 830 
genetics, 384 
infradian, 382-384 
parasitism, 386-387 
predation, 386 
sex, 385 
social factors, 385-386 
ultradian, 381 
Adrenal gland 
endocrinology, 704-716 
ultrastructure, 241-243 
Agonistic behavior, 360-364 
genetics, 867-869 
Agricultural habitats, 304-305 
Allophaiomys, 6, 8, 9, 11, 105 
Allozymes (see Genetics, allozymic 
variation) 
Amphibians, predation by, 558-559 
Anatomy 
gross, 118-159 
circulatory system, 138-140 
digestive system, 140-155 
integument, 118-121 
musculature, 136-138 
reproductive system, 155-159 
skeleton, 121-136 
teeth, 140-150 
ultrastructure, 177-247 
adrenal gland, 241, 243 
brain, 179 
dentition, 196-202 
digestive tract, 216-240, 242, 
244 
eyes, 180-193 
integumentary glands, 194-196 


pituitary gland, 179-180 
reproductive tracts, 243, 245- 
247 
salivary glands, 202-217 
tarsal (Meibomian) glands, 
193-194 
Arborimus, 91 
Artichoke method in taxonomy, 75- 
76 
Avian predation, 537-550 


Baculum 
function, 159 
macroanatomy, 155-157 
Baubellum, macroanatomy, 158 
Beetles, as parasites, 481-482 
Behavior, 340-366 
nonsocial, 341-344 
social, 344-366 
activity rhythms, 385-386 
agonistic, 360-364, 867-869 
communal nesting, 354-356 
copulatory, 353-354 
genotypic causes, 592, 602-604, 
867-869 
mating systems, 344-353 
olfactory communication, 356- 


359 

phenotypic causes, 590-592, 
600-602 

role in demography, 590-592, 
600-604 


social structure, 344-353 

vocalization, 359-360 
spacing, 389-413 

climate, 409-411 

dispersal, 405, 432-434 

dispersion, 405-406 

energetics, 406-407 


* This index is primarily a guide to subject areas covered in the text. 
Topics and species briefly mentioned in the text or in abstracts, summaries, 
figures, references, or appendices may not be indexed. Check CONTENTS 


for broad subject areas. 


884 


home range, 398-401 
interspecific interactions, 409 
movement types, 402-405 
role in demography, 589-590, 
598-600 
sex, 407-408 
social factors, 408-409 
territoriality, 401-402 
Biomes and biogeographical prov- 
inces, 85-105 (see also Zooge- 
ography, ecological) 
cloud forest, 101-102 
grassland, 99, 101 
shrubland and woodland, 97-99 
taiga, 90-97 
temperate deciduous forest, 101 
tundra, 88-90 
Body size 
affect on competition, 327 
demographic consequences, 605- 
607 
Brain, ultrastructure, 179 
Breeding season 
length, 728-739 
timing, 687-688 
Bruce effect, 602, 699-700, 742-745 
Burrowing, 332 


Caecum 
fermentation, 154, 780 
macroanatomy, 153-155 
osmoregulation, 238 
ultrastructure, 238 
Carnivore (mammalian) predation, 
551-558 
Cecum (see Caecum) 
Chilotus, 91, 107 
Chionomys, 108 
Circadian rhythms, 381-382 
Circulatory system, 138-140 
Cladistics, 78 
Cladograms, 61 
Clethrionomys 
distribution, 91 
prenatal development, 257-262 
systematics, 54, 56 
taxonomic key, 62-66 


Index 885 


Climate 
effect on activity, 387-389 
effect on spacing behavior, 409- 
411 
effect on species diversity, 316-318 
Cloud forest biome, 101-102 
Communal food storing, 354-356 
Communal nesting, 317, 354-356, 
402 
Communication 
olfactory, 356-359 
vocalization, 359-360 
Community ecology, 310-334 
biomass, 331-332 
climate, 316-318 
competition, 321-324 
influence of Microtus, 325-329 
predation, 324-325 
role of Microtus, 329-332 
species diversity, 310-316 
substrate, 318-319 
vegetation, 319-321 
Competition, 297-300, 321-324 
effect on activity, 386-387 
effect on demography, 577 
Control, 621-642 
barriers, 626 
chemicals, 631-639 
environmental hazards, 639-641 
habitat manipulation, 626-628 
hoofed animals, 628 
monitoring, 624-626 
predators, 630 
repellents, 628-630 
trapping, 630 
Coprophagy, 384, 780 
Copulatory 
behavior, 353-354 
plugs, 159 
success, 742 
Corpus luteum, 697-698 
Cranium, 121-135 
foramina, 129-133 
morphometrics, 121-129 
Cycles (see Demography) 
Cytogenetics, 849-853 


Damage to agriculture, 621-623 


886 Index 


Demography, 567-612 
causes, 588-609 
food, 588-589, 594-597, 804- 
806 
genotypic behavior,592, 602- 
604 
multifactorial, 592-594, 604- 
609 
phenotypic behavior, 590-592, 
600-602 
predation, 589, 597-598 
quantitative inheritance, 870- 
875 
role of dispersal, 590 
spacing behavior, 589-590, 598- 
600 
effect on communities, 326-327 
fence effect, 440 
impact of predation, 556-563 
mathematical models, 609-610 
methods of study, 569-572 
patterns, 572-588 
relation to dispersal, 427, 430-432, 
436-442 
Dentition (see also Teeth) 
macroanatomy, 140-150 
ultrastructure, 196-202 
Development, 255-280 
neonatal, 263-265 
post-implantation, 258-259 
postnatal, 270-277 
pre-implantation, 256-257 
stages, 262 
Dicrostonyx 
systematics, 54, 56-57 
taxonomic key, 62-66 
Diet, 329-332, 781-790 (see also 
Nutrition) 
Digestive system 
macroanatomy, 140-155 
ultrastructure, 216-240, 242, 244 
Diseases (see Pathology) 
Dispersal, 420-448 
behavioral features, 432-434 
categories, 425-429 
demographic causes, 436-442 
demographic consequences, 436- 
442, 590 


demographic features, 427, 430- 
432 

evolutionary issues, 442-445 

fence effect, 440 

genetic features, 434-436, 865- 
867 

relation to spacing behavior, 405 

techniques of study, 422-425 

Dispersion, 405-406 


Ear, internal, macroanatomy, 133- 
135 
Ectoparasites, 455-504 (see also 
Parasites) 
Electrophoresis (see Genetics, allo- 
zymic variation) 
Endocrinology, 685-718 
adrenal gland, 704-716 
Bruce effect, 699-700 
corpus luteum, 697-698 
estrus, 693-697 
gestation, 698-700 
lactation, 701-702 
ovulation, 693-697 
postpartum estrus, 700-701 
testicular activity, 702-703 
thyroid gland, 703-704 
timing of reproduction, 686-693 
nutritional cues, 689-691 
photic cues, 688-689 
seasonality, 687-688 
sexual maturation, 686 
social cues, 691-693 
Endoparasites, 528-534 (see also 
Parasites) 
Energetics, 812-839 
effect on activity, 384 
effect on spacing behavior, 406- 
407 
energy acquisition, 817-821 
energy allocation, 821-836 
activity, 830 
growth, 830-834 
reproduction, 834-836 
temperature regulation, 821- 
824 
thermogenesis, 824-830 
methods and terminology, 815-817 


models, 814, 816, 837-838 

role in community structure, 332 
Esophagus, ultrastructure, 218-222 
Estrus, 693-697, 700-701 
Evolution (see also Fossil record, 

Systematics) 

karyotypic, 852-853 

of dispersal, 442-445 
Eye, ultrastructure, 180-193 


Fence effect, 440 
Fish, predation by, 558-559 
Fleas, 484-503 
Flies, as parasites, 482-484 
Food (see also Plant secondary com- 
pounds, Nutrition) 
digestibility, 790-797, 818-821 
gathering, 818 
habits, 781-787 
palatability, 789-790 
reproductive cues, 689-691, 729- 
730 
role in demography, 588-589, 
594-597 
role in litter size, 763 
selection, 329-332, 787-790 
Fossil faunas, 37-51 
Fossil record 
definition, 1-2 
Microtus group, 15-29, 105-113 
Pitymys group, 5-15 
sites, 3 
systematics, 5-29 
time chart, 5 


Gall bladder, macroanatomy, 153 
Genetics, 845-878 
allozymic variation, 853-864 
natural selection, 857-864 
polymorphisms, 853-857 
cytogenetics, 849-853 
pelage coloration, 846-849 
quantitative genetics, 864-875 
age at sexual maturity, 869 
aggressive behavior, 867-869 
dispersal, 865-867 
growth rates, 868-869 


Index 887 


heritability, 864-865 
population regulation, 870-875 
role in activity, 384 
role in demography, 592, 602-604 
role in dispersal, 434-436, 603- 
604 
Gestation, 262-263, 698-700 


Glans penis, macroanatomy, 156- 
157 
Grassland biome, 99, 101 
Growth 
demographic consequences, 605- 
607 


energetics, 830-834 
genetics, 867-869 
post-implantation, 256-258 
postnatal, 270-275 
pre-implantation, 256-257 
Gut, macroanatomy, 152-155 


Habitats, 287-305 
agricultural, 304-305 
cover, 298-299 
graminoid, 291-292 
human activities, 302-305 
insular, 300-301 
moisture regimes, 295-298 
non-graminoid herbaceous, 293 
nutritional differences, 803-804 
patchiness, 301-302 
rocky, 294-295 
species diversity, 310-316 
succession, 327-329 
wooded, 293-294 

Home range, 398-401 

Hormones, affects on aggression, 

601-602 (see also Endocrinol- 


ogy) 


Infradian rhythms, 382-384 
Insular forms, 85, 109 
competition, 323-324 
demography, 599-600 
habitats, 300-301 
Integument 
macroanatomy, 118-121 
Meibomian glands, 120 


888 Index 


plantar foot pads, 120-121 
skin glands, 118-120, 356-359 
ultrastructure, 194-196 
Interspecific interactions 
effects on activity rhythms, 386- 
387 
effects on spacing behavior, 409 
Intestine 
macroanatomy, 153-155 
ultrastructure, 233-240, 242, 244 


Karyotypes, 109-110 (see also Cy- 
togenetics) 

Kin selection, 591-592 

Kite predation, 541-550 


Laboratory management, 647-657 
breeding, 655-656 
housing, 653-657 
records, 653 
Lactation, 701-702 
Lagurus 
systematics, 54, 56 
taxonomic key, 62-66 
Lasiopodomys, 17 
Lemmings, taxonomic key, 62-66 
Lemmus 
systematics, 54, 56-57 
taxonomic key, 62-66 
Lice, 478-481 
Light cues, 688-689 
Litter sizé, 266-268, 751-766 
Liver, macroanatomy, 153 


Macroanatomy, 116-169 (see also 
Anatomy) 
Mammalian predation, 550-558 
Mammary glands, macroanatomy, 
157-158 
Management (see Control) 
Mating systems, 344-353, 591 
Meibomian glands 
macroanatomy, 120 
ultrastructure, 193-194 
Microanatomy, 177-247 (see also 
Anatomy) 
Microtus 
fossil record, 15-29 
general characteristics, 59-60 


skin glands, 118-120 
taxonomic characters, 55-57, 166- 
167 
taxonomic key, 62-66 
zoogeography, 105-113 
Muicrotus abbreviatus 
distribution, 89 
endoparasites, 529, 531 
fleas, 491 
mites, 461 
Microtus agrestis 
breeding season, 738 
similarity to Microtus pennsylvan- 
(CUS. Zi 
Muicrotus breweri 
adrenal glands, 243 
breeding season, 731 
caecum, 238 - 
demography, 583, 585, 587 
distribution, 90 
endoparasites, 529 
fleas, 491 
lice, 480 
ticks, 476 
Mucrotus californicus 
breeding season, 733-734 
demography, 577, 580, 582-583, 
587 
distribution, 97, 100, 107 
endoparasites, 529, 532 
fleas, 491-493 
fossil record, 20-21 
lice, 480 
mites, 461-462 
pre-implantation development, 256 
social organization, 346, 351-352 
ticks, 476 
Muicrotus canicaudus 
distribution, 91, 94, 110 
fleas, 493 
prenatal mortality, 245 
ticks, 476 
Maicrotus chrotorrhinus 
breeding season, 733 
distribution, 95, 99, 108 
endoparasites, 529, 532 
fleas, 493-494 
fossil record, 23-24 


mites, 462-463 

Old World affinities, 55 
pelage, 118 

ticks, 476 


Microtus coronarius, distribution, 96 
Microtus deceitensis, 16-17, 107-108 


Microtus gregalis, distribution, 111 


Microtus guatemalensis, distribution, 


101, 106 

Microtus llanensis, 8 

Microtus longicaudus 
breeding season, 731-732 
demography, 583, 585, 587 
distribution, 92, 95-96, 108 
endoparasites, 529, 532 
fleas, 494-495 
fossil record, 22 
lice, 480 
mites, 463-464 
Old World affinities, 55 
skin glands, 119-120, 195-196 
ticks, 476 

Microtus mexicanus 
breeding season, 731-732 
demography, 585-587 
distribution, 99, 102, 109-110 
endoparasites, 529, 532 
fleas, 495 
fossil record, 20 
karyotype, 109 
lice, 480 
mites, 464 

Muicrotus miurus 
communal nesting, 355-356 
distribution, 89, 110-111 
endoparasites, 529, 532, 533 
fleas, 495-496 
fossil record, 18, 20 
lice, 480 
Meibomian glands, 120 
Old World affinities, 54 
ticks, 476 

Microtus montanus 
breeding season, 735-736 
distribution, 91-92, 94-95, 110 


endoparasites, 529-530, 532, 534 


fleas, 496-497 
fossil record, 22-23 


Index 889 


karyotype, 110 

lice, 480 

mites, 464-465 

nutritional cues, 689-691, 729 
pituitary gland, 179-180 

skin glands, 118-120 

social organization, 346-348 
ticks, 476-477 


Microtus nesophilus, distribution, 90 
Microtus oaxacensis, distribution, 101, 


106 


Microtus ochrogaster (see also Pity- 


mys ochrogaster) 
breeding season, 736-737 
communal nesting, 356 
demography, 577, 581, 587 
distribution, 99, 101, 103 
endoparasites, 528, 530, 532 
fleas, 497 
lice, 480 
mites, 465-466 
retina, 185 
social organization, 346, 348-349 
ticks, 477 


Microtus oeconomus 


breeding season, 737 
demography, 585-587 
distribution, 88-90, 110-111 
endoparasites, 530, 532, 534 
fleas, 497-498 

fossil record, 18 

lice, 480-481 

mites, 466 

skin glands, 119-120, 195-196 
ticks, 477 


Microtus oregoni 


breeding season, 734 
demography, 583-584, 587 
distribution, 91, 93, 107-108 
fleas, 498 

lice, 481 

mites, 467 


Microtus paroperarius, 17-18, 107 
Microtus pennsylvanicus 


activity rhythms, 381-384 
adrenal glands, 241, 243 
brain, 179 

breeding season, 737-738 


890 Index 


C-3 and C-4 grasses, 27 
communal nesting, 354-355 
demography, 575, 577-580, 587 
digestive tract, 218-240, 242, 244 
dispersion, 405-406 
distribution, 89-91, 107, 109 
endoparasites, 529, 530-531, 533, 
534 
eye, 180-193 
fleas, 498-501 
fossil record, 25, 27, 50-51 
home range, 398-401 
karyotype, 109 
lice, 481 
mites, 467-470 
movement types, 402-405 
salivary glands, 203-217 
similarity to Microtus agrestis, 27, 
5D 
skin glands, 119-120, 194-196 
social organization, 345-347 
teeth, 198-202 
ticks, 477-478 
wounding, 362 
Microtus pinetorum (see also Pitymys 
pinetorum) 
breeding season, 738-739 
distribution, 101, 104 
endoparasites, 529, 531, 533 
fleas, 501-502 
lice, 481 
mites, 470-471 
reproductive system, ultrastruc- 
ture, 243, 245-246 
social organization, 346, 350-351 
ticks, 478 
Microtus quasiater, distribution, 101- 
105 (see also Pitymys quasiater) 
Microtus richardsoni 
breeding season, 732-733 
distribution, 95, 98, 108 
endoparasites, 531, 533 
fleas, 502 
fossil record, 20 
mites, 471 
Old World affinities, 55 
pelage, 118 
social organization, 346, 351 


Microtus sp. 
fossil record, 28 
mites, 472 
ticks, 478 
Microtus speothen, 18 
Microtus townsend 
breeding season, 733-735 
demography, 574-577 
distribution, 91-92, 109 
fleas, 502-503 
karyotype, 109 
lice, 481 
mites, 471-472 
ticks, 478 
Microtus umbrosus, distribution, 101, 
106 
Microtus xanthognathus 
breeding season, 732-733 
communal nesting, 355 
demography, 586-587 
distribution, 95, 97, 108 
endoparasites, 531 
fossil record, 25-26 
pelage, 118 
social organization, 346, 349-350 
Mimomys, 7, 64, 108 
Mites, 457-472. 
Molt, 273, 276 
Mortality 
postnatal, 273 
prenatal, 259, 261-262 
Movement types, 402-405 
Multi-factorial demographic mech- 
anism, 592-594, 604-609 
Musculature, macroanatomy, 136- 
138 


Neodon, 6, 55, 65, 106 
Neofiber, systematics, 65, 71 
Neonatal development, 263-265 
Nesting, 343-344 
Non-social behavior, 341-344 
Nutrition, 779-806 (see also Diet, 
Food, Plant secondary com- 
pounds) 
diet, 329-332, 781-790 
digestibility, 790-797, 818-821 
forage quality, 790-797 


habitat differences, 803-804 

nutrients, 797-800 

optimal foraging, 801-803 

role in population dynamics, 804- 
806 


Ontogeny, 254-280 

Olfactory communication, 356-359 
Optimal foraging, 801-803 

Oral cavity, macroanatomy, 150-151 
Orientation, 181 

Outbreaks, 304 

Ovulation, 693-697 


Parasites 
ectoparasites, 455-504 
beetles, 481-482 
fleas, 484-503 
flies, 482-484 
lice, 478-481 
mites, 457-472 
ticks, 472-478 
endoparasites, 528-534 
acanthocephalans, 528-529 
cestodes, 529-531 
nematodes, 531-533 
trematodes, 533-534 
Parasitism, affects on 
rhythms, 386-387 
Parental behavior, 270 (see also So- 
cial structure) 
Parturition, 262-270 
Pathology, 657-676 
bacterial infections, 662-669 
constitutional diseases, 674-676 
fungal diseases, 671, 673 
neoplasms, 672-674 
protozoan infections, 670-671 
viral infections, 657-662 
Hedomys,.679, 11,.13=14, 55.66 
Pelage coloration, 846-849 
Phaiomys, 6, 9, 66, 106 
Phallic morphology, 156-157 
Phenacomys, taxonomic key, 62-66 
Pheromones, 691-693 
Pituitary gland, ultrastructure, 179- 
180 
Pitymys 
fossil record, 5-15 


activity 


Index 891 


pelage, 118 

Pleistocene distributions, 105-107 
skin glands, 118-120 

systematics, 54-57 

taxonomic key, 62-66 

teeth, 5-7 

Pitymys aratai, 12 

Pitymys cumberlandensis, 11 

Pitymys dideltus, 12 

Pitymys guildayi, 9-11 

Pitymys hibbardi, 12 

Pitymys involutus, 11-12 

Pitymys llanensis, 12-13 

Pitymys mcenown1, 13 

Pitymys meadensis, 15 

Pitymys ochrogaster, fossil record, 13- 
14, 49-50 (see also Microtus 
ochrogaster) 

Pitymys pinetorum, fossil record, 14- 
15, 48-49 (see also Microtus pi- 
netorum) 

Pitymys quasiater, fossil record, 15 
(see also Microtus quasiater) 

Pitymys sp., fossil record, 7-9 

Plant secondary compounds, 790- 
797, 800-801, 821 (see also 
Food) 

role in demography, 588-589, 
596-597 

Plantar footpads, 120-121 

Pleistocene distributions, 105-113 

Population cycles (see Demography) 

Population dynamics (see Demog- 
raphy) 

Postcranial skeleton, 135-136 

Postnatal development, 270-277 

Postnatal mortality, 273 

Postpartum estrus, 700-701 

Predation, 535-563 

by amphibians, 558-559 

by birds, 537-550 

by fish, 558-559 

by mammals, 550-558 

by reptiles, 558-559 

during outbreaks, 304 

effects on activity rhythms, 386 

effects on demography, 589, 597- 
598 


892 Index 


impact, 547-550 
role in species diversity, 324-325 
role of cover, 589, 597 
Pregnancy, 740-745 
Prenatal development, 255-262 
Prenatal mortality, 259, 261-262, 
763-766 


r- and K-selection, 277-280, 332 
Raptors, predation by, 538-550 
Reproduction 
energetics, 834-836 
hormonal timing, 686-693 (see 
also Endocrinology, timing of 
reproduction) 
Reproductive patterns, 725-768 
breeding intensity, 740-751 
pregnancy, 740-745 
sex ratio, 748-751 
sexual maturity, 745-748 
breeding season, 728-739 
duration, 730-731 
environmental cues, 729-730 
patterns, 731-739 
litter size, 751-766 
effect of age, 761-762 
effect of parity, 761-762 
mortality, 763-766 
variation, 760 
Reproductive system 
female tract, 158-159 
gross anatomy, 155-159 
male accessory glands, 157, 159 
Reptiles, predation by, 558-559 
Retina, ultrastructure, 243, 245-247 
(see also Eye, ultrastructure) 
Runways, 343-344 


Salivary glands, ultrastructure, 202- 
217 
Scent marking, 357-359 
Sebaceous glands (see Integument, 
Skin glands) 
Secondary compounds (see Plant 
secondary compounds) 
Sex 
effects on activity rhythms, 385 
effects on spacing behavior, 407- 
408 


mex ratio, 206-274 
demographic consequences, 607- 
609 
patterns, 748-751 
Sexual maturation, 276-277, 745- 
748, 869 
Shrew predation, 550-551 
Shrubland and woodland biomes, 97, 
99 
Skeleton, 121-136 
cranial, 121-135 
postcranial, 135-136 
Skin glands 
in olfactory communication, 356- 
359 
macroanatomy, 118-120 
ultrastructure, 194-196 
Social behavior (see Behavior, so- 
cial) 
Social organization (see Social struc- 
ture) 
Social structure, 344-353 
Spacial heterogeneity, 593 
Spacing behavior (see Behavior, 
spacing) 
Species diversity, 310-321 
role of climate, 316-318 
role of competition, 321-324 
role of predation, 324-325 
role of substrate, 318-319 
role of vegetation, 319-321 
Stenocranius, 20, 54, 89 
Stomach 
macroanatomy, 152-153 
ultrastructure, 221, 223-233 
Stress hypothesis, 590-592, 600-602 
adrenal gland, 704-716 
Subspecies concept, 127-129 
Substrate, role in species diversity, 
318-319 
Succession, role in species diversity, 
327-329 
Swimming, 296, 342-343 
Synaptomys 
systematics, 56 
taxonomic key, 62-66 
Systematics, 53-81 
artichoke method, 75-76 


cladograms, 61 

fossil record, 5-29 

historical viewpoints compared, 
74-81, 159-169 

history at the genus level, 55-68 

history at the species level, 68-74 

karyotypes, 853 

synonyms, 57-59 

using macroanatomy, 159-169 


Taiga biome, 90-97 
Tarsal glands (see Meibomian 
glands) 
Taxonomic key, 62-66 
Teeth 
macroanatomy, 140-150 
terminology, 4-5 
ultrastructure, 196-202 
Temperate deciduous biome, 101 
Temperature regulation, 821-824 
Territoriality, 401-402 
Testicular activity, 702-703 
Thermogenesis, 824-830 


Index 893 


Thermoregulation, 812-839 (see also 
Energetics) 

Thyroid gland, 703-704 

Ticks, 472-478 

Tongue, macroanatomy, 151 

Tundra biome, 88-90 

Tunnels, 343 


Ultradian rhythms, 381 
Ultrastructure (see Anatomy, Mi- 
croanatomy) 


Vegetation, role in species diversity, 
319-321 
Vocalization, 359-360 


Weasel predation, 551-554 
Wounding, 362-364 


Zoogeography, 84-113 
ecological, 85-105 
historical, 105-113 
species numbers, 84-85 


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