an ay i t SFE oe : ¥, erences a asic i iS) h ahs Hh riy fe Sa oa : : Leaner ose Se = Se ae BS ax i 2 Ree nm a = SAS Te ee a Sop re ae ee : ee Sa ee eT, Sores nai " Mey HARVARD UNIVERSITY e 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 2010 oo ee pe, 60 | : Bgel;Ge © be---- ; 1 55> eS 0, 54 5p - BLAS 28 \161-162 % 4 (154 153 165; 3132+ 66-67: 148-152) oe am 69°70~___! 136-147 3 Wxigg~“-|--} 68 eSB, | 169 334 43-44 52 |! 1442-12 fo.) af ' \ \42 1 121 < 77,80 72:115-120 ~ga-st” \\ 73;76114 199- 113:\ ~~ eae = 108 81-83 87/93 98-107 “9495 96 86 ‘ 85 ~ 84 cot ce 1 a) Co See 6 | \ 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) uJ = 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 ‘payioyd jou st (y xipuaddy) ¢¢z aig “s[relap 40J syuNoo0e satoads pue y xtpueddy aa¢g 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 ‘panoyd jou st (y xtpuaddy) ¢¢z a1tg ‘s[ielap 10j syunosoe satoads pue y xtpuaddy 3ag ‘paisodas usaq aaey Snjo121py jo satoads JOUNxI YOIYM WOJJ saeig pallu, snon3nuos pue epeuery UI sais Jo uoTeOO] aewIxoddy ‘9 ‘O14 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. Selected Bibliography* ANDERSON, E. 1974. 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(64) 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. Literature Cited ANDERSON, S. 1960. The baculum in microtine rodents. Univ. Kansas Publ. Mus. Nat. Hist., 12:181-216. 1974. Patterns of faunal evolution. Quart. Rev. 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The glans penis in Neotropical crice- tines (Family Muridae) with comments on the classification of muroid rodents. Misc. Publ. Mus. Zool., Univ. Michigan, 123:1-57. Howe LL, A. H. 1920. Description of a new race of the Florida water-rat (Neofiber alleni). J. Mamm., 1:79-80. Hrasé, V. 1978. Tarsal glands of voles of the genus Pitymys (Microtidae, Mam- malia) from southern Austria. Folia Zool., 27:123-128. JANNETT, F. J., JR. 1975. ‘Hip glands’ of Microtus pennsylvanicus and M. longi- caudus (Rodentia: Muridae), voles without hip glands. Syst. Zool., 24:171- 175: JANNETT, F. J., JR., AND J. Z. JANNETT. 1974. Drum-marking by Arvicola rich- ardsoni and its taxonomic significance. Amer. Midland Nat., 92:230-234. KIRKLAND, G. L., AND F. J. JANNETT, JR. 1982. Mucrotus chrotorrhinus. Mamm. Species, 180:1-5. Kretzol, M. 1969. Skize einer Arvicoliden-Phylogenie Stand 1969. Vertebrata hungarica, 11/1-2:155-193. MarsHALL, L. G. 1980. Systematics of the South American marsupial family Caenolestidae. Fieldiana (Geol.), 5:1-145. MartTINn, L. D. 1979. The biostratigraphy of arvicoline rodents in North America. Trans. Nebraska Acad. Sci., 7:91-100. MatTTHEy, R. 1957. Cytologie comparée, systématique at phylogénie des Micro- tinae (Rodentia-Muridae). Rev. Suisse, Zool., 64:39-71. MerRIAM, C. H. 1891. Results of a biological reconnaissance of south-central Idaho. 2. Annotated list of mammals, with descriptions on new species. N. Amer. Fauna, 5:31-87. MILLER, G. S., JR. 1896. Genera and subgenera of voles and lemmings. N. Amer. Fauna, 12:1-78. 1912. Catalogue of the mammals of western Europe. British Mus., Lon- don, 1019 pp. Taxonomy and Systematics 83 1923. List of North American Recent mammals. Bull. U.S. Natl. Mus., 128:1-673. NADLER, C. F., ET AL. 1978. Biochemical relationships of the Holarctic vole genera (Clethrionomys, Microtus, and Arvicola (Rodentia: Arvicolinae)). Canadian J. Zool., 56:1564-1575. NELSON, G., AND N. PLATNICK. 1981. Systematics and biogeography, cladistics and vicariance. Columbia Univ. Press, New York, 567 pp. Quay, W. B. 1954a. The meibomian glands of voles and lemmings (Microtinae). Misc. Publ. Mus. Zool., Univ. Michigan, 82:1-23. 19546. The anatomy of the diastemal palate in microtine rodents. Misc. Publ. Mus. Zool., Univ. Michigan, 86:1-49. ——. 1968. The specialized posterolateral sebaceous glandular regions in mi- crotine rodents. J. Mamm., 49:427-445. REPENNING, C. A. 1968. Mandibular musculature and the origin of the subfamily Arvicolinae (Rodentia). Acta Zool. Cracoviensis, 13(3):1-72. ——. 1983. Pitymys meadensis Hibbard from the Valley of Mexico and the classification of North American species of Pitymys (Rodentia: Cricetidae). J. Vert. Paleontol., 2:1-482. SCHWARTZ, A. 1953. A systematic study of the water rat (Neofiber alleni). Occas. Papers Mus. Zool., Univ. Michigan, 547:1-27. Simpson, G. G. 1945. The principles of classification and a classification of mam- mals. Bull. Amer. Mus. Nat. Hist., 85:1-350. WaAHLERT, J. H. 1978. Cranial foramina and relationships of the Eomyoidea (Rodentia, Geomorpha). Skull and upper teeth of Kansasimys. Amer. Mus. Novitates, 2645:1-16. WINGE, H. 1941. The interrelationships of the mammalian genera. Vol. II. Ro- dentia, Carnivora, Primates. C. A. Reitzels Forlag, Copenhagen, 376 pp. YOUNGMAN, P. M. 1967. Insular populations of the meadow vole, Microtus penn- sylvanicus, from northeastern North America, with descriptions of two new subspecies. J. Mamm., 48:579-588. 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. 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On the biology and systematic position of Microtus abbreviatus Miller, a vole endemic to the St. Matthew Islands, Bering Sea. Z. Saugetierk., 33:65-99. REPENNING, C. A. 1980. Faunal exchanges between Siberia and North America. Canadian J. Anthropol., 1:37-44. SAINT GIRONS, M.-C. 1973. Les mammiféres de France et du Benelux. Doin, Paris, 481 pp. SCLATER, P. L. 1858. On the general geographical distribution of the members of the class Aves. J. Proc. Linn. Soc. (Zool.), 2(for 1857):130-145. SHELFORD, V. E. 1963. The ecology of North America. Univ. Illinois Press, Ur- bana, 610 pp. Upvarpby, M. D. F. 1969. Dynamic zoogeography with special reference to land animals. Van Nostrand Reinhold Co., New York, 445 pp. —. 1975. World biogeographic provinces. Map, in A classification of the biogeographic provinces of the world. Internatl. Union Conserv. Nature and Nat. Resour. (IUCN), Occas. Paper, 18. VAN DER MEULEN, A. J. 1978. Miucrotus and Pitymys (Arvicolidae) from Cumber- land Cave, Maryland, with a comparison of some New and Old World species. Ann. Carnegie Mus., 47:101-145. WALLACE, A. R. 1876. The geographical distribution of animals. Harper and Bros., New York, 1:1-503; 2:1-607. WILEy, E. O. 1981. Phylogenetics. J. Wiley and Sons, New York, 439 pp. Woops, C. A., W. Post, AND C. W. KILPATRICK. 1982. Muicrotus pennsylvanicus (Rodentia: Muridae) in Florida: a Pleistocene relict in a coastal salt marsh. Bull. Florida State Mus., 28:25-52. YOUNGMAN, P.M. 1975. Mammals of the Yukon Territory. Natl. Mus. Nat. Sci. (Canada), Publ. Zool., 10:1-192. 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 144 xX snyJDUsOY]UDX x upuasumo} x (xX) snoiupajksuuad SNULOUODIIO (X) xm x x KKK KKM KKM KM ~ x xX xX SISUBIDXDO X X snjiydosau (x) XK snup]UOUL SNUDIIXIAUL (X) snpnooguo0) (X) bd >t dd OS ot tO ot OO ~*~ SNULYALOJOLYI xxx x SNPNDIVUDI xX (x) x sno1uLofrj09 xX xX 14ana1q SNJOLIYAT (X) a a a et ee aT aS sisuajpulajons ~ ~ ~ ~ ~ skuojaqgazy xX xX xX xX x 1u0daL0 Snqopy’) Xx X (x) X (x) xX x 1UOSPLDYIUL stuoovjny 19S. £9 “TLC Ur £9C To Wes Pr Pe Lo 2 ©°ol ec Tr Ler ec satsads pue + TLL? + TL + 9Z + 9€ +97 + LIE snuesqng SNJOLIIT ATUOM MAN NI NOILLVIYVA IVLNAQ TWdIONIYg c ATaVL 145 Macroanatomy ‘satoads jo UeIIeA UOUIUIOD ‘(X) ‘satoads jo a}e}s Jajoeseyo juayeAaid ‘yx ‘door assaasuen “Ty, ‘door s01saisod ‘Tg ‘sajsuern ‘7 ‘uado ‘o ‘pasop ‘9 :suonemaiqqy ne X (X) X (X) x X stumiud > 4 xX xX xX xX SNIDINILGGD smiup.z0uays x 4 xX xK (x) xX saqoisonb x x xX Xx unsojaurg shui (xX) xX x X x xX 43]SDB0LYI0 skuopadi xX (X) xX xX xX 4 snso.quin SKULOILY ILE) a a ee ee ee ee ee ed L9Z Lo TLE Db LC 199 LS Lp Le LOZ LE LOL L9%Z Lr Lol L-¢ satoads pue + TL + *1Le oC +9¢ +92 + LI€ snuasqng cu cul [ur CW CW CaNNLLNOD c ATaViL 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 juasaig uswelo} [eipedeig <— juasqy uswei0y Arey[ixewousyds juasqy usWIesIOJ [eyUOIJoUsYydS — 1Uasaig SNIJOSSIIIV I[VAO UIWILIO.T — UasoIg uawiesoy Alojyeonseyy <— spud [eAO UIWeIO} IAISIOUT WUasaIg syd jeieleg a8pliq + s8pry ayejed Auog snousaAeo ‘passaidwior) esso} prosAsaideieg S.J UsaMI0q SpudIx| aessoy prosAsajdosayy jJoys syoe'T Wqs0191UT juasaig ssao0id je11q101s0g Ajanbrygo paiusuO aiejd snewosh7 juasqy yoiou onewosh7 Woyus UINJISOI pue STeSeNy Apoq + peray> TEL U013[94S [leu peoiq syxor'T X3]]0d - xIS spedioo} sequel spur]3 QI > spur]s ueIWOgIIjy [— dry] — yuely Spur[s ULYS }UIUINSIIUT snq IPR] [PAI]-[equL, deprfooraly eaplomnyy sajeIeYo pue sulaishs ueBIC) “0490 ‘JO [AAI] OTWOUOXe} JY} 1k UISIIO 97e1S Ja}ORIeYY) SNJOLINAT AM GALIGIHXY SUYALOVUVHD AO AOVLIVAH{ AO STAAAT TWOIHOUVAI ¢ WIAVL 163 Ase][txeu [BUJU a S jeudios01eg 8 luasqy 8 ssa00id pt090.107) 8 p2onpoey = aB1e'] UONIISUL [eIPIyy ysnqol ‘Suo'] Ay[eIsIp pared ulstio Asaiie otwyeyidga wiaishs AlOIeNIIIT) UISIIO SNIpPIoAYyoTAIS snaprodyojnsn{- UONIISUL IOUT ST]eI0IIg apeoie snoutpuay dsesiq prosAsaid jeusaiuy snpunjoid sijesaie] Jajasse yyy UOpUa} Isa [eUGIOISOg ainiepnosnjAy umnauegyeo Jo ssa00id sea Yoo T, quasqy uauesoj repApuooidaiugq quasqy otoer0yi puz jo aulds [ena [9:1] 9:C 1 ones JeEquinjooRsOY J yuasIIg JAOOIS JUT[OOTAIY parearoxy esso} [esodwia} sepnqipueyy pesaie] paiutog ssao0id sepnsuy Jepnotpuadsag sna][eW anulyy umuedurA} Arossa0V a1e1IpO|] uOoneyUr JeT[ng eidas snasscC ae[nq Asoupny snq IPL] [PA2]-Tequ IePIfOOAIY eaploinyjy sJa}RIeYI pue sulaIsAS URSIC) -OLDIPAT ‘JO [9A] DIWOUOX} IY) 1k UISIIO 91e1S JaIOeIeYD SS —————— EE 0680606060686 daNNILNOD € AIAVL Carleton 164 aye[nooes “Suo'T umn3ae7) jUIsaIg Jappeyq [ep paqo]-uasaag JOAVT ease het Ploj Sutsapsog Jepnpurlsoosiqq uoIsar JepNpuely JepNosoj1g WO} YIeUIOIS padoyjaaapuc, sayonod ya—ay juasaid 3uQ aeyided areypeaumoity quasqy aSpli [RUIpN SUC] JOM IIUY pasny jou ngy siorsadns qe] Wxayuy peiqe] SuoT yrved s0stoul JaMorT juasqy saaoo0138 s1ostour saddq — sdooy] assaasues ¢ JVJOW JIMOT PTY], -— sy uado Z ‘pasojo Z JRJOU JIMOT PUOIIG - sy uado Z ‘pasoyo ¢ JeJOW JIMO] ISILT <— SY pasopo Z Jejour saddn party yf, — SV pasop ¢ Jejow saddn puosag jenby sa[sue juRIUs—I Jo yidaq Uasaig }UIWIT) BUIMOIBIIAI “JUISqY S]OO1 IR]OJ oneustd ‘uoposdA fy UMOID Ie[OJ wa}sks dANSaSIC] snq OPPO [PAI]-[equ deplpoorasly eaploinyAy sia}oeIeYS pue sula}shs ueSIC) -OLDINT ‘JO [9AI] OTWIOUOXe} JY) 1 UIZIIO a}e1s J9}OeIeYD CaANLLNOD € ATAV.L 165 Macroanatomy ‘snjoszy JO Satsads auIos UT puNo} SUONIPUOD paaluap s10W UIA = — ‘AqIIEJOd a1eIs Jajoereyo jo uonejaidsajur aaneusayye = | _— w«\j\_—— eee 0 cc Le CC i i I a eer = rm =TCT CCE spurls Areurweyy sired ¢ Spur]s aieIsoIg 1UISaIg Spur[s re[ndIsa A, 1UISIIg spurs Areypndwy UISaIg spurs [esyoinoq ng jUdSaIg spurs jenndaig [adAq xajduion] adA) xaduiory stuad sur[y [asoyideg] asoyideg WI Ja1eID [— 1151p yerpayy] Wuopld |, wuin[noeg waisks aanonpoiday JUSSGV TAS e222.) S]l0o G-¢ sdoo] o1]07p snq Ipelo [aaa]-Tequy, seplpoousy eaploinjy Sia}9eIeYD pue sulaishs ueSIO) -OLD1JAT ‘JO [2AI] OTWOUOXk} JY} 1e UIZIIO a}eIs JIIDeIeEYD 86G0u0ua—ou—q00 tooo GaNNILNOr) € ATaVL 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. 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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 € 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 {ae hs 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. Literature Cited AMSTERDAM, A., M. SCHRAMM, I. OHAD, Y. SALOMON, AND Z. SELINGER. 1971. Concomitant synthesis of membrane protein and exportable protein of the secretory granule in rat parotid gland. J. Cell Biol., 50:187-200. Barry, R. E., JR. 1976. 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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) ? 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 (1861 ‘O861) 49491 -pry pue YIOM {(0861) BHIOM SOX Sax oaBuel auofzy [eto J, snoudSAjog SNYJDUBOYIUDX “JA (L86L) 3tmpn'y < é yewowss3y sues aWwoTPy snouASAjod /snonostwo0ig 1UOSPLDYILL "AJ (SaT10}1I19} (C861 ‘186L) yeunuuos Butids dnou3 jeunwiwo0s uosIpey pue pless3zi1 7 a SOX -o pue ‘ayewiay ‘ayeyy) UTYIIM SNonostwWolg wunsojaurd “JA (1861) SYOOIg PUL 19}Sqa AA ‘(P861) ‘Te 19 Uost “PRI “(1861 “0861 “70861 ‘DO861 ‘BL6T) UOSIPeI ‘(8Z6L ‘ZLO6L ‘1961) 219D Sox So [e092 T a3uel fo) 60 (0) 8 SNONISIWIOIg snoiuvajtsuuad W (6261) Aeusig pue sewoyy (1861) ‘Te 12 2195) {(O86]) J9UeD pure 22D sox é [elsoy12 JT, [elojssa JT, snowesou0jy 43JSDBOLYIO ' JAI (Z861 AweSouou ‘O861 ‘8Z6l ‘LL6]) Heuuel < é [el0jI19 [ets0WI9 [, aaryeynoey /snoudsAl[og SNUD]UOU ‘JAY (096) UOsseag Awesouour ‘O861 “OL6I “EL6L) 494IPIT = (GBT) SAX é IE ELO ONE [EMO Moo aaneynoey/snoudsAjog sngiusofijD9 “Wl S2UdIIJIY sulio}s Busou soTewa J sae waysks Buneyy poo Ia os aera Fie reunut wiaysAs [e1I00g -w0r) SAIOAdS SNJOLI1JAJ TWAAAAS AO NOLLVZINIOYUO TWIOOS AHL JO SYALANVAVD LNAAIAIG c ATAVL 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. 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JOHNSON. 1979. Scent marking in taiga voles. J. Mamm., 60:400-403. WoLrr, J. O., AND W. Z. LIDICKER, JR. 1980. Population ecology of the taiga vole, Microtus xanthognathus, in interior Alaska. Canadian J. Zool., 48: 1800-1812. 1981. Communal winter nesting and food sharing in taiga voles. Behav. Ecol. Sociobiol., 9:237-240. WrRABETZ, M. J. 1980. Nest insulation: a method of evolution. Canadian J. Zool., 58:938-940. YOUNGMAN, P. M. 1975. Mammals of the Yukon Territory. Natl. Mus. Nat. Sci., Ottawa, 192 pp. 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. 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Ang (OL61) oxeuryIy =(pyo5E SI ELLEN OC 0 ‘a ‘ds ‘Mm ‘Vv ‘ns Be NM hi (M) [eurniq, (1861) (ns) ‘Te 19 dsopsultry Suidde. y, refnosndasry OZ J ‘ds ‘mM SV ‘ns (ns) yeusnq90N (961) UURULIDISC S(PESt (M) Teusniqd 0'¢ O ‘A ‘dg ‘Mm ‘W ‘NS (ZLOL) ‘Te 19 PUNTYIN sadojostorpey = O1S-0'1 Ag (0861) Sieqssour 49} é(dg ‘vy ‘ns) -wog pue uueUlya'T -unoo adesseg otmyydyiry = (MA) [eUINIG 07 a ‘ds ‘Mm ‘Vv ‘ns 301n0¢ anbruyoa,T, JIm1O UeIPedIID ueIpen{Q ,suonmpuos Apnig satadg f{sumyiAys AATDY GaNNILLNOD 1 HTaVL 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 (LE61) uo} IWR FY a< 4 A sutddesy, fs) ‘M > %S OOF 6 2 (X) (OL61) 2295 0 B

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. Literature Cited ADAMS, W. H., R. W. EMMONS, AND J. E. Brooks. 1970. The changing ecology of murine (endemic) typhus in southern California. Amer. J. Tropical Med. Hyg., 19:311-318. Parasites 505 ALLRED, D. M. 1952. Plague important fleas and mammals in Utah and the western United States. Great Basin Nat., 12:67-75. ——. 1968a. Fleas of the national reactor testing station. Great Basin Nat., 28: 73-87. ——. 190686. Ticks of the national reactor testing station. Brigham Young Univ. Sci. Bull., Biol. Ser., 10(1):1-29. ———. 1970. Mites and lice of the national reactor testing station. Brigham Young Univ. Sci. 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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 s[Mo sited 77 L178 symey sited pp ZE JIUIWING 8p6] S[MO cl CC Ire 91 LLL7 1 symey /Z SS 000°SZ JNUIM 8b6l sjmo sated [Z L718 symey sited Zp 87 JIWUINS ZP61 Ss[_MO C9 97 LEv'6Ll 1:S06'1 SYMPY 96 L8 000‘C0€ JUIN Zh61 uae uae ones s0jdes sioj}des Jo ‘ON yop s0jde4 uonetndod uonejndod SNJOLIIJAT -SNJOLIIJAT 9ATIII][OO SNJOLIIJAT SNJOLILJAT jo ‘ON UI SNJOLIIPAT jo JUZ0I9g jo uonejuas -aidai ju3019g (9S6L) GVAHDIVUD AGNV GVAHDIVAD dO SAYALdVHY) LNAYAAAIG] WOWd GATANASSY JWIM VLVC AHL ‘NVOIHOI NI VIYY AGALS ZWA-€6 V NO $NJ0491JA7 NO SIMO ANV SYMVH Ad NOILVGANd l ATAVL 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. 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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. 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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 sul -z1uojoo atiteid ‘gq ‘ssersantq ‘gq jenuuy é O€ “BITES WV MoT jenuuy ¢ SI 9L-SLOL d 4ajsv501Y490 "W 0€ Ad Ol 0S 9L-9L6T d (6261) ‘Te 19 219 Sj ‘stouly]] ‘puepure yy fenuuy = (9 OL 9L-SL6L Vv s1ojjeduioo ou MOT jenuuy SIZ S99 (€861) PPPY pue ensuoog b ‘o1sejUQ “puElUIe|] MoT jenuuy s9Z SIP MOT yenuuy SIE 00S 18-8261 0) PIPY PIO ‘AO ‘ssei3 10YS “NS (1861) ‘s1oynjaduros ou MO jencuy —0S O0¢: 9L-VL6l AO syoolg pue 19xeq ‘O1eUQC ‘purluleyy ese) | [BRU Sl $9¢ = 9L-VLOT OS (1861) s1oijeduioo ou SHOOIG PUL I9ISGI AA c ‘o1eUQC ‘puryureyy MOT ce ENULN SS 08 OOF 8L-LLO6L MOT jenuuy ¢¢ SS MOT [ENE = Oe 09 siojjeadui09 ou MOT jenuuy O€ 0S (ssard ut) Your C ‘eqouueyy “purpureyy Or apAy ST 06 SL apAQG S8 8 -8961 ©) SIOUIIIJIY (1 314) S310N xas Ajyts usloneg MOT YSIFT sIvaX pug uon -u3q ene 5 l ey/Alsuaq -2900] dey sormeudp Suds | ATAV], JO SALONLOOY FAS ‘sno1unapXsuuad ‘Py AOA ONIddVUL-AAI'T WOU SALLISNAC, NOLLV1NdOd f ATAVL 579 Population Dynamics and Cycles OST yenuuy SS 06 LL-9LO61 S MO'T jenuuy 0 SI snjojno MOT jenuuy Or Cll -1uDUL snoskKwolag MOT jenuuy Or SII (1861) ‘Te 19 Jasand 6 “BIUISITA ‘purpUreyy apAn OV S¢c = BL -F LOT I puepiom “TM ‘s10]NaduIo9 ou ‘v10s MO'T Jenuuy OL c6 (9L61) ‘Te 19 Aung 8 ~sUUTTA] ‘pueluleyy Cali UAsnone ns Ol 08 SL-CLol IM sndoonay ‘g ‘svias Auo 9 SL aA OF GSZ SL-ZLOL A (LL61) Ulrewe TL, L “nyoesseyy ‘puryure yy Ajuo 9 Sel apAn 0 Occ 3=9SL-CLOI d a . 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. Literature Cited ABRAMSKY, Z., AND C. R. TRAcy. 1979. Population biology of a non-cycling pop- ulation of prairie voles and a hypothesis on the role of migration in reg- ulating microtine cycles. Ecology, 60:349-361. ANDERSON, J. L. 1975. 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Social organization in cyclic subarctic populations of the voles Clethrionomys rufocanus (Sund.) and Microtus agrestis (L.). Ann. Zool. Fen- nica, 14:53-93. Watson, A., AND R. Moss. 1970. Dominance, spacing behaviour and aggression in relation to population limitation in vertebrates. Pp. 167-218, zn Animal populations in relation to their food resources (A. Watson, ed.). Blackwell Sci. Publ., Oxford, 477 pp. WEBSTER, A. B., AND R. J. BROOKS. 1981. Social behavior of Microtus pennsyl- vanicus in relation to seasonal changes in demography. J. Mamm., 62:738- Tole White, T. C. R. 1978. The importance of a relative shortage of food in animal ecology. Oecologia, 33:71-86. WHITNEY, P. 1976. Population ecology of two sympatric species of subarctic mi- crotine rodents. Ecol. Monogr., 46:85-104. Wotrr, J. O. 1981. Refugia, dispersal, predation, and geographic variation in snowshoe hare cycles. Pp. 441-449, in Proceedings of the world lago- morph conference, Guelph (K. Myers and C. D. MaclInnes, eds.). Univ. Guelph, Ontario, 983 pp. Wo irr, J. O., AND W. Z. LIDICKER, JR. 1980. Population ecology of the taiga vole, Microtus xanthognathus, in interior Alaska. Canadian J. Zool., 58: 1800-1812. WYNNE-EDWarDs, V. C. 1962. Animal dispersion in relation to social behaviour. Oliver and Boyd, Edinburgh, 653 pp. ZIMMERMAN, E.G. 1965. A comparison of habitat and food of two species of Microtus. J. Mamm., 46:605-612. 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 ‘(QZ6] ‘Ssunox pue sszkg wodJ) (SQ'Q < 7) 189} adues afdnynw s.uesuNng Aq WaJayIp Aypeonsneis jou aie Janay sures ay} SuIAeY suUNJO UIYIIM s]UIOog “UaUNeat] A[UO-aploIqsey ay} YUM JOU. 100d a}0U OSTy ‘QUOTe S]UIUNeII] IploIqsay IO UONRAN[ND Jaye UY) SajoA duId Jo JoNUOD Ja}Eq AAeS JUIUTeII] aprloIqsay-sn{d-uoNeAN[Nd ayi J10N ‘uoneorydde jo aun 0} Jajar smodue yim spoquidg ‘(snotaaid y pz shemuni ut paoeyd uayM sysew-y100) ajoa Buraey sajdde jo yuaosad) Aytarjoe juaosied uo ‘s}req paoed-puey (NqO) euouteydoso[ys pue (Nqq) euouleydip pue ‘ainino preyoso jo pay “¢ “Ol (2261-9261) YUONW (SL61-vL61) YsUOW 12) ouwooe6ee29?92s » € 2 | 2 woot6 @ £4 8 € © € 2 1 zt to 6 @ 2 e §¢ &» € 2 1 @woesea (AON* KIN) QUeHegind ao Od (AON + Ainge Kom) sing og (AINC) quen os (AON) 41ND © 10445u05 0 06 ool e e q eq q 2 2 9 q > 4 2 q q 25 307 ip q 44 q e e q qq 929 9 deed ie! e e e e qe q 2g 2 q ge 2 q 2 q q 2 3q 2 qe q qe q e e qe qeqe qexq2q 2q ge qe e e e ee q 2q 2q q e qq q q qe 2q qe 2q qe e ge e e e qe qeqe qexq qq e ee e e e ee q qe qe qe e qe q qe qe qe qe e qe qe e ge e e e qe qeqe qe qqe qe e ee e e e e e e e e e e e e e e e e e e e e e e e e e ee eee e e e: Ayiansoy % 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 ‘ajdde ay) uo syxseU-Y100) dTOA aJaM IJ9Y} YOTYM 1k says [fe 0} stajar AWATIOe JUV.IIg “}UIUIDe|d Jaye Y $7 paururexd s19M YUN) 991) & Jo saprs aytsoddo uo aoejans [Ios aYy1 MOTaq WO G][-G sUNI JO safoy OM} UT pade{d sajddy , ‘yuaujeV9.44 Jad sjoyd ajeotdas aary1 (S0'0 < qd) 3893 a8ues afdnynu s.ueounq Aq juasayIp AT[eoNsNeis JOU a7e 419}1a] JUIeS ayi Aq PIMOT[OJ SUNOS UTYIIM sraqUINN , "9911 YOR 1e Sa[SuIYS JapuN suoTed0] OM) 1e paoe{d-puey sem jUIUNeIIT ; “SqUIT] 99.1] JopuN pueq ke UI Jseopeoiq Sem JUIUT}eIIT , ‘aprydsoyd ourz ‘quz ‘auoureydip ‘Ngq ‘euouteydosoyp ‘NVgD ‘auoyetpowosg ‘9 .Jq :suonetAsiqqe JUsUNeAL +6 P 200 PL JP 61 & 68 2S 9 (sqe'T 19d) 119d %7—dUZ SI 76 POL‘0 PEC 2P? 67 2 68 Sc 87 (Sqe'T 119A) 119d %7—i1dUZ “bl 99 2q Zb'0 2g OT IGP 6S B C8 2S 9 sweOQ + UIOD %7—quUZ ‘¢€] 19 q 6r'0 qOorl qe 19 eg 6l 1Z sO + WOD %7—.dUZ “TI L9 oq 1F'0 oq 01 pod Or Lets} 201 Gi Ndd %S00':0—41wey 1] 18 Pq +7'0 P29 09 9q 1S & $8 We bZ Ndd %S000—:4tweY “Ol $8 P29 610 Po L'+ Pq bb e 18 07 Ze Tad %S000—1RXW “6 16 P ILO PLZ poq ¢¢ B 88 4 v7 (VSN) NdD %S00'0—119204 °8 66 P 10'0 P¢O JO & 88 GG Sc (youetq) NdD %S00'0—119Z0Y °L 86 P00 POT Pr e 18 cL 8 OA %S00°0 yoyord—,yRJOA ‘9 86 P c0'0 P¢O Ps ecg 97 67 OA %S000'0—iARIOA “S 86 P 700 PLO Ps & 88 LI 6l OAA %1000— ARICA “b 66 P 10°0 PCO P9 B C8 81 02 OA %SZ7O0'O— ARICA “€ 86 P £00 PLO JP SI & 88 6l 1Z OAA %S00'0— APIA “Z 0 2 G7] LTE cB L8 & 68 a = jonuoy '] JonUoD % (L-€ Wig O¢ “AON 6 “AON (oe/sqt) (ey /B¥) jusUNeaI YT, JIQUIID9 JOQUI999 a aC aan ae ial ann TC a ean aa. a payee AUATDW % pad 6L61 ‘SI-+1 WAGWNAAON GALVAYL SCYVHOUO NI TOALNOD ATIOA ANIG YOA SAGIOILNAGOY AAOVId-GNVH{ GNV LSvodvoug AO NOILVATVAY ATaly ¢ ATAV4L 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 Hs 3} 2 9 lo UW 12 1 2 3 4 5 ' 2 3 4 5 6 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 ANONYMous. 1957. 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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. 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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 damage to coniferous plantations. J. Forestry, 44:745-749. Luke, J. E., AND R. J. SNETSINGER. 1975. Apple trees protected from voles with thiram. Science in agriculture, Pennsylvania State Univ. Agric. Exp. Sta., 23:7-8. 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- degradation symposium (J. M. Sharpley and A. M. Kaplan, eds.). Applied Sci. Publ. Ltd., London, 1138 pp. MEEHAN, A. P. 1980a. The rodenticidal activity of reserpine and related com- pounds. Pesticide Sci., 11:555-561. 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. 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Rept., Mas- sachusetts Fruit Growers Assoc., North Amherst, Massachusetts, 7:60-—606. 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. HorsFALL, JR. 1973. Toxicity studies in endrin-susceptible and resistant strains of pine mice. Toxicol. Appl. Pharmacol., 25:42-47. Witte, L. 1965. Biological and ecological considerations in meadow mouse pop- ulation management. Bull. California Dept. Agric., 54:161-171. WoopsIDE, A. M., R. N. JEFFERSON, R. C. Moore, AND E. H. Gtass. 1942. Control of field mice in apple orchards. Virginia Polytech. Inst., Virginia Agric. Exp. Sta. Bull., 344:1-16. WYSOLMERSKI, J. C., R. E. BYERS, AND J. N. CUMMINS. 1980. Laboratory eval- uation of some Malus clones for susceptibility to girdling by pine voles. J. 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. 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(9) aun) potusad Sutuevsja yewoajeuw sulppog (wo) Busey satadg S -eradway, -o10yg jo Sunsan s Aguanba.iq 648 SHIDAdS SNJOLIAT AO LNAWAOVNVIY, AYOLVAOEV'T T aTaVL 649 Laboratory Management and Pathology (LL61) ‘Te 19 Aguuay (0861) noauuef pue uyais (LLOT) ‘Te 19 W2Ieg (6961) Aemeuory pure puoulysry (9961) AAPUIH (OL6T) UATOD pue ulAjorn (9261) ‘Te 19 Avis SIOUIIIJIY $180 ‘90NI}2] “MOY ISNOJ sjatjad WIqqes ‘MOYO 1ey sjatjed 1qqey JaAoyo ‘sseis ‘9onq ~12] “MOY 1qqey MOY) Ted ‘sinoids 1234 AA sadde ‘spaas Jamoyuns ‘gonyaq] ‘s10171e9 ‘Aayreq ‘Moyo Japaaiq asnoyy 99N})9] ‘sjaqjed 1qqey pooy aN d8"T91 aN ds8'T91 LO-1% dcl-Tcl CCC dcl'Icl jueisuory = juRIsSUuOT) LEVY dL ‘ILI (yes -19AII 1ystu -Aeq) queisuory) $8: 191 (69) aan} potuad -esaduiay, = -010Ug SYIIM Z dN aN Ares -S200U SY dN sym 9-€ aN sutueayo jo Aoguanbaly GaNNILNOD | aTaVL aN MBI1S ‘u01107) u0j10") Ary ‘sseiny dN uoj0r) 1BPISAN yelaieuw SUNISIN aN ISNPMeS ISNPMeS ISnpMeg aN yead pue [log [90-1-ues sulppog CaN onseid cl xX 81 x 9S eqjour SI x S€ x 02 yeqour GLE X COC X CE aN sqni [ej €l x 61 X 6¢ (wo) Sulser) 13]S08 -OLYIO “JJ satoads Mallory and Dieterich 650 (6261) uuewy pure [sw] (PLL61) Uorsaig pue yolsiIq (OL61) uIA[Or) puke UTATOT) (LL61) UoIsaig pue yosjiaIq (1861) 2199 pue sinyofyq (9261) ‘ye 19 UNIey $IDUIIIJIY Moy) Ja}suIeYy pue ssnour ‘ey $101.19 ‘sinoids Aayreq ‘was 1eIYyM ‘s}e0 ‘Moyo Japaaiq asnoyy sajdde ‘spaas Jamoyuns ‘gonjja] ‘s}orre9 ‘Aapreq ‘moyo Japaaiq asnoyy sjnoids Aayareq ‘s}o11e9 ‘s}eo ‘W393 yeayM ‘Moyo Japaaiq asnoyy mou uqqey Moy 1uqqey pooy CC Oc Lo-vb Oc aN aN (60) ean -eraduia COL Irl aN a8"191 AT499.M CUZ Ee 225122 0 eC a8'191 AT92.MA C8191 aN aN CaN potsad sutueay]o -0}0Ud ag Aouanba..q daNNILLNOD l aTaVL aN ansst} jepey u01}07) anssn jeoey uonon MPLS yetsaieul SUTISIN, aN ISNPMESY qead [10g isNnpMeG ISNPMES IsNnpMeS Surppog aN sse[sioqy SI x 91 x $8 sqni [ela sse[s1aqy St x ot * S38 a1IM Ov x OC Xx 02 SI x S@ x OF (wo) Suse, snaiupa -)Xsuuad “Pw 1U0BaL0 “JA snu -0U0240 ‘JA satoadg 651 Laboratory Management and Pathology ‘elep ou ‘QQ ‘uOneIAaIqqy spaas Jamoyuns ‘sjaqjed 31d sse[3 (0861) J9IPeEYyIS kaUINS ‘moyD 1eY_-B I-91 dcl'Icl dN suUON = IsNpMeS Ip x c9 x OF (O861) sjatjad MBAS onseyd und neuuef’ pue uyrig = uqqea ‘Moyo 1ey aN C8191 GN ‘uonoy) IsnpMesg cl x 81 x 9S -ojauid “J (1861) onseyd Te 19 JaisqaMq = Moup BId evauIny 02 as 191 GN 2UON Wid WIOD GTI xX 81 x 62 spaas (€Z61) Aouury Jamoyuns “OW pue Aajseg ‘MOYP Ino] vc dOl-Trl dN dN aN aN sadde eliesita [ew (pZ61) neuuel’ ‘moyp uqqey LZ 1-Z1— d8T91 GN = woneD KOS ‘sued UOTIeS) (LL61) sye0 *99N}}3] ‘Te 19 Asuusy ‘MOY) IsNoy] aN d8'191 S122MiG dN CN aN saqno 17es onse|d (OL61) ‘Te 39 99°] ‘sioqfed eyTesTV CC dOol-Trl Appemig = uonoD WB W0_D €l x OL X 6¢ (Lol ‘OL6T) AsO] s]0119 onseyd TIZIND RUE SOIT ‘$780 ‘MOY 1eY SC d9"'T81 Ajyaomig = UoNOTD ss SNpMEg ZT x SLT Xx $'87Z SIIUIIIJIY poo. (3) aan. ~—s potsad sutuesja jelaieu Surppog (wo) Bulge satadg -eladuiay, = -0104ug jo Sunsan AoguanbalJ GaNNILNOD Tl HTaVL 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. 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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 (OL) OST ¥ 06S (Ol) 6b + OO€ (Ol) 2h ¥ P8L‘T (6) 9721 ¥ SL9 OL (OL) 1SZ ¥ 766 (OL) 7@S + FOE (OL) E61 F C€9'F (Ol) 602 + 9S0°I 09 (6) L8 ¥* 099 (Ol) Lb + 8I¥ (Ol) €S9 ¥ S7S‘¢ (Ol) 6z€ ¥ ¥S0°Z OS (1) 9ST ¥ ZL6 (Ol) LS ¥ 96¢ (6) IL = LOO (IL) O€l + FPO'L Or (OD 6G1L = OLE (6) +6 ¥ b6r (Ol) 12S ¥ FIZ + (Ol) +92 + LOS‘T O¢ (L) SSL ¥ €88 (S) LIZ + €LL (L) €9b = OSI‘b (S) 877 l ¥ SS8‘Z 02 (S) LpZ ¥ L06 (S) ZSI F S16 iS) Jel Loe (S) 6246 ¥ €€L‘€ Ol (9) OLF F Z9S‘I CONC + 21601 (9) €80'l F 09€'8 (9) 69¢'l = 1506 I Se)iaerek | SITeI So[PUl2 J SoTeW Aeq ({w1/suier30ueu) Wnteg (Gm Apog 3 QQ] /sureisoueu) [eusIpy Nene ee ee ee ———————eee—— SOOO Eee 0000 OOOO (EL61 ‘WOOTAVaS ANV NISIQ YILAV) ALIALLdV dO SGOIMAG ONIAUVA AWALAV Snoiuvapdsuuad snjosnpy NI [(N) FS F X)] STAT INOWLSOOLLAOD S HTaVL 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 712 ‘(SQO'O > d) sasuodsas usaMieq SaUdJIYIP JULIYTIUBIS saijouIGq , ‘aatoeul ‘JT ueudeid ‘g ynpe ‘y npeqns ‘yg ‘attuaanf ‘f :ore sassejo aBe jo suonetAaiqqy x X > 4 x XxX xX X Xx Xx x X x X X x X x d Vv d Vv I Vv f cl epee x *X Vv vs Vv I Vv f Vv fh cLOL cLOl cLOL IL6l ILol Joumuins Ajieq suds -LL6I Tea JauIUINS 33e'T JOqUT MA 98¢ ocr 8LL 96¢ SS6 EVE LOv cov 89r PLe 98h 00S OSt Ice Cle Clp 9Ce agsuodsai jeusipy Staete atta < VS etintun ct sseo assy ZL6[ Jawuns Apey ZL6| Butsds ZL-1L61 J2IUTM TZol ed LL6[ Jawuns aie] so]eula J ZL6[ Jawuins Apeq ZL61 Butidg ZLOI-LLOL J91UTM TZol PA LL6] Jowuins 21e'7 Sate uoseag (SL61 “IV LA WOOTHVAS YALAV) Ssnguvaj{suuad snjos2py AO SIVNAAGY GaLVIAWILS-H LOV JO NOISsnNddadNS ONIMOTIOY (LHOIAM AGOG O OOL/ALVSNaAdAdNS IW G/SNVYDONVN) STAADT ANOUALSOOILUOD 9 ATAVL 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. 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The mouse: its reproduction and development. Burgess, Minne- apolis, 430 pp. SANDERS, E. H., P. D. GARDNER, P. J. BERGER, AND N. C. Necus. 1981. 6- methoxybenzoxazolinone: a plant derivative that stimulates reproduction in Microtus montanus. Science, 214:67-69. SCHADLER, M. H. 1980. The effect of crowding on the maturation of gonads in pine voles, Microtus pinetorum. J. Mamm., 61:769-744. —. 1981. Postimplantation abortion in pine voles (Microtus pinetorum) in- duced by strange males and pheromones of strange males. Biol. Reprod., 25:295-29 /. —. 1982. Strange males block pregnancy in lactating pine voles, Microtus pinetorum, and effect survival and growth of nursing young. Proceedings of the eastern pine and meadow vole symposium, 6:132-138. SCHADLER, M. H., AND G. M. BUTTERSTEIN. 1979. Reproduction in the pine vole, Microtus pinetorum. J. Mamm., 60:841-844. 724 Seabloom SCHULER, H. M., AND H. T. Grier. 1976. Duration of the cycle of the seminiferous epithelium in the prairie vole (Microtus ochrogaster). J. Exp. Zool., 197: 1-12. SEABLOOM, R. W. 1965. Daily motor activity and corticosterone secretion in the meadow vole. J. Mamm., 46:286-295. SEABLOOM, R. W., AND N. R. SEABLOOM. 1974. Response to ACTH by superfused adrenals of wild and domestic house mice (Mus musculus). Life Sci., 15: 73-82. SEABLOOM, R. W., S. L. IVERSON, AND B. N. TURNER. 1978. Adrenal response in a wild Microtus population: seasonal aspects. Canadian J. Zool., 56:1433- 1440. 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- ogy, 54:967-981. 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 activity in the meadow vole (Microtus pennsylvanicus). Gen. Comp. En- docrinol., 36:111-118. VAN TIENHOVEN, A. 1968. Reproductive physiology of vertebrates. Saunders, Philadelphia, 498 pp. VAUGHAN, M. K., G. M. VAUGHAN, AND R. J. REITER. 1973. Effect of ovariectomy and constant dark on the weight of reproductive and certain other organs in the female vole, Microtus montanus. J. Reprod. Fert., 32:9-14. VAUGHAN, M. K., R. J. REITER, G. M. VAUGHAN, L. BIGELOW, AND M. D. ALTSCHULE. 1972. Inhibition of compensatory ovarian hypertrophy in the mouse and vole: a comparison of Altschule’s pineal extract, pineal indoles, vasopressin, and oxytocin. Gen. Comp. Endocrinol., 18:372-377. 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. Keller fia2 (LL61) DA Eee AL, eBossUUTYY “OF YOOD ST I v SG PIUIBITA IS9AA “SOT JayON T, (L261) PUePTY pue ‘ydjopuey ‘seiuoyeoog S7 c 8 S-?@ 88°C (LL61) une Apnys winasnur Ajasre"] cS Fig IL'€ (LE61) AUaAO0TD ole ‘tureseua [, Jet2aag_ G S-Z 9S°¢ SNUIYLLOJOLYI “JA (SL61) JaSA.L, Auojoo A10ye10qe'T tr 61) uosoure [’ (OL61) uTA]Or) pue uTA]Or) (S961) Jauig pue sn3anN a0n0g Auojoo A1oyer0qe'yT Auojoo A107ye10qe'T stout] “orn ustedureyyy stoul]]] “oD usredueyy sesuey ‘0D se[snoq Ayonquay “on uossayal” eUueIpuUyT “sory UMOIG pUe s01U0PY sesuey ‘a[qeiue A eCURIPUT ‘Or) OSTA sesuvy ‘OD se[snoqg sesuvy “OD se[snoq sesuevy “orn se[snoq Apsoyy Auojoo Aroyeroqe’y Auojoo Asoyeloqe’y (s)uoneso] peotydess0a5y S$ dS S78dS dS 78 MC Del A* dél O0e 06 {pa;dures syuoyy I ol NN +2 Nr (G.O 0 | Teste 5 eh el saeak uoneing daNNLLNOD ¢ WTAVL 8c L-I O87 8-1 8C 6l 181 I¢ OI O91 19-1 861 bel L=G 8 Sieve G9 9-1 8S i= (Gy 6-€ €Sc Sd OI I N 4 SIUI91} “xo SOY ZS aeaal uray 4]SDGOLYIO "JA satoads 755 Reproductive Patterns (9S61) PIPPMD eqonurey] WWIsIq samy dol CC OVC 671 t0'S (€S6]) Sue H pueyAreyy “OD sosayotod. «= M + SAt c oF SES (€P61) Ulory erueafAsuuad “OF ploymesy) SA9 +1 v7 So S09 (LEO) Wore FY YOK MAN “O- surydwo yp, OSS v i LOS o1reqUg ‘xed (LE6L) Anusa0;y umnbuosyy pue twesewoe |, SAt I €7 de Ser (LE61) AnuaaoD O1reJUD “OWUOIO TL, SAP I 81 6-€ ts Ss (S€6]) pussuMoO T, YOK MIN “Or esepuoug AVA € It 6-2 LOS snoiupajdsuuad ‘Jy (O61) UIA]Or) puke UTAjOr) Auojoo A1oje10qe'T SI 9I-I g¢ (pS61) WNeUssIY pue ueMor) Auojoo Arole10qe'T 87 S-I GING (yS61) NeUasIY pue temo) ee cl I 9 Se Ile uoBIICQ “son (2261) saTImyses uUT] pure “sue'] ‘seuIExE[D AVA 91 81 |! LG iuowe10 "Wy PEEG) uoIsaIg pue yoraiaiq Auojoo A101e10qe'T 86 o€ (LLO1) Aout eysely ‘syueqiiey AVA v L 69 (SL61) UeWSUNOA AsO], UOYN A SZ Or 985°S (9561) 1[@H pue 2g eysely ‘odoyjs onosy S¢ 16 69 SNU0U0I—a0 “JAY 201n0G (s)uoneoo] festydess8095 {pa;dures steak NN ,souo 4 zis satads syUuoyy uoneind -xq Jan] ued da ANILNOD c ATEAVL Keller 756 (OL61) UIA[OT) pUue UTA[OT) (PLL6) Ulseue T, (9261) JousIN TL, pue UOSIIAT (SLoL) UeWBUNCA (OL61) SsqoIy pue J9[[9Iy (L961) WNYWOD (9961) stared pue uenysiyy (€961) uos -uIqoy pue noy (€961) UOS -uIqoy pure Noy (1961) poa'T VJ pue Jog (096]) Jouu0r (LS61) Ja}soyJ pue yitwg 20N0g Auojoo Aroyes0qe’T s}jas -snyoessey] ‘sory 2[qQeIs -uleg pue ysnosoga ppl eqonuryy ‘emeuld AlOWIII J, UOYN A eueIpU] “sor uMOIGg pue s01U0;I eueIpuy “0D OIA etueajAsuuad “OD Ul[yxUeI Ole}UG ‘O}UOIO TL, OLIeIUGD ‘0}UO0IO T, eJOsaUUTPY “OD aye'T ‘e10xeqG yIOX MIN “son alreyousg pure 032819 eqouueyyy “TPyonyD (s)uoneso] Teotydes30a5y OLC AVA SP Ole OTT ONCI Ss {pojdures syUuoyy daNNILLNOD ¢ WTaVL v sreah uoneing I¢ LS CVE eye vst cSt OL vel LE ISc /E\ N 8-C eS) 18-2 i Dit cB O1-Z cS iL-T vo Gal 9b'Y 989'P 8-1 S Since 60'P 3) Sa CLS OI-¢ Les cl-+ 69 4 S9W9.1} 4 2ZIS -xq Jay] ues on ——————— snaiuvapksuuad "W satoadg 757 Reproductive Patterns (8261) ‘Je 19 Jesuay eIuIsIIA “OC yoouueyeddey OTT I S€ 010°C (TL61) 2905) BWOYR|YO “OD audeg AVA9 c o1 GC ¥S'7 (0261) sprnedyiry eS TN PIUISITA “OD eruRAyAsntg Ocl I IS gal 0o'T (9961) Ined eulfoley) YON ‘sanunos g d0e c 8el Sail VOC PIUIBITA (€961) IejsioH “SO-) ayouvoY puke 11N01210g Ocl I al bol 0? wniojaurd study snuasqns (0861) J949Ipry eyseTy “eulunyoulypy PEEIOM 212] pue surged MN VEE OSE M1 se ic IZ Climo 88 (SL6[) Weusuno Xx AIOVWIIIT, UOYNZ SI I 1 OI-ZL 08 SnyJoUsOYIUDX “AT (92861) AOfACL, Poe e LEH ORIN eIquIN[o-D Yysniig ‘1oupey Oc Lema 09 (6261) elsucog eIquinjor ysniuig pue uosiapuy ‘Aauepy pue purysy weyisarA J6I Z 812 OLS upuasumo} “JA (QLL61) uolsoig pue yo1i3iq Auojoo Arojles0qe'] 99 lv 201n0g (s)uoneso] [eorydesB005) {pojdures sea N ,Seuiay 4aZzis satoadg sy Uo] uoneing -x¥ Jou] urea GaNNILNOY) ¢ ATEAVL (LL61) UMoIg BUEIUOTN Ue} 52 YIN Sc 92 O19. Sol Buiwok AA “OD yIeg (L961) ened pue ‘eurluoy “O) woe 91 SPs (6S61) A> -puly pue sn3aN Buiwod AQ “OF JUOUIIIT SZ Ol 6-S 09 1UOSPLDYIUL “IAT pjon1aip snuasqns (9261) ‘Te 19 UOSTIIOJAY Auojoo A10ye10qe'T eb (ts (9S61) IEE Pus sed BSLV, 4 cl-¥ c8 STEMAUE N. (9L61) ‘ye 19 UOSTIIOVY Auojoo A10ye10qe"T OG 5njv12aa1qqv ‘JAI sniupi20uayg snuasqng (661) uosjay pue [eH znsoeisA ‘edeyel Ll t-I OL Layoisonb JA (6261) UleIsi93 -Ing pue s2[;peys Auojoo A10ye10qGe"J OSI 9-1 LVe (8261) yey psusy = eIUIBIIA “OD youueyeddey og! I a n9T a 301n0¢ (s)uoneosoy testydess0a4) {patdures seh N sews 4 2ZIS sataads suo uoneind -x] Jouqy uray Se ——— EEE — ——————— EEE LE dgaNNLLNOD c ATaAVL 759 Reproductive Patterns SOAIQUId IO SIBvdS [e}UIeTd Jo JaquINU ULI~y Hg pieyoio pauopuegqy ,, PpseYyIIO psUuleUILY] 9, sanyea Apreak ‘x sdes ul us0g , SYUOUL I9}UTM ‘AA uonendod oj pappe poo , Jeah ul a[qeisea paydures syjuou ‘gj. pafood sarpnis om} wos eIeEG , sieak sreak [e1aaas WO} pajood eieq , suowe a[qeisea pafdures syjuow ‘AVA OL6I ‘WI0Ig pue JaseTY WOLY , sajdures S3urids ‘qs Sa[BUa} aUIOS Jo saydures pajeaday , so[dures sauruins ‘¢ puryssei8 yetuuatag , sanjea pajood ‘gq puryssei3 Jenuuy ; pe[dures syjyuour aatmnoasuod-uoUu “ON (s)1oy ine pejdures syyuow aatnsasuos ‘5 [eursio jo Asaqinoo ‘paysyqnduy , :pa|dwres syjuour ‘suonersiqqy 4 :9ZIs 19] “BUIPOD , dgaNNILNOD ¢ ATEAVL 760 Keller 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 764 (PLL61) UeUe LL ry 0 cl 0 ce 0 LS 8c LS v9 (061) 59251 (PELE sooo 6L°0 8c 0 PSO 6ST a9 cst S°6 (LS61) ‘Te 9 499g 6r'0 bee 8c0 IS¢ ol 1SZ vo snaiuvaptsuuad (8261) SOUTER DT) PUR SSO tr 0 S00 80 L81 A! c8l OO (OL61) eee IE eC | 8r'0 Sc'0 €20 IST 69 srl 9S9 4aqs501y90 "Wl (8S6]) UUrUyOH S90 tc 0 cr'0 OLl Le Ol 6'S SRD UOUE TN (PLL61) UldeUe T, 640 L£o0 cs'0 cOl 18 col na eset SN a01n0¢ Aqtyeqoul uone} uone} N soAiquia N SO] BAO savadg yeyeuaid -ueduit -uejduit Sul quaaI9g pazipear Jaye a10Jaq -qiosal 210... SSO] SSO] U9019g Jv] 839 ued uv LX4], FHL NI GALON SV ‘SYVAX TVAAAAS OL ANC YAAO AGASSASSY SVM SSO'T TVLVYNAYd HOIHM NI SAIGALS YO SALVNILSY AGNVUL) AUV SANTIVA ‘SATOA AO SAIDAdS WNOY NI ALITVLYOW NOLLVLNV Td NJ-LSOd CNV -dud NVAW AO AUVWINAS ¢ ATAVL 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. 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Zool., 10:1-189. 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, 9 0 cl (G3 OS TSIUTAA, 6 € ZI 69 II JOWIUINS PIPY BIBT PIO 6 if €Z ZI SS JOVUT AA Ol 8 €Z 8r 11 JOWIUING ainqsed sseisanjq plo G G o¢ BE Ge JOqUI MA 0 is c¢ BE 072 JOWIUINS (6L61) auield [ze pue 219) StOuT]|T [e4}usr) (S961) ebZ S 4 Or LZ reak ITV UPULIOUIUWITZ Sp[ey Plo ‘eueIpuy LIJSDBOLYIO "JA I 0 if Ol 88 JOVUT MA I 0 €L 072 9 JOUIUING (1L61) B41 Nd pur] pure [zZ1egq -ssei3 yenuue ‘erusojpeg sno ULOf1]D9 WwW 201n0¢ I2yWIO spodoryiy yWNIy S]OO1 ‘SUIZ}S $}001 ‘SUI3}S uoseas JO spa “Sava ‘Sdaea] UO ‘uoneso] ‘satoad P2298 I eye EO NS 31930S) uopayAjoo1q] -a,A1090U0 Jy SUID}I Poo. Batzli ALIS GNV NOSVAS HOVY YOA SATANVS AMO YO NAT HALIM SLNALNOD TvOay GaALOANAOT AO HOVWOLS NO Gasvg AAV VLVG ‘SLNIGOY ANLLOWOIAY NVOIAWY HLYON AWOS AO (NOLLISOdWOD LNAIDWAg) SLAIG AO NOSIAVdINOT) | ATAVL 782 783 Nutrition 0 C 9¢ tr 6l JOIUT AA a€ 4 91 Or i uum ny ac G I 69 82 JIUIUING av Il L cS Ge suds (9861) NZIeg aed pue yyoipul'yT stouly |] yeUer) 49 + 81 OL 9 uuininy (iy ut) a€ G rd OF Lv JOUIUING PAIISITAT atiteid ‘stoul[] UlayON (S961) 6 v 0 rl on ieah [TV UPUIISUIUITZ sp[ey Plo ‘eueripuy snaiuvajksuuad snjosuay C 0 0 fd 96 JOVUIMA, SC + 0 8Z Lt JIUIUING SMOpeIUuI pue (PL6L) S2L sdoq ‘pue[uly UsJaYy1ION (0861) G 1 € 9€ 96 JOUIUINS sun{ pue yzieg eipun} sore “exsely SNULOUOIIGO ‘W 90.INO0G JIyIO spodoiyisy WNJy $]OO1 ‘SUI9}S S$}00.1 ‘SUI9}S uoseas JO spaa “SJAv9 ‘SJAR2] UO ‘uoneoo] ‘satved P22 I | uop I [ Setvedg uopazyAjoo1q, = -ayAJoD0U0 JJ SUId}I poo daNNILNOD lL AaTaVL 2 eee 0¢ 0 + OL Ol TOUT NM, G + I €8 Il Jgwiuing (0861) sieuiqey pare, sun{ pure rz1eg eIpun} oNdIe “eysely snyonbio} xkuojso1siqe ac 9 c6 as 0 UUM yjNy OE v c9 v 0 JIWIUING “61 ts €L 8 0 auld (Z861) 189M esrey “eysely sipyns suouor.yjayy) PbL 0 I cl a TOVUT MA, (0861) J949!PIT P&P 0 cl yl BE eM OES pue YOM eSie} ‘eyse[y SNYIDUBOYIUDX "JAY al Cc cl Ic £9 JOVUT AA, aOl c c 99 0c CUI} INV ab 0 6 09 LC SS 09 € I Ip 0s Burids ainjsed ssei8an|q plo aornog INO spodoiyiy uNIy S1OOJ ‘SUI9]S S}]OOI ‘sUId}S uoseas JO sp39¢ “SQARI| ‘sdAva] UOp ‘uonje20] ‘satsadg uopayAloo1q, -ayAJOD0U0 AT is SUID}I Poo %4 danNNILNOY) Tl ATaVvL 784 785 Nutrition ‘(dds wnjasinby) streiass0fy » ‘SISSOJY ‘Idunj pue suayory « ‘uonejaB9A paynuspiuy . (% >) syunowe sel, + Se ee ee ee ae a JaWUINS EE 0 at v £9 so3ply CP 0 0 4 vS JOVUT AA, (€861) PMP IC 0 aE S 69 SEU as pue yzieg suosAjod ysizy OF 0 a5 S SS TOUT MA, 9C 0 I el 09 TSUN (Lol) Haeg suo3Ajod morq OL ar S € c8 JETDALE EUAN (0861) syeqiqey pare, sunf{ pue yzieg eipun} snore ‘eysely SNIILIGIS SNULWIT (€861) PAlMNd tS + : €8 cl nS pue lz1eg saspry 201N0g J3MN10 spodoiyisiy Ny $}0O1 ‘SUIa}S s}]OOJ ‘sUId}s uoseas JO spaag *‘SOARI| ‘saaeva] UOp ‘uoneso] ‘sataadg uopsjAjoo1lq,_ -ajAoI0U0 JAY Sud} poo _——<———— 5 ——— ee GaNNILNOD lL YTaVi 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. 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House Czech. Acad. Sci., Praha. —. 1967. Evolution of the alimentary system of myomorph rodents (transl.). Indian Nat. Sci. Doc. Centre, New Dehli, 346 pp. West, S. D. 1982. Dynamics of colonization and abundance in central Alaskan populations of the northern red-backed vole, Clethrionomys rutilus. J. Mamm., 63:128-143. Westosy, M. 1974. An analysis of diet selection by large generalist herbivores. Amer. Nat., 108:290-304. 1978. What are the biological bases of varied diets? Amer. Nat., 112:627- 631. WHITNEY, P. 1976. Population ecology of subarctic microtine rodents. Ecol. Mono- gr., 46:85-104. WILLIAMS, O. 1962. A technique for studying microtine food habits. J. Mamm., 43:365-368. Wo rr, J. O., AND W. Z. LIDICKER, JR. 1980. Population ecology of the taiga vole, Microtus xanthognathus, in interior Alaska. Canadian J. Zool., 58: 1800-1812. ZIMMERMAN, E. G. 1965. A comparison of habitat and food of two species of 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. 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Shifts of thermo- genesis in the prairie vole (Microtus ochrogaster), strategies for survival in a seasonal environment. Oecologia, 29:11-26. 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 (O€6L) JapAus ON uonendod jenjen Injiapun Jynq YM sy AA (O€61) sapAug soho yrep “(Sb61) YW pue ziny Sok uonendod jeimen YIM UOWWeUID 1YSIT (8E6L) WARIO SOK uonendod jeinien sada yep YUM Wedir (Zh61) PLOJTayORYS pue UIMO ON uonendod jeinen MOTI A (Zr6l) PosaxeYS pur UIMO “(O€E6L) HEH ‘(SZL61) Nese ON uonendod yeimen ouIq| Vy snaiupajksuuad snjoLsauyy (PE61) aN ON uonendod jeinen UWISIUR]II SNULOUOIBO SNJOLIAT (PL61) ‘Te 12 ayweHY Sok Aioyeloqe’y BSumods ai1y A (LL61) sn3aN pue sajUIg sox Azoyeioqe'] Ayouls (€L61) Joucswag SIX uonendod jeinjen sprig (€L61) Pouosuas sox Aroyeroqe’y paszea-Aar5y (p96) ureysulg pue shePy ON uonejndod jenjen oulqiy LAJSDBOLYIO SNJOLINAT (SS61) nama ON uonejndod jeinieny UWISIURTIJY (6L61) 191UIg sox uonejndod jeunieny Suniods atu AA (OL6L) URATPIY pue J9IUIg SoK Aroye1oge’y ssapie YY (LL61) SnBaN pue saquIg SOK Aloye10qe’y uonnytp 949-yuIg (6961) ‘Te 19 Jase ON uonendod jeinien MOTI A (6761) UIE AA “(1 861) NouUel? sak uonendod jeinien oulqyy SnuDJUOWL SNJOLIIFAT (Zr61) JOUSTA ON uonendod jeinien sIvd UMOIG YIM ITY AA (961) IO SOX uonejndod yeinieN Sumods ay (1b61) 4O ON uonendod jeinjen MOTI (€961) J9x9Ipry SIX uonendod jeimien Ayng SNNULO{IDI SNJOLIA SIDUIIIJIY elep uustydsourAjod uoneI0[Oo a8elIg satoadg Sulpaaig jo uIsIIO SAIDAdS SNjo4L91JA. UTAOM, MAN NI SWSIHCYOWATOd YOTOD-FOVTAgd AO AAUVWWNS LT aTaVL Gaines 848 (Zr6L) PLOJJayIVYUS pue UIMO ON uonendod jeinjen uMmMosq 1USI'T (Zh6L) PlOJJaYOeYS pue UIMO ON uonendod jeiniey MOTPA (0961) ZIUeUDS ‘(P961) [Neg ON uonendod yeinjey OuIg|y wunLojaurd snjo191yAy (Zh6]) Wossolg ON uonendod jenjen UISTURIJAY (O€61) 49pAug “(ZP6L) PLOjayoVyS pue uaMO ON uonendod jeinjen Butods sity AA (O€61) sepAus ON uonejndod yeinjeny yng yieqg SIOUIIIJDY elep wistydsourAjod uOTe1O[OD aBelIg saradg Sulpssig jo ulz1ICG daNNILLNOD L @TaVvi 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. Gaines 854 (Z) SOS" ayesk[Owa FY] JWI d9d9 (Z) 88° EUISeld AOUIOUO TN dvV'l (8Z61) ‘Je 19 J91PeN (€) OLO' eulsel[g JaUIOUO JAI AL snulouo0rao ‘JA (8261) ‘Te 19 49]pPeN (Z) bel aresAjowa YY JoCarG d9d9 STMT SAT me BUISe ld —_ I-Ld (Z) 160° eusseyd ‘Aoupry Jou] Id) (Z) OF vUIse[d JaWOUoy dv — ayesA[owa Py — b-SA = Le Ca > €-Sa (S) 119° Aouply JOMOUSIN c-Sa — ayesA[owa Py — L-Sa (Z) 182 Agupry JowoUc| 7-WOd (Z) SOL’ ayesAjoway ‘Aaupry Jou 17109 (Z) vol ayesAjouray ‘Aoupry caedoesl 4 Gh d9d9 (Z) 020" Agupry Jou 1-HdI (Z) O81" Aauply ae c-AWN (Z) 650° Aouply tote L191 q-Hd'l (0861) IID (Z) Z10° Agupry Jaued}9 TL, V-Hd1T ‘(8L61) Suez pure uamog (Z) 811 Aauply a dd) snaiusofiyoo (L961) somney (8Z6]) UleWe] pue uyoy (Z) OOL’ PUISe[g JaWIOU0I AL 1uamalq ‘Al SIDUITIJIY “AAN) H anssly aunjyonsys Snoo'_T satoadg JepNoa]OJJ GALNASAAd AYV SWSIHAYOWATOd NALLOUg O€ YOU (AN) SHAMOWOULOATY JO WAIWAN AHL ANV “(Z7) ALISUAAIC, OINAD) ‘SISAYOHAOUL “OATY AOA ANSSLY, AO AOANOG “AYNLONALS AVINOATIOWF AHL, “$N704L21y AO SAIOAMS ATYOMA MAN NAATS NI SWSIHAYOWATO”D NIDLOU € ATAVL 855 Genetics ‘sapaqye ¥ Jo yi aya Jo Aouanbasy uesu ay} st 'x a1ayM ;'x i = — Fiz “ULLaJsue “TT faseinutp aprxosadns ‘GOs faseuaSoipAyap ayeutoons ‘FCS ‘aseuasoupAyap [eiqsos ‘EFC YOS ‘ursioid [essuas ‘Ld ‘aseuasoipAyap aieuoon[soydsoyd-9 ‘qog9 ‘aseinwoon[Soydsoyd ‘og ‘outueyetAona] asepndad ‘gag ‘asesauiost aieydsoyd asouueul ‘TqJN {eutAzuUa seu “APY ‘aseuaSospAyap aieyew ‘FY ‘esepndadourwe surong] ‘qy’] ‘eseuesoipAyap ayer] ‘FCT ‘aseu -a80ipAyap aiesoost ‘F{q] {uIqo[Zousy ‘gy ‘eseuaZor1pAyap aieydsoyd-¢-apAyapyess04]3 ‘GQ g¢ey ‘eseuasoipAyap aieydsoydo.sao4]3-0 ‘dd5»v ‘aseua8o0ipAyap aieydsoyd-¢-josa94[3 ‘Gg faseuturesues) 93e}290vO[eXO-a]eUIeINIS ‘TOD ‘eseuesoipAyap aieydsoyd-9-asoonys ‘dd9 ‘asesaisa ‘Sq ‘asejopye ‘qT Vy ‘aseuaZoupAyap joyooye ‘FyqyY ‘utunaqye ‘q7yy ‘esereydsoyd pre ‘qoy ‘ere suoneAsiqqy , (SL61) Sqery pur onde] (Z) €Sh" euse|d SOON dV LS IAM — ayesA[OUuIa FY Belial d9d9 (€) 6rP" i eesh | fa JIUIOUC YN dv (8/6) UeWUe] pue uyoy (+) CLP euse[d JOWIOUOJAT AL snnuvatsuuad “JAy (Z) Shr eUuIse|d JI UIOUOT A b-Sa (t) — euse[g IaWOUOJ c-Sa (Z) S9€° aiesAoula fy JOUIOUO JAI 1-Sa (€) 6ST ayesAoula H FENG d0d9 (CLG) )ajOUCsiIos (Z) SZe" eulse ld JOULOUO TA] dv1 ‘(Q/6L) ‘Te 19 Souter) (+) PIT euse[d JgUIOUOJY AL La]SDBOLYIO “JA S3DUI1IJOY “AAN) H ansst J], aunqonsys Snoo'_T satoadg Je[Ndz]OJ| GaNNILLNOD € ATAVL 856 Gaines 1.00 0.80 [___] Mammals (N = 892) Microtus (N = 72) Frequency = S 8 9.20 0 0.1 0.2 0.3 0.4 0.5 0.6 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. Literature Cited ANDERSON, J. L. 1975. Phenotypic correlations among relatives and variability in reproductive performance in populations of the vole Microtus townsendit. Unpubl. Ph.D. dissert., Univ. British Columbia, Vancouver, 207 pp. ATCHLEY, W. R., AND J. J. RUTLEDGE. 1980. Genetic components of size and shape. I. 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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 MW a AO a i ——<—<——— —— + a ’ of) fan bien 4 u ee on StH a q RA A bite Hit i} Este wv, is Ue Ay ts ay ony Dreads) yt 7 } i 1 if ‘ats et a) on ate SHU HEH a ees abet a eaitgle y Daa Naa is esa i Ny pegh i MAO Heit i () eaesete * aati #3 ‘} ta 4 Dt 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