HARVARD UNIVERSITY e Library of the Museum of Comparative Zoology t tent 4 SEVENTY-FIVE YEARS OF MAMMALOGY (1919-1994) ELMER C. BIRNEY AND JERRY R. CHOATE Editors 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 mam- mals. Correspondence concerning manuscripts to be submitted for publication in the series should be addressed to the Editor for Special Publications, Michael A. Mares (address below). Copies of Special Publications of the Society may be ordered from the Secretary- Treasurer, H. Duane Smith, 501 Widtsoe Bldg., Dept. Zoology, Brigham Young Uni- versity, Provo, UT 84602. COMMITTEE ON SPECIAL PUBLICATIONS MIcHAEL A. Mares, Editor Oklahoma Museum of Natural History University of Oklahoma Norman, Oklahoma 73019 JosepH F. Merritt, Managing Editor Powdermill Biological Station Carnegie Museum of Natural History Rector, Pennsylvania 15677 ll SEVENTY-FIVE YEARS OF MAMMALOGY (1919-1994) EDITED By ELMER C. BIRNEY Bell Museum of Natural History 100 Ecology Building University of Minnesota St. Paul, Minnesota 55108 JERRY R. CHOATE Sternberg Museum of Natural History Fort Hays State University Hays, Kansas 67601 SPECIAL PUBLICATION NO. 11 THE AMERICAN SOCIETY OF MAMMALOGISTS PUBLISHED 27 May 1994 il MCZ LIBRARY OCT 19 1994 HARVARD UNIVERSITY Library of Congress Catalog Card No. 97-71464 © 1994 ISBN No. 0-935868-73-9 lv LIST OF AUTHORS Sydney Anderson American Museum of Natural History Central Park West at 79th Street New York, NY 10024 David M. Armstrong Department of Evolutionary, Population, and Organismic Biology University of Colorado Boulder, CO 80309 Robert J. Baker Department of Biological Sciences and the Museum Texas Tech University Lubbock, TX 79409 Elmer C. Birney Bell Museum of Natural History 100 Ecology Building University of Minnesota St. Paul, MN 55108 James H. Brown Department of Biology University of New Mexico Albuquerque, NM 87131 Guy N. Cameron Department of Biology University of Houston Houston, TX 77004 Jerry R. Choate Sternberg Museum of Natural History Fort Hays State University Hays, KS 67601 Mark D. Engstrom Department of Mammalogy Royal Ontario Museum 100 Queen’s Park Toronto, Ontario, CANADA MSS 2C6 John F. Eisenberg Florida Museum of Natural History Department of Natural Sciences and School of Forest Resources and Conservation University of Florida, Gainesville, FL 32611 Gregory L. Florant Department of Biology Temple University Philadelphia, PA 19122 Hugh H. Genoways University of Nebraska State Museum University of Nebraska-Lincoln Lincoln, NE 68588 Ayesha E. Gill Institute of Health Policy Studies University of California 1388 Sutter Street, 11th Floor San Francisco, CA 94109 Present Address 2308 Jefferson Avenue Berkeley, CA 94703 Mark S. Hafner Museum of Natural Science and Department of Zoology and Physiology Louisiana State University Baton Rouge, LA 70803 Robert S. Hoffmann Smithsonian Institution Washington, D.C. 20560 Donald F. Hoffmeister Museum of Natural History University of Illinois Urbana, IL 61801 Rodney L. Honeycutt Department of Wildlife and Fisheries Sciences and The Faculty of Genetics 210 Nagle Hall Texas A&M University College Station, TX 77843 Murray L. Johnson 501 N. Tacoma Avenue Tacoma, WA 98403 G. J. Kenagy Department of Zoology University of Washington Seattle, WA 98195 Gordon L. Kirkland, Jr. The Vertebrate Museum Shippensburg University Shippensburg, PA 17257 James N. Layne Archbold Biological Station P.O. Box 2057 Lake Placid, FL 33852 William Z. Lidicker, Jr. Museum of Vertebrate Zoology University of California Berkeley, CA 94720 vl Jason A. Lillegraven Departments of Geology/Geophysics and Zoology/Physiology The University of Wyoming Laramie, WY 82071 Michael A. Mares Oklahoma Museum of Natural History University of Oklahoma Norman, OK 73019 Bruce D. Patterson Field Museum of Natural History Roosevelt Road at Lake Shore Drive Chicago, IL 60605 Oliver P. Pearson Museum of Vertebrate Zoology University of California Berkeley, CA 94720 Randolph L. Peterson (Deceased) Royal Ontario Museum 100 Queen’s Park Toronto, Ontario, CANADA MS5S 2C6 Carleton J. Phillips Department of Biological Sciences Illinois State University Normal, IL 61790 Duane A. Schlitter Edward O’Neil Research Center Carnegie Museum of Natural History 5800 Baum Blvd Pittsburgh, PA 15206 David J. Schmidly Texas A&M University P.O. Box 1675 Galveston, TX 77553 James H. Shaw Department of Zoology Oklahoma State University Stillwater, OK 74078 H. Duane Smith Department of Zoology Brigham Young University Provo, UT 84602 Keir Sterling 324 Webster Street Bel Air, MD 21014 J. Mary Taylor Cleveland Museum of Natural History Wade Oval, University Circle Cleveland, OH 44106 B. J. Verts Department of Fisheries and Wildlife Oregon State University Corvallis, OR 97331 John O. Whitaker, Jr. Department of Life Science Indiana State University Terre Haute, IN 47809 Don E. Wilson National Museum of Natural History Smithsonian Institution Washington, D.C. 20560 Vil Jerry O. Wolff Department of Fisheries and Wildlife Oregon State University Corvallis, OR 97331 W. Chris Wozencraft Division of Natural Sciences Lewis-Clark State College Lewiston, ID 83501 Bruce A. Wunder Department of Biology Colorado State University Fort Collins, CO 80523 Terry L. Yates Department of Biology and Museum of Southwestern Biology University of New Mexico Albuquerque, NM 87131 Richard J. Zakrzewski Department of Geosciences and Sternberg Museum of Natural History Fort Hays State University Hays, KS 67601 PREFACE he ad hoc committee to plan the 75th anniversary of the American Society of Mammalogists (abbreviated ASM here and throughout this book), was established by President Hugh Genoways, seemingly only a short time after we celebrated our 50th anniversary. The first meeting of that committee that we recall was at the annual gathering of ASM in Madison, Wisconsin, in 1986, and was chaired by Craig Hood. The coeditors of this book volunteered early in that meeting to oversee the preparation of a book covering the 75 years that ASM had been in existence, 1919-1994, admit- ting at the time that we had no specific plan but that we thought we could get something of this nature done in the 8 years avail- able. We are not the first, nor will we be the last, to learn that every job expands to con- sume all available time. Certainly, this book was no exception. It was remarkably easy for authors to agree to participate and for editors to develop ‘“‘firm’’ deadlines when the target dates were such a long time in the future. Today, 10 February 1994, as we are drafting this final note to accompany the 21 chapters in this book, we still lack and shall never see one important chapter, and Allen Press is bending over backwards to get page proofs to the authors. Managing Editor Joe Merritt and Special Publications Editor Mi- chael Mares are probably the only authors and editors who did not have time to pro- crastinate! Nevertheless, production pres- ipa fe ently is on schedule to have this book in the hands of ASM members at the anniversary meeting in Washington, D.C., as promised so long ago. As we employ the latest in word-process- ing software to draft this document, send e-mail messages between Kansas and Min- nesota in seconds, fax manuscripts between authors and editors, and generally make the most of this electronic era and its infor- mation superhighways, we contemplate 1919, the year ASM was founded. The First World War had just ended, Woodrow Wil- son was President of the United States, and Mexico was experiencing a revolution. What was the state of the discipline of mammal- ogy, and what has ASM done in its 75-year existence to promote and facilitate the sci- ence? That is the topic of this book, which was conceived without much forethought in an otherwise forgotten committee meeting, and which underwent early embryogenesis along the banks of Lake Mendota on the beautiful University of Wisconsin campus, then survived a lengthy period of delayed development following some rapid growth that took place while the list of chapters was finalized and authors were recruited. A few individual cells underwent mitosis now and then, but real gestation began in the spring and summer of 1992. Subsequently, all chapters were subjected to two reviews by peers, mostly during the spring of 1993, and final revisions of most chapters were com- pleted that summer. The book is in two parts, one on the so- ciety and its members (the first eight chap- ters) and the other on the intellectual growth and development of the discipline of mam- malogy during the past 75 years. The charge to authors of the two parts was different. Those writing chapters for Part I were asked simply to treat the topic, and in all cases the emphasis was on ASM, its members, its growth, and its activities to promote mam- malogy. Thus, those chapters address his- tory, and their topics are less about science than its facilitation. Authors writing chapters for Part II were given the following, much more specific, guidelines: ““We envision that chapters in this section will briefly review the pre-1919 state of knowledge of the assigned subdis- cipline, if appropriate, then trace the intel- lectual development of the field through the 75-year period that ASM will have been in existence. Chapters in Part II are expected to take a global perspective of the history, with no special emphasis on either ASM or its members, of the field’s development.” We judge that all authors have more than adequately fulfilled the charge. Authors originally were selected in pairs with an eye toward diversity. In some pairs our strategy was to select collaborators rep- resenting different eras, in others different schools of thought, and in still others we sought authors whose expertise encom- passed the extremes of a broad or complex subdiscipline. A few prospective authors re- signed for one reason or another, one died, one pair decided their chapter was not nec- essary, and fora host of other reasons author lines changed. We attempted to maintain the two-author-per-chapter philosophy throughout in order to get the best ideas of at least two individuals into every chapter, but in three instances that was not possible and in one a third author was recruited. Historical details of author selection pale in comparison to the heartfelt thanks we ex- tend to all authors—it was our very real pleasure to work with each of them. We are equally appreciative of the con- siderable effort donated by Jane Waterman, who drew the vignettes used on the first pages of chapters. We like each one very much, Jane. Our thanks go also to a long list of reviewers, some of whom dropped everything in order to help us meet our deadline, then employed fax and e-mail as necessary to provide nearly instantaneous turn-around of excellent, insightful reviews. We greatly appreciate the time and efforts of all reviewers, several of whom reviewed more than a single chapter: Sydney Ander- son, David M. Armstrong, Robert J. Baker, Patricia J. Berger, James H. Brown, William A. Clemens, Mark D. Engstrom, James S. Findley, G. Lawrence Forman, Enk K. Fritzell, Hugh H. Genoways, Sarah B. George, Donald W. Kaufman, Gordon L. Kirkland, Jr., Thomas H. Kunz, Norman C. Negus, Bruce D. Patterson, Anne E. Pu- sey, O. J. Reichman, Eric A. Rickart, Duke S. Rogers, Robert K. Rose, William D. Schmid, Robert S. Sikes, Donald B. Siniff, Norman A. Slade, H. Duane Smith, Robert H. Tamarin, Robert M. Timm, Michael R. Voorhies, Jane M. Waterman, Michael R. Willig, Don E. Wilson, and Robert M. Zink. Finally, we thank three people who made our jobs easy, and without whose untiring energies at crucial times this book would not have been completed in time for the anniversary celebration: Joseph F. Merritt, Managing Editor for Mammalian Species and Special Publications, put a prodigious amount of time and energy (with occasional lapses into jocularity) into making certain that no important detail of production was slighted; Michael A. Mares, Editor for Spe- cial Publications, processed manuscripts as fast as the two of us could send them to him; and Ken Blair at Allen Press adopted this project and simply made it happen on time no matter what the obstacle. The proof of the pudding, as always, is in the eating. We hope that you, the reader, like our idea of pudding. ELMER C. BIRNEY St. Paul, Minnesota JERRY R. CHOATE Hays, Kansas February 1994 CONTENTS PART I. History of ASM and Its Most Prominent Members ORIGIN Donaid F ehojmeisterand Keir B. Stine, tse pec culo. 14 ee De eee ese RIO O CHR GUO Mie tk vc ee Ree rhea hee haan coy an aanias versie ita a pee 4 ke eee MRS net A The Development of Scientific Societies in Europe in the 18th and 19th Centuries ...... North American Mammatogy Before the 20th Century «2.2... d22c2 2 nocecee cies ce sen: The Early History of the American Society of Mammalogists ......................... EN CLCEUCI OT ASIN CACTI ES pert te asec ai aubecie ana ep i taed Gad tte he an es ara neh ate oak Oa ee catia aad tc rare Site dh 0 Aachen eee oe ood eGo Oe ok 8 tae eek tee hg ee a 2 PRESIDENTS James N. Layne and Robert S: HOPMOnNN 2.2 oss edhe thea eed sesS EHROGUCHION Wace Mist 22 dui, eq: pain ich aes Bu anes yeah cates mat msad Sate Slates Ee SIC ential p PEO lier Sets errant tat aot ham eee Rett tean dae Sa ea ale hg aes ee orale BIOS rap MICS KEICNES a man oa ba aS od ott aaa doe hs ee ee espana oem Mee cat eden eee NClMOWICGRINEDS Sn eG Oar eaiee cages se ee he alae ee ete Ae be 3.65 bau ee oot aes Tre neitnpres CGM tes aN tig, Rag sree ey tan pe teh ta ne al oh ants a _ateee ca AWARDEES J. Mary Taylorand Duane A, SCHUMCl 2) nce oo ee ow eee Pees goa deeeees TALEO GU GLIOM pee Mets e5.2 Mire ee re ae ale eee a tt tare EM Ree nis SG Ae ete ILONORARY IVICINDErS ite a ate eG SRO AT FR erates a Neg Se ae Caan MERaInek WaldCeS da.0e. hoe ae Naoto en CAA a hae PER Uae ee Bee nee eee Brantley Elli FAGKSOMUAWATOUCES Daren: gals a.com ae eatin nnn cde a areas eds is eed occas CEQ CIU SIO tS ree ee aaa OR ple tee ca etm care Sete ie 2 laa, Mat cols lhe, LI eS a O FACRMOWICGO MENUS cde, Sidi sete ack ee eahe 2 Bon acar meat Thon anal ke ier tee ee eae? We eal ate oe OTHER PROMINENT MEMBERS David M. Armstrong, Murray L. Johnson, and RONG OWNER RELErSOMs fans tte eee ae ee ee eG eae ees, anaes IU OGUCIOler eee haere eae en eat eet oie rancor Ake Ne tune ee Rae a BU gl 22 0h oe cee eee eae eee vee EL ag Se ey eC ee 2 eee gn OES ny VEL pYoroal 108183 0 ILO nen om teed ea OF tegen En ES) OCT SO rg ARE reg ates OE errs sc eee BURLY 1090) ae ere cree nce eee en a ee pC Sn an ek Cy nS A. Ua Ge lbs) Serene rete, 0, PR eee TR oe eee, ante eI Et A as Allee Wi ea cha BING sD. Sareea wees erates wer ee ee ee eee ee cate ke aes ee ne ees GE 0 an) AS 27 (San aS cS ea e Y e e a ae e ACADEMIC PROPINQUITY SONMLO AVUILGKCI gy ere ee este =, Ae, ee MVE THO CUNG ENO TIC ce enero ae eee ee ay eee ek eric nape ears ern Ihe: NViemiam: Group) 4, ...242. 055. eo ee ee ces een ee Me the Agassiz/Glover Allen Group (Harvard) {is.i..2..0e07-8 eee ose eee ee III. The Joseph Grinnell/E. A. Hall Group (Berkeley and Kansas) ..................... IV Phe Walliam. Hamulton, Jr. (Group (Cornell) 2). os eo oe i ee LALO 18 Fes col S100) 6 oo ae ae era en ne ne a Dy no Og Oe oP Acknowledgments ite rapinkc: Cie creamy eee yee ee ce ee a ee me ere nan weve ee PUBLICATIONS Bio). Verts and bner GC. BUney wen ones a6 cask on tes es een eae ee Ja eC (0 117) 50) 1 eee eee nme Oem RY 0> SPEER Te SETA PORE tS TR RE RE TY Ec eee ee ee lieed ournal Of MIGWIMNGIOCY .24. -chsacs gem bats eae nk eo ne ee ee BR eg ok VA GITIIGUI GANS DECICS ie awe ay esa rues ee ee ek ee ES ces HN og ae Monographs and Special Publications 3.25 24. 2c. eens an cesta ces eee eene Seana ee: Cumulative Indices and Miscellaneous Publications ................0.0 0000 ce cece ACKHOWICCOTMCIUS: = ote. i ees ee See ee, Uae Be Geter ee Redeem eee Piteratune riled, a422 aaa ane ee ee ee ee ce Ae ie ee eee eee ema N NO — NO S&S CO he Kee N COMMITTEES AND ANNUAL MEETINGS Ayesha E. Gill and W. Chris Wozencraft .. INMtFOGUCUON 4.252.025 fas 358826 bitte ere ete ere aa Oe eee oe ese a ts ae eee Histor or che Comumittees of ASM 1c... 222/502 ites nc alacuat ee een eeteeee ee aa ihe Hlustory of ASMcAnnial Mecunes: . 2 sic 2 6.50, ee gon sha ion a eng See ee oe Biterature: Cited % 202 2 ie certs ec oa hike oe AS Sea ee on es a een ee een eee MEMBERSHIP AND FINANCE Gordon L. Kirkland, Jr. and H. Duane Smith ......... RTEPOCUCHON:” 4, 358 ba a arnien se Qe oe nS any on hae oan eee ras ee See ee Mero bership Glassesir oucctesy sce xs tau as ea ater ado cots atl a ra ee Membership History... Wee 25 2 dar0 ind. iut aud baat als Cate ae eet Intemational Micmibersiiip 2, gaint sa ere soars acs orate eae ne ire ee ee Corresponding Secretary, Treasurer, and’ Secretary- lireasurer ...22...2.. sae. 2 eee eee RESET V Gai TUINC AS errata eaten cc icici eer Ng Bars Nes LeU en coe eens a AAS MAV BUC BCES Au ecte cestia se dens) eR asics wo ous waa 6 aaah tact n eee: ee a ae ne po] 10060 800) @) OMe sae ieee tena Cee eek eG Rrra hme © Gelea eeebed terran ede ne Nee Meee ee nerarerinnes tn ree a AACKMNOWICASINGIIS. 2 (orem. anaes dene wee eee tee en aed nn ae ee Heiterature | Wed oo. ed ee ee eae ee ne es Le ck en ee rae PART II. Intellectual Development of the Science of Mammalogy TAXONOMY Mark D. Engstrom, Jerry R. Choate, and Hugh H. Genoways ........... | Goi ieova Ub Tey oY) ote memrebmeaer eearaee Wl ultra Ur patty rae ural verge esir ream we arse nr erie) Met yw ery es eanny rae eee ee ck A Histoncall Perspective qe ee ne ns ee eee ee eee ee BiglopicaleSpecies Concept... ei ie ets se ee ee te ea eee SUIOSWECICS CC OMCs eer ae em eg ye Seen eee Figher evel axOnOmiy ger. eee oe ee aa ee eee ease ee auinal@Survicy Sse icc ae ere eer eis eee rae cir ene a een cee mice see eg PREKTOW ECO IT TALS tent eee ee eee eg eee ee Wikerature:Citedi ee a. eee ete eee ea Stee ete ae eee er eee PALEOMAMMALOGY Richard J. Zakrzewski and Jason A. Lillegraven .............. DtEO CIC TIO ae eros oes eee eee apres yore ne Sa Ee pe ee Compartmentalization of Mammalopgy +22... 1. -.o2-.225..-24s 224560105 ss asntee nee General Advancements...) 4-e oe et ee e e e e eee Geologically Directed Paleomammialogy ...::....2-. 2.246.462.5454. 004-6eu140sse08 Biologically Directed Paleomammmalogy ...... 2.2.4 ..-202h26..605 ne sndnendw toned sees The Blending of Geologically and Biologically Directed Paleomammalogy ............. EDilOSUC se ce et oe aoe te So tae Meta AME Ate te ooh 2 ieee Ue Se ct ACKNOWICAUSIMENIS 66 okct ean ened xP Fo Ed Pods Ga £ LA Sod we antl dis 4 atin ho ee eee MiteratureCed: 25.456 ea ok eh oe eee adeee ee tee the. hey hele Peele eee BIOGEOGRAPHY Sydney Anderson and Bruce D. Patterson ......:4:.. 5202002 ee IntrodUCtION( «54 = eccidelenc eaddlonandtee Echadoe garde cates aoa ganaus nee s eee Histoncal Trends. 23 422644 28 4 Soden Pad aod toned oar ood nhae eninge ce te Oe pe eee Species Over Ecological Time Penods.2.222...4 424.2022 oo sss eon es soos cae eee Biotas Over Ecolopical Time Periods. .¢2.).%).4.4.-6.4%40060% mtn der sake eaeesaes seems Species Over Evolutionary Time Permods:,¢. 52.42. 4.40452552e02se4nsee eee eee Bietas Over Evolutionary Time PerodS<22...2224c2. 222. 340805e ne se a eee eee iterature Cited) =) 3.5.4.ceddi6 8a Crd. Sasha cba eh ee See Reheat ea eee eee ANATOMY Carleton TS GPITS: 4 Peres S6 Ge ok Bo CaS Oyo SA ee ee Introduction... ...«. odes See 28 Wi ih eao Det ea ea aa aula th @ a dtd bE dee Gale Se Ng eee Paradiems.and Conceptual Frameworks 2.4; auc n¢ani+ ac. 2 6ee eal ee eee eee he BarivieHlistOny: £5 «4 e\sck 2, fam canhealeracidon tate: ind 4 ae ghs panes ee Gen Oe ee ee ihelnivence:of Laxonomy 2.4.5.6 Ss cheno fnew eae ee eee ee oe ‘Phe Iniluence of Natutal History: <..2..4 428.4 icn Sa eRe ee ee es ee The Future-of Mammalogical Anatomy: 3442.6 2005 ine das fa aoe ce oe ee ACkKnOWIEdSINEGHtS, 24.4 uaete © Site in mode CE Oe Reh SP oe Clone Lue waren cee ae ane HeTte TAGE CNC! Fs 216.0 Bho arcicgia ec beare ae wid Eee PASE Ge ee eee ee PHYSIOLOGY Bruce A. Wunder and Gregory L. Florant .......0. 00000000 ccc eee. INET EINE UT Oe a ree res tes he eaters weer iat eae ty Le ne SE tee a a anon eas toe a Physiology Backoroundhy 63.6 2526.05 5s Soe thee 1 hae nates dhe vetoed we baued andes RG Views MICUMOOUS, 24 xc. nenaet yet an tear eA tone eee eae heute eee sehen feo Ep MUG Ue ine Ne gc NN a ec 2 1 abs dae tee eM Rae a ee SO be tain yah daha teh PERS OUI Se OILEO Mat oa etn Lh etl te ete ees een ears akarmeeet ns ae not eee ec ola ra REPRODUCTION Oliver’? Pearsonand Go J. ReEnGoy 2) ces, bite oa oe is St he ITSO CEC UTOTE ee cis 5 Pie cal tacts Mie ate ete lls Sati tans iecasea cea nent sto, Ren A Ste bak Sok eee Fae Panly22 OUR Cent uiys ato oa os SO coe tan on wate hones Ones ewes aeuacen the Cambria se keg ag re elena ck aied edeee Nee cannes eit te nd btn ne Vols 1OpKInS* beCAaCy me. 3 cokes OO he Be es ae all ae cee Gece th aoe: ONT EC SACI CS erat ee Mt PANN eich senses ans 2 S0E tsa Eeas ets SOs ein aeeR ald elie ee PuntheriNotablesPUblicatlons @ saserees os ey oes Sea nik we Beek 6 ns ke ec KG Bate 20 thi Gemtunny ae... crs een aaa Oe old rate a hae ake Pens e a ts tag oe ano Reproduction, Neuroendocrinology, and Molecular Biology .......................... Environmental ‘Physiology and Regulatory Processes i... . 0421054 5:-5.605.-¢c08es uns Reproduciuycienerey Ie xpencivures sete ky manok cw niche cet ens any Gees eee oe nd go tna 9 ak Oltiction and Regulation of Reproduction. .¥24.0ye soe tase See te eee eee oe Behavior and Neuroendocrinology «22: 225.2 eee s en od eh eo es dns See ae eta eae eee INTARS UPI alSeerre mete et ee te cM so a Cc ed i 7 acer cs ae anes ’Chacma Inc., New York. three books, and he has served as editor of five other books. He has received major grant support, and has supervised research projects of 26 students, mainly at the doc- toral level. In 1980 he started the Large An- imal Research Group within the Depart- ment of Zoology at Cambridge. That same year he also became Chairman of the IUCN Deer Specialist Group. In recognition of his prodigious scholarly work, Tim has received several major hon- ors that include the Award for Best Book from the Wildlife Society of America in 1983, the Scientific Medal from the Zoo- logical Society of London, and the Fellow of the Royal Society in 1993. Tim is married to Dafila Kathleen Scott, daughter of the well-known ornithologist, the late Sir Peter Scott. Guy G. Musser, 1992 Born 10 August 1936 in Salt Lake City, Utah; B.S. (1959) and M.S. (1961), Uni- versity of Utah; Ph.D., University of Mich- igan, 1967 (Fig. 5). One year before receiving his Ph.D., Guy Musser was appointed Archbold Assistant Curator in the Department of Mammalogy at the American Museum of Natural His- tory. He has remained at that institution to the present day. Guy became Chairman of the Department in 1981, five years after be- ing promoted to Archbold Curator. Since 1983 he also has held the appointment of Research Associate in the Department of Vertebrate Zoology at the National Muse- um of Natural History. Although born in the West and loving the 104 TAYLOR AND SCHLITTER wilderness country of the region, Guy moved to the crowded core of New York City be- cause he was drawn to the resources of the mammal collections of the museum. He has made the large rodent collections his re- search tool in his lifelong commitment to the complexities of rodent systematics. As a graduate student, first of Stephen D. Dur- rant at Utah and later of Emmet T. Hooper at Michigan, Guy’s training and background helped him become outstanding in this field. He has worked in Costa Rica, the United States, and particularly in southeast Asia, gathering field data and specimens for anal- ysis. He has lived for years at camp sites in Sulawesi in an attempt to comprehend the subtleties of distributional limits of species in different altitudes and habitats. One only has to read his papers to realize the depth of his comprehension of environmental fac- tors that relate to distributions and habits of species of rodents. He has described a number of species and genera of rodents and has proposed several changes at the higher taxonomic levels. Guy’s publications are generally long and comprehensive papers, many of mono- graphic length. He is recognized interna- tionally for his outstanding contributions to the systematics of muroid rodents. Hartley H.T. Jackson Awardees The Hartley H. T. Jackson Award was established in 1977 and was first given to W. B. Davis in 1978. This award recognizes members of the society who have given long and outstanding service to the society (Jour- nal of Mammalogy, 58:709, 1977). The re- cipient is given a certificate that includes a sketch of Jackson, and a plaque that has the ASM pronghorn logo on it. The Jackson Award Committee was established with the guidelines that the committee should re- main small (5 members), it should be unan- imous in its recommendation, and the Board of Directors should support the committee’s nomination by a two-thirds majority if it is to be approved. The recipient is announced at the annual banquet. In 1981 the Board of Directors further decided that there should be no more than one recipient of the Jackson Award and of the Merriam Award in any given year, and that the awards need not be given each year if, in the opinion of the selection committee, suitable candidates are not available (un- abridged minutes of the 1981 Board of Di- rectors’ meeting). Since the inception of the Jackson Award, 12 mammalogists have received it through 1992. Of these, four are past presidents, sev- en have been elected Honorary Members, and one isa recipient of the Merriam Award. One woman (Marie Lawrence) has received the Jackson Award. Recipients have, by the nature of the award, all been members of the society for a long time and to date all have been from the United States. The av- erage age of the recipient at the time of re- ceiving the award has been 66, ranging from 54 to 76. Bryan P. Glass, 1980 Born 21 August 1919 in Mandeville, Lou- isiana; A.B., Baylor University, 1940; MLS., Texas A & M University, 1946; Ph.D., Oklahoma State University, 1952 (Fig. 6). Bryan spent his entire childhood in Chi- na, where he graduated from the China In- land Mission School, Chefoo, Shantung Province in 1953. He served in World War II, primarily as an intelligence officer in Chi- na with the 14th Air Force and OSS, and was awarded the Asiatic-Pacific Medal with two battle stars and a Presidential Unit Ci- tation. Bryan has spent his professional life at Oklahoma State University from 1946- 1985, progressing through all the profes- sorial ranks; he became Director of the Uni- versity Museum in 1966. Bryan’s research focus is primarily on mammals, particularly on microchiropter- an bats. His publications reflect a special interest in distributional records, status, and AWARDEES 105 in regional faunal surveys, primarily in Oklahoma, but he also made a survey of the mammals of Ethiopia and of a new national park in Brazil. Throughout his professional career, Bry- an Glass has given generously of his time and expertise to his university, his church, his city, and to the ASM. He is the recipient of Oklahoma State University’s Outstand- ing Service Award (1965) and Outstanding Teacher Award (1966), and recently was elected 2nd Vice-President at the 20th Bap- tist General Convention, and is Past Pres- ident of the Arts and Humanities Council in Stillwater. Bryan was elected Corresponding Secre- tary of the ASM in 1956, and from 1957 to 1977 he served as Secretary-Treasurer. Dur- ing those 20 years, membership grew from 1,500 to 3,900. He inaugurated the portrait file of Past Presidents and of group photo- graphs at annual meetings. Assisted by his wife, Carolyn, Bryan maintained the mail- ing list of members and subscribers and oversaw the printing of the program for the annual meeting each year, all in pre-com- puterization years. During his tenure, he was the major writer of the Society’s constitu- tion. Bryan’s tangible contributions to the ASM have led to both strength and growth of the society, but so have his undocumented con- tributions. Bryan is often one of the first to welcome student mammalogists at annual meetings and make them feel at ease by in- troducing them to fellow scientists. Murray L. Johnson, 1986 Born 16 October 1914 in Tacoma, Wash- ington; B.A. (1935) and M.D. (1939), Uni- versity of Oregon School of Medicine (Fig. 6). After postgraduate training in surgery at Union Memorial Hospital in Baltimore, Maryland, Murray joined the U.S. Naval Medical Corp and served for 3 years. He has been in the practice of medicine from 1946 through 1983, becoming a certified member of the American Board of Surgery in 1948. Along with his medical practice, Murray has been a research biologist in mammal- ogy, spending almost 50% of his time in this field and, since his retirement, even more. From 1949 through 1983 he was Curator of Mammals at the Puget Sound Museum of Natural History, also chairing the Exec- utive Board there for many years. He was principal investigator in the Marine Mam- mal Program Project Chariot (AEC) through the Arctic Health Reseearch Center in An- chorage from 1959 through 1964. From 1963 to 1983 he was Research Professor of Biology at the University of Puget Sound, held a number of National Science Foun- dation grants, and from 1984 to date has been an Affiliate in Mammalogy and Cu- rator of Mammals at Burke Memorial Washington State Museum, University of Washington. From 1989 to 1992, he has been a member of the Scientific Advisors, U.S. Marine Mammal Commission, and 1984 to date the Secretary for the Foun- dation for Northwestern Natural History. Murray has been the invited participant in many scientific meetings, international as well as within North America. He is a mem- ber of numerous scientific organizations, 1n- cluding a Fellow of the American Associa- tion for the Advancement of Science. In 1978, he was named Distinguished Citizen of the Year in Tacoma, Washington. He is the author of many papers on marine mam- mals and rodents, and some on reptiles and birds. He has special interest in blood pro- tein electrophoretic studies in mammalian taxonomy. His investigations are largely centered around the Pacific Northwest. His wife and strong supporter, Sherry, accom- panies Murray to every annual meeting of the ASM. Marie A. Lawrence, 1989 Born 20 October 1924 in Poughkeepsie, New York; B.A., Vassar College, 1945; 106 TAYLOR AND SCALITTER M.S.S., Smith College School for Social Work, 1952; M.A., New York University, 1970; died 21 September 1992 (Fig. 6). Marie Lawrence began her career, not as a mammalogist or even as a biologist, but as a social worker in New York, a career she continued for almost 30 years. Her last position was Adjunct Associate Professor, New York University of Social Work, which she left in 1975. For the final two years, she was also Scientific Assistant, Department of Mammals, at the American Museum of Natural History. She held this position for nine years, during one of which she was also Assistant Professor of Zooarchaeology at Northwestern Archaeology Field School in Illinois. In 1982, she became Senior Sci- entific Assistant at the Museum, a position she held until her death. Although driven by a keen interest in zooarchaeology, Marie concentrated her re- search on Old World arvicoline rodents, megachiropteran nectar feeders, Myospa- lacine rodents, and the assessment of Me- dieval knowledge of mammalian natural history. Marie did yeoman’s service to produce Recent Literature in Mammalogy for 16 years until the ASM discontinued it in 1985. She served on the Board of Directors and on several standing committees. She was the recipient of several prestigious awards, in- cluding a Ford Foundation Fellowship and the Margaret Mead/Kreiser Fellowship in Anthropology. She was not only the first woman to receive the Jackson Award, she was the first AfroAmerican to be honored by an award from the ASM. John O. Whitaker, Jr., 1991 Born 22 April 1935 in Oneonta, New York; B.S. (1957) and Ph.D. (1962), Cornell University (Fig. 6). While still a graduate student, John worked as a field assistant during summers for the New York State Museum and the New York Conservation Department. Im- mediately following his doctoral work on Zapus hudsonius, under the direction of William J. Hamilton, Jr., John joined the Department of Life Sciences, Indiana State University, as Assistant Professor to teach vertebrate zoology, mammalogy, and other courses, including one on mammalian ec- toparasites. He now holds the rank of Pro- fessor. To date, John has been the mentor for more than 50 graduate students in both M.A. and Ph.D. programs. The diversity of thesis titles, as well as his more than 230 publications, reflects his extraordinary di- versity of interests and expertise within the breadth of vertebrate biology and mam- malian parasites. He has written keys, an- alyzed diets, recorded new distributions, and studied herps and birds, as well as mam- mals, across a wide spectrum of research. John is the recipient of numerous grants and contracts that have sustained portions of the studies made by him and his students. He was elected a Fellow in the American Association for the Advancement of Sci- ence in 1968, a Fellow in the Indiana Acad- emy of Science in 1976, and was one of the first two people to be given an Indiana State University “Research and Creativity Award,” in 1981. Just as impressive as John’s contributions to the field of mammalogy and students in that field are his staggering contributions to the discovery and description of over 130 new taxa of mammalian parasites, largely from North American mammals. His mem- bership in professional societies also mir- rors his breadth of interests and his extraor- dinary competence as an eclectic biologist. B. J. Verts, 1992 Born 19 April 1927 in Nelson, Missouri; B.S., University of Missouri, Columbia, 1954: M.S. (1956) and Ph.D. (1965); Southern Illinois University. B. J.’s doctoral thesis on the biology of the striped skunk was the basis of his first book of that name published in 1967. Ear- lier, however, he was author of several pa- pers in the Journal of Mammalogy and oth- AWARDEES 107 er major journals, having published 15 refereed scientific papers on a wide variety of mammals before receiving the Ph.D. His first position after earning the MLS. degree was as District Biologist, North Car- olina Wildlife Resources Commission, fol- lowed by that of Field Mammalogist and Project Leader, Illinois Natural History Survey, a position held during his tenure as a doctoral student. Upon receiving his doc- toral degree, Verts was appointed Assistant Professor, Department of Fisheries and Wildlife, Oregon State University, where he has remained throughout his career, ad- vancing to the rank of Professor. He spent one year as Visiting Professor at Pennsy]l- vania State University. At Oregon State University he also curated the collection of mammals, developing it into the best col- lection of mammals from Oregon at any institution in the state. His endeavors are especially valuable because Oregon has no significant museum of natural history. In 1979, B. J. married fellow mammal- ogist Leslie Carraway. They collaborate ex- tensively, not only in revision of B. J.’s in- valuable ““Keys to the Mammals of Oregon,” but on virtually half of B. J.’s publications since 1980. Currently, they are completing a book on the Mammals of Oregon, the first of its kind since Vernon Bailey’s book writ- ten in 1936. B. J..s work focuses heavily on small mammals of Oregon, especially life histo- ries and distributions. His interest in rabies and other diseases communicated by wild mammals is prevalent in his earlier publi- cations. He has a long-term interest in de- vising techniques, such as those of ageing, baiting, and sexing. He is a major contrib- utor to Mammalian Species. The deep commitment that B. J. has to the ASM is reflected in the extent to which he contributes to the society. He has served as Managing Editor, Journal Editor, and As- sociate Editor of the Journal of Mammal- ogy, as Editor and Associate Editor of Mam- malian Species, as Chairman of the Local Committee for the ASM’s 59th Annual Meeting, as Chairman of both the Merriam Award Committee and the Grants-in-Aid Committee, and as a member of 5 other committees. He served two terms on the Board of Directors. In addition, B. J. has served in leadership capacities in other sci- entific societies related to wildlife. B. J. has supervised 18 M.S. students and 2 Ph.D. students particularly on projects fo- cusing on cottontail rabbits. Students under his guidance learn the art of scientific writing. B. J. is a rigorous master, having coauthored with D. E. Wilson and A. L. Gardner the ASM’s 1989 Guidelines for Manuscripts and taught courses on science writing and on manuscript preparation at Oregon State University. He has guided many authors in the Journal of Mammalogy in his editorial capacities. Conclusions Altogether, 76 mammalogists have been honored by the ASM between 1919 and 1992 (Tables 1, 2 and 3). Of these, 24 are Charter Members (no Jackson or Merriam awardees are in this group). The recipients come from 13 countries and represent near- ly every discipline related to the biology and evolution of mammals. Edouard-Louis Trouessart, who was made an Honorary Member in 1921, was the first foreign re- cipient, and in 1966 Erna Mohr, also from Europe, became the first woman to be hon- ored by the ASM. The only person to re- ceive all three honors—the Merriam Award in 1977, the Jackson Award in 1983, and Honorary Membership in 1992—1is the late J. Knox Jones, Jr., who also had been Pres- ident of the society. Of the 58 persons who have been given Honorary Membership, 14 are still alive; of the 12 people to receive Jackson Awards, 9 are living; of the 14 recipients of the Mer- riam Award, 13 are living. Two of these three honors keep alive the names of two eminent founders of the ASM. C. Hart Merriam, first President of the so- ciety and one who not only began the North American Fauna series but also had a pro- 108 TAYLOR AND SCHEER TABLE |1.—Honorary Members of the American Society of Mammalogists. (P) Past President of ASM. Joel Asaph Allen (1919) Edouard-Louis Trouessart (1921) Max Weber (1928) M. R. Oldfield Thomas (1928) Henry Fairfield Osborn (1929) Edward W. Nelson (1930) (P) C. Hart Merriam (1930) (P) William Berryman Scott (1936) Alfred W. Anthony (1936) Leonhard Stejneger (1937) Gerrit S. Miller, Jr. (1941) Ernest E. Thompson Seton (1941) Marcus Ward Lyon, Jr. (1942) (P) Rudolph M. Anderson (1947) Angel Cabrere Latorre (1947) A. Brazier Howell (1951) (P) Theodore S. Palmer (1951) Edward A. Preble (1952) Hartley H. T. Jackson (1952) (P) William K. Gregory (1954) W. P. Taylor (1954) (P) Harold E. Anthony (1955) (P) Lee R. Dice (1956) Albert R. Shadle (1956) Francis Harper (1959) Nagmaichi Kuroda (1959) Magnus A. Degerbol (1962) Remington Kellogg (1963) (P) Tracy I. Storer (1963) (P) TABLE 2.— Recipients of the Merriam Award. (P) = Past President of ASM; (Hon.) = Honorary Member of ASM; (Jack.) = recipient of the Jack- son Award. James N. Layne (1976) (P) J. Knox Jones, Jr. (1977) (P) (Hon., Jack.) James S. Findley (1978) (P) Terry A. Vaughan (1979) Robert J. Baker (1980) John F. Eisenberg (1981) James L. Patton (1983) (P) Michael H. Smith (1985) William Z. Lidicker, Jr. (1986) (P) Hugh H. Genoways (1987) (P) Jerry R. Choate (1988) James N. Brown (1989) (P) Timothy H. Clutton-Brock (1991) Guy G. Musser (1992) V. G. Heptner (1963) E. Raymond Hall (1964) (P) Stanley P. Young (1964) William J. Hamilton, Jr. (1965) (P) Erna Mohr (1966) Klaus Zimmerman (1966) William H. Burt (1968) (P) William B. Davis (1968) (P) George Gaylord Simpson (1969) Robert T. Orr (1970) (P) Stephen D. Durrant (1971) (P) Kazimierz Petrusewicz (1972) Charles S. Elton (1973) Emmet T. Hooper (1976) (P) Vladimir E. Sokolov (1976) Oliver P. Pearson (1979) Victor B. Scheffer (1981) Donald F. Hoffmeister (1982) (P) Z. Kazimierz Pucek (1982) Bjorn O. L. Kurtén (1983) John Edwards Hill (1985) Bernardo Villa-Ramirez (1986) Randolph L. Peterson (1986) (P) Francis Petter (1987) Wuping Xia (1988) Karl F. Koopman (1990) Philip Hershkovitz (1991) J. Knox Jones, Jr. (1992) (P) Sydney Anderson (1992) (P) TABLE 3.—Recipients of the Hartley H. T. Jackson Award. (P) = Past President of ASM; (Hon.) = Honorary Member of ASM; (Mer.) = recipient of Merriam Award. William B. Davis (1978) (P) (Hon.) William H. Burt (1979) (P) (Hon.) Bryan P. Glass (1980) J. Knox Jones, Jr. (1983) (P) (Hon. Mer.) Oliver P. Pearson (1984) (Hon.) Sydney Anderson (1985) (P) (Hon.) Murray L. Johnson (1986) Donald F. Hoffmeister (1987) (P) (Hon.) Karl F. Koopman (1988) (Hon.) Marie A. Lawrence (1990) John O. Whitaker, Jr. (1991) B. J. Verts (1992) AWARDEES 109 found effect on the development of the sci- ence of modern mammalogy; and Hartley H. T. Jackson, eleventh President of the so- ciety, who chaired the initial Organizing Committee of the society and served as its first Corresponding Secretary for six years. Acknowledgments Recognition of the invaluable assistance pro- vided by several people at The Cleveland Mu- seum of Natural History in the preparation of this chapter is due. First ofall, the extensive work of B. Hallaran, Executive Secretary, is deeply appreciated. So is the help of librarians W. Was- man and D. Condon. We also are grateful to many members of the ASM, who helped to sup- ply informational details. To all we owe a debt of gratitude in helping to bring this chapter to- gether. OTHER PROMINENT MEMBERS Davip M. ARMSTRONG, MurrRAy L. JOHNSON, AND RANDOLPH L. PETERSON Introduction his chapter is based on the observation that many of the mammalogists who have had enduring impacts on mammalogy in the past 75 years have not been honored formally by the ASM as Honorary Members or recipients of Merriam or Jackson awards; not all have served the society as senior of- ficers. Given the organization of this vol- ume, such individuals might have been overlooked. This chapter has had a sadly difficult his- tory because one of the original authors, Randolph L. Peterson, passed away as con- ceptualization of the chapter was in an early stage. It was Peterson who drafted the first list of noteworthy mammalogists who— having neither been honored previously by ASM nor served as a senior officer of the society — might go unmentioned in this vol- ume. Peterson listed 76 names, and then more were added. The list quickly became unmanageable; difficult decisions eventu- ally had to be made. We understood at the outset that this chapter was unlikely to please everyone— and indeed might please no one—because space alone limited numbers of individuals included. Limits imply choice, and choice 110 implies valuing, which no two mammalo- gists are likely to do in the same manner. There was early agreement that to be in- cluded an individual must be retired or de- ceased. Further, it was abundantly clear that treatment could not be comprehensive. Eventually, some organizational principles emerged: the chapter would be organized by decades, and biographies would be limited to no more than about five individuals who had left an indelible stamp on the mam- malogical ‘“‘character’’ of that decade. Fi- nally, based on the premise that one cannot really recognize importance or a “classic” until its enduring impact can be gauged, we have not presumed to extend our subjective analysis beyond the 1970s. With standards and procedures so obviously judgmental, who could fault us for having omitted a fa- vorite theriological character or a particu- larly inspirational academic “aunt” or “‘un- cle,’ an esteemed mentor or field tutor? We do not harbor any illusion that the history of the ASM is the history of Amer- ican mammalogy. Mammalogy was well es- tablished as a branch of natural history and biology well before 1919. Many would date the origin of American mammalogy from OTHER PROMINENT MEMBERS 111 1858, with the publication of Spencer Ful- lerton Baird’s monumental Mammals, Vol- ume 8 of the Pacific Railroad Surveys. Oth- ers would dig deeper for roots, to Colonial naturalists like Mark Catesby and William Bartram, distinguished visitors like Sir John Richardson, or to the extraordinary zoolog- ical explorers and publicists ofa new nation: Lewis and Clark, George Ord, James DeKay, John Godman, Thomas Say, or Audubon and Bachman. The late 19th and early 20th centuries were times of extraordinary pro- ductivity (see, for example, Hoffmeister and Sterling, 1994; Wilson and Eisenberg, 1990), and eminent mammalogists left marks that still inspire and influence our work, among them Harrison Allen, J. A. Allen, W. H. Osgood, G. S. Miller, Jr., C. Hart Merriam (who continues to sign the register annually at meetings of ASM a full half-century after his death). The 1920s The roster of the organizational meeting of ASM in 1919 reads like a ““Who’s Who” of late 19th and early 20th century mam- malogy. Many of the luminaries present went on to give distinguished service to mam- malogy and ASM and are noted elsewhere in this volume. The decade in mammalogy was characterized by self-evaluation and def- inition, and dominated by the pioneers. Early numbers of the Journal of Mammal- ogy published earnest correspondence about taxonomic issues, the dubious value of common names for organisms neither com- monly seen nor much discussed by common folk, still-useful lists of desiderata for life history studies, and the relative exchange value of specimens of mice and mink. Browsing through early volumes of the Journal and minutes of early meetings, one readily agrees that we continue to stand on the shoulders of those giants and continue to earn interest on the intellectual capital they invested. Of nine authors in the in- augural number of the Journal (28 Novem- ber 1919), six served as President of the ASM, five eventually were named Honor- ary Members, and three received both of those recognitions. Here we note a few other individuals who left a mark during the first decade of ASM. Outram Bangs (1863-1932) was born in Watertown, Massachusetts, and graduated from the Lawrence Scientific School of Har- vard College in 1884. In the 1890s, Bangs published 50 papers on mammals. Ina sense, Bangs represents a sizable class of individ- uals, largely unsung—the local naturalists. Like dozens of other noteworthy local mammalogists of his era, he began to collect mammals asa child. Eventually he built one of the finest private collections in the U.S., which was purchased by Harvard’s Muse- um of Comparative Zoology in 1899, and Bangs was named Assistant in Mammalogy, although his research interests soon shifted to birds. Ned Hollister (1876-1924) was the orig- inal editor of the Journal of Mammalogy, setting the high standards for editorial qual- ity that are matched by few other scientific journals. Born in Delavan, Wisconsin, he collaborated with Ludwig Kumlien of Mil- ton College on Birds of Wisconsin (1903), accompanied Vernon Bailey on a Biological Survey expedition to Texas (1902), and worked with W. H. Osgood in Alaska (1903). He formally joined the staff of the Bureau of Biological Survey in 1904. Reputed to have a genius for museum work (Osgood, 1925), he was appointed Assistant Curator of Mammals in the U.S. National Museum in 1909; in 1916 he became Superintendent of the National Zoological Park. In his brief career, Hollister collected 26 holotypes, named 162 taxa, and published 150 papers and monographs, including several works of enduring value, among them work on mammals of the Philippines (1913) and re- views of East African mammals in the U.S. National Museum (1918, 1919, 1924). A. H. Howell (1872-1940) was the only author in the inaugural number of the Jour- nal of Mammalogy who did not go on to 12 ARMSTRONG ET AL. the presidency of ASM or election to hon- orary membership. However, his impact on systematic mammalogy continues to be great, largely because he provided (mostly in North American Fauna) the first mono- graphic treatments of a number of mam- malian genera: striped skunks (1901), spot- ted skunks (1906), harvest mice (1914), marmots (1915), flying squirrels (1918), pi- kas (1924), chipmunks (1929), and ground squirrels (1938). His biological survey of Al- abama (1921) was the only such product of the Bureau of Biological Survey outside the Mountain West. Mostly self-trained, How- ell farmed and worked as a stock-clerk be- fore being stimulated to a career in natural history through an association with the Lin- naean Society of New York. He received a temporary appointment in 1895 as assistant to Vernon Bailey for field work in the Northern Rockies and Pacific Northwest. He continued with the Bureau of Biological Survey (and the Fish and Wildlife Service) until his death 44 years later. H. H. Lane (1878-1965) was the original Recording Secretary of ASM, serving from 1919 until 1932. Born in Bainbridge, In- diana, and educated at DePauw, Indiana, Cornell, and Chicago, he received a Ph.D. from Princeton in 1915. Lane taught at Hir- am College, the University of Oklahoma, and Phillips University before moving to the University of Kansas as Professor of Zoology and Paleontology in 1922. Mostly a paleontologist, he nonetheless influenced the classic generation of mammalogists at the University of Kansas, including Wil- liam Henry Burt, E. Raymond Hall, Claude W. Hibbard, and Jean M. Linsdale. The 1930s The 1930s saw progress in a number of areas of mammalogy, especially in mam- malian ecology, and some of the most no- table contributions remain classic autoeco- logical studies. Robert T. Hatt (1902-1989) served as Corresponding Secretary of ASM from 1932 to 1934. Born in Lafayette, Indiana, and educated at Michigan and Columbia, Hatt spent several years at the American Muse- um of Natural History and then directed the Cranbrook Institute of Science from 1935 to 1967, remaining as Senior Scientist until his retirement in 1971. Hatt’s enduring contributions included fine autecological studies, especially of squirrels (e.g., Hatt, 1943), and work in anatomy (Hatt, 1932). Robert K. Enders (1899-1989) pursued an extraordinarily diverse career, centered on academic work at Swarthmore College. He conducted field work on Panamanian mammals for more than 40 years, from 1929 to 1971. Although he served as Recording Secretary of ASM from 1933 to 1937, and in a variety of scientific organizations and agencies in leadership capacities, his most indelible mark on mammalogy may have been indirect, a consequence of his stew- ardship of the Rocky Mountain Biological Laboratory at Gothic, Colorado, as Director (1959-1968) and President (1969-1978). He also stimulated students, such as Oliver Pearson and Phil Myers, to pursue careers in mammalogy. Jean M. Linsdale (1902-1973) was part of that legendary “‘bumper-crop” of mam- malogists born in Kansas, and educated at the University of Kansas and the University of California, Berkeley, that included W. H. Burt and E. R. Hall. He may have described his most important legacy to vertebrate zo- ology best in the acknowledgments to his monumental work, The California Ground Squirrel (1946); among the list of students at the Hastings Natural History Reservation who contributed as observers were Lamont C. Cole, Carl Koford, Lloyd Tevis, P. Q. Tomich, G. A. Bartholemew, Jr., W. W. Dalquest, H. S. Fitch, W. V. Mayer, and C. G. Sibley. Linsdale spent his professional career with the Museum of Vertebrate Zo- ology, joining in 1922 the “fur book”’ pro- ject begun three years earlier by Grinnell and Dixon (Grinnell et al., 1937). His pains- taking work on the dusky-footed woodrat OTHER PROMINENT MEMBERS 113 (Linsdale and Tevis, 1951) helped inspire the career of a younger great neotomologist, R. B. Finley, Jr. Olaus J. Murie (1889-1963) was born in Moorhead, Minnesota, and served from 1920 to 1946 as a field biologist with the Bureau of Biological Survey, including work in the Canadian Arctic, Labrador, and the Aleutians. His work on the elk of Jackson Hole (begun in 1927) is an enduring classic, in part culminating in E/k of North America (O. J. Murie, 1951). A Field Guide to Animal Tracks (1954) remains an invaluable re- source for naturalists who would read sto- ries of mammals not in the library but in dust, mud, or snow. A confirmed conser- vationist, Murie retired from government service to help found The Wilderness So- ciety, of which he was President from 1950 to 1957. Adolph Murie (1899-1974) pursued his distinguished research career at the Uni- versity of Michigan (where as recently as 1968 a pair of his boots occupied a place of honor in a specimen case), the U.S. Fish and Wildlife Service, and the National Park Service. After classic studies of moose on Isle Royale (A. Murie, 1934), he began re- search on gray wolf—Dall sheep interactions in Mount McKinley National Park in 1939. The Wolves of Mount McKinley (A. Murie, 1944) and The Grizzlies of Mount McKinley (reprinted, 1981) continue to inspire. Like his older brother Olaus, Adolph Murie was passionately committed to conservation and the ideal of national parks: ““The national park idea is one of the bright spots in our culture. The idealism in the park concept has made every American visiting the na- tional parks feel just a little more worthy” (A. Murie, 1981:241). Aldo Leopold (1887-1948) continues to enrich our science and our philosophy near- ly a half-century after his untimely death. It is difficult to know which decade deserves to be identified with his remarkable contri- butions. The publication of his seminal Game Management (1933) essentially re- defined the field as applied ecology, nudging it hard from folk-art toward science. A Sand County Almanac appeared posthumously (1949), with sensitive, sensible insights into ecological ethics that continue to inspire students and their elders alike. In another dimension of his enduring legacy, several of Leopold’s children went on to distinguished scientific careers, in wildlife biology (Stark- er), paleobotany (Estella), plant physiology (Carl), and earth sciences (Luna). Francis B. Sumner (1874-1945) had an extraordinary career, documented in a re- markable autobiography (1945), The Life History of an American Naturalist. Educat- ed at Minnesota and Columbia, he taught at the College of the City of New York, and worked on fish development as Director of the Biological Laboratory of the Bureau of Fisheries at Woods Hole. Remarks by Da- vid Starr Jordan about the importance of long-term studies of the effects of environ- ment on evolution inspired his mammalog- ical work, which was made possible by an appointment at the Scripps Oceanographic Institute. Thus began a remarkable career in mammalogy, centered on painstaking laboratory studies of the genetics of geo- graphic variation in species of Peromyscus (see Sumner, 1932). The 1940s In the 1940s, many of a generation of mammalogists saw military service in World War II. An earlier generation of scholars continued to work despite limited academic and agency budgets and rationing of such theriological essentials as paper, gasoline, and tires, producing works that must still be consulted daily, such as G. G. Simpson’s Principles of Classification and a Classifi- cation of the Mammals. Victor H. Cahalane (1901-1993) was a Director of ASM at various times from the 1930s to the 1960s. Director of the Cran- brook Institute of Science from 1931-1934, his scientific career was spent mostly with the U.S. National Park Service, resulting in 114 ARMSTRONG ET AL. such studies as his survey of Katmai Na- tional Monument (1959). Chief of the Bi- ology Branch from 1944-1955, he remained as a collaborator until 1970 while Assistant Director of the New York State Museum. Perhaps Cahalane’s most enduring contri- butions were in the genre of popular natural history. Mammals of North America (1947), with its charming illustrations by Francis L. Jacques (1887-1969), remains an important landmark in mammalogical publishing, and The Imperial Collection of Audubon Mam- mals (Cahalane, 1967) made Audubon and Bachman’s illustrations of mammals readi- ly available to the 20th century. Paul Errington (1902-1962) received his Ph.D. from the University of Wisconsin and spent his entire academic career at Iowa State University. He devoted much of his too— brief scientific career to a single species, the muskrat, a keystone in the glacial marshes of the Midwest, research that began “... with muddy feet on the family farm in east- central South Dakota” (Errington, 1967:x1). His central question was what determines numbers of free-living animal populations, a question pursued in remarkable depth, as “the study of predation is no field for snap judgments” (1967:xi). Muskrat Populations (1963) remains a standard reference, and Errington did not hesitate to apply lessons learned from muskrats to humankind, as he did in Of Men and Marshes (1957), and the posthumous works, Of Predation and Life (1967), and The Red Gods Call (1973). D. Dwight Davis (1908-1965) was born in Rockford, Illinois, and joined the Field Museum in 1930, rising from Assistant in Osteology to Curator of Anatomy. His memoir on the functional morphology of the giant panda is a landmark in mammal- ogy (Davis, 1964), setting a new standard for morphological studies of species. In- deed, Gould (1980) called Davis’s mono- graph “... probably the greatest work of modern evolutionary comparative anato- my.” Ian McTaggart Cowan was born in 1910 in Scotland and educated at the universities of British Columbia and California. His dis- tinguished academic career at the Univer- sity of British Columbia was marked by honorary degrees from Simon Fraser Uni- versity and the universities of Alberta, Wa- terloo, British Columbia, and Victoria. Cowan’s study of geographic variation in native American sheep (1940) was a pains- taking example of the possibilities of deep insights from fragmentary material. With Charles Guiguet, the Curator of Birds and Mammals at the British Columbia provin- cial Museum, he authored The Mammals of British Columbia (Cowan and Guiguet, 1956), which has gone through three edi- tions. Philip L. Wright was born in 1914 and reared in New Hampshire, earning his doc- torate from the University of Wisconsin in 1940. His entire professional career was spent at the University of Montana, where he retired in 1985. Wright’s research was focused mostly on reproductive cycles of endotherms, and his enduring contributions to mammalogy include a number of pio- neering papers on reproductive cycles of mustelids (e.g., Wright, 1942), as well as more recent work to maintain Boone and Crockett Club records on big game mam- mals. The 1950s The 1950s were optimistic years typified not only by big projects—of which E. R. Hall and K. R. Kelson’s Mammals of North America surely stands as the grandest— but also by big questions, on the nature of pop- ulation regulation, for example. Through the decade governmental support of mammal- ogy increased in North America, resulting in patterns of funding and academic rewards that prevail today. A. W. F. Banfield (born in Toronto in 1918) studied at the universities of Toronto and Michigan and served as a mammalogist in several Canadian governmental agencies, including the National Park Service, the OTHER PROMINENT MEMBERS 1 Us) Wildlife Service, and the National Museum. He was Director of the Museum of Natural Science from 1964 to 1969 and later taught at Brock University. His contributions to mammalogy included definitive studies of the caribou over three decades (Banfield, 1951, 1961), a faunal survey of Banff Na- tional Park (1958), and his comprehensive The Mammals of Canada (1974). Donald R. Griffin (born in 1915 in South- ampton, New York) has had two distin- guished careers in mammalogy, either of which would have earned him a prominent place in this chapter, in any of several de- cades. His academic career began at Cornell. While at Harvard, he published his classic Listening in the Dark (1958), which—along with Echoes of Bats and Men (1959)—con- tinues to inspire chiropterologists. In 1965 he moved to Rockefeller University. The Question of Animal Awareness (1976) de- fined the new field of cognitive ethology and posed anew questions that had been dis- missed as scientifically inaccessible a cen- tury earlier. A recent Festschrift for Griffin (Ristau, 1991) provided appropriate rec- ognition for a distinguished mammalogist. John J. Christian was born in Pennsy!l- vania in 1917 and educated at Princeton and Johns Hopkins. In a research career in various commercial, federal, and academic laboratories, he pursued intensive experi- mental studies of the relationships among population density, reproduction, and the endocrine system, especially the adreno-pi- tuitary axis (reviewed in Christian, 1963), stimulating renewed interest in field studies of fluctuations of numbers of small mam- mals. He received the Mercer Award from the Ecological Society of America in 1957 and was a professor at SUNY Binghampton from 1969 until his retirement. John B. Calhoun was born in Elkton, Ten- nessee, in 1917, and educated at the Uni- versity of Virginia and Northwestern. He taught at Emory, Ohio State, and Johns Hopkins. His research focused on principles of population dynamics, and he realized that “derivation of these principles requires more data than can be obtained by the efforts of a single individual” (Calhoun, 1956). In 1947 he organized and initiated the North American Census of Small Mammals (NACSM), sponsored first by the Rodent Ecology Project at Johns Hopkins, later by Jackson Laboratory at Bar Harbor, Maine, and finally by the National Institutes of Mental Health (where Calhoun moved in 1954). NACSM inspired volunteer field- work across the continent for a dozen years. By using consistent protocols, it not only developed a very large data set but under- scored the importance and the difficulties of achieving a quantitative understanding of mammalian distributions in space and time. Calhoun’s (1963) monograph on the ecology and sociology of the Norway rat was a landmark in considering in evolutionary and ecological terms the sociopathology of mammalian populations, both rats and peo- ple. Carl B. Koford (1915-1980) was selected in 1939 by Joseph Grinnell and Alden H. Miller to study the California condor with the support of the National Audubon So- ciety. Associated throughout his career mostly with the Museum of Vertebrate Zo- ology, Koford’s work was characterized by extraordinary attention to detail and thor- ough pursuit of connections and relation- ships. Fortunately, he turned these skills to understanding the ecology of the black-tailed prairie dog, providing (Koford, 1958) a clas- sic study of the species in the context of the dynamic and overused, but poorly known, ecosystem in which it is a kind of keystone. Fortunately, too, he invested his mono- graph with passionate concern for conser- vation that—in concert with the voices of such other committed mammalogists as Victor Cahalane, the brothers Murie, and E. R. Hall—finally is beginning to bear fruit. The 1960s The 1960s saw the advent of new tools and concepts like digital computers, mul- 116 ARMSTRONG ET AL. tivariate statistics, and the use of ““biosys- tematic” characters in mammalogy. How- ever, several of the landmarks of the decade were broad summaries in their fields, in- cluding J. A. King’s edited Biology of Pero- myscus, Anderson and Jones’ edited Recent Mammals of the World, and Walker’s Mammals of the World. Barbara Lawrence (born in Boston in 1909) was educated at Vassar College and was associated with the Museum of Com- parative Zoology at Harvard from 1931 un- til her retirement in 1976. In addition to important work on mammals of New En- gland, the Caribbean, and Central America, Lawrence collaborated with William Bos- sert to produce a ground-breaking multi- variate morphometric study of North American Canis (Lawrence and Bossert, 1967) that demonstrated the power of new kinds of statistics in gaining insights into complex evolutionary and ecological ques- tions. E. Lendell Cockrum (born in 1920 in Ses- ser, Illinois) published a comprehensive systematic work on the mammals of Kansas (1952) and went on to pursue a distin- guished academic career at the University of Arizona. One of his most influential con- tributions to mammalogy was his textbook, Introduction to Mammalogy (1962), which served a generation of students. Cockrum also co-authored textbooks in general zo- ology and general biology and produced ma- jor studies of mammals of Organ Pipe Na- tional Monument (e.g., Cockrum, 1981). B. Elizabeth Horner (born in 1917 in Merchantville, New Jersey) received her Ph.D. from the University of Michigan in 1948 and taught zoology at Smith College from 1940 until her retirement in 1982. In 1970, she was named Myra M. Sampson Professor of Biological Science. Her mam- malogical contributions included classic studies of the biology of rodents, especially ecomorphology of Peromyscus (e.g., Hor- ner, 1954) and marsupials. W. Frank Blair (1912-1985) was born in Dayton, Texas, and educated at the uni- versities of Tulsa and Florida, as well as the Laboratory of Vertebrate Biology at the University of Michigan. Perhaps best known for his work in herpetology at the University of Texas, he left an indelible stamp on the development of mammalogy in several ways, and over a period sufficiently long that it is difficult to ascribe his influence to a particular decade. His works on the biotic provinces of Oklahoma (Blair and Hubbell, 1938) and Texas (Blair, 1950) are still valu- able, and Vertebrates of the United States (Blair et al., 1957) was consulted by gen- erations of mammalogists. He was among the first ecologists to develop mark-recap- ture methods in studies of population ecol- ogy. Moreover, his leadership of the United States International Biological Program in the late 1960s and into the 1970s (see Blair, 1977; Mares and Cameron, 1994) allowed deep insights into the functional role of mammals in ecosystems, and facilitated in- ternational cooperation among mammalo- gists that continues to expand. Ernest P. Walker (1891-1969) first made a mark on zoology with a 1913 book on birds of Wyoming. His monumental mam- malogical project, Mammals of the World, began in 1930 while he was Assistant Di- rector of the National Zoological Park, and continued for 30 years, resulting in the stan- dard semi-technical reference on the extant genera of mammals, now in its fifth edition (Nowak, 1991). The work was painstakingly thorough and attempted to include a pho- tograph of a representative species 1n each genus. The first edition (Walker et al., 1961) included a remarkable third volume, a clas- sified bibliography of the literature of mam- malogy, based in large part on the “Recent Literature” section of the Journal of Mam- malogy, which remains an efficient entry to the literature of mammalogy to about 1960. Walker’s original dedication was “‘To the MAMMALS, GREAT AND SMALL, who contribute so much to the welfare and hap- piness of man, another mammal, but re- ceive so little in return, except blame, abuse, and extermination.” OTHER PROMINENT MEMBERS Tt7 The 1970s The investigational and analytic tools of the 1960s bore rich fruit in the 1970s. It is too early to guess just which works will turn out to be classics, of course, but the decade had more than its share of classic workers, many of whom figure prominently in other chapters in this volume. Rollin H. Baker (born in Cordova, Illi- nois, in 1916) was educated at the Univer- sity of Texas, Texas A&M University, and the University of Kansas. He established a reputation as an ornithologist with his monograph on the avifauna of Micronesia (1951), but his professional efforts at the University of Kansas, and later at Michigan State University, soon focused on mammals of Mexico and Michigan. He and his stu- dents did pioneering work on the biosys- tematics of Sigmodon, and his monumental Michigan Mammals (1983) is a paragon of state mammal books. Baker retired in 1981. Karl Kenyon (born in 1918 in La Jolla, California) was educated at Pomona and Cornell. After service in the U.S. Navy, he taught at Mills College. In 1947, he joined the U.S. Fish and Wildlife Service, under Victor B. Scheffer at the Fur Seal Laboratory (later the Marine Mammal Laboratory), pursuing a distinguished research career that made him the preeminent authority on the biology of the sea otter. His monograph on the biology of the species (Kenyon, 1969) will remain a classic of its genre. Ralph M. Wetzel (1917-1984) received his Ph.D. from the University of Illinois in 1949. His professional career was spent mostly at the University of Connecticut, en- riched by research appointments at the U.S. National Museum. He retired in 1982 and moved to a courtesy appointment at the University of Florida State Museum. Wet- Zel’s well-known work in the Gran Chaco of Paraguay began in 1972. It was there that he discovered that the Chacoan peccary (Catagonus wagneri), previously known only from pre-Hispanic, subfossil deposits, re- mained alive (Wetzel, 1977), perhaps en- couraging a younger generation of mam- malogists to turn toward South America with the heightened sense that really remarkable discoveries remain to be made. Charles H. Southwick was born in Woo- ster, Ohio, in 1928, graduated from the Col- lege of Wooster, and earned master’s and doctoral degrees from the University of Wisconsin. After faculty appointments at Hamilton College, Ohio University, and Johns Hopkins (and research appointments at Oxford and Stanford), he moved to the University of Colorado in 1979 and retired there in 1993. Southwick’s research career is focused on population and behavioral ecology. He continues to make fundamental contributions to our knowledge of mam- malian species as diverse as grasshopper mice, pikas, and mule deer, but his enduring legacy surely will be in understanding the biology of species of Macaca. His longitu- dinal research effort on Indian populations of rhesus macaques (reviewed in Fa and Southwick, 1988), now over three decades long and continuing, may be unequalled for any species in the history of mammalogy. Further, he has shared his deep insights into the problems and prospects for global en- vironmental conservation through texts such as Ecology and the Quality of Our Environ- ment (Southwick, 1976) and Global Ecology (Southwick, 1988). William A. Wimsatt (1917-1987) was ed- ucated at Cornell and spent most of his ac- ademic career there. His research career fo- cused on the ecology and physiology of reproduction in eastern bats, especially My- otis lucifugus, and he pioneered techniques and insights (see Wimsatt and Kallen, 1957) that have since been applied to numerous other species. His edited series, Biology of Bats (1970a, 19706, 1977), brought togeth- er a vast quantity of information and atten- dant literature and made it accessible to a new generation of chiropterologists. Robert L. Rausch was born in 1921 in Marion, Ohio. From Ohio State University he received a bachelor’s degree in 1942 and a D.V.M. in 1945. He then earned an M.S. 118 ARMSTRONG ET AL. from Michigan State University in 1946 and a Ph.D. from the University of Wisconsin in 1949, in parasitology and wildlife man- agement. He joined the Arctic Health Re- search Center of the U.S. Public Health Ser- vice, serving as Chief of the Zoonotic Disease Section from 1950 until its closure in 1974. Rausch was Adjunct Professor at the Uni- versity of Alaska from 1967 to 1974 and Professor of Zoology from 1974 to 1975. He served as Professor of Parasitology at the University of Saskatchewan from 1975 to 1978 and then moved to the University of Washington, where he was Professor of Pathobiology in the School of Medicine and Adjunct Professor of Zoology until his re- tirement in 1992. As a mammalogist, Rausch established an international repu- tation for his systematic insights on Arctic mammals (e.g., Rausch, 1953) and received honorary degrees from the universities of Saskatchewan, Alaska, and Ziirich. Rausch’s wife, Virginia (Reggie), is a scientist in her own right and a frequent collaborator on joint projects (e.g., Rausch and Rausch, 1975). Claude W. Hibbard (1905-1973) was born in Toronto, Kansas, and educated at the universities of Kansas and Michigan. He worked and taught at Kansas from 1928 to 1946 and then moved back to Ann Arbor, where he pursued a highly productive career as an energetic and insightful student of Pliocene and Pleistocene faunas of the Great Plains, with a strong emphasis on mam- mals. His most lasting scientific contribu- tions were the development and use of a technique for collecting microfossils (de- scribed by Zakrzewski and Lillgraven, 1994). Walter W. Dalquest (born 1917) is difh- cult to identify with any particular decade, for his career has been long and diversely productive. Educated at the University of Washington and Louisiana State, he pub- lished comprehensive faunal treatments of mammals of Washington (1948) and San Luis Potosi (1953) and went on to a distin- guished academic career at Midwestern State University, Texas, making important con- tributions to the study of vertebrates (es- pecially mammals and fishes) of south-cen- tral United States and Mexico. Over the years, his research focused increasingly on fossil vertebrates, especially those of Plio- cene and Pleistocene localities. A well-de- served Festschrift (Horner, 1984) celebrated his contributions to students and science. A Final Word Given the diversity and purview of mam- malogy and mammalogists and the richness of research during the past three-quarters of a century, the foregoing survey can hardly hope to be definitive; indeed, it can be little more than suggestive. There was not even full agreement among the authors on whom to include. Peterson would have included more Canadians and chiropterologists, Johnson more northwesterners and theriol- ogists from beyond North America, and— unrestrained by wiser colleagues—Arm- strong would have been biased toward his own local heroes and mentors. Whether one agrees with our commis- sions or omissions is hardly the point, how- ever. 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(ED.). 1970b. Biology of bats. Academic Press, New York, 2:1-—477. (ED.). 1977. Biology of bats. Academic Press, New York, 3:1-651. Wimsatt, W. A., AND F.C. KALLEN. 1957. The unique maturation response of the Graafian follicles of hi- bernating vespertilionid bats and the question of its significance. Anatomical Record, 129:115-131. WriGut, P. L. 1942. Delayed implantation in the long-tailed weasel (Mustela frenata), the short-tailed weasel (Mustela cigonanti), and the marten (Martes americana). Anatomical Record, 83:341-349. ZAKRZEWSKI, R. J., AND J. A. LILLEGRAVEN. 1994. Paleomammalogy. Pp. 200-214, in Seventy-five years of mammalogy (1919-1994) (E. C. Birney and J. R. Choate, eds.). Special Publication, The American Society of Mammalogists, 11:1-433. ACADEMIC PROPINQUITY JOHN O. WHITAKER, JR. Introduction here have been at least three major pa- pers on the history of North American mammalogy and the ASM (Hamilton, 1955; Hoffmeister, 1969; Storer, 1969). However, none of these papers presented information on the “roots” or “‘academic genealogy” of North American mammalogists. The 75th anniversary of the birth of the ASM is a good time to examine this topic. The idea arose from a paper given by J. Knox Jones, Jr., at the 1985 annual meeting of ASM at Orono, Maine. It was titled ““Genealogy of Twentieth Century Systematic Mammalo- gists in North America: The Descendants of Joseph Grinnell,” and was subsequently published (Jones, 1991). Jones indicated that the descendants of Joseph Grinnell at the University of California, Berkeley, along with a major subcenter founded by E. Ray- mond Hall at the University of Kansas, ac- counted for an academic dynasty that in- cluded perhaps 75% of North American systematic mammalogists. Elmer Birney, president of ASM in 1989, suggested this topic be examined in more detail and other “dynasties” be included as a chapter in a 121 history of the society to be presented in con- junction with its 75th anniversary. This study is an attempt to trace the roots of mammalogy in North America during the first 75 years of the society. The base data for this paper are given (Table 1) asa listing of many mammalogists who “have made their mark or are making their mark” on North American mammal- ogy. Most are or were associated with the ASM. I have drawn heavily from Jones (1991) for the material on the Grinnell dy- nasty but there is no other published set of data to which one can go for related infor- mation. It had to be obtained by word of mouth and through correspondence. At- tempts were made to include as many of the more active North American mammalo- gists in this table as possible. However, not all could be included in the text, and little information could be obtained for some. I hope that omissions and oversights will not detract too greatly from the overall picture. The data accumulated should serve to in- dicate the source of our collective roots. The earliest group listed, the field mammalogists 122 WHITAKER assembled for the United States Biological Survey by C. Hart Merriam, is not an ac- ademic group, but nevertheless made a ma- jor impact on North American mammalo- gy. Three major academic groups are included: the Harvard Group (Agassiz/Al- len), the Berkeley/Kansas Group (Grinnell/ Hall), and the Cornell Group (Hamilton). Besides those obtaining their training from members of these groups, there are some smaller groups (Florida, Purdue, Tulane, Wisconsin), and a number of mammalogists have received their degrees in related fields, such as ecology, ornithology, wildlife, and genetics. I. The Merriam Group Before discussing the academically-ori- ented dynasties, it is important to mention the group formed in the latter part of the last century under Clinton Hart Merriam of the U.S. Biological Survey (Table 1, Section I). C. Hart Merriam was trained as an M.D. in New York and practiced medicine from 1879 to 1885 (Storer, 1969). However, Mer- riam was a field naturalist at heart and had written early natural history books on the birds of Connecticut (1877) and the mam- mals of the Adirondacks (1884). In 1885, he became chief of the federal bureau that later became the U.S. Biological Survey. He gathered under him a staff of outstanding mammalogists that published numerous papers and books and greatly influenced the development of mammalogy in this cen- tury. Members of his team included Vernon Bailey, Albert K. Fisher, Edward A. Gold- man, Ned Hollister, Arthur H. Howell, Har- tley H. T. Jackson, W. L. McAtee, Edward W. Nelson, Wilfred Osgood, Theodore S. Palmer, and Edward A. Preble. Merriam sent collectors into the field, stimulated nu- merous studies of distribution of mammals, and initiated the North American Fauna se- ries, which included the first comprehensive taxonomic studies of North American mammals. Six individuals within this group became presidents of the ASM, including the first president, Merriam himself (Layne and Hoffmann, 1994). Some of C. H. Mer- riam’s underlings said C. H. stood for “Christ Himself.” Merriam produced nearly 500 publica- tions, and he and his colleagues in the U.S. Biological Survey published numerous pa- pers and books that were largely responsible for the growth and development of system- atic mammalogy in North America in the late 1800s and early 1900s. It must be re- membered, however, that these men gen- erally were not associated with academic institutions and therefore had no means to train students except by example and ap- prenticeship. IT, The Agassiz/Glover Allen Group (Harvard) The Harvard group also originated before the formation of the ASM (Table 1, Section II), and traces back to Louis Agassiz at the Museum of Comparative Zoology at Har- vard College. J. A. Allen (1838-1921), or- nithologist and mammalogist, studied un- der Agassiz before moving to the American Museum of Natural History in 1895, as did another of the early notable mammalogists, Gerrit Smith Miller, Jr., who graduated from Harvard in the class of 1894. Miller first worked for the U.S. Biological Survey, but in 1898 moved to the U.S. National Mu- seum where he remained until retirement in 1940. Agassiz was at the base of this ac- ademic line, but one of his students, Glover M. Allen, was Curator of Mammals at Har- vard’s Museum of Comparative Zoology and sponsored most of the early mammal- ogists from Harvard. Allen earned three de- grees from Harvard, including his Ph.D. in 1904. Glover Allen produced some of the giants of our time—George A. Bartholo- mew, Jr., David E. Davis, Donald R. Grif- fin, Charles Lyman, and Oliver P. Pearson. George Bartholomew was one of the most eminent physiological ecologists in this PROPINQUITY 123 TABLE |.— Academic genealogy of selected 20th TABLE |.— Continued. century North American mammalogists. Harold Reynolds I. C. Hart Merriam Group (U.S. Biological Barbara Lawrence Scheville Survey, Washington) C. Hart Merriam Vernon Bailey Albert K. Fisher Edward A. Goldman Ned Hollister Arthur H. Howell Hartley H. T. Jackson W. L. McAtee Edward W. Nelson Wilfred Osgood Theodore S. Palmer Edward A. Preble Stanley P. Young II. Harvard University (The Agassiz/Allen Group) Louis Agassiz Bryan Patterson Craig C. Black J. Sutton Lloyd E. Logan L. Kristalka I. Johnson Glover M. Allen George A. Bartholomew, Jr. Mark A. Chappell William R. Dawson Richard W. Hill Alan R. French Jack W. Hudson, Jr. James G. Kenagy Richard E. MacMillen Daniel K. Odell Thomas Poulson Barbara H. Blake Bruce Wunder David E. Davis John J. Christian Edward N. Francq Ronald E. Barry Frank B. Golley Rexford D. Lord Jan O. Murie Steven H. Vessey Donald R. Griffin Jack Bradbury Katherine Ralls Charles Lyman (Allen/Hisaw) Richard W. Thorington, Jr. (Ernst Mayr) Oliver Pearson (Allen/Hisaw) Daniel H. Brant Donald R. Breakey Gilbert S. Greenwald Stuart O. Landry Bert S. Pfeiffer J. A. Allen Herbert W. Rand Harold B. Hitchcock III. The Joseph Grinnell/E. Raymond Hall Group (Berkeley and the University of Kansas) Joseph Grinnell Seth Benson Robert L. Rudd Guy N. Cameron Peter Schramm Charles S. Thaeler Enrique P. Lessa Alan C. Ziegler (technically with W. B. Quay) W. H. Burt A. W. Frank Banfield Fred S. Barkalow Harold E. Broadbooks Robert K. Enders (Burt was mentor but not advisor) Lowell L. Getz Joyce Hoffman Donald H. Miller Harvey L. Gunderson Evan B. Hazard Timothy E. Lawlor Richard H. Manville (final examination chaired by Hooper) Illar Muul William O. Pruitt Dana P. Snyder Wendell E. Dodge Andrew Starrett Ian McTaggart Cowan Joseph F. Bendell Fred C. Zwickel Walter A. Sheppe William B. Davis Dilford C. Carter Patricia Dolan Richard K. Laval Donald A. McFarlane Ronald H. Pine Raul Valdez Paul W. Parmalee Randolph L. Peterson (Ph.D. with J. R. Dymond) Charles S. Churcher Judith L. Eger M. Brock Fenton Robert M. R. Barclay Gary P. Bell R. Mark Brigham Joe E. Cebek 124 TABLE 1.— Continued. WHITAKER James H. Fullard Robert M. Herd C. G. Van Zyll de Jong Lee R. Dice W. Frank Blair David L. Jameson Michael A. Mares Ruben M. Barquez Thomas E. Lacher, Jr. Ricardo Ojeda Michael R. Willig W. Howard McCarley Paul G. Pearson Richard D. Sage James R. Tamsitt Wallace D. Dawson Van T. Harris Don W. Hayne Paul C. Connor B. Elizabeth Horner Walter E. Howard Daniel B. Fagre John A. King Lee C. Drickamer C. Richard Terman Harley B. Sherman B. A. Barrington Joseph C. Moore Dale W. Rice Arthur Svihla E. Raymond Hall Ticul Alvarez-S. (Masters) Sydney Anderson Rollin H. Baker Donald P. Christian Peter L. Dalby James M. Dietz Gary A. Heidt Gordon L. Kirkland, Jr. John O. Matson Alan E. Muchlinski Howard J. Stains M. D. Bryant E. Lendell Cockrum Robert J. Baker John W. Bickham Luis Ruedas William J. Bleier J. Hoyt Bowers Robert D. Bradley Ira F. Greenbaum David Hale Philip Sudman Mike Haiduk Meredith Hamilton Rodney L. Honeycutt TABLE |.— Continued. Craig S. Hood David C. Kerridge Rick McDaniel Margaret A. O’Connell Calvin A. Porter Mazin B. Qumsiyeh Lynn W. Robbins (actual advisor was Francis Rose) Fred B. Stangl, Jr. Ron Van Den Bussche Terry L. Yates Joseph A. Cook Scott L. Gardner Sarah George Gregory D. Hartman Laura L. Janacek Dwight W. Moore David Reducker Brett R. Riddle Robert M. Sullivan Glen Bradley Russell P. Davis Bruce J. Hayward Keith Justice Peter L. Meserve James D. Layne C. Brian Robbins Robert G. Schwab Charles L. Douglas Stephan D. Durrant Richard M. Hansen Donald R. Johnson Keith R. Kelson M. Raymond Lee Fred Elder Mark L. McKnight William S. Modi Earl G. Zimmerman C. William Kilpatrick John V. Planz James S. Findley Kenneth W. Anderson Hal L. Black Michael A. Bogan William Caire Eugene D. Fleharty Patricia W. Freeman Kenneth N. Geluso Anthony L. Gennaro David J. Hafner Arthur H. Harris Clyde Jones John F. Pagels (co-chairs were Negus and Jones) Karen E. Petersen Daniel F. Williams PROPINQUITY 125 TABLE |.— Continued. Don E. Wilson Robert B. Finley Donald F. Hoffmeister Wayne H. Davis Luis de la Torre Victor E. Diersing L. Scott Ellis John S. Hall W. Z. Lidicker, Jr. Blair A. Csuti K. T. DeLong Ayesha E. Gill Edward J. Heske David T. Krohne William F. Laurance Richard S. Ostfeld David O. Ribble Jeffy O. Wolff Charles A. McLaughlin Iyad A. Nader David J. Schmidly Paisley S. Cato (co-chaired with Clyde Jones) James N. Derr (co-chaired with John Bickham) Robert C. Dowler (co-chaired with John Bickham) Mark D. Engstrom James G. Owen Stephen A. Smith (co-chaired with Ira Greenbaum) William D. Severinghaus H. Duane Smith Richard G. Van Gelder David B. Wright Robert E. Wrigley J. Knox Jones, Jr. David M. Armstrong Kathleen A. Scott Fagerstone James C. Halfpenny Joseph F. Merritt (actual advisor was Olwen Williams) Elmer C. Birney Richard Lampe Lynn L. Rogers Robert M. Timm (actual advisor was Roger Price) John B. Bowles Alberto A. Cadena Jerry R. Choate Larry L. Choate G. Lawrence Forman Hugh H. Genoways Robert R. Hollander Thomas H. Kunz Edythe L. P. Anthony TABLE |.— Continued. Peter V. August Martha S. Fugita Allen Kurta Richard W. Manning Carleton J. Phillips Ronald W. Turner James Dale Smith Philip L. Krutzsch Charles A. Long George H. Lowery, Jr. Walter W. Dalquest Alfred L. Gardner Ronald M. Nowak Robert L. Packard Robert E. Martin Robert J. Russell Henry W. Setzer Duane A. Schlitter (actual advisor was Richard Highton, a herpetologist) Terry A. Vaughan Cindy Rebar O. J. Reichman Bernardo Villa-R. (Masters with Hall, Ph.D. from Univ. Mexico) Jose Ramirez Pulido John A. White John Eric Hill Emmet T. Hooper James H. Brown Michael A. Bowers Gerardo Ceballos James C. Munger Andrew T. Smith Michael D. Carleton Theodore H. Fleming Charles O. Handley, Jr. David G. Huckaby David Klingener James A. Lackey Guy G. Musser Albert Schwartz David H. Johnson A. Remington Kellogg (actual chair was William D. Mathew) Jean M. Linsdale Quentin P. Tomich Alden H. Miller (ornithologist) Richard F. Johnston (ornithologist) Gary Schnell (ornithologist) Troy L. Best Janet K. Braun Ronald K. Chesser E. Gus Gothran Michael L. Kennedy George D. Baumgardner Floyd W. Weckerly 126 TABLE |.— Continued. Robert D. Owen Carl B. Koford A. Starker Leopold Joseph G. Hall William J. Hamilton III Robert S. Hoffmann Fernando A. Cervantes-Reza Lawrence R. Heaney Donald L. Pattie Barbara R. Stein Merlin D. Tuttle John E. Warnock W. Christopher Wozencraft John H. Kaufmann Frank J. Bonaccorso Richard R. Lechleitner Frank A. Pitelka George O. Batzli Russell F. Cole Elizabeth A. Desy Richard Lindroth Stephen D. West Charles A. Reed Emily C. Oaks J. Mary Taylor Barry Thomas Marla L. Weston Robert T. Orr Tracy I. Storer (actual chair was Charles A. Kofoid) Walter P. Taylor Bryan P. Glass Stephen R. Humphrey Hector T. Arita Jacqueline Belwood Ralph Kirkpatrick Frederick H. Test IV. The Hamilton Group (Cornell University) William J. Hamilton, Jr. Roger W. Barbour Michael J. Harvey Marion Hassell Allen V. Benton Arthur H. Cook Robert A. Eadie Kyle R. Barbehenn Richard W. Dapson Harold G. Klein Jack W. Gottschang Everett W. Jameson Duncan Cameron, Jr. John D. Phillips, Jr. James N. Layne Harrison Ambrose William Platt Andrew A. Arata WHITAKER TABLE |.— Continued. Dan W. Walton Dale E. Birkenholz Llewellyn M. Ehrhart James V. Griffo John McManus Elizabeth S. Wing William O. Wirtz James L. Wolfe Robert J. Esher John G. New William G. Sheldon William Werner John O. Whitaker, Jr. Wynn W. Cudmore Thomas W. French Gwilym S. Jones Howard H. Thomas David Pistole Steven J. Ropski From Professors in Related Fields Ecology Marston Bates John W. Twente Arthur D. Hasler Kenneth B. Armitage Orlando A. Schwartz Charles Elton Dennis Chitty Rudy Boonstra Charles J. Krebs Michael S. Gaines Leroy R. McClenaghan Robert K. Rose Barry L. Keller Robert H. Tamarin Steven R. Pugh Francis C. Evans Lee H. Metzgar Stanley C. Wecker Richard R. Miller John T. Emlen Garrett C. Clough William A. Fuller Evelyn Hutchinson Donald Livingston Peter D. Weigl Robert H. MacArthur M. L. Rosenzweig Joel S. Brown Burt P. Kotler Cliff Lemon Gene D. Schroder John C. Neese Tim W. Clark TABLE |.— Continued. Eugene Odum W. Wilson Baker Gary W. Barrett Richard S. Mills Reed Fantin Clyde L. Pritchett William Prychodko Mary Etta Hight William Reeder Frank A. Iwen Victor Shelford S. Charles Kendeigh Robert M. Chew John A. Sealander, Jr. Donald W. Davis Philip S. Gipson Dana Snyder Ralph Wetzel Robert L. Martin Genetics Peter Brussard (ecological genetics) Gary F. McCracken Robert Lacey Theodosius Dobzhansky Karl F. Koopman W. B. Heed James L. Patton John C. Hafner Mark Hafner Philip Myers G. K. Creighton Robert Voss Duke S. Rogers Margaret F. Smith Donald O. Straney A. Christopher Carmichael Ethology M. W. Fox Marc Bekoff Joel Berger Peter Marler John F. Eisenberg Cheri Jones John G. Robinson R. Rudran Nicholas C. Smythe C. Wenimer Franz Sauer Michael H. Smith Mark C. Belk Donald W. Kaufman Paul L. Leberg PROPINQUITY 127 TABLE 1|.— Continued. Susan McAlpine Paul R. Ramsey Kim T. Scribner Wildlife/Conservation Aldo Leopold James R. Beer Charles F. MacLeod Charles M. Kirkpatrick Thomas W. Hoekstra Russell E. Mumford Virgil Brack, Jr. David A. Easterla Harmon P. Weeks William H. Marshall John R. Tester Donald B. Siniff Douglas P. DeMaster J. Ward Testa Jeannette A. Thomas Robert A. McCabe Lloyd B. Keith Thomas A. Scott/Edward Kozicky Willard D. Klimstra B. J. Verts Leslie N. Carraway (actual advisor was Charles Warren) Joseph A. Chapman Kenneth L. Cramer George A. Feldhamer Entomology & Parasitology H. S. Fitch/Joseph Camin Richard B. Loomis Cluff Hopla Donald Gettinger (co-chaired with Michael A. Mares) Adrian Marshall Donald W. Thomas Anatomy/Physiology Howard Adelmann William A. Wimsatt Roy Horst Alvar W. Gustafson Gary G. Kwiecinski William J. McCauley Henry Mitchell G. Clay Mitchell Eugene H. Studier Roland K. Meyer (endocrinologist) William H. Elder Richard F. Myers Phillip L. Wright Clinton H. Conaway 128 WHITAKER TABLE 1.— Continued. Larry N. Brown Milo E. Richmond Frederick J. Jannet John P. Hayes Rodney A. Mead Andrew V. Nalbandov (Univ. IIl., animal science) Glen C. Sanderson Alfred C. Redfield (Harvard, physiology) Peter R. Morrison Brian K. McNab Herpetology Robert Stebbins Paul K. Anderson Ornithology Arthur A. Allen Ralph S. Palmer Eugene Dustman Norman Negus Pat Berger Robert K. Chipman Jack A. Cranford Alicia T. Linzey Edwin Gould John F. Pagels (co-chaired with Clyde Jones) Aelita S. Pinter Carol N. Rowsemitt Thomas E. Tomasi Miles Pirnie Durwood L. Allen Frederick F. Knowlton Charles E. Harris L. David Mech Michael E. Nelson Rolf O. Peterson Fred A. Ryser, Jr. John R. Gustafson Herbert W. Rand Harold W. Hitchcock Miscellaneous William King Gregory (palaeontologist) Albert E. Wood Bjorn Kurten (palaeontologist) Phillip M. Youngman William F. Porter Paul F. Steblein S. David Webb (palaeontologist) Kenneth T. Wilkins Training in Other Professions Physicians H. Allen Elliot Coues Murray L. Johnson TABLE |.— Continued. Marcus Ward Lyon, Jr. Edgar A. Mearns C. Hart Merriam George Wislocki Veterinarians Denny J. Constantine Training in Museum or Field, No Ph.D. Rudolph M. Anderson Harold E. Anthony Benjamin P. Bole, Jr. Philip M. Blossom Victor Cahalane T. Donald Carter J. Kenneth Doutt Alfred J. Godin George F. Goodwin Arthur M. Greenhall Philip Hershkowitz A. Brazier Howell Laurence M. Huey Carl W. Kenyon Thomas J. McIntyre Gerrit S. Miller, Jr. John Paradiso Victor B. Scheffer Ermest Thompson Seton Albert R. Shadle Viola S. Shantz G. H. H. Tate Lloyd P. Tevis Hobart M. Van Deusen Ernest P. Walker country and trained a number of students at UCLA. Davis and Lyman have been ex- tremely influential in studies of hibernation: Davis at Penn State and North Carolina State; Lyman at Harvard. Griffin has had immense effect on studies of bat echoloca- tion and behavior from positions at Har- vard, Cornell, and Rockefeller University. Oliver Pearson of Berkeley is an ecological physiologist, well known for his work with poison glands of shrews, mammalian re- production, and ecology and systematics of South American mammals. Pearson, like William J. Hamilton, Jr., was greatly influ- enced by Francis Harper. Harper had earlier been a high school teacher, but was editing for the American Philosophical Society and frequently used the library at the Philadel- PROPINQUITY 129 phia Academy of Science. Oliver Pearson used the library in conjunction with his work for Robert Enders and thereby came in con- tact with Harper, who had obtained his Ph.D. from Cornell in 1925 with the her- petologist, Albert Hazen Wright. All five of these Glover Allen-progeny have now pro- duced academic offspring of their own. The influence of Harvard on the development of North American mammalogy cannot be overestimated. ITI. The Joseph Grinnell/ E. R. Hall Group (Berkeley and Kansas) Early in this century, another intellectual dynasty was born on the West Coast, at Berkeley (Table 1, Section III). It was fos- tered by Annie Montague Alexander, who played an outstanding role in the develop- ment of mammalogy at Berkeley (H. Grin- nell, 1958). She was the founder and a life- long patron of the Museum of Vertebrate Zoology at Berkeley. She early developed a love for travel, hunting, and the natural sci- ences. Alexander also befriended C. Hart Merriam, and collected or purchased many of the bears that were studied by him; she supported and led three collecting expedi- tions to Alaska (1906, 1907, and 1908). Alexander had thought for some time about establishing a museum at the Uni- versity of California. When she returned from Alaska in the autumn of 1906 she be- gan serious discussions with Merriam about this. She had come to realize how fast the native game birds and mammals of the west were disappearing and felt specimens (in- cluding skeletons) should be preserved, as was happening in the east. At this time she happened to meet Joseph Grinnell, and was impressed with his “energy and enthusiasm and the neat and scholarly way in which his records were kept.” She mentally noted him as a possible coworker. Upon returning from her 1907 Alaska ex- pedition, Alexander presented her plan for the establishment of a museum of verte- brate zoology at The University of Califor- nia to President Benjamin Wheeler. The re- gents accepted her plan and a contract establishing the museum was signed on 23 March 1908, with Joseph Grinnell appoint- ed as its director for | year. Many letters were exchanged between Al- exander and Grinnell in order to ensure the greatest possible usefulness for the museum. Alexander preferred that young biologists be enlisted, ‘““men with their accomplish- ments ahead of, rather than behind them,” and that the time of staff members should be divided between curatorial, field, and re- search work. There was effort to obtain bal- ance between specimens for research and for display in order to kindle popular interest in natural history. Alexander contributed monthly sums from 1908 to 1919, then she presented $200,000, plus another $225,000 in 1936, as perpetual endowments. How- ever, she also gave many smaller amounts through the years until her death, and con- tributed hundreds of specimens collected by herself and her lifelong friend, Louise Kel- logg. The University of California wanted Grinnell to teach freshman Zoology, but Al- exander objected. She wanted his time spent on research and development of the mu- seum. However, Grinnell did become editor of the Condor in 1908 and continued in this position until his death in 1939. Head- quartering the Condor at Berkeley provided practice in editing to numerous students. Joseph Grinnell was born in 1877 in the Indian Territory, about 40 miles from Ft. Sill, in present-day Oklahoma. His family settled in California after his father’s retire- ment. Grinnell earned the bachelor’s degree from Throop Polytechnic Institute, which eventually became the California Institute of Technology, in 1897. He earned the M.A. and Ph.D. degrees from Leland Stanford, Jr., College in 1901 and 1913. This insti- tution was named for its benefactor, Leland Stanford, Jr., and later became Stanford University. His major professor or at least 130 WHITAKER one of them was Charles Henry Gilbert (Hall, 1939). Grinnell taught at Throop Polytechnic for a time before becoming Di- rector of the Museum of Vertebrate Zoology in 1908. He held this post for 30 years, until shortly before his death at 62 in 1939. Grin- nell had styled himself after C. Hart Mer- riam; thus the roots of the Grinnell Dynasty go back partly to Merriam. However, the roots also reached back to another giant in vertebrate zoology of the time, David Starr Jordan. Jordan was primarily an ichthyol- ogist, but had broad interests in other ver- tebrates as well. Jordan did his undergrad- uate work at Cornell, where it is said that he camped out on campus. He earned an M.D. at Indiana Medical College in 1875, and a Ph.D. from Butler University (Indi- anapolis) in 1878. Jordan was President of Indiana University from 1885 to 1891, and in 1891 he became the first President of Leland Stanford, Jr., College. Grinnell was an excellent mammalogist and ornithologist, and an expert on birds and mammals of the West Coast, especially California. He was very shy, but an ener- getic worker in the field. His shyness man- ifested itself, for example, in instinctively placing his own hand behind his back when a newcomer offered to shake it. He was an excellent scientist, editor, and museum cu- rator. Emmet T. Hooper, one of Grinnell’s students, said that Grinnell would drive on trips into the field and would point out in- teresting geological, vegetative, or faunal features. On the return trip, however, he would let a student drive while he sat in the back, in order to work up his field notes and even start work on the papers to be pub- lished from the specimens and data ob- tained. During his tenure at Berkeley, Grinnell advised numerous graduate students in or- nithology and mammalogy, and also some in herpetology, but not all were his students in the strict sense that he was their major advisor. Charles A. Kofoid also played a major role in the education of many Berke- ley graduate students. Berkeley students fanned out over the land; they have played a major role in systematic mammalogy, and in vertebrate zoology as a whole throughout the world. Some of Grinnell’s better known students, not all of whom he directed to the doctoral degree, were the following (Table 1, Section ITI). Seth Benson and Alden H. Miller (Berkeley) William H. Burt, Lee R. Dice, Emmet T. Hooper, and Fred R. Test (University of Michigan) Ian McTaggart Cowan (University of Brit- ish Columbia) William B. Davis and Walter P. Taylor (Texas A&M University) E. Raymond Hall (Berkeley and University of Kansas) John Eric Hill (American Museum of Nat- ural History) David H. Johnson and Remington Kellogg (U.S. National Museum) Jean M. Linsdale (Hastings Natural History Reservation) Robert T. Orr (California Academy of Sci- ence) Tracy I. Storer (University of California at Davis) Burt, Davis, Hall, Hooper, Kellogg, Orr, Storer, and Taylor each served as President of the ASM. Cowan served as Vice Presi- dent. Many members of this group estab- lished centers of learning of their own, from which additional students were trained, but others were in positions where having stu- dents was not an option. Some of the centers of learning and many of Grinnell’s progeny are discussed below. Berkeley.—Alden Miller was an orni- thologist on the staffat Berkeley and became director of the Museum following Grinnell’s death. He and Seth Benson, another Grin- nell student, were much involved in the training of students in mammalogy at Berkeley. Today the fine tradition of mam- malogy at Berkeley is continued by Oliver Pearson (a Harvard product), William Z. Lidicker, Jr. (a Grinnell “‘grandson’’), and James L. Patton (the incumbent ASM pres- PROPINQUITY 131 ident). Patton studied under W. B. Heed, a geneticist, at the University of Arizona. University of Michigan. —Four of Grin- nell’s students, William H. Burt, Lee R. Dice, Emmet T. Hooper, and Fred H. Test, joined the staff at the University of Michigan, thus creating a major center for mammalogical training there. Burt sponsored a number of students, including A. W. Frank Banfield, Fred S. Barkalow, Lowell L. Getz, Timothy E. Lawlor, Richard H. Manville, and Illar Muhl. Students of Lee R. Dice included W. Frank Blair, Wallace Dawson, Don W. Hayne, B. Elizabeth Horner, and John A. King. Students of Emmet Hooper included James H. Brown, Michael D. Carleton, Theodore H. Fleming, Charles O. Handley, Jr., David Klingener, Guy G. Musser, and Albert Schwartz. Robert K. Enders deserves special note as he obtained his degree at Michigan, and then taught at Swarthmore where he was one of the great inspirational teachers. From Swarthmore he inspired Da- vid E. Davis, Philip Myers, and Oliver Pear- son to enter the field. University of British Columbia. —Ian McTaggart Cowan, born in Scotland, estab- lished his career at the University of British Columbia. Dennis Chitty, a student of Charles Elton (Oxford), and Cowan trained Charles Krebs, formerly of Indiana Uni- versity and now also of UBC. Krebs stu- dents include Michael Gaines, Barry Keller, and Robert Tamarin. J. Mary Taylor was also at UBC for many years. Texas A&M University.— At Texas A&M, a program developed under the leadership of William B. Davis and Walter P. Taylor, both Grinnell students. Some of Davis’s most notable students were Dilford Carter, Bryan P. Glass (Oklahoma State Universi- ty), and Randolph Peterson (Royal Ontario Museum at Toronto). Peterson’s students included C. G. Van Zyll de Jong, Judith Eger, and Brock Fenton. Fenton has estab- lished an excellent program in chiropteran biology at York University, York, Ontario. Dilford Carter returned to curate the mam- mal collection at Texas A&M, then moved to Texas Tech University. David Schmidly, a student of Donald F. Hoffmeister at IIli- nois, now serves as Curator of Mammals at Texas A&M. University of Kansas.—An outstanding program arising from the Grinnell dynasty was begun by E. Raymond Hall at the Uni- versity of Kansas. The Grinnell contingent of mammalogists would not be nearly as spectacular if it were not for Hall; thus it appears best to title this the Grinnell/Hall dynasty rather than simply the Grinnell dy- nasty. Hall earlier spent 15 years at Berke- ley, where he advised some students of Grinnell after Grinnell’s death. Hall’s first Ph.D. students were trained at Berkeley as well. Hall produced a large number of stu- dents, many of whom started programs at other institutions. To date, five of Hall’s academic “‘sons”’ (Anderson, Durrant, Fin- dley, Hoffmeister, and Jones) and six of his “grandsons” (Birney, Brown, Genoways, Lidicker, Van Gelder, and Wilson) have served as President of the ASM. Most of Hall’s students are indicated in Table 1, but those who established major Ph.D. pro- grams in their own right are: Rollin H. Baker, first at Kansas and later at Michigan State E. Lendell Cockrum at Arizona Stephen D. Durrant at Utah James S. Findley at New Mexico Donald F. Hoffmeister at Illinois J. Knox Jones, Jr., first at Kansas then at Texas Tech George H. Lowery at Louisiana State Terry A. Vaughan at Northern Arizona Rollin Baker, a student of Hall’s, and John King, a student of Dice’s, thus both “‘grand- sons” of Grinnell, trained a large number of students at Michigan State, including Donald P. Christian, Gary A. Heidt, and Gordon L. Kirkland, Jr. Mammalogy con- tinues at Michigan State today under the leadership of Donald O. Straney and Rich- ard W. Hill. From Cockrum’s program at Arizona came Robert J. Baker, who has established 132 WHITAKER a major research program at Texas Tech, where he has trained a number of students, including John W. Bickham, Ira F. Green- baum, Rodney L. Honeycutt, and Terry L. Yates. At Utah, Stephen Durrant sponsored Richard M. Hansen, Keith R. Kelson, and M. Raymond Lee. Lee in turn sponsored Earl G. Zimmerman at the University of Illinois. An interesting sidelight related by Kelson is that Durrant, although a senior professor, had not yet finished his work on a doctorate at Kansas under Raymond Hall when he presided at Kelson’s Ph.D. final. A year later, Durrant came to Kansas for his final oral defense of the Ph.D. thesis and was examined by Kelson. Another major program arose under the tutelage of James S. Findley at the Univer- sity of New Mexico. Some of Findley’s out- standing students are Michael A. Bogan, William Caire, Eugene D. Fleharty, Patricia (Trish) Freeman, Arthur H. Harris, Clyde Jones, Daniel F. Williams, and Don E. Wil- son. Findley was subsequently joined at New Mexico by J. Scott Altenbach, Terry L. Yates, and James H. Brown, all Grinnell descendants. At least four faculty members associated directly or indirectly with Grinnell pro- duced outstanding students at the Univer- sity of Illinois. Faculty members were Don- ald H. Hoffmeister, M. Raymond Lee, George O. Batzli, and Lowell L. Getz along with ecologist S. Charles Kendeigh, a stu- dent of Victor Shelford. Some of the stu- dents of Hoffmeister are Wayne H. Davis (University of Kentucky), John S. Hall (Al- bright College), William Z. Lidicker, Jr. (Berkeley), David J. Schmidly (Texas A&M), H. Duane Smith (Brigham Young), and R. G. Van Gelder (American Museum). Mark L. McKnight (U.C. Davis) and Earl G. Zim- mermann (North Texas State University) were students of Lee. Richard Lindroth (University of Wisconsin) was a student of Batzli, Joyce Hoffman (Illinois Natural His- tory Survey) was a student of Getz, and Dana Snyder (University of Massachusetts) and Ralph Wetzel (University of Connecticut) were students of Kendeigh. One of Hall’s most productive students, J. Knox Jones, Jr., trained many fine stu- dents, first at Kansas, then at Texas Tech University, where he became Dean of the Graduate School and Vice President for Re- search. A team of six mammalogists on the faculty was assembled at Texas Tech, each with a Ph.D. from a different university — Arizona (Robert J. Baker), Texas A&M (Dilford C. Carter), Kansas (J. Knox Jones, Jr.), New Mexico (Clyde Jones), Oklahoma (first Ronald K. Chesser and currently Rob- ert D. Owen), and Pittsburgh (Michael R. Willig). All are academic descendants of Jo- seph Grinnell. Some of Jones’ most accomplished stu- dents are David M. Armstrong (University of Colorado), Elmer C. Birney (University of Minnesota), Jerry R. Choate (Fort Hays State University, Hays, Kansas), Hugh H. Genoways (Carnegie Museum and Univer- sity of Nebraska), Thomas H. Kunz (Boston University), Carleton J. Phillips (Hofstra University and Illinois State University), and James D. Smith (Fullerton State Uni- versity, California). Some of Jones’ notable academic grandsons are Joseph F. Merritt whose mentor was Armstrong (officially Ol- wen Williams), Robert M. Timm with Bir- ney (officially Roger Price, an entomolo- gist), and Edyth Anthony and Allen Kurta with Kunz. At Kansas, Hall was replaced by Robert S. Hoffmann, and subsequently Jones and Hoffmann were followed by Rob- ert M. Timm and Norman R. Slade. Ken- neth B. Armitage and Michael H. Gaines also have advised many students at Kansas as that center continues to train mammal- ogists. The major centers of mammalogical in- struction established by the first two gen- erations of Grinnell students are indicated in Fig. 1. Four major centers of learning were established by Grinnell’s first genera- tion students at British Columbia, Kansas, PROPINQUITY 199 TORONTO N. ARIZONA LOUSIANA ARIZONA UTAH & Peterson Vaughan Lowery Cockrum Durrant Jones TEXAS A&M UNIV. OF MICHIGAN BRITISH Davis & COLUMBIA Burt, Dice Taylor Cowan & Hooper BERKELEY Grinnel & Miller KANSAS TX TECH Hoffmeister N. MEXICO MICHIGAN STATE Rollin Findley Baker BERKELEY & KANSAS Hall Fic. 1.—Outline of the main branches of the Grinnell Academic tree through the second generation students. Michigan, and Texas A&M, whereas nine were established by the second generation, most through E. Raymond Hall at Kansas. Other particularly successful students of Hall were Sydney Anderson at the Ameri- can Museum of Natural History, R. M. No- wak with the U.S. Fish and Wildlife Service, Henry W. Setzer who retired from the Smithsonian, and Terry A. Vaughan who for many years was at the University of Northern Arizona. Ticul Alvarez and Ber- nardo Villa-R. obtained the Masters degree with Hall, but have provided the backbone of mammalogy in Mexico. Villa-R. even- tually obtained the Ph.D. at the University of Mexico. There are many other academic relatives whose Grinnellian attachments are not as obvious, but are nonetheless very real. For example, Robert S. Hoffmann, now at the Smithsonian Institution, is a “great-grand- son.” His major professor at Berkeley was A. S. Leopold, who started working with Grinnell but finished with Alden H. Miller after Grinnell’s death. However, Miller’s advisor was Grinnell! An academic pro- gram has developed at Oklahoma with Gary D. Schnell and has produced Ronald K. Chesser, Troy L. Best, Janet K. Braun, Mi- chael L. Kennedy, and Robert D. Owen. Schnell’s Ph.D. is from Kansas, with Rich- ard F. Johnston, an ornithologist, serving as mentor. However, Johnston’s Ph.D. is from Berkeley and his major professor was Grinnell’s “‘son’”’ Miller. Michael A. Mares at Oklahoma studied under W. F. Blair at Texas, whose doctorate was completed un- der L. R. Dice at Michigan. Grinnell was Dice’s mentor, although not his major ad- visor, at Berkeley. Several Grinnellites are currently at the U.S. National Museum of Natural History or with the Fish and Wildlife Service in Washington, D.C. They include Michael D. Carleton, Alfred L. Gardner, Charles O. Handley, Jr., Robert S. Hoffmann, Ronald M. Nowak, and Don E. Wilson. In Mexico, the principals in the growth of systematic mammalogy were Ticul Al- varez and Bernardo Villa-R. Both earned 134 WHITAKER their masters degrees at Kansas while study- ing with Hall. In Canada, Ian McTaggart Cowan and Donald L. Pattie in the west and, in the east, A. W. Frank Banfield, Ran- dolph L. Peterson, M. Brock Fenton, and Robert E. Wrigley are all Grinnell descen- dants. The Grinnell group has had tremendous impact on the ASM. Grinnell himself served as president in 1937-1938. Since 1940, when Walter P. Taylor was elected the 12th pres- ident, only three of the presidents in the succeeding 52 years—E. A. Goldman, W. J. Hamilton, Jr., and Hamilton’s academic “son” James N. Layne—are academically unrelated to Joseph Grinnell. Every recording secretary since 1938 has been a Grinnellite, as have all but three ed- itors of the Journal of Mammalogy since 1941, including one unbroken string for the past 27 years. IV. The William J. Hamilton, Jr., Group (Cornell) The other large and important North American dynasty in mammalogy is that of William J. Hamilton, Jr., at Cornell Uni- versity (Table 1, Section IV). While the Grinnellian dynasty centered around sys- tematic mammalogy, the Hamiltonian dy- nasty centered around mammalian ecology and natural history. Hamilton received his B.S., M.S., and Ph.D. degrees in vertebrate zoology from Cornell University under A. H. Wright, ap- parently with much “unofficial’’ guidance from Francis Harper. Francis Harper was a teacher in a Long Island school class when Hamilton was reportedly “‘cutting up.”’ Harper asked Hamilton what bird he was holding and Hamilton correctly identified it as an immature female rose-breasted gros- beak. That brought Hamilton and Harper into lifelong friendship. Hamilton’s inter- ests were in life history and ecology of ver- tebrates, with specialties in food habits, re- production, and to some degree, parasites. He believed in obtaining as much infor- mation as possible from all animals sacri- ficed, and in working with the common- place rather than always with the exotics. In that way one could better obtain ade- quate data to make generalizations. He passed these interests and philosophies on to his students. James N. Layne, who taught at the Uni- versity of Florida, and at Cornell, and is now at Archbold Biological Station, Lake Placid, Florida, was an academic “‘son”’ of Hamilton’s. He has done much work on reproduction and development of mam- mals. This tradition has also been carried on by Harrison Ambrose and Andrew A. Arata, both academic “sons” of Layne. Also, Layne has had a longtime interest in para- sites, especially fleas. Some other students of Layne who worked with ecology and be- havior of mammals are James V. Griffo, Elizabeth Wing, Llewellyn Ehrhart, Dale Birkenholz, John McManus, and James Wolfe. Wolfe is now Dean of Graduate Studies, Emporia State University in Kan- sas, after several years as Executive Director of the Archbold Biological Station. Wolfe has produced “offspring” of his own, in- cluding Robert J. Esher, currently at Mis- sissippi State University. James V. Griffo is at Fairleigh Dickinson University, and Bir- kenholz is at Illinois State University. Wing is presently Curator of Zooarcheology, Flor- ida Museum of Natural History. William Platt started a Ph.D. with Layne at Cornell, but finished with Harrison Ambrose when Layne moved from Cornell to the Archbold Biological Station. Dan W. Walton, a stu- dent of Andrew Arata, is presently with the Australian Biological Resources Study, and is an editor of, and contributor to, the re- cently published mammal tome of the Fau- na of Australia series. John McManus died a few years after he received his Ph.D., but was extremely productive while at Fairleigh Dickinson University. Everett W. (Bill) Jameson, Jr., has carried on the tradition of parasite work far beyond his graduate student days with Hamilton PROPINQUITY 135 where this interest began. Jameson is well known among parasitologists for his work on fleas and mites. Two of his ‘“‘sons” are John Phillips, a Research Biologist at the San Diego Zoological Society; and Duncan Cameron, at York University near Toronto. Allen H. Benton, now retired from the New York State University at Fredonia, is an- other of the Hamilton students who became interested in parasites, greatly furthering our knowledge of fleas. Roger Barbour carried on the tradition of studies in vertebrate natural history. For many years, Barbour was at the University of Kentucky, where he and Wayne Davis teamed up to teach, train students, and do research. Davis is a student of Donald Hoff- meister and therefore also a descendant of the Grinnellian dynasty. Michael J. Harvey, an academic “grandson” of Hamilton, is presently department head at Tennessee Tech University. Another is Marion D. Hassell, who taught at Murray State Uni- versity until his recent death. Harrison Am- brose and Jim Griffo were undergraduate students inspired by Roger Barbour. John O. Whitaker, Jr., was Hamilton’s last student in mammalogy. He took a po- sition at Indiana State University, which became a satellite for continuing studies of food habits of vertebrates and ectoparasites of mammals in the Hamiltonian tradition. He teamed up with a Grinnellian student trained by Burt, Russell E. Mumford, for long-term studies on the mammals of In- diana. Some of his students, the academic grandchildren of Hamilton, are now making their mark. Gwilym S. Jones (who took his master’s degree with Mumford) has estab- lished a center for vertebrate studies at Northeastern University in Boston. Tho- mas W. French is Assistant Director of the Massachusetts Department of Fish and Game. David Pistole is on the staff at In- diana University, Indiana, Pennsylvania. Robert W. Eadie, long associated with Hamilton at Cornell, had several students, including Kyle Barbehenn (EPA, Washing- ton), Richard W. Dapson (now in private industry), and Harold Klein (Plattsburg, NY). For many years, Jack W. Gottschang, a Ph.D. under Hamilton, has been at the Uni- versity of Cincinnati, where he chaired the Department of Biology and taught many students in the Hamiltonian tradition. And last, but not least, there is W. J. Hamilton III. “Young Bill’? took his Ph.D. at Berkeley with Grinnell’s ‘“‘son’’ Alden Miller, and is now at the University of Cal- ifornia, Davis. He has worked with behav- ior of primates, birds, and insects, and on growth and development of the red tree mouse. Early in his career, he worked on bird migration with Franz Sauer. Hamilton did not restrict his work to mammals, and likewise, many of his aca- demic descendants do not. Several have worked with parasites, notably Benton, Jameson, Layne, and Whitaker. Whitaker has also worked with herptiles and fish, and Layne with birds and herptiles. Ralph Yer- ger (Florida State University) and Margaret Stewart (State University of New York at Albany) are two of Hamilton’s students who work primarily with fish and herps, respec- tively. There are of course crossings of lines, and much inspiration at the undergraduate lev- el. Recording this type of contribution would be endless, but a few notable examples fol- low. Bill Jameson was a student of Hall’s at Kansas before going to Cornell. George Bar- tholomew got his M.A. with Alden Miller at Berkeley before going to Harvard. Robert K. Enders inspired David E. Davis, Oliver Pearson, and Philip Myers to pursue further studies. Jerry R. Choate at Fort Hays State University has inspired numerous students in mammalian systematics. Jerry has pro- duced 32 master’s students, at least 24 of whom have earned or are candidates for the Ph.D. These include Mark D. Engstrom, Sarah B. George, Cheri A. Jones, Nancy D. Moncrief, Philip D. Sudman, Michael P. Moulton, Lynn W. Robbins, Jerry W. Dra- goo, and Brett R. Riddle. James B. Cope (Earlham College, Richmond, Indiana) is 136 WHITAKER another of the outstanding undergraduate teachers. He was originally inspired as an undergraduate student by Bill Hamilton and went on to teach at Earlham college at Rich- mond, Indiana. Earlham has no graduate program, but the influence on bat biology exerted through Cope and his students is considerable. Some of Cope’s undergradu- ate students at Earlham were Richard F. Myers (who influenced Thomas H. Kunz at the undergraduate level), Wilson Baker, Nixon Wilson, Anthony F. DeBlase, Steven R. Humphrey, Charles Thaeler, and Rich- ard Mills. Of course there has been continuous ex- change between the Hamilton and Grinnell/ Hall schools. Some outstanding workers that were influenced by Hamilton as undergrad- uates at Cornell, then went on to study un- der Grinnellian descendants are William Z. Lidicker, James H. Brown, Norman O. Ne- gus, and Edwin Gould. E. W. Jameson start- ed in the Grinnell school and did his Ph.D. with Hamilton. Earl G. Zimmerman, an eventual Grinnellite, began his productive career while working as an undergraduate student (and publishing his first paper) with Whitaker at Indiana State. V. Other Groups There are a few other centers of learning that have produced students in the field of mammalogy. These tend to be smaller, but have made many excellent contributions to the field. Florida. —A group of biologists has come together in recent years at the University of Florida, and Florida now can be thought of as a center for training mammalogists. Stev- en Humphrey (a student of Bryan Glass at Oklahoma State University), John H. Kauf- mann (Grinnellite via A. S. Leopold), and John F. Eisenberg (student of behaviorist Peter Marler) are there. James N. Layne (Archbold Biological Station) has been in- fluential in the development of this group. This group is supported by paleontologist S. David Webb, and ornithologists J. C. Dickinson and Franz Sauer. Jackie Belwood (student of Stephen Humphrey), Cheri Jones (student of John Eisenberg), Paul Pearson (student of Archie Carr), and Michael H. Smith obtained their training there. Mike Smith has headed the Savannah River Ecol- ogy Laboratory at Aiken, South Carolina, for many years. Purdue. —Purdue University has had its influence on mammalogy, earlier under Durwood L. Allen and Charles M. Kirk- patrick, both essentially conservationists, and later under two of Kirkpatrick’s stu- dents, Russell E. Mumford and Harmon P. Weeks. Some of the more notable students from this group are L. David Mech and Rolf O. Peterson, two wolf biologists, and Virgil Brack, Jr., a bat biologist. Tulane.—Norman C. Negus and James S. Findley grew up together in suburban Cleveland, Ohio. Their ‘Bible’? was Ham- ilton’s Mammals of the Eastern United States (1943). Negus studied under Eugene Dustman, an ornithologist, at Ohio State. Findley ended up heading the Kansas sub- group at New Mexico, and Negus then es- tablished a mammal center at Tulane, with Jack A. Cranford, Edwin Gould, John F. Pagels (co-advised with Clyde Jones), Aelita J. Pinter, and Thomas E. Tomasi among his students. Negus now heads a research group at the University of Utah. Wisconsin. —The University of Wiscon- sin has also served as a center, although neither of the two principals, John T. Emlen and Roland K. Meyer, is a mainstream mammalogist. Meyer is an endocrinologist and Emlen is a preeminent ecologist. Phillip L. Wright emerged from this program and established a program in mammalogy at the University of Montana. He was joined there for a time by Robert S. Hoffmann, who also had students at the University of Kansas and is now at the Smithsonian Institution. Garrett C. Clough and William A. Fuller PROPINQUITY 13y/ were students of Emlen, and John E. War- nock, Rodney A. Mead, and Tim W. Clark are notable mammalogists from the Wis- consin and Montana programs. Other Sources. — Many “‘mammalogists”’ have entered the field from other fields but are now working primarily with mammals. Several physicians have made names for themselves in mammalogy, one being C. Hart Merriam. Others include Marcus Ward Lyon, Jr., who wrote Mammals of Indiana in 1936 and who is also a past president of the ASM; Murray L. Johnson, who received his M.D. from Oregon Medical School; and George Wislocki, an anatomist at Harvard Medical School. Denny G. Constantine, who has made many valuable contributions con- cerning bat rabies, is a veterinarian. A number of individuals have received degrees in ecology, then have done concen- trated work in mammalogy. For example, Dennis Chitty and Francis C. Evans worked with Charles Elton at Oxford, Michael Ro- senzweig with Robert MacArthur at Penn- sylvania, E. V. Komarek with W. C. Allee at the University of Chicago, and Wilson Baker and Gary Barrett with Eugene Odum at the University of Georgia. Charles Krebs, in turn, worked with Dennis Chitty. Several individuals are associated with mammalogy from a wildlife biology back- ground, including both the principles of the Purdue group, Durwood L. Allen and Charles M. Kirkpatrick, and also Willard D. Klimstra, B. J. Verts, Joseph A. Chap- man, George A. Feldhamer, and Glen C. Sanderson. Several have entered mammalogy from a genetics background, such as Gary F. McCracken, who worked with Peter Brus- sard; and James L. Patton, who worked with W. B. Heed at the University of Arizona, where he also was closely associated with E. Lendell Cockrum. Karl F. Koopman took his Ph.D. with T. H. Dobzhansky at Co- lumbia. His doctoral dissertation, on nat- ural selection and reproductive isolation be- tween two closely related populations of Drosophila, was a classic of its day and fre- quently is cited in courses in evolution and genetics. Koopman has made numerous contributions on bats and is now an Hon- orary Member of ASM. Other examples given in Table I include William A. Wimsatt and Roy Horst, who worked with a morphologist; Duane A. Schlitter, Paul K. Anderson, Paul Pearson, and Kenneth Wilkins, who worked with herpetologists; and Albert E. Wood, who worked in palaeontology. There is another group of mammalogists who, similar to the Merriam group, did not have Ph.D.’s and thus did not have stu- dents, yet they have made major impacts on the field. These include individuals such as Rudolph M. Anderson, a long-time worker in Canada; G. H. H. Tate, who worked with mammals of eastern Asia and South America; Harold E. Anthony (mam- mals of North America); Hobart M. Van Deusen of the American Museum (mam- mals of New Guinea); and Phillip Hersh- kovitz of the Field Museum (South Amer- ican mammals). Karl Kenyon (marine mammals) and Olaus Murie (large carni- vores) are also high profile examples of this group. Present day mammalogists of North America come from a few major lineages and several other sources and backgrounds. The few earlier stems stimulated the field but the great diversity present today allows for diverse methods and ideas to be applied to problems in mammalogy and should help us to continue to make major intellectual advances. Systematics and life history studies led the way and are still exceedingly important, but today many other areas, no- tably genetics, behavior, ecology, physiol- ogy, conservation biology, and many other fields make their contributions. Although our roots to this point are relatively few, diversity continues to increase as specialists continue to add to the field of mammalogy, and the genealogy of mammalogists be- comes ever more complicated. 138 WHITAKER Acknowledgments This paper would not have been possible with- out the cooperation of many individuals too nu- merous to mention. However, special thanks are due to Elmer C. Birney, James H. Brown, Donald F. Hoffmeister, J. Knox Jones, Jr., William Z. Lidicker, Jr., Oliver P. Pearson, and Don E. Wil- son, all of whom have read and greatly improved the manuscript. Literature Cited GRINNELL, H. W. 1958. Annie Montague Alexander. Grinnell Naturalists Society. Museum of Vertebrate Zoology, University of California, Berkeley, 27 pp. Hatt, E. R. 1939. Joseph Grinnell (1877 to 1939). Obituary. Journal of Mammalogy, 20:409-417. HamILTon, W. J., JR. 1943. Mammals of eastern United States. Comstock Publishing Co., Ithaca, New York, 432 pp. 1955. Mammalogy in North America. Pp. 661-668, in A century of progress in the natural sciences 1853-1953. California Academy of Sci- ences, San Francisco, 807 pp. HOFFMEISTER, D. F. 1969. The first fifty years of the American Society of Mammalogists. Journal of Mammalogy, 50:794-802. Jones, J. K., Jk. 1991. Genealogy of twentieth-cen- tury systematic mammalogists in North America: the descendants of Joseph Grinnell. Pp. 48-55, in Latin American mammalogy: history, biodiversity, and conservation (M. A. Mares and D. J. Schmidly, eds). University of Oklahoma Press, Norman, 468 pp. LAYNE, J. N., AND R.S. HOFFMANN. 1994. Presidents. Pp. 22-70, in Seventy-five years of mammalogy (1919-1994) (E. C. Birney and J. R. Choate, eds.). Special Publication, The American Society of Mam- malogists, 1 1:1-433. STORER, T. 1969. Mammalogy and the American So- ciety of Mammalogists, 1919-1969. Journal of Mammalogy 50:785-793. MEeErRRIAM, C. H. 1877. A review of the birds of Con- necticut, with remarks on their habits. Transactions Connecticut Academy of Arts and Sciences, 4:1—150. ME_ErRRIAM, C. H. 1884. The vertebrates of the Adi- rondack region: the Mammalia. Transactions of the Linnean Society of New York, 1:1-124. PUBLICATIONS B. J. VERTS AND ELMER C. BIRNEY Introduction Rn to the Bylaws and Rules adopted by the American Society of Mammalogists on 3 April 1919, “The ob- ject of the Society shall be the promotion of the interests of mammalogy by holding meetings, issuing a serial or other publica- tions, aiding research, and engaging in such other activities as may be deemed expedi- ent” (Article I., Sec. 2.). Of the budget ap- proved by the Board of Directors for 1992, $122,000 (74.1%) of the total $164,630 was allocated for expenses related directly to ed- itorial activities of the society. Throughout the 75 years of the existence of the society, no single activity has been of higher priority, received a larger share of the budget, or, arguably, had a greater impact on the development of the discipline than has pro- duction of the society’s publications, es- pecially the Journal of Mammalogy. It is the purpose of this chapter to provide a brief summary of the 75-year history of the pub- lications of the ASM, with special emphasis on trends observed in the content of the Journal of Mammalogy during this period. 139 Journal of Mammalogy American Society of Mammalogists The Journal of Mammalogy The Journal of Mammalogy has served the role of the serial publication authorized in the Bylaws and Rules since the ASM was founded. It also has functioned as an “‘of- ficial” publication of the society in that it includes announcements and minutes of meetings, lists of officers and committee members, and other announcements and communications. However, nowhere have we found that the Journal of Mammalogy ever was designated the official publication of the American Society of Mammalogists. The Journal of Mammalogy commenced publication on 28 November 1919, <8 months after the society was founded. Vol- ume | (259 pages) consisted of five numbers (issues); the four published in 1920 almost certainly were intended to establish the Feb- ruary, May, August, and November pattern of publication, but each actually was pub- lished in the following month. Authors of the articles published in the first volume included some of the most renowned and 140 VERTS AND BIRNEY | 72 VOLUME Fic. 1.—Strata-surface graph of the number of pages devoted to feature articles, general notes, and other components in volumes 1-72 (1919- 1991) of the Journal of Mammalogy. revered names in American mammalogy: Glover M. Allen, J. A. Allen, H. E. An- thony, Vernon Bailey, Lee R. Dice, James W. Gidley, Joseph Grinnell, G. Dallas Han- na, Francis Harper, Arthur H. Howell, A. Brazier Howell, Hartley H. T. Jackson, Stanley G. Jewett, C. Hart Merriam, Gerrit S. Miller, Jr., W. D. Matthew, Wilfred H. Osgood, John C. Phillips, Ernest Thompson Seton, Arthur de Carle Sowerby, H. L. Stod- dard, Walter P. Taylor, P. A. Taverner, and Edward R. Warren. Interestingly, only a sin- gle article was coauthored (by G. S. Miller, Jr., and James W. Gidley), only one was by a researcher from other than North America (by A. de C. Sowerby of England), and only eight (10.8%) of the 74 articles published were about mammals other than those in North America (one each on African car- nivores, cats, and monkeys; neotropical bats and cats; Asian bears; Japanese bats; and Brazilian tapirs). The initial issue of the Journal of Mam- malogy was a 51-page number consisting of 7 feature articles (37.3 pages), 4 general notes (4.6 pages), 3 reviews and 49 references in a recent-literature section, an editorial com- ment (1.6 pages), and the Bylaws and Rules adopted on 3 April 1919 (2.6 pages) when the society was founded. Both feature arti- cles and general notes tended to be short; the former averaged 4.5 pages, the latter <1 page. The comments by Editor Ned Hollis- ter consisted of a paragraph-long history of the organization of the society, a description of the scope of the Journal, solicitation of manuscripts for the Journal, a plea for members to recruit new members, an ac- knowledgment of Ernest Thompson Seton’s contribution of the sketch of the pronghorn for the front of the Journal, a report of the election of J. A. Allen as an Honorary Mem- ber, and acomment on the paper by C. Hart Merriam titled “Criteria for the recognition of species and genera.”” Volume 1, number 4 contained a list of members, some of whom were listed subsequently as other than char- ter members (Journal of Mammalogy, 3: 203-218, 1922). Although the basic composition of the Journal of Mammalogy was established at the onset, numerous changes have occurred in the proportion devoted to each of the sections. For example, during the first 3 de- cades of publication, general notes com- posed about 20—50 pages, irrespective of the total number of pages published in each vol- ume (Fig. 1). However, after about 1950, more and more space was devoted to gen- eral notes; in both 1988 and 1989, >290 pages of general notes were published (Fig. 1). Editorial policy was altered in 1990 to limit the number of general notes published as a means of enticing bibliographic services to include references to more of the shorter papers published in the Journal. The gen- eral-note format was abandoned commenc- ing with volume 73 (1992). Over the years, some minor evolution has occurred in components of the Journal of Mammalogy: “Editorial Comment” in vol- ume | (1919-1920) became “‘Correspon- dence” in volume 2 (1921) and remained so until volume 6 (1925) when it became ‘Comment and News,” which in volume 35 (1954) became ““Comments and News.” The “Recent Literature” section was an in- tegral part of the Journal from its inception through volume 50 (1969), published as a supplement to volumes 51-66 (1970-1985) of the Journal, then discontinued com- mencing with volume 67 (1986). Member- PUBLICATIONS 141 ship lists were published in volumes 1 (1919-1920), 3 (1922), 5 (1924), 11 (1930), 15 (1934), 18 (1937), 21 (1940), 29 (1948), 31 (1950), 35 (1954), 40 (1959), and 46 (1965), and as supplements accompanying volumes 54 (1973), 59 (1978), 65 (1984), and 70 (1989). Other supplements were published irregularly and include three edi- tions of “Guidelines for manuscripts,” “Roles of standing committees,” “Survey of North American collections of Recent mammals,” and “Acceptable field methods in mammal- ogy.” The “Bylaws and Rules,” or, when amended, parts thereof, were included in several issues. Reviews of recent publications were in- cluded in the first issue and in most, but not all, subsequent issues of the Journal of Mammalogy. Until volume 17 (1936), re- views were included in the recent-literature section, but afterward were afforded a sec- tion of their own with the subheading “‘Re- views.” Reviews occupied 4-11 (¥ = 4.7) pages in volumes | 7-32 (1936-1951), 5-17 (X = 11.7) pages in volumes 33-50 (1952- 1969), 20-31 (X¥ = 23.6) pages in volumes 51-66 (1970-1985), and 12-19 (¥ = 15.7) pages in volumes 67-72 (1986-1991). Greater emphasis was placed on the pub- lication of reviews commencing with vol- ume 73 (1992); 26 pages were devoted to reviews in that volume. An author-subject index is published in the last issue of each volume; however, the index to volume 52 (1971) was published as a supplement to the first number of vol- ume 53 (1972). Commencing with that in- dex and continuing to present, an alpha- betical (by last name of author or editor) listing of books reviewed in the volume fol- lowed by the page number on which the review may be found concludes each index. Also, commencing with volume 67 (1986) author and subject indices were separated. Announcements of the death of members of the American Society of Mammalogists were included in the Journal of Mammalogy for the first time in the fourth number of volume | (1919-1920). Like other com- ponents of the Journal of Mammalogy, death notices underwent considerable evolution. At the end of the first membership list, names of three deceased numbers were list- ed. The general-notes section of the same issue included a seven-line obituary for one of those listed (Thomas M. Owen) and a nearly page-long obituary for a Canadian naturalist and agency official (James M. Ma- coun) who apparently was never a member of the society. The second volume con- tained no death notices, but the third vol- ume (1922) contained a list of nine deceased members, including the three listed in vol- ume | (1919-1920); this appeared at the end of the new list of members. Seemingly, the intent initially was to include a list of all deceased members with each membership list, but the practice was abandoned after publication of the second such list. The first extensive obituary was the 7-page “‘appre- ciation’”’ for one of the founders of North American mammalogy, Joel Asaph Allen, published in volume 3 (1922); a second obituary for Allen was published in volume 11 (1930) and, with a photograph, included >13 pages. However, no bibliography ac- companied the text of either. For about 25 years, either lists of deceased members (usu- ally in bold-face type) published in the com- ments and news section or short (from 6- 10 lines to a page or so) obituaries for de- ceased members were common. Sometimes a deceased member’s name appeared in one of the lists and an obituary for that member was published subsequently, but more often a deceased member was honored only once. Occasionally, obituaries for prominent members covered 3-5 pages or more and one that included a bibliography and cor- respondence (for President Edward A. Goldman) required 22 pages [volume 28 (1947)]. Since about 1950, names of de- ceased members were listed in the com- ments and news section under the subhead- ing ““Deaths Reported.” Names were in boldface, but cities and states of residence and membership status (honorary, life, or emeritis), when included, were set in italic. 142 VERTS AND BIRNEY Also, since about 1950, obituaries have been limited to past presidents and prominent mammalogists. In a few instances, a death notice or obituary has been included in the Journal of Mammalogy for a mammalogist or naturalist (usually foreign) for which there is no published record of their having been a member of the society. Miscellaneous items published in the Journal of Mammalogy from time to time include letters to the editor, letters from the president, publication policies and sugges- tions to authors, personal notices (mostly items for sale and items wanted), member- ship application forms, advertisements of society publications, and paid advertise- ments for equipment, supplies, and publi- cations of interest to mammalogists. One issue, the third of volume 11 (1930), con- tained 64 pages of papers resulting from a symposium on predatory animal control. The fourth issue of each volume commenc- es with a series of roman numbered pages (usually 8 pages, 2 of which are blank) that contain a list of editors, a reprinting of the verso of the front cover, and a reprinting of the contents of all four issues of the volume. The artwork of Seton graced the cover of the Journal of Mammalogy for a decade, but commencing with the first issue of vol- ume 11 (1931), a new cover designed by A. Brazier Howell and dominated by the head and cape of a pronghorn appeared. Howell’s artwork appeared on the cover through vol- ume 43 (1962). A new design depicting a standing pronghorn appeared on the cover of volumes 44-48 (1962-1967) and was fol- lowed by another head and cape view of the pronghorn in volumes 49-72 (1968-1991). Artwork for both cover designs was signed; “Hines” signed the former and the cryp- tographic signature on the latter is the ini- tials of Frances L. Jacques. No “‘Hines’”’ was listed as a member of the American Society of Mammalogists in membership lists pub- lished in 1959 or 1965, so likely the cover design used for volumes 44—48 (1962-1967) was drawn by a commercial artist. Jacques was an artist at the American Museum of Natural History and the James Ford Bell Museum of Natural History. A radical de- parture from the traditional green and black cover dominated by a pronghorn com- menced with volume 73 (1992). The prong- horn, although still present and still the art- work used in volumes 49-72 (1969-1991), no longer dominates the cover, but is rele- gated to a small circle. The central figure, consisting to date of artwork depicting some mammal, is unique to each issue. Green, although a different shade, remains featured on the somewhat thicker and smoother cov- er, but on the front, the lettering, a square enclosing the central figure, and the small circle enclosing the drawing of the prong- horn are white. On the back cover, large lettering and a rectangle containing a list of officers and directors also are white. Also, the first color plate for a research article was published in volume 73 (1992); however, the first and only other color plate published in the Journal was that of Rupicapra rupi- capra by F. Murr from Erna Mohr’s Sdau- getiere included in the review by R. H. Man- ville of that book published in volume 40 (1959). Through volume 57 (1976), the entire Journal of Mammalogy was printed 1n sin- gle-column format. Commencing with vol- ume 58 (1977), literature-cited sections were printed in double-column format, but the text remained single column until volume 73 (1992) when the space-saving and the easier-to-read double-column format was adopted. The Williams and Wilkins Com- pany, Baltimore, Maryland, printed the first 37 volumes of the Journal of Mammalogy, but commencing with volume 38 (1957) of the Journal, Allen Press, Lawrence, Kansas, has served as the printer for all publications of the American Society of Mammalogists. Throughout the history of the Journal of Mammalogy, all editorial services have been provided by members who volunteered; for the first 37 volumes (1919-1956) all edi- torial services were provided by one person, designated the “editor.” Subsequently, sev- eral systems of dividing the ever-growing PUBLICATIONS 143 editorial responsibilities were employed (Table 1). The present system, stable for the last 14 volumes (60-73) consists of a man- aging editor (the editor of record) respon- sible for production of the Journal, a journal editor responsible for matters of style and presentation, several associate editors re- sponsible for conducting the review process and judging the scientific merit of manu- scripts, an editor for reviews responsible for soliciting and editing reviews of books and assembling and publishing a “books re- ceived” list of books submitted but not re- viewed, and an editor for advertising re- sponsible for personal notices and commercial advertising. Since its inception, only 62 mammalogists have served the Journal of Mammalogy in one or more ed- itorial capacities (Table 1); the length of ser- vice ranged from | to 16 years and averaged 4.6 years. The Journal has had only 17 ed- itors of record; length of service averaged 4.5 years (range, 1-7 years). From the onset, the Journal of Mam- malogy was provided free to all members and was available to institutions by sub- scription. Just as there has been an increase in number of pages published (Fig. 1), there has been an increase in both membership dues and subscription rate (Fig. 2). Since 1953 (when publication of a summary of the annual budget in the Journal com- menced), neither subscription rate nor membership dues has kept pace with funds budgeted for publication of the Journal of Mammalogy (Fig. 2). Income from the J. A. Allen Memorial Fund and other invest- ments managed by the society’s trustees (Kirkland and Smith, 1994) make it pos- sible to continue to provide members and subscribers with a quality publication at a modest cost. In his initial solicitation of papers, the first editor, Ned Hollister, emphasized the need to make the Journal of Mammalogy an essential tool for workers in all phases of mammalogy. To ascertain the effective- ness of this and similar pleas by subsequent editors, we analyzed trends related to length, 120 100 80 35 25 x 1,000 $ 40 15 20 (Se pee emcee aes {e) | 72 VOLUME Fic. 2.—Line graphs of membership dues (heavy line) and subscription rates (light line) for volumes 1-72 (1919-1991) on left ordinate and histogram of funds budgeted by the Board of Directors (as published in the Journal of Mam- malogy) for production and distribution of vol- umes 34-72 (1953-1991) of the Journal of Mam- malogy on right ordinate. subject matter, and authorship of papers published in the Journal of Mammalogy by sampling alternate volumes from volume 1 (1919-1920) to volume 71 (1990). Length measured to the nearest 0.1 page, the con- tinent of origin for species reported on, number and residence of authors, number of references cited, and major topic covered were recorded for each article published in volumes sampled. Editors and authors have maintained a diversity of topics among articles published in the Journal of Mammalogy; after an ini- tial paucity of papers on morphology, re- production, and behavior they have main- tained a more even balance among topics. Articles published as feature articles (Fig. 3a) cover more diverse topics than general notes (Fig. 3b) as > 20% were on topics other than the six classifications that we used to present results of our analysis. Overall, ap- proximately one-fourth of all articles pub- lished as feature articles were devoted to ecology and life history, and, among general notes, the same proportion was devoted to articles describing distributions and new lo- cality records (Fig. 3). Since about 1964, the number of general notes devoted to distri- VERTIS AND BIRNEY 144 sauof “D Joyeg “{ “Y Jassny “9 ") If ‘souof “y ‘f bs €L6l uuewyoH “S “Y Joyeg “f Y Jassnw “DD If ‘souof y “f €¢ ZL61 uueUyoH “SY Jassny “DD Joye) ‘Dd If ‘souot “y “f (AS 1L61 uuewlyoH “S “Y Wismel “yf Jae) ‘D'd If ‘sauof “yf “f IS OL6I uueWyOoH “S “Y wismel “yf Joye) ‘O'd If ‘souof “yf “f os 6961 SMOIAOI s9}0U [e1oUId sgpoIwe sinyeoj JOVps ouINOA Tea X JO} 1OVIPA JOJ 10IPA JO} 1OUIPA sulseury| 1YysUM “Td ueysne, “YL ‘If ‘souof “yf 6b 8961 YSU “Td ueysned “YL ‘If ‘souof “yy “f 8b L961 SMOIADI PUP SopoIe sin eoj IOVpo durseueyy oUINJOA Tea $9}0U [e1ouad JO} JOVPY JOj 1011Pq Aend “@ “A “Af “OxOIpIT “Z “AM ‘OUART ON “f ‘ouasulpy “ff “Cd ‘AI10D “@ “A ‘Z19D “TT 977 “UW Lv 9961 Aend “dM “JOA SU “If “IOYOIPYT “"Z “AA OUART CN “f ‘2199 “TT 971 YW OP $961 Aend “@ “A “VBL “Td ‘SIAR “HM “JO9" “HU Joog “a ‘f Cr b961 Aend “@ “A “WSL “Td ‘SIAR “HM “JOx"G “HU Joog “UY ‘f br £961 JOIN “SU WSU Td “OXNG “TM “Oye “H “UY ayftAueW “HU ev 7961 JON “SU WSU Td “O4NG “TM “oxeG “HU ayftauey] “HY (47 1961 JON SU BUM Td ‘2NG “TM “Oe “HU aytAuey] “HY Iv 0961 JON “SU BLA Td ‘ONG “TH ‘Oe “HU ayftAuey] “HY Or 661 BUA “Td ‘NG “TH ‘Joye “H “A ayiAueyl “HY 6£ 8561 BUM “Td ‘xn “TM ‘Oe “HU ayfiaueyy “HY SE LS6l SIOJIPS 9e1IDOSSY JOUpY oUIN[OA Jeo sped UM LE-vE 9S6I-€S61 ung H'M ~~ ££€-67 7S61-8r61 SIAR “AM ~—- 87-7 Lv6I-IP6l IlPMOH “HV 17-61 Or6I-8E61 I9MOH “AV 8I-LI LE6I-9€61 Wid VA O9I-II SE6I-O£6I uosyoef -L ‘H‘H OI-9 6761-S76I1 Ja\st]JOH *N c-I p761-6161 JOWUPA (s)ouIN[OA (s)189 X ‘£661-6161 ‘Adojewweypy jo jeumor ay) fo ssojipa pun ffp]s Jv1sojipa ay —"| ATAVL, 145 PUBLICATIONS 0909090999000 sdityd “f°D IOUDYIIN “YD sole “VW HIAPW “Sf “If ‘souof “yf ‘f suOsSuULTY “Wd Joyeg “f° souof *D 99 C86l sdityd “f°O IOUDYII “YD UOIDWIBD “ND NIIPW 'S ‘f ‘If ‘souof “y “f suoNsuLIY “W ‘dd AsUIIG “DA Joyeg “f “Y $9 r86l sdityd “f°O UOIDUIBD “ND NIITPW 'S ‘f ‘If ‘souof yf suONISULIY "Wd ADU “DA Joyeg “f[ Y 9 £861 JojAeL ‘Wf UOIDWRD “ND VIAPW S ‘f uoned “Tf uedog ‘Vv ‘W AQUI “D “A Joyeg “fa £9 C86l SLIDA ‘fg uOIIWIRD “ND VIPW S ‘f uoned “Tf uesog “VY ‘W uOsTIM “AC IO[MET “FAL Aug “D “A c9 186] SIDA “[ “E UsTTTADW “A “a VIIPW 'S ‘f uoned “Tf uesog ‘VY W uOsTIM “AC JO[MET “AL Aoung “Dy 19 0861 SHIA “fA USTTTAD I “A a HITTPW 'S “f uoyed “Tf ToupIey) "TV UOSTIM “A “Cd Jo[MeT “FAL Aout “Dd 09 6261 JOWps SMOIADI S10}Ipa JOVps ;euNos IO}Ip JOIps dUINjOA eax SUISILISAPY JO} JOUPY a1e1ID0SsVy surseuew surseueyy a1eID0SsyV (10}Ipo ‘oOsse ‘UOSTIMA “A “C) Jap[aH ueA ‘N'Y uoneg “Tf JOUpIey "JT “Vv A[Ptulyys “fq uUuRWYOH “SY sAB@MOUDD “HY “H 6S 8L6l TopjeD ueA "DU uoned “Tf UOSTIM “A Cd ATpruryys “f “q uuewyoH Su skemousy “H “H 8¢ LL6I Jop[eyH ueA “DY souof ‘dD A[ptwiyys “f “Gq JoussulTy “f °d uueuWoH ‘Ss ‘Yy skB@MOUSD “HH LS 9L61 souof ‘dD Joussulpy “fd Jayeg ‘fu uuReWYOH SY skemoudy “HH 9¢ CL6l souof ‘Od IouasulTy “fd Jayeg “[ -u uueWYyoH ‘S$ “Yy skBmOUdy “HH cS PL6l JOJIpa SMOTADI s9}0U [e19ua8 sgporse oinjeay JOJIps JOIps dUINJOA IeaX SUISILISAPY JO} 101IPA JOJ 1O1IPA JOJ 1OIIPY sulseuew suiseuep| a1e1ID0ssyV ‘panuljuoy) —"| ATaV VERTS AND BIRNEY 146 9soy Ma uesog ‘VW ues0g ‘VW uesog “VY “W ues0g ‘V ‘W uesog “VY ‘W ues0g ‘VW JOVps BUISILIOAPY uosioiieg ‘qd ‘d ‘If ‘souof “yy ‘f ‘If ‘souor “yf ‘f ‘If ‘souof “yf ‘f ‘If ‘souof “yf ‘If ‘souof “yf ‘f af ‘sou0l it SMOTADI J0J JONIPY JOUdYI “UY SUONSWIY ‘WW IouoyoI, “YU SUONSULIY “A NO pe be a ae race ‘M- SUDTTTM “L * ulewey “He HUIS “A” - “M- eae Oe ely ee d uensiuy ullewe Sole JoujeH “Oe uensuy. ‘d Re 1 “M TAN De ewe “H JoujeH ‘S* YW ‘d LH ive Sole “VY ° uensuyD ‘d soley “VW ° uensiyD ‘d Ree cee Oo Fe ee ee S1O]IPo aye1ID0ssy og “TL oq “TL SHA “fd SHIA “f “a SUDA ‘f “d soyeg f Y Joyeg “f “a IOWps jeuinor ‘panuljuoy —"| ATV, Joyeg “f° SHIA “fA souof “D sauof “D souof ‘O sauof ‘OD souof ‘OD IOUpPs sulseuryyy CL CL IZ 89 Lo JUINJOA C661 1661 0661 6861 8861 L86l 9861 Jeo TABLE |.— Continued. Publications Journal Associate Editor for Advertising Managing editor R. K. Rose editors reviews editor T. L. Best editor R. M. Timm editor R. J. Baker Volume Year B. D. Patterson . W. Freeman McBee 74 1993 PUBLICATIONS 147 butions and new locality records has de- clined steadily (Fig. 3b); manuscripts com- posed largely of descriptions of extensions of geographic ranges of taxa based on single locality records were specifically excluded from the Journal by publication policy com- mencing in 1988. No other major trends in the diversity of topics of articles published in the Journal are discernable. Authorship has remained largely North American; of 1,691 feature articles and 2,613 general notes published in alternate vol- umes from volume | (1919-1920) to vol- ume 71 (1990), 1,555 (91.9%) and 2,456 (94.0%), respectively, were written exclu- sively by North American authors. Never- theless, a trend toward more articles au- thored by researchers outside of North America seems to be becoming established. In volume 71 (1990), 23.8% of the 63 fea- ture articles and 30.8% of the 39 general notes were authored by one or more re- searchers from other continents. Although 84.8% of the 2,613 general notes and 81.8% of the 1,691 feature articles were about North American taxa, a trend established after World War II toward publication of more articles on mammals from other con- tinents continues. In volume 71 (1990), 34.9% of 63 feature articles and 38.5% of 39 general notes were about mammals from other than North America. Coauthorship became an increasing trend for feature ar- ticles and general notes; however, three or more authors were rare before volume 27 (1946) for feature articles, and volume 39 (1958) for general notes (Fig. 4). In volume 71 (1990), the last for which we separated papers by type, 84.6% of general notes and 55.6% of feature articles were written by more than one author (Fig. 4). Thus, not only is the number of authors increasing, but both the scope and the clientele of the Journal of Mammalogy are becoming more international. After the initial volume, average length of feature articles (Fig. Sa) was 6-9 pages during most years until volume 45 (1964) when the average length began a steady climb 148 VERTS AND BIRNEY All Other Topics Morphology Ecology and Natural History VOLUME Ecology and Natural History Distribution and Locality Records | 7I VOLUME Fic. 3.—Surface graph of proportions of the total number of articles on each of several topics in alternate volumes for volumes 1-71 (1919- 1990) of the Journal of Mammalogy: a, feature articles; b, general notes. that reached a peak of > 14 pages in volume 56 (1975). The peak was followed by a somewhat precipitous decline to a plateau of <10 pages. During only | year before volume 45 (1964) did the average length of general notes exceed | page (Fig. 5b), but after volume 45 (1964), average page length increased gradually to >4 pages in volume 69 (1988), but declined to 3.0 in volume 71 (1990) in response to efforts by editors to emphasize feature articles. The number of references cited per paper averaged <10 for feature articles and less than two for general notes in most volumes before volume 45 (1964; Fig. 6). However, commencing about 1945, the average num- q 100 < % c; TI VOLUME 100 7 oe %e er Ta VOLUME Fic. 4.—Surface graph of proportions of the total number of articles authored by one, two, and three or more authors in alternate volumes for volumes 1-71 (1919-1990) of the Journal of Mammalogy: a, feature articles; b, general notes. ber of references proliferated greatly, at- taining an apex of >35 for feature articles and > 15 for general notes published in most recent volumes. No doubt, the almost log- arithmic increase in number of references cited per paper in both feature articles and general notes was a response to both the greater need to document previous findings and the greater availability of information on all aspects of mammalogy (Anderson and Van Gelder, 1970). In the first volume, new taxa were de- scribed in 12 (36.4%) and new names were applied to named taxa in three (9.1%) of the 33 feature articles. Describing and naming new taxa remained a common topic of ar- PUBLICATIONS 149 | 7 PAGES a ion | 7 VOLUME Fic. 5.—Bar graphs of the average number of pages per article published as: in alternate vol- umes for volumes 1-71 (1919-1990) of the Jour- nal of Mammalogy: a, feature articles; b, general notes. ticles published in the Journal of Mam- malogy in the first 20 volumes; subsequent- ly, alpha taxonomy was the topic of <10% of the articles published. Overall, only 3.6% of 4,304 articles published in alternate vol- umes of the Journal of Mammalogy con- tained descriptions of new taxa. Rodents, bats, and carnivores, in that or- der, were the most popular topics of articles published as general notes in the Journal of Mammalogy (Fig. 7a). Fewer general notes on insectivores or on more than one order were published in the last 15 years that pa- pers were segregated by type. Among feature articles, however, trends toward publication of more and more articles on rodents and fewer and fewer articles on taxa representing more than one order of Mammalia were evident almost from the beginning of pub- lication of the Journal (Fig. 7b). A similar trend was noted in oral presentations at an- nual meetings (Gill and Wozencraft, 1994). Obviously, manuscripts containing infor- mation on more than one order of mam- mals were not converted to general notes as the proportion of general notes on multior- dinal topics also has declined in recently published volumes (Fig. 6a). Likely, the or- 40 REFERENCES De) oO C TI VOLUME Fic. 6.—Line graph of the average number of references cited per feature article (heavy line) and general note (light line) published in alter- nate volumes for volumes 1-71 (1919-1990) of the Journal of Mammalogy. dinal topic chosen reflects the abundance, diversity, and ease of catching and handling rodents and bats. From this brief analysis, we conclude that the Journal of Mammalogy has filled and All Other Orders VOLUME Chiroptera Rodentia | VOLUME ia Fic. 7.—Surface graph of proportions of the total number of articles devoted primarily to each of several orders of mammals (and to more than one order of mammals) published in alternate volumes from volumes I-71 of the Journal of Mammalogy: a, feature articles; b, general notes. 150 VERTS AND BIRNEY continues to fill the role and scope that the founders of the American Society of Mam- malogists envisioned for it. The diversity of subjects and orders of mammals treated, and the diversity in length and depth of treat- ments remains its greatest strength. Likely, this strength is one of the major binding forces of the American Society of Mam- malogists. Mammalian Species Mammalian Species is the most recently established serial publication of the Amer- ican Society of Mammalogists. The objec- tive of Mammalian Species “is to provide a critically compiled, accurate, and concise summary of the present state of our biolog- ical knowledge (and ignorance) of a species of mammal in a standard format...” (In- structions for contributors to Mammalian Species, 1987). Each account includes a complete synonymy and sections in which context and content, diagnosis, distribu- tion, general characters, fossil record, form and function, ontogeny and reproduction, ecology, behavior, and genetics are consid- ered. A remarks section, commonly con- taining an explanation of complex nomen- clature, and an extensive literature cited section completes each account. One ac- count in each genus must contain a generic synonymy and context and content sec- tions. Most accounts contain a photograph or artist’s depiction of a representative of the species, photographs or line drawings of dorsal, ventral, and lateral views of the skull, and a map depicting the geographic distri- bution of the species. Some accounts con- tain photographs or line drawings of certain diagnostic features such as the baculum, phallus, specific teeth or parts of toothrows, and karyotype. The intention was to limit the length of accounts to 8 pages (printed double-column), but several accounts, es- pecially those on well-researched species, exceed that length. The concept of Mammalian Species was presented to the Board of Directors at the 1968 meeting (Journal of Mammalogy, 49: 844, 1968) and was approved by the board at the 1969 meeting as a publication “‘to be sold by subscription” (Journal of Mam- malogy, 50:908, 1969). At the latter meet- ing, the board budgeted $2,000 for initial publication of the series. An announcement in the same issue of the Journal (p. 913) indicated that the first account (on Macrotus waterhousil) would be mailed to all mem- bers with a price list and subscription form. The following year an announcement (Jour- nal of Mammalogy, 51:842, 1970) indicated that the cost of a subscription to Mam- malian Species would be $9.60 to members and $12.00 to nonmembers; the first fascicle of six accounts was published 16 June 1971. Although timing of publication and number of accounts per fascicle were variable during the first 10-12 years, during recent years, two fascicles consisting of 8-20 accounts each were published annually. The present cost of subscriptions for members and non- members is $10 per year; individual ac- counts may be purchased (accounts in same order: $2 each for five or fewer, $1.50 each for six—10, and $1 each for = 11) and special packages of accounts (grouped by region, taxa, or other classification) are available at 25% discount. Initially, authors for Mammalian Species accounts were solicited from among those especially knowledgeable of a taxon, but, more recently, prospective authors have re- quested assignment of exclusive privileges to produce accounts on specific species. Currently, assignments are made by the managing editor for a period of 3 years with authors retaining the option of requesting an extension of | year to complete accounts in progress. On the matter of timely com- pletion of assignments, editors have been flexible, to a point. As of 23 April 1993, 443 accounts in- cluding 452 species had been published (nine accounts each covered two closely related species). Through the first 443 accounts, numbers of accounts by order of mammal was strongly correlated (7? = 95.04, n = 20) PUBLICATIONS ies with numbers of species classified by order (Anderson and Jones, 1984:5-8). Orders that deviate most within this relationship are Primates with accounts published for only 3 (1.7%) of 180 species and Carnivora and Artiodactyla for which accounts have been published for 54 (20.1%) of 269 species and 27 (14.6%) of 185 species, respectively. As 215 (48.5%) of the 443 published accounts are on North American mammals north of Mexico (comprising 50.6% of the species native to the region—Jones et al., 1992), the series is particularly valuable for North American researchers. Not only was Mammalian Species the brainchild of Sydney Anderson, but he sought and obtained approval for the new publication, demonstrated the concept by writing the first account, and nurtured the publication by serving in an editorial capac- ity for 312 of the accounts published. During the first year of publication he even sold the subscriptions to Mammalian Species. Others who served Mammalian Species in a regular editorial capacity for the first 443 accounts were D. F. Williams, T. E. Lawlor, B. J. Verts, J. K. Jones, Jr., A. L. Gardner, C. J. Phillips, T. L. Best, K. F. Koopman, G. N. Cameron, C. S. Hood, J. A. Lackey, and D. E. Wilson. Several others served as guest editors of single accounts when authorship constituted a potential conflict of interest. Monographs and Special Publications Three Monographs of the American So- ciety of Mammalogists were published, one each in 1926, 1927, and 1928. These were: number |, Anatomy of the Wood Rat by A. Brazier Howell; number 2, The Beaver by Edward R. Warren; and number 3, Animal Life of the Carlsbad Cavern by Vernon Bai- ley. Hartley H. T. Jackson served as editor for all three, but was assisted by Edward A. Preble, Ethel M. Johnson, and Emma M. Charters on the last volume. All volumes were published by the Williams and Wilkins Company, Baltimore, Maryland. Number | was priced at $5.00, numbers 2 and 3 at $3.00 each; members of the American So- ciety of Mammalogists were afforded an 8% discount. Anatomy of the wood rat consists of nine chapters in 225 pages that include 4 tables, 37 line drawings (seven overprinted with red and blue), 3 plates (photographs), a 3-page bibliography, and a 5-page index. The beaver consists of an introduction, ac- knowledgments, and 13 chapters in 177 pages that include 78 illustrations (70 pho- tographs), a 5-page bibliography, and a 3-page index. Animal life of the Carlsbad Cavern consists of eight chapters in 195 pages that include 67 figures (62 photo- graphs, 2 maps, and 3 drawings by L. A. Fuertes), and a 9-page index; no bibliogra- phy was included. In addition to chapters on mammals, the volume contained chap- ters on birds, reptiles, and invertebrates. Strangely, minutes of the meetings of the Board of Directors or of the members at large published in the Journal of Mam- malogy in the years before publication of the monographs contain no mention of of- ficial sanction or other involvement of the society. However, the minutes of the eighth annual meeting contain a statement an- nouncing the forthcoming publication of the first monograph (Journal of Mammalogy, 7:241, 1926). Advertisements of the avail- ability of the monographs appeared on the inside of the back cover of the Journal of Mammalogy for several years. The minutes of the meeting of the Board of Directors at the 44th annual meeting held at Ciudad Universitaria, Mexico City, D.F., Mexico, include the statement, “‘The reviv- al of a monograph series was approved” (Journal of Mammalogy, 45:668, 1964). However, no mention was made in those minutes or those of subsequent meetings regarding the decision not to continue the monographs series per se, but to initiate an entirely new series. According to J. K. Jones, Jr. (pers. comm., 8 August 1990), a member {52 VERTS AND BIRNEY of the committee involved in reestablishing a monograph series, the 25-year period be- tween publication of the third monograph and consideration of reestablishment of the series, and the desire to change the focus of the monograph series, were paramount in the decision. At a special meeting of the Directors at the 45th annual meeting, “A maximum of $8,000 was authorized for the publication of an acceptable manuscript for the first Special Publication of the Society” (Journal of Mammalogy, 46:731, 1965). The first Special Publication, The natural history and behavior of the California sea lion, by Richard S. Peterson and George A. Bartholomew, was published 5 December 1967. On page 11 of this number the series was described as follows: “This series, pub- lished by the American Society of Mam- malogists, has been established for papers of monographic scope concerned with some aspect of the biology of mammals.”’ William H. Burt was editor of the initial number, and J. Knox Jones, Jr., James N. Layne, and M. Raymond Lee were listed as additional members of the Committee on Special Pub- lications. The original price of the 91-page clothbound book was $3.50. Eleven numbers in this series have ap- peared, the most recent being the present volume in 1994. Published numbers, au- thors or editors, and dates of publication of Special Publications, in addition to the first, are as follows: number 2, Biology of Pero- myscus (Rodentia), edited by John A. King, 20 December 1968; number 3, The life his- tory and ecology of the gray whale (Eschrich- tius robustus), by Dale W. Rice and Allen A. Wolman, 30 April 1971; number 4, Pop- ulation ecology of the little brown bat, My- otis lucifugus, in Indiana and north-central Kentucky, by Stephen R. Humphrey and James B. Cope, 30 January 1976; number 5, Ecology and behavior of the manatee (Tri- chechus manatus) in Florida, by Daniel S. Hartman, 27 June 1979; number 6, Loco- motor morphology of the vampire bat, Des- modus rotundus, by J. Scott Altenbach, 22 August 1979; number 7, Advances in the study of mammalian behavior, edited by John F. Eisenberg and Devra G. Kleiman, 11 March 1983; number 8, Biology of New World Microtus, edited by Robert H. Tam- arin, 12 September 1985; number 9, Dis- persal in rodents: a resident fitness hypoth- esis, by Paul K. Anderson, 30 March 1989; number 10, Biology of the Heteromyidae, edited by Hugh H. Genoways and James H. Brown, 20 August 1993; and number 11, Seventy-five years of mammalogy (1919- 1994) edited by Elmer C. Birney and Jerry R. Choate, 1994. Although all monographic in scope, these 11 Special Publications can be categorized by scientific content and organization. Numbers 1, 3, 4, 5, and 6 each concentrate on one mammalian species, contain 79-153 (Y = 118) numbered pages, and typically concern natural history and related topics. Of these, number 6 focuses exclusively on locomotor morphology, thus is the most specialized in terms of topics covered. Numbers 2, 7, 8, and 10 (which has a dou- ble-column format) contain 593-893 (X = 740) numbered pages and consist of several (14-22) contributed manuscripts on a topic selected by an organizing editor. Numbers 2 and 8 focus on a particular genus of mam- mals and number 10 pertains to a family of mammals, whereas number 7 covers a gen- eral topic (animal behavior). Number 9 fits neither of these categories, thus is unique within the series in that it presents and ad- vocates a new hypothesis (on dispersal in rodents) and compares and contrasts it with competing hypotheses. Number 11 also is unique, reviewing 75 years of mammalogy, as influenced by the ASM. Several members of the American Society of Mammalogists have served as editor or managing editor of the books in the Special Publications series. In addition to editing the first number, William H. Burt also ed- ited number 2. Beginning with number 3, each number had both an editor and a man- aging editor; the former was responsible for PUBLICATIONS 153 selection, content, and quality control, the latter for matters related to production. James N. Layne served as editor and J. Knox Jones, Jr. as managing editor for numbers 3-6; Hugh H. Genoways (editor) and Tim- othy E. Lawlor (managing editor) edited numbers 7 and 8; and Elmer C. Birney and Carleton J. Phillips served in these two ca- pacities, respectively, for number 9. Addi- tionally, Jerry R. Choate served as editor and Don E. Wilson as managing editor for a brief period, and Michael A. Mares (edi- tor) Craig S. Hood (managing editor) edited volume number 10. Mares (editor) and Jo- seph F. Merritt (managing editor) were re- sponsible for number 11. Cumulative Indices and Miscellaneous Publications Four cumulative indices to the Journal of Mammalogy have been published to date, and a fifth is scheduled for publication. The first was a 20-year index to volumes 1-20 (1919-1939) edited by Viola S. Schantz and Emma M. Charters; it consists of 219 pages and sold for $2.50 in paperback, $3.50 clothbound, when published on | August 1945. Each of the next three published in- dices covered a 10-year span: volumes 21- 30 (1940-1949), 31-40 (1950-1959), and 41-50 (1960-1969). The second index also was edited by Schantz and Charters, the third by Schantz and a committee of four others, and the fourth was prepared by James S. Findley and six additional members of the Index Committee. The fifth index is to cov- er a 20-year period (volumes 51-70) and is being prepared by Michael Carleton and the four or five other members of the 1983- 1990 Index Committees. The cumulative index for the decade of the 1940s consists of 146 numbered pages, appeared on 27 Oc- tober 1952, and sold originally for $3.25 in paperback, $3.75 in clothbound. That for the 1950s has 150 pages, a publication date of 18 May 1961, and sold for $5.00 in cloth- bound only. The fourth cumulative index consists of 109 numbered pages, is dated only as 1974, and sold for $5.00 in cloth- bound only. Each of these indices contains a few (4-10) pages of introduction and ex- planation in addition to the numbered pages. Six indices to Mammalian Species have been published; these are to species ac- counts numbered 1-100, 1-200, 1-300, 1- 400, 101-200, and 201-306. Except for the indices to accounts numbered 1-300 and 1- 400, which lack author indices, each index contains systematic, generic, and author lists. These accounts were distributed to subscribers with fascicles containing appro- priately numbered accounts. In April 1981, the American Society of Mammalogists published a limited edition of a pamphlet titled “Career trends and graduate education in mammalogy,” by Gary W. Barrett and Guy N. Cameron. An announcement of the availability of publi- cation and a notice of publication of a quar- terly newsletter for graduate students ap- peared in the comments and news section of the Journal of Mammalogy (62:875, 1981). In June-July 1985, the American Society of Mammalogists cosponsored with the Australian Mammal Society publication of a special issue (volume 8, numbers 3 and 4) of Australian Mammalogy containing pa- pers presented at symposia at the 1984 joint meeting of the two societies in Sydney, New South Wales, Australia. Number 3 con- tained six papers from a symposium titled ‘““Niche spaces and small mammal com- munities’; number 4 contained papers from two symposia: “A” titled “Form-function analyses: the teeth and skulls of carnivores” with five papers, and “B”’ titled ‘Studies in the biology of bats’? with nine papers. Each of the three sections was edited by a different pair of editors: the first by Barry Fox and Roger A. Powell, the second by Roger A. Powell and Michael Archer, and the third by Leslie S. Hall and Suzanne J. Hand. Each section also included a preface in which one 154 VERTS AND BIRNEY of the editors summarized and synthesized material presented by the participants. Last- ly, an envelope attached inside the back cover contains a microfiche with appendices to a paper in the niche-space symposium and contains abstracts of other papers pre- sented at the joint meeting. The issue of Australian Mammalogy (volume 8, num- bers 3 and 4, 1985) was available from the secretary-treasurer of the American Society of Mammalogists for $10 for those attend- ing the joint meeting and $15 for others. For several years, the secretary-treasurer has published brochures that contain lists and descriptions of Special Publications and Mammalian Species accounts with appro- priate order forms. Another brochure titled “The science of mammalogy” includes a de- scription and a brief history of mammalogy in North America and of the American So- ciety of Mammalogists. Lastly, a brochure titled “Careers in mammalogy” contains brief descriptions of the types of work that mammalogists do and of career opportu- nities in mammalogy. The latter two bro- chures were produced by the Committee on Education and Graduate Students. All of the brochures are revised or updated from time to time. Acknowledgments Thanks are due L. N. Carraway and L. F. Al- exander for assistance with the analyses. This is Technical Paper No. 10,041, Oregon Agricul- tural Experiment Station. Literature Cited ANDERSON, S., AND J. K. JoNEs, JR. 1984. Introduc- tion. Pp. 1-10, in Orders and families of Recent mammals of the world (S. Anderson and J. K. Jones, Jr., eds.). John Wiley & Sons, New York, 686 pp. ANDERSON, S., AND R. G. VAN GELDER. 1970. The history and status of the literature of mammalogy. BioScience, 20:949-957. GmLL, A. E., AND W. C. WozENCRAFT. 1994. Com- mittees and annual meetings. Pp. 155-170, in Sev- enty-five years of mammalogy (1919-1994) (E. C. Birney and J. R. Choate, eds.). Special Publication, The American Society of Mammalogists, 11:1—433. Jones, J. K., JR., R. S. HOFFMANN, D. W. Rice, C. JONES, R. J. BAKER, AND M. D. ENGstTrRom. 1992. Revised checklist of North American mammals north of Mexico, 1991. Occasional Papers, The Museum, Texas Tech University, 146:1-23. KIRKLAND, G. L., JR., AND H. D. SMitH. 1994. Mem- bership and finance. Pp. 170-178, in Seventy-five years of mammalogy (1919-1994) (E. C. Birney and J. R. Choate, eds.). Special Publication, The Amer- ican Society of Mammalogists, 1 1:1—433. COMMITTEES AND ANNUAL MEETINGS AYESHA E. GILL AND W. CHRIS WOZENCRAFT Introduction he first meeting of the ASM was held 3-4 April 1919 in Washington, D.C., 2 years after the end of World War I. This was the year that Prohibition, the 18th Amendment to the United States Consti- tution, was ratified and that the great Mex- ican leader, Emiliano Zapata, was killed. This organizational meeting was attended by 60 members of a charter membership of over 250. After discussion and approval of by-laws and a constitution, six officers and 10 councilors (now called the Board of Di- rectors) were elected. An editor was selected for the society’s Journal of Mammalogy that was to start publication that year. Five standing committees were formed: Publi- cations, Life Histories of Mammals, Study of Game Mammals, Anatomy and Phylog- eny, and Bibliography. The policy of the society set forth at its organizational meet- ing was “to devote its attention to the study of mammals in a broad way, including life histories, habits, evolution, palaeontology, relations to plants and animals, anatomy, and other phases.’ The annual dues were $3 (Kirkland and Smith, 1994). ASM currently (1993) has nearly 4,000 members residing in 60 countries. The so- ciety has held a general membership meet- ing every year since 1919 except for 2 years i ers) Publications Life Histories Study of Gane Pamrals Anatorsy and Phylogeny Bibliography during World War IT (1943 and 1944), when only the directors met. General member- ship meetings have been held in Washing- ton, D.C., Canada, Mexico, and 30 states of the U.S. ASM has had 38 presidents be- tween 1919 and 1993 (Layne and Hoff- mann, 1994). During this period, 74 vol- umes of the Journal of Mammalogy, 10 Special Publications and close to 450 Mam- malian Species accounts have been pub- lished (Verts and Birney, 1994). New stand- ing and ad hoc committees were formed and old ones phased out; the current number of standing committees is 23. Hartley H. T. Jackson, a young staff member of the U.S. Biological Survey, played a prominent role in planning for the establishment of the ASM (ASM 50th An- niversary Program, 1969; Hoffmeister, 1969; Hoffmeister and Sterling, 1994). History of the Committees of ASM Many members have served the ASM by actively participating in the work of the so- ciety’s committees and thus have contrib- uted to its development and vigor. Standing committees have functioned since the in- ception of ASM to promote the goals of the 156 GILL AND WOZENCRAFT society through ongoing activities between annual meetings. These committees and their chairpersons are appointed by the president. The committees have a two-fold purpose—to conduct affairs of the society and to accord members the responsibilities and rewards of active participation in it. An ad hoc committee was appointed in 1982 under the presidency of J. Mary Taylor to evaluate the standing committees and ex- plore all facets of their roles in the society. Past and present members of standing com- mittees and other members of the society were contacted with questions pertaining to the committees. Through their responses, the ad hoc committee compiled detailed re- ports on standing committees, including their history, function, effectiveness, and recommendations of committee members on the continued need and role of each com- mittee. These reports are sent to members of the committees so that they can have a better understanding of the committee’s purpose and how to serve on it effectively. Shorter descriptions of the functions of the current standing committees were first pub- lished as a supplement to Vol. 68, No. 1 (1987) of the Journal of Mammalogy (‘Roles of Standing Committees of the American Society of Mammalogists’’). We have up- dated the list of Standing Committees of the ASM from its inception to extend it to the present (1993) (Table 1). In addition to the 40 standing committees formed during the society’s history, ad hoc committees have been established frequently to perform spe- cific tasks. They cease to exist when their charge is completed. Often, however, a standing committee develops from an ad hoc committee, if a more lasting need for its function is perceived by the Board of Directors. Current standing committees and their members are listed on the inside of the back cover of each issue of the Journal. The standing committees created during the history of ASM can be divided into cat- egories concerned with the promotion of mammalogy, the development of the soci- ety itself, or the interactions of ASM with non-mammalogists. Committees have dealt with publications and particular topics in mammalogy (such as physiology and anat- omy, ecology, and conservation); some have dealt with taxonomy in general and others with specific taxa. Committees have been created to encourage young mammalogists and to build the society, to honor and re- ward its outstanding members and other mammalogists, and to record its history. Committees exist to promote the interac- tion of the society’s members with other mammalogists and to present the society’s views on critical national and international issues affecting mammalogy. Brief descrip- tions of the committees involved in each of these areas of activity follow. Promotion of mammalogy. —The original Publications Committee formed in 1919 evolved in 1930 into the Editorial Com- mittee, which remains active. It oversees production of the Journal of Mammalogy, Mammalian Species, Special Publications, and miscellaneous publications such as membership lists. It sets editorial policy for the ASM, nominates new editors for ap- proval by the Board of Directors, and man- ages the publication budget. The committee is composed almost entirely of current ed- itors, who can be divided into two groups: those involved in the review process and judging the scientific merit of papers and those involved in the technical production of the publications. As the Journal of Mam- malogy grew over the years, the need de- veloped for a committee to prepare the in- dex for each volume. The Index of Journal of Mammalogy Committee was formed in 1947, chaired by Viola S. Schantz, who also served the society for 23 years (1930 to 1952) as Treasurer. The name of this committee was abbreviated to Index Committee in 1972. Besides preparing the index for each volume of the Journal, it prepares summary indices. The Bibliography Committee, which existed for 67 years, compiled the list of Recent Literature in Mammalogy for many years before it ceased to exist. This information is now available through other TABLE |.— Standing committees of the ASM from its inception in 1919 to 1993. Year formed ASM President 1919 C. H. Merriam 1920 C. H. Merriam 1921 E. W. Nelson 1922 E. W. Nelson 1927 G. M. Allen 1928 G. M. Allen 1930 W. Stone 1945 R. Hall 1947 R. Kellogg 1950 T. I. Storer 1953 W. H. Burt 1956 W. B. Davis COMMITTEES AND MEETINGS Committee Publications Life Histories of Mammals Study of Game Mam- mals Anatomy and Phylog- eny Bibliography Conservation Marine Mammals Economic Mammal- ogy J. A. Allen Memorial Life Histories and Ecology Conservation of Land Mammals Nomenclature Editorial Membership Special Committee on Trapping Methods Ecology (including life histories and popu- lations) Economic Mammalo- gy and Conserva- tion Index of Journal of Mammalogy Means for Encourag- ing Young Mam- malogists Dues Status of Re- tired Members Honoraria for Gradu- ate Students Resolutions Original chairperson/members G. S. Miller, Jr./E. A. Preble, W. P. Tay- lor, H. H. T. Jackson C. C. Adams/R. M. Anderson, V. Bailey, H. C. Bryant C. Sheldon/G. B. Grinnell W. K. Gregory/J. C. Merriam, H. H. Don- aldson, A. Wetmore, H. von W. Schulte, J. W. Gidley T. S. Palmer/W. H. Osgood, H. H. T. Jackson W. H. Osgood/E. W. Nelson, J. Dwight E. W. Nelson/G. S. Miller, Jr., T. S. Palm- er, B. W. Evermann, R. C. Murphy, G. M. Allen A. K. Fisher/W. B. Bell, H. C. Bryant M. Grant/H. F. Osborn, C. Frick, G. B. Grinnell, H. E. Anthony W. P. Taylor/C. S. Adams, V. Bailey E. A. Preble/J. C. Phillips, T. S. Palmer W. H. Osgood/G. M. Allen, A. H. Howell, G. S. Miller, Jr., T. S. Palmer E. A. Preble/G. M. Allen, A. H. Howell, R. Kellogg, G. S. Miller, Jr., G. B. Wis- locki W. P. Harris, Jr./T. Gregory, V. Bailey, R. M. Anderson, M. R. Thorpe, J. Dix- on, W. P. Taylor W.E. Sanderson/C. C. Adams, E. A. Preb- le, W. A. Young D. L. Allen/F. S. Barkalow, Jr., C. D. H. Clarke, W. J. Hamilton, Jr., J. M. Lins- dale E. R. Kalmbach/D. L. Allen, R. M. An- derson, A. E. Borell, H. J. Coolidge, T. I. Storer, C. T. Vorhies V. S. Schantz/H. H. T. Jackson, D. H. Johnson, R. Kellogg D. E. Davis/F. S. Barlow, Jr., P. D. Dalke A. R. Shadle/J. K. Doutt, R. I. Peterson W. R. Eadie/F. S. Barkalow, Jr., S. D. Durrant, R. T. Orr K. R. Kelson/E. T. Hooper, W. V. Mayer, S. D. Durrant, G. C. Rinker 157 Year ended 1930 LOD, 1922 1948 1985 1922 active 1953 1929 1947 active active active active 1947 1948 1948 1972 1951 1951 active active 158 GILL AND WOZENCRAFT TABLE 1.— Continued. Year formed Year ASM President Committee Original chairperson/members ended 1957 Honorary W. H. Burt/E. R. Hall, W. J. Hamilton, active W. B. Davis Membership Jr. 1960 International A. De Vos/W. O. Pruitt, Jr., H. M. Van active S. D. Durrant Relations Deusen 1962 Anatomy and L. C. Dearden/K. L. Duke, M. Hilde- 1983 E. T. Hooper Physiology brand, P. H. Kurtzsch, P. R. Morrison, W. B. Quay 1966 Historian D. F. Hoffmeister 1986 R. G. Van Gelder 1971 Grants In Aid J.S. Findley/R. Horst, H.M. Van Duesen, active J. N. Layne J. L. Wolfe 1971 Program B. E. Horner/L. N. Brown, O. P. Pearson, active J. N. Layne M. H. Smith, H. M. Van Duesen 1972 Information S. Anderson/L. de la Torre, H. H. Gen- active J. K. Jones, Jr. Retrieval oways, R. S. Hoffmann, C. Jones, D. R. Patten, J. L. Patton, H. W. Setzer Index D. E. Wilson/R. D. Fisher, C. Jones, J. L. active Paradiso, R. H. Pine, H. W. Setzer, R. W. Thorington, Jr. Systematic J. R. Choate/J. H. Brown, E. T. Hooper, active Collections M. L. Johnson, C. Jones, J. L. Patton, T. A. Vaughan 1974 Merriam Award J. K. Jones, Jr./C. C. Black, W. H. Burt, active S. Anderson J. F. Eisenberg, M. E. Hight, T. A. Vaughan, J. Whittaker 1976 Legislation and Regu- H.H.Genoways/M.M. Alexander,S.An- active W. Z. Lidicker, Jr. lations derson, M. A. Bogan, J. R. Choate, R. C. Dowler, C. A. Hill, A. M. Johnson, C. Jones, T. J. McIntyre, J. L. Paradiso, R. L. Peterson 1977 Jackson Award R. L. Peterson/W. H. Burt, J. S. Findley, active W. Z. Lidicker, Jr. D. F. Hoffmeister, C. Jones Mammal Slide J. A. Lackey/P. V. August, S. J. Bleiweiss, active Library P. L. Dalby, D. C. Gordon, H. L. Gun- derson, J. G. Hall, G. C. Hickman, L. L. Master, J. S. McCusker, G. L. Tweist 1978 Education and Grad- G. W. Barrett/A. E. Baker, G. N. Cam- active R. S. Hoffmann uate Students eron, A. F. DeBlase, S. R. Humphrey, K. A. Shump, Jr. 1982 Checklist K. Koopman/J. H. Calaby, F. Dieterlen, active J. M. Taylor R. S. Hoffmann, J. H. Honacki, J. G. Mead, G. G. Musser, P. Myers, R. W. Thorington, Jr. 1986 Archives D. F. Hoffmeister, Historian; W.C. Woz- active D. E. Wilson encraft, Archivist 1989 Development S. R. Humphrey/S. Anderson, J. R. active E. C. Birney Choate, H. H. Genoways, W. Z. Lidick- er, Jr., R. L. Peterson, D. J. Schmidly, J. M. Taylor, R. G. Van Gelder, M. R. Willig, D. E. Wilson COMMITTEES AND MEETINGS 159 TABLE |.— Continued. Year formed ASM President Committee 1990 Animal Care E. C. Birney and Use Year Original chairperson/members ended T. H. Kunz/R. J. Baker, T. Carter, J. R. active Choate, J. A. Cranford, G. Glass, I. F. Greenbaum, L. R. Heaney, G. R. Mich- ener, T. H. McIntyre, D. K. Odell, R. S. Ostfeld, A. Pinter, V. Scheffer, S. D. Thompson, R. A. Van Den Bussche Source: Journal of Mammalogy, Volumes 1-73, Supplement to Vol. 68, No. 1 (1987). Summary: In 1993, 23 active ASM committees, 17 extinct. See Layne and Hoffmann (1994) for additional information on presidents. means, such as computerized literature searches. The Mammal Slide Library Committee was established in 1977 to provide low-cost slides of mammals, often in natural habi- tats, principally for educational purposes. It now also stresses use of its slides for world- wide conservation efforts. The committee solicits, selects, and catalogs slides, and ad- vertises their availability to potential users world-wide. By 1993 over 1,000 different slides depicting 756 species in 19 orders were available. Over 100,000 duplicate slides were sold between 1978 and 1993. Many of the ASM committees that dealt with specific topics in mammalogy no lon- ger exist. These include the Life Histories of Mammals Committee (1919-1927), which evolved into the Life Histories and Ecology Committee (1927-1947) and final- ly into the Ecology Committee (including life histories and populations) (1947-1948). One committee focused on morphology, the Anatomy and Phylogeny Committee (1919- 1948), and again in 1962-1983 (Anatomy and Physiology) but, although lasting for much of the society’s history, is no longer in existence. One special topics committee has proved remarkably resilient. The Ma- rine Mammals Committee, established in 1921 when the society was just 2 years old, is still functioning. It provides the society membership with information about ma- rine mammalogy, including conservation and legislative issues, spearheads resolu- tions and legislation involving marine mammals, and serves as a liaison between ASM and the Society for Marine Mam- malogy (SMM). Committee members fre- quently are active in both ASM and SMM. The committee is particularly active on leg- islative issues regarding marine mammals. Several of the society’s committees have been concerned with economic mammalogy and conservation, of which one still exists. The earliest of these committees, the Study of Game Mammals, was initiated in 1919 and lasted only 4 years; the Conservation Committee (1920-1922) also was short- lived. The successor to these committees, however, lasted much longer. The Com- mittee on Economic Mammalogy lasted 33 years (1921-1953). The Committee on Eco- nomic Mammalogy and Conservation had a brief life (1947-1948), but the Committee on Conservation of Land Mammals, estab- lished in 1927, is one of the oldest active committees of the society. It monitors state, national, and international governmental activities and other activities that relate to conservation of land mammals, and it ad- vises officers and members of the society on issues of concern. The committee responds to these issues via formal resolutions to the membership, letters to responsible individ- uals or agencies, and other appropriate means. It serves as a clearinghouse for in- formation, leads or facilitates collective or individual responses to conservation issues, and, in a related function, establishes and 160 GILL AND WOZENCRAFT maintains liaison with other conservation groups. Conservation always has been a concern of the society and, today, with the increasing loss of genetic variability in the world, remains a major concern. The society has four active committees concerned with taxonomy and systematic collections. The earliest, the Nomencla- ture Committee, was formed in 1928 to give advice to members of ASM on prob- lems pertaining to nomenclature and to answer any taxonomic questions that members might pose. About 1977 the committee also assumed an advisory re- lationship with the International Com- mission of Zoological Nomenclature. It screens applications involving North Amer- ican mammals to ascertain whether the facts as presented are both correct and complete and provides an opinion on what the general effect of the requested ruling will be on tax- onomic and nomenclatural practice. The Systematic Collections and the In- formation Retrieval Committees both were formed in 1972. The former was an out- growth of an ad hoc committee established at the request of the National Science Foun- dation to evaluate mammal collections for support by the NSF Biological Research Re- sources Program. The original charge in- cluded advising the society on matters per- taining to systematics and systematic collections and reviewing criteria for ap- praising collections. It also reviewed pro- posals submitted to granting agencies for monetary support of systematic collections. The present role of the committee focuses on the general objective of promoting prop- er maintenance of systematic collections. The committee has established minimal standards for proper maintenance of collec- tions, and it serves, on behalf of the society, as an informal inspecting and accrediting agency for the curatorial status of collec- tions. It also is responsible for surveys of collections of Recent mammals published periodically in the Journal of Mammalogy. The birth of the Information Retrieval Committee is indicative of the revolution that has occurred in information-retrieval systems and computers. Its original charge was to examine the feasibility of developing a national data-retrieval system for Recent mammal collections and, if possible, to de- velop funding for such a system. The com- mittee’s activities have involved develop- ing standardized documentation and retrieval methods, producing a publication on automatic data processing, and provid- ing information on computerization of mammal collection data. The evolving interests of the committee include, but expand beyond, collection-based informa- tion to bibliographic data and other natural- history data bases in mammalogy. The Checklist Committee was estab- lished in 1980 to provide advice on Mam- mal Species of the World, edited by J. H. Honacki et al. (1982) and published by Al- len Press and the Association for System- atics Collections. The first edition was pre- pared by 189 professional mammalogists from 23 countries and was coordinated by the Checklist Committee, with R. S. Hoff- mann as the Project Coordinator. During the last 10 years it has become the inter- national standard for mammalian taxono- my. The dynamics of mammalian taxono- my demand periodic updates of this vast amount of information. ASM and the Checklist Committee assumed responsibil- ity for the maintenance of this data base and its periodic revisions. The committee serves as both scientific consultant to editors and final arbitrator of nomenclatural, or other, decisions on content. The material has been transferred from a text-based manuscript to an information retrieval data base to facil- itate future updates and to enhance the abil- ity of the user to interactively access this information. The second edition of Mam- mal Species of the World (Wilson and Reed- er, 1993) was published in cooperation with the Smithsonian Institution Press. Development of the society. —The society has established five committees to encour- age young mammalogists, and four of these are still extant. The Committee on Hono- COMMITTEES AND MEETINGS 161 raria (originally Honoraria for Graduate Students), formed in 1953, selects graduate students to be honored for their research in mammalogy. At present, three awards are given: the Anna M. Jackson, the A. Brazier Howell, and the American Society of Mam- malogists awards. Recipients are awarded an honorarium to attend the annual meet- ing, where they present results of their re- search at a plenary session. The Grants- in-Aid Committee was created in 1971 to solicit applications and select recipients for grants-in-aid of research and a nominee for the Albert R. and Alma Shadle Fellowship in Mammalogy. The grants are presently given to 11 students, with a monetary limit of $1,000 per student. The highest ranking student is honored with the B. Elizabeth Horner Award and gets a bonus of $100. The Shadle Fellowship, usually about $3,000, is awarded annually by the Buffalo Foundation and is intended to promote a professional career for a mammalogy stu- dent showing great promise. The ASM Grants-in-Aid Committee nominates the student and an alternate. Nominees for this award do not have to be members of the ASM but must be citizens of the United States. The recipient of the Shadle Fellow- ship is invited to speak on his or her re- search at an annual ASM meeting. The Committee on Education and Grad- uate Students was formed in 1978, with the purpose of assisting students of mammal- ogy to make more informed choices of ca- reer, to improve their scientific expertise, and to find employment in the discipline. These aims are achieved through prepara- tion of brochures and reports and through sponsoring of workshops related to educa- tion of mammalogists, career opportunities, research support, and other topics of inter- est to students. The Development Com- mittee began as an ad hoc committee in 1989. It has raised monies for the Future Mammalogists Fund, established by R. L. Peterson in 1985, through a variety of means, including contributions to patron membership ($1,000), the Seventy-five Year Club ($75), and other individual contribu- tions. The initial goal of raising $100,000 for the Fund was achieved in 1991. In 1993, at the recommendation of this committee, the Board of Directors initiated a major pro- gram of planned giving, including living trusts, pooled income funds, and wills and bequests. The Membership Committee and the Program Committee are instrumental in maintaining the society. The Membership Committee was established in 1930 to en- courage persons with an interest in mam- mals to become members of the society. In recent years an emphasis has been placed on making new members feel ‘‘at home” in the society and encouraging retention of members through writing welcoming letters to new members, pursuing any problems in the mailing of journals, and writing to 2-year delinquents to determine their reasons for dropping membership. In 1990-1991 the committee wrote to non-member authors who submitted manuscripts to the Journal (171 persons), inviting them to join the so- ciety; 14% of them did, accounting for 6% of the new members at that time. The Program Committee was established in 1971 in response to the need for a more effective method of selecting sites for and improving the organization of the annual meeting. It promotes the annual meeting and assists in its organization and conduct. This committee selects the basic format of the meeting, solicits, reviews, and selects symposia and workshops, and develops guidelines to increase the effectiveness of presentation of papers and posters. It also explores possibilities for special meetings, such as joint meetings with other mammal societies, and participates in planning the content and format of such meetings. It ad- vises local committees and provides liaison between successive local committees. The Program Committee constantly re-evalu- ates the organization of annual meetings, based on the accumulated experiences of local host committees. The society takes pride in honoring in- 162 GILL AND WOZENCRAFT dividuals who have made outstanding con- tributions to mammalogy and has set up a number of committees to evaluate and se- lect these outstanding mammalogists. The Honorary Membership Committee was formed in 1957 to recommend candi- dates for honorary membership in ASM in recognition of distinguished service to the science of mammalogy, but honorary mem- bers have been chosen since the first meet- ing of the society, when Joel A. Allen was selected (Hoffmeister, 1969). The commit- tee is comprised of the five most recent past presidents with the chair held for a 2-year period by the second-most senior member. The C. Hart Merriam Award was estab- lished in 1974 to provide recognition for outstanding contributions to mammalogy by a member of the society. It was named in honor of one of the foremost early North American mammalogists, who also was first president of the society. The award is now given in recognition of excellent scientific research and either education of mammal- ogists or service to mammalogy (Anony- mous, 1992). Nominations for the Merriam Award are open to all mammalogists, re- gardless of country or membership in ASM. The Jackson Award Committee was estab- lished in 1977 to provide recognition of per- sons who have rendered long and outstand- ing service to the society. The committee evaluates nominations received and, based on supporting documentation, makes its recommendation of a recipient to the Board of Directors. These awards need not be made each year, as they are reserved for truly wor- thy candidates. The position of Historian was created in 1966 when it was realized that important historical material of value to the society was not being preserved. Donald F. Hoff- meister has served as the society’s historian since the inception of this committee. The material originally was preserved in the Mu- seum of Natural History, University of II- linois, but in 1986 the decision was made to move all materials to the care of the Ar- chives of the Smithsonian Institution. At that time the Archives Committee was formed, consisting of Hoffmeister, who con- tinued as Historian, and W. Chris Wozen- craft as Archivist. The archives include in- formation on annual meetings; minutes of board meetings and business meetings; pho- tographs of past presidents, honorary mem- bers, and some other award recipients; an official set of the Journal of Mammalogy and other society publications; and a variety of miscellaneous materials, including cor- respondence of many past presidents. Interactions of ASM with the broader so- ciety. — Throughout its history, ASM has as- sumed a responsible role in expressing its views on issues relating to mammals and mammalogists, partly by means of resolu- tions passed by the membership of ASM. A Resolutions Committee was established in 1956 primarily to avoid the problem of hastily submitted and poorly drafted last- minute resolutions on subject matter of di- rect concern to the society. The purpose of this committee is to provide a mechanism for the society to express its views and to try, collectively, to influence local, national, and world issues relating to mammals. These views are expressed in the form of resolu- tions proposed by ASM committees or members, or, sometimes, initiated by the Resolutions Committee itself, which re- views proposed resolutions with the pro- posers and other knowledgeable persons to ensure their accuracy and appropriateness. The committee decides through which agencies or channels to send resolutions that have been approved by a majority vote of the membership. Reports of this committee are available in the abridged minutes of ASM meetings in issue number 4 of each volume of the Journal of Mammalogy. A partial listing of resolutions passed by ASM is available from the archivist. Con- servation issues have been and remain an overriding concern of ASM and this is re- flected in its resolutions. Conservation and protection of large mammals especially, such as cetaceans, carnivores, and artiodactyls, have been the subject of many resolutions. COMMITTEES AND MEETINGS 163 The society consistently has urged the pro- tection of national parks, threatened habi- tats, and endangered species and popula- tions, including recent resolutions on the conservation of biological diversity and support for the National Institute for the Environment. It has opposed the use of in- humane methods of predator control and those that poison the environment. The so- ciety has advocated forcefully the humane treatment of mammals in the wild and in captivity, with resolutions ranging from op- position to den hunting to destroy wolves in Minnesota and Wisconsin to support for humane and professional maintenance of mammals in captivity. An ad hoc commit- tee on Animal Care and Welfare updated acceptable field methods and proper labo- ratory care in the collection and use of wild mammals in research and teaching. This committee became the standing committee on Animal Care and Use in 1992. The so- ciety has taken a stand against scientific cre- ationism, supported biological surveys and studies of threatened populations and of the effects of animal introductions, and has hailed the establishment of new societies such as the Mexican Society of Mammal- ogists (1984) and the Society for Marine Mammalogy (1984). ASM also acts through its Legislation and Regulations Committee, established in 1976, to bring its expertise to bear on this area. The committee was established in re- sponse to the need for monitoring and pro- viding input into the rapidly burgeoning state and federal legislation and regulations in such areas as endangered species, steel- trapping regulations, and use of animals for experimental purposes of direct concern to mammalogy. The committee also interacts with the legislative monitoring group of AIBS. Members of the committee are fa- miliar with federal and state agencies and operations and they attend agency hearings when necessary. The International Relations Committee was formed in 1960 to maintain and en- hance communication between ASM and mammalogists outside North America. It is truly an international committee with many of its members living outside North Amer- ica. It maintains liaisons with counterpart societies Overseas, participates in the Inter- national Theriological Congresses (ITC), which it helped initiate, and organizes joint meetings with other societies. ITC has held meetings in Russia, Czechoslovakia, Fin- land, Canada, Italy, and Australia. Joint meetings have been held with mammal so- cieties in Australia, Argentina, and China. The International Relations Committee maintains names and addresses of mammal societies and mammalogists throughout the world. It facilitates exchange of material on mammalogy, encourages foreign colleagues to attend annual ASM meetings, and fosters good relations between mammalogists in- ternationally. Members outside North America provide a link for international ac- tivities and serve as representatives of ASM in their own countries. The History of ASM Annual Meetings Population dynamics. —The membership of the ASM quickly grew from its initial 252 members, breaking the 1,000 mark in 1930, but throughout the 1930s and most of the 1940s the number of members returned to a range between 800 and 900 (Hoffmeister, 1969). In 1948 the membership again ex- ceeded 1,000, passed 2,000 in 1963, and topped 3,000 in 1968; in recent years the membership figures have hovered around 3,700 (Secretary-Treasurer’s annual report, 1993). There presently are five categories of membership in ASM: annual (at $30 one of the best bargains in any professional soci- ety), life (currently $750), patron (currently $1,000), honorary, and emeritus. Emeritus membership was established in 1951 for persons who had regular membership in the society for 25 years or more, were in good standing, and requested such membership (Hoffmeister, 1969). In 1993, ASM had 636 164 GILL AND WOZENCRAFT Number of papers, ASM meetings (1920-1990) 240 60 0 1920 1930 1940 1950 1960 1970 1980 Fic. 1.—The number of papers and posters presented at ASM meetings, 1920-1990. life, 16 patron, 13 honorary, 147 emeritus, and 2,938 annual, for a total of 3,750 mem- bers. The number of papers and, more recently posters, presented by persons attending an- nual meetings has remained relatively con- stant over the years at 42-55% of the total number of registered participants. Although the general trend has been an increase in the number of papers presented, mirroring the increase in membership, this increase was gradual during the first four decades, in- creased more rapidly in the fifth decade, and increased dramatically in the mid-1970s (Fig. 1). There was a doubling of the number of papers in the first half of the 1970s, a high that was maintained from that time on, with active participation of graduate students be- coming a major factor in oral and, later, poster presentations and greatly affecting the atmosphere and emphasis of the meetings. The membership of ASM always has been skewed toward males. It is difficult to obtain a reliable estimate of the sex ratio of biol- ogists at annual meetings, so two approxi- mate methods were employed here. The number of females in annual meeting pho- tographs was counted, although this method has the bias of including some non-mem- bers. This was especially a factor for some of the earlier meetings, where non-members frequently appeared with their spouses for the photographs. This estimate was com- pared to the number of papers presented at annual meetings for which the first author was female (Fig. 2). Although women have increased significantly in a society that was essentially male (with active support from wives) at the beginning, in 1991 they still constituted only 20-30% of the member- ship and were first authors on about the same percentage of papers. This increase in the number of women has occurred prin- cipally since the early 1970s and largely as a result of an influx of female graduate stu- dents, corresponding to the dramatic in- crease in the number of graduate students, in general, participating in meetings. Only one of the 38 presidents of the ASM (through 1993) has been a woman, J. Mary Taylor, who was elected in 1982 (Layne and Hoff- mann, 1994). Four of the chairpersons of COMMITTEES AND MEETINGS 165 Estimation of Female biologists at ASM annual meetings | First Author 40 30 20 Percent 10 1920 1930 1940 1950 —— Group Photo 1960 1970 1980 Fic. 2.—Estimation of the number of female biologists at ASM annual meetings, based on the first author of papers presented (bar graph) and the group photo (line drawing). the 23 current standing committees of the society are women, lower than the percent- age of women in the society. An ad hoc committee on Women and Mi- nority Issues is currently functioning and it is hoped that its activities will facilitate greater involvement of women and minor- ities in leadership positions in the society in the future. Even more stark than the skewed sex ratio of ASM members is the obvious lack of visible minority members in ASM. We do not have figures on minority membership in ASM, but it is minimal as judged by those attending annual meetings, where the participants are predominantly white. Minority membership in ASM may reflect low numbers of minorities in mam- malogy in the U.S. This immediately sug- gests the urgency of outreach by ASM to attract minority students to the study of bi- ology. Geographic distribution. —Throughout its history, ASM has attracted mammalogists from all states of the U.S. as well as from Canada and Mexico. Nearly all states typ- ically are represented at each annual meet- ing. Representation of each state and Can- ada and Mexico was determined by noting the home region of the first author of each paper at annual meetings (Fig. 3, Table 2). Canadians have participated in notable numbers since the founding of the society. During its 70-year history, 10 states, listed in decreasing order, have accounted for half of the participants at annual meetings: Cal- ifornia, New York, Texas, Michigan, Dis- trict of Columbia, Kansas, Massachusetts, Illinois, Florida, and New Mexico. This re- flects the strong foundation of the society in mammalian systematics collections, as these 10 states also contain the 10 largest collections in North America. It was not until the 21st meeting in 1939 that an an- nual meeting was held at an institution not dominated by a large museum, and, during the first 5O meetings, more than two-thirds 166 GILL AND WOZENCRAFT ASM Annual Meetings Home state of First Authors No. First Authors CI] 4 to 46 FA 46 to 115 8 115 to 640 Fic. 3.— Map of the distribution in the U.S. of first authors of papers given at ASM annual meetings, 1920-1990. of the meetings were held in association with large systematics collections. Since the mid- 1960s this trend is less noticeable, with a gradual shift away from ““museum”’ insti- tutions to more general academic settings. When started, the society was principally an East Coast organization, with only one of the first 20 meetings held west of the Ap- palachians. By the third decade, states from the Far West and Midwest were having a much greater influence at society meetings. The states with the fewest representatives at annual meetings are Alabama, Arkansas, Delaware, Idaho, New Hampshire, Rhode Island, West Virginia, Nevada, Hawaii, and Maine. Meetings have been rotated throughout the United States for many years, with only two areas, the Northern Great Plains states (no meetings) and the southern U.S. (seven states have not hosted meetings) being under-represented. A map of the states that have hosted annual meetings closely resembles the map of the home state of first authors (Fig. 3), with the states heavily rep- resented there all having hosted meetings. Geographic rotation of the meetings con- tributes significantly to participation by graduate students, who may find it difficult to attend distant meetings. Topical and taxonomic emphasis of pa- pers at annual meetings. —The 51st annual meeting of the society at the University of British Columbia in 1971 established the format for annual meetings that has been used since: organized around topics, with a plenary session and concurrent sessions COMMITTEES AND MEETINGS 167 Topical emphasis of papers at ASM annual meetings, by decade ee] Genetics : 8 Systematics Ree Paleontology Es Morphology 100% 80% 60% 40% 20% 0% 1930 1940 1950 QM Conservation Peay Techniques EEE] Ecology 1960 ZZ Miscellaneou canal] Behavior 1970 1980 1990 Fic. 4.—Topical emphasis of papers given at ASM annual meetings, by decade, 1920-1990 (key: 1930 represents papers from 1920-1929, etc.). throughout the meeting. The topical em- phasis of papers at ASM annual meetings was examined, based on the titles of papers in the program of the annual meetings. Pa- pers were placed in one of nine categories: genetics (including all types of biochemical analysis); systematics (including evolution and geographic variation); conservation (only those papers specifically identified as dealing with conservation); techniques; pa- leontology (papers dealing with fossil taxa); morphology (including reproductive biol- ogy, physiology, and anatomy); ecology (in- cluding community and population); be- havior; and a catch-all field, miscellaneous, for all papers that could not be assigned clearly to one of the above categories or that cut across several topics. Several trends can be seen from changes in the relative representation of these cat- egories during the last 70 years (Fig. 4). Ear- ly in our society’s history, broadly based papers that covered a variety of topics were TABLE 2.— Ranked sequences by largest num- bers of presentations of the 10 political units listed as address of first authors on papers and posters listed in the program at ASM annual meetings 1920-1990. Political units included were U.S. states and the District of Columbia (U.S. postal zip code abberviations), Canada (CD), Central America, and Mexico (the latter two not yet in top 10). Meeting numbers (number of political units represented by first authors) 1-10 11-20 21-30 31-40 41-50 51-60 61-70 Rank (11) (26) (35) (39) (49) (50) (54) DG NY NY CA CA CA” CA NY DC MI MI NY MI TX PA MI CA NY MI NY _ KS Cl ‘CA De. IL 6 CD NY MA MA TX CD CD_ KS_— FL MD PA CD UT TX FL MN CD MD PA €O CO TIL CD MI CD IL AZ LA SC MA KS IN KS DC SC MN MI VT WA MD WI NM WA _ PA COMmANANINAMNHRWN —_ 168 GILL AND WOZENCRAFT Taxonomic emphasis of papers at ASM annual meetings, by decade S| Rodents LIZZ \nsectivores Carnivores a Primates EEE} Ungulates Marine Es Marsupials — Other Bats ees] Mixed 100% 80% 60% 40% 20% F- 0% 1930 1940 1950 epee, 1960 1970 1980 1990 Fic. 5.—Taxonomic emphasis of papers given at ASM annual meetings, decade, 1920-1990 (key: 1930 represents papers from 1920-29, etc.). a significant component of the meetings (miscellaneous category). As the field has become more specialized, broadly based pa- pers have decreased and are now only a small part of the papers presented at annual meet- ings. This situation is typical of the in- creased specialization in society, in general, and of teaching and research in academic institutions, in particular. One of the dominant foci for the estab- lishment of ASM, which was reflected in titles of papers, was concern for the conser- vation of mammals. The trend, as illus- trated here, reflects a decrease in titles spe- cifically identifiable as conservation issues; however, many of the papers in other cat- egories have implications to the field of con- servation biology and could appropriately be presented at conservation meetings. Morphology and physiology have always been a major component of annual meet- ings; within this category there is a general trend of a decreasing number of anatomy and an increasing number of physiology pa- pers. It appears that most papers on anat- omy are now presented within the broader framework of evolutionary or systematic theory. Genetics, a topic present since the earliest days of the society, did not become a significant part of the meetings until the 1970s, increasing with the proliferation of biochemical and molecular techniques in mammalian research. The actual number of papers in this category may be much greater, as many authors may not have used key- words in their titles that would lead to in- clusion of their papers in this category; therefore, they were not counted in this sur- vey. Perhaps the most noticeable trend among papers at the meetings is the dom- inance of ecology and behavior, which start- ed about 1970. Roughly half the papers pre- sented in the last 20 years fall into these two categories. There are other professional so- COMMITTEES AND MEETINGS 169 cieties that overlap with the ASM in cov- ering these two topics, but they have had no noticeable effect on the topical makeup of papers at the mammal meetings. The taxonomic emphasis of papers at ASM annual meetings also was examined based on titles from annual meeting pro- grams. Papers were placed in one of 10 cat- egories: Rodentia, Insectivora, Marsupialia (sensu lato), Carnivora (excluding pinni- peds), Primates, ungulates (Artiodactyla, Perissodactyla, Proboscidea), Chiroptera, marine mammals (pinnipeds, Cetacea, Sire- nia), other (groups not mentioned), and mixed (papers not identifiable with a par- ticular taxonomic group or those that deal with multiple groups). Papers were tallied by decade (Fig. 5). Several trends can be seen from changes in the representation of these categories dur- ing the last 70 meetings. Studies of Rodentia have increased from less than 20% of the total papers to nearly halfin the last decade. This category probably would be inflated more if those papers that deal with small mammal ecology in their titles (included here in mixed) were counted. The represen- tation of most other taxonomic groups re- mained rather consistent over the years, with the notable exception of the Chiroptera and the Primates. Chiroptera were poorly rep- resented in the early meetings, but now are a much larger portion, the number of papers on bats peaking in the 1960s. The Primates were well represented in early meetings but are nearly absent from the later half of the 70-year span. Most poorly represented in terms of taxonomic diversity are Insectiv- ora, generally only included here in the mixed category. Another marked difference between the first and last decade is in the number of papers that cut across taxonomic boundaries or are on topics that are not re- stricted to specific taxa (e.g., animal welfare, trapping, remote sensing, and the like), which were close to 50% in the 1920s and are less than 20% in the 1980s. We believe that this change is a direct reflection of the increasing specialization of mammalogists throughout this time period, an effect also apparent in the increasing specialization of topics at annual meetings. During the 70-year period that ASM has had annual meetings, several more special- ized societies have developed in which some ASM members have joint membership. Pri- matologists and physical anthropologists have a professional history as long, if not longer, than ASM and some of the early founders of ASM were drawn from this group. After the first decade, however, per- haps with the initial retirement or with- drawal of the founding primate biologists, the society has failed to attract this subject matter at annual meetings. Three new so- cieties have developed in the last two de- cades. When bat biologists began to meet on an annual basis, there was a marked de- crease in the number of papers on the Chi- roptera at the annual meetings. Effects of the newly formed Society for the Study of Mammalian Evolution may have a similar effect on papers in systematics and evolu- tion. When the Society for Marine Mam- malogy was formed, however, it did not produce a corresponding drop in the num- ber of papers on marine mammals at ASM meetings. Many profound changes that affect the lives and work of mammalogists have oc- curred in the world during the first 75 years of the ASM. In 1927, Charles Lindbergh’s historic flight ushered in the age of com- mercial aviation. Now mammalogists fly all over the globe to conduct research and to interact with colleagues at ITC and other international meetings. The U.S. urban population exceeded the rural in 1920 and another major shift occurred in the 1940s, during World War II. Economic changes that accompanied these and later population shifts, such as new agricultural methods with intensive use of fertilizers, irrigation, pes- ticides, and herbicides, have had a dramatic impact on the habitats and well being of mammalian populations. The society con- 170 GILL AND WOZENCRAFT tinues its struggle for the conservation of mammals, meeting these new challenges through the research of its members, edu- cation, and activities to influence legisla- tion. World War II deeply affected the mem- bership of ASM and was the only period during which meetings were not held each year. Major growth in the membership of ASM occurred in the 1950s and 1960s, with an increase in graduate students in the 1970s. The interests, as well as numbers, of ASM members have changed over the decades. There has been increased specialization in teaching and research, and in papers at an- nual meetings, no doubt mirroring the sit- uation in society at large. The revolution in biotechnology and information systems, al- though facilitating research and exchange of information, has contributed to this in- creased specialization. Some events, how- ever, appear cyclic: the teaching of evolu- tion was banned in Tennessee and the “monkey trial’’ was held in 1925. Now there is a renewed onslaught against the teaching of evolution, to which the society has re- sponded. Over the past seven and a half decades the society has continued to grow and change. An enduring curiosity about and concern for mammals, a determination to conserve natural habitats, and the plants and animals that live there, and a continuing enjoyment of the work itself, of field biol- ogy, and of the fascinating mammals we work with, sustains the fundamental spirit and camaraderie of the ASM. Literature Cited ANONYMous. 1992. Nominations for the Merriam Award. Journal of Mammalogy, 73:951-952. HOFFMEISTER, D.N. 1969. The first fifty years of the American Society of Mammalogists. Journal of Mammalogy, 50:794-802. HOFFMEISTER, D. N., AND K. STERLING. 1994. Origin. Pp. 1-21, in Seventy-five years of mammalogy (1919- 1994) (E. C. Birney and J. R. Choate, eds.). Special Publication, The American Society of Mammalo- gists, 11:1-433. Honackl, J. H., K. E. KINMAN, AND J. W. KOEpPPL (EDs.). 1982. Mammal species of the world: a tax- onomic and geographic reference. Allen Press, In- corporated and The Association of Systematics Col- lections, Lawrence, Kansas, 694 pp. KIRKLAND, G. L., JR., AND H. D. SmitH. 1994. Mem- bership and finance. Pp. 171-178, in Seventy-five years of mammalogy (1919-1994) (E. C. Birney and J. R. Choate, eds.). Special Publication, The Amer- ican Society of Mammalogists, 1 1:1—433. LAYNE, J. N., AND R.S. HOFFMANN. 1994. Presidents. Pp. 22-70, in Seventy-five years of mammalogy (1919-1994) (E. C. Birney and J. R. Choate, eds.). Special Publication, The American Society of Mam- malogists, 1 1:1—433. Verts, B. J., AND E. C. Birney. 1994. Publications. Pp. 139-154, in Seventy-five years of mammalogy (1919-1994) (E. C. Birney and J. R. Choate, eds.). Special Publication, The American Society of Mam- malogists, 1 1:1-433. WILson, D. E., AND D. M. REEDER. 1993. Mammal species of the world: a taxonomic and geographic reference. 2nd ed. Smithsonian Institution Press, Blue Ridge Summit, Pennsylvania, 1,206 pp. MEMBERSHIP AND FINANCE GORDON L. KIRKLAND, JR. AND H. DUANE SMITH Introduction he American Society of Mammalogists has a deserved reputation as one of the most fiscally conservative and finan- cially successful scientific societies in North America. The society’s current dues of $30 are among the lowest of major professional societies in biology. This reflects in large measure the substantial contribution made each year to the general operating fund by the society’s Reserve Fund, which is man- aged by the society’s three trustees. Ap- proximately one-fifth to one-quarter of each year’s general operating budget comes from income earned by the Reserve Fund, which had a net value in excess of $1,000,000 on 1 June 1992. Funds transferred to the gen- eral operating account represent income de- rived principally from the investment of life membership payments and special be- quests. As we review the membership and financial history of the American Society of Mammalogists during its first 75 years, we will document and salute the foresight of the founding members in terms of estab- lishing the firm financial base upon which the society continues to operate. Wd TIME Membership Classes The American Society of Mammalogists has five classes of membership: active, life, patron, emeritus, and honorary. Active members pay annual dues and receive the Journal of Mammalogy and other corre- spondence, such as the ‘‘Call for Papers” and program of the annual meeting, from the society. An individual may become a life member by making a payment equal to 25 times the current annual dues. This may be a single payment or may be made in four equal an- nual installments. The dues structure for life memberships has remained unchanged since the founding of the society in 1919, at which time annual dues were $3.00 and life mem- berships were $75.00. Life members receive the Journal of Mammalogy for life or until they no longer wish to do so. Life members currently comprise 17% of total ASM mem- bership. By contrast, in 1920 only 2.5% of ASM members were life members. During the succeeding four decades, the percentage of life members fluctuated slightly but had 172 KIRKLAND AND SMITH TABLE 1.— Pattern of growth in life member- ships. Total Life % life Year membership members members 1920 443 11 2-5 1930 1,005 62 6.2 1940 898 51 Se) 1950 1,232 49 4.0 1960 1,765 115 6.5 1970 BE315 342 10.3 1980 3,862 530 13.7 1990 3,661 611 16.7 risen only to 6.5% in 1960. Since then, the proportion of life members has increased by about 3% per decade (Table 1). This in- crease may reflect the desire of many mem- bers to save money by becoming life mem- bers just before dues increases, which have been more frequent during the past three decades (Table 2). Patron members are individuals who make a $1,000 payment to the society with- in a one-year period. Such individuals are entitled to receive the Journal and all other ASM publications for life. Although this membership category has existed through- out the history of the society, the first patron membership was not purchased until 1990. Today, patron memberships represent the society’s best financial bargain if viewed from the perspective that today’s patron memberships can be obtained for the same payment of $1,000 as in 1919. If the cost of patron memberships had kept pace with increases in dues over the past 75 years, patron memberships would cost $10,000. The emeritus membership category was established in 1951. Individuals who have been active members for at least 25 years may request emeritus membership status. These individuals pay no dues and do not receive the Journal of Mammalogy, but they do continue to receive other ASM corre- spondence. Emeritus members also do not have voting rights at annual meetings. The highest honor bestowed by the so- ciety is honorary membership, which is con- ferred in recognition of distinguished ser- TABLE 2.— Annual dues and subscription rate changes for American Society of Mammalogists. Year Dues Subscriptions 1919 $ 3.00 $ 3.00 1947 4.00 4.00 1952 4.00 6.00 1959 4.00 7.00 1967 4.00 9.00 1968 5.00 9.00 1969 7.00 9.00 1971 7.00 11.00 1974 7.00 15.00 1975 12.00 17.00 1977 16.00 17.00 1978 16.00 23.00 1986 20.00 28.00 1988 23.00 33.00 1993 30.00 45.00 vice to mammalogy. Fifty-eight individuals have been thus honored. These individuals are chronicled in this volume by Taylor and Schlitter (1994). The American Society of Mammalogists has always had one of the highest benefits to dues ratios among professional societies. Annual dues were $3 in 1919 and have in- creased to only $30 today. Historically, the society has been reluctant to raise dues, and it has been able to maintain its modest dues because many of the services that other so- cieties pay for are provided to the ASM on a volunteer basis by its members. Thus, ASM dues largely go to pay the costs of publishing the Journal of Mammalogy. As a consequence, increases in dues over the years (Table 2) have largely mirrored in- creases in the costs of publishing the Journal (Table 3). The philosophy that has supported reten- tion of lower dues also has been applied to subscription rates. During the society’s first 33 years subscription rates were the same as member dues, but in 1952 the subscrip- tion rate was increased to $6 per year while dues remained at $4 (Table 2). There has been a differential between dues and sub- scription rates since that time. With pro- ceeds from the Reserve Fund subsidizing society services to members, the subscrip- MEMBERSHIP AND FINANCE ies) tion rate is still comparable in value to the subsidized membership dues. Subscription rates have increased since 1967, when they were $9 per year, to the current $45 per year (Table 2). Membership History The American Society of Mammalogists had 252 charter members—1.e., individuals who joined the society in 1919. The first member, based on payment of dues, was Dwight D. Stone (3 April 1919). Ernest Thompson Seton was the first life member and seventh member overall. The first woman member was Viola S. Schantz, who served as the society’s treasurer from 1930 to 1953. Annie M. Alexander was the so- ciety’s first woman life member. The last surviving charter member was Vasco M. Tanner, who died in 1989, 70 years after joining the society. The society grew rapidly during its early years. Membership more than doubled within the first three years to 527 in 1921 (Fig. 1). The society reached the 1,000- member level (1,005) in 1930. Membership exceeded 1,000 members (1,017) the fol- lowing year, but the Depression had a sig- nificant negative impact on the society’s membership, which dropped to 931 in 1932 and reached a low of 770 in 1935 (a decrease of 24% in four years). Membership re- mained below 1,000 throughout the re- mainder of the Depression and during the war years (Fig. 1). Numerous ASM mem- bers who served on active duty in World War II were carried on the society’s books as inactive members during the war years. All such members were required to reacti- vate their memberships by 31 January 1948 or be dropped from membership. It was not until 1948 that membership again exceeded 1,000 (1,071). Membership grew steadily during the next 15 years, finally surpassing 2,000 in 1963, but it took only five more years to reach 3,000 (3,194 in 1968). This rapid increase in membership corresponded 4500 4000 3500 3000 2500 2000 1500 NUMBER OF MEMBERS 1000 500 1920 1930 1940 1950 1960 1970 1980 1990 YEAR Fic. 1.—Growth in the membership of the American Society of Mammalogists from 1919 to: 1992. to the dramatic expansion of graduate train- ing in the 1960s and the establishment of many new programs in mammalogy by ASM members who received their Ph.D.s during the 1950s and 1960s. Although member- ship exceeded 3,900 in 1975, 1976, and 1979, it has yet to reach 4,000. During the past decade, membership has stabilized at 3,600-3,700 (Fig. 1). International Membership Despite its name, the American Society of Mammalogists is an international sci- entific organization with a strong contingent of members who reside outside the United States. The international nature of the so- ciety’s membership dates from its earliest years. For example, the first List of Mem- bers published in the Journal of Mammal- ogy (1922, vol. 3, number 3) contained the names of 50 members who resided in 19 countries outside the United States and its territories. These individuals represented 9% of the society’s 555 members in 1922. As of October 1992 the society’s 718 non-U.S. members comprised 19% of total member- ship. These non-U.S. members resided in 174 KIRKLAND AND SMITH 70 countries. The society’s strong interna- tional focus is also reflected in the individ- uals elected to honorary membership in the ASM during its first 75 years. Of 58 indi- viduals thus honored, 17 (29.3%) were non- U.S. mammalogists, including Prof. E. L. Trouessart, Museum d’Histoire Naturelle in Paris, who was the second individual elected to honorary membership in 1921. The society’s International Relations Committee, which was established in 1960, has endeavored during the past decade to coordinate activities with mammal socie- ties in other countries. These efforts have resulted in four joint meetings between the ASM and mammal societies in Australia (1985), Mexico (1987), China (1988), and Argentina (1990). These meetings have pro- vided opportunities for many ASM mem- bers in those countries to participate in an ASM activity for the first time. Corresponding Secretary, Treasurer, and Secretary- Treasurer From 1919 to 1957 the membership of the society was served by the separate offices of Corresponding Secretary and Treasurer. Eleven individuals held the office of Cor- responding Secretary: H. H. T. Jackson (1919-1925), A. Brazier Howell (1925- 1931), Francis Harper (1931-1932), Robert T. Hatt (1932-1935), William H. Burt (1935-1938), William B. Davis (1938- 1941), Emmet T. Hooper (1941-1947), Donald F. Hoffmeister (1947-1952), Keith R. Kelson (1952-1954), George C. Rinker (1954-1956), and Bryan P. Glass (1956- 1957). Six of these individuals (Jackson, Howell, Burt, Davis, Hooper, and Hoff- meister) subsequently served as presidents of ASM. The tenures of treasurers were lon- ger and only five individuals held this po- sition: Walter P. Taylor (1919-1920), J.W. Gidley (1920-1921), Arthur J. Poole (1921- 1930), Viola S. Schantz (1930-1953), and Caroline A. Heppenstall (1953-1957). Wal- ter P. Taylor subsequently served the so- ciety as its president. In 1957 the offices of Corresponding Sec- retary and Treasurer were combined into a single office of Secretary-Treasurer in order to conduct the business affairs of the ex- panding society more efficiently. To date, four individuals have held this office: Bryan P. Glass (1957-1977), Duane A. Schlitter (1977-1980), Gordon L. Kirkland, Jr. (1980-1986), and H. Duane Smith (1986- present). The Secretary-Treasurer is the chief ad- ministrative officer of the ASM and is re- sponsible for the society’s day-to-day op- erations. Duties include managing the society’s general operating account and the accounts for Mammalian Species and Spe- cial Publications, maintaining membership records, corresponding with ASM members and others seeking information or assis- tance, printing and mailing the “Call for Papers” and the program for the annual meeting, assisting with preparation of the annual budget, arranging for the annual au- dit for the society’s financial records, send- ing mailing labels for the Journal of Mam- malogy and Mammalian Species to the printer, processing orders for Special Pub- lications, and distributing copies of the res- olutions passed at the annual meetings. Reserve Fund The founders of the society showed ex- ceptional foresight in establishing a mech- anism to invest life and patron membership dues and gifts to the society in a permanent fund, some of the income from which was to be used to subsidize various functions of the society. This provision was incorporat- ed in the society’s first By-laws and Rules adopted in April 1919. The year 1922 marked the first major initiative to develop the permanent fund, namely the J. A. Allen Memorial Fund. The initial goal of that fund was $10,000. The campaign to achieve that goal was supervised by the J. A. Allen Me- MEMBERSHIP AND FINANCE L75 TABLE 3.—Growth of the Reserve Fund and contributions to the general operating budget (val- ues rounded to nearest whole dollar). Reserve Fund Reserve Fund contribution contribution as Value of to annual % of Year Reserve Fund budget Reserve Fund 1930 $ 11,070 $ 500 4.5% 1940 $ 23,235 $ 500 2.2% 1950 $93,517 $: 1,500 2.8% 1960 $124,747 S 3/51 3.0% 1970 $208,603 $11,506 5.5% 1980 $475,370 $20,234 4.3% 1990 $809,376 $39,000 4.8% morial Committee. The first contributions to the fund, by W. D. Matthew, T. G. Pear- son, J. T. Nichols, B. S. Bowdish, and C. W. Richmond, totalled $105.00. The Allen Fund grew rapidly. The value of the fund was $6,335.42 in 1924, $7,606.12 in 1925, $8,525.24 in 1926, and $9,156.01 in 1927. With the fund at $9,975 in 1928, a special collection was taken among members at- tending the annual meeting to raise $25, with the following contributing: A. Brazier Howell, H. H. Lane, Carl Hartman, C. C. Adams, Lee R. Dice, M. W. Lyon, Jr., R. T. Hatt, H. C. Raven, and A. W. Leighton. The fund officially reached its goal on 9 April 1929 when the fund totalled $10,465.27. Two hundred and seventy-three contribu- tors had given $8,428.78, with the differ- ence of $1,848.90 representing interest and bond coupons. Upon achieving its goal, the Allen Memorial Committee was dissolved and the funds subsequently were managed by the society’s trustees. In 1923, the by-laws were amended to provide for three trustees to administer the permanent fund. Trustees are elected by the Board of Directors and serve three-year, ro- tating terms. The first three trustees were Henry Bannon, Childs Frick, and Charles Sheldon. Thanks to the efforts of these and subsequent trustees, the Reserve Fund has experienced sustained growth during the past 70 years. In general, the value of the Reserve Fund has doubled each decade (Table 3). TABLE 4.— Relationship between funds trans- ferred by the Reserve Fund to support the general operating account and funds transferred to the Reserve Fund for investment. Mean annual transfer to Mean annual general transfer to operating Reserve Fund Ratio of A Decade account (A) (B) to B 1930s $ 470.00 $ 549.10 0.86 1940s $ 670.00 $ 747.10 0.90 1950s $ 2,300.60 $1,720.90 1.34 1960s $ 6,489.10 $2,278.20 2.85 1970s $16,865.90 $5,386.00 3.13 1980s $27,553.50 $4,790.60 3.75 As the value of the Reserve Fund has grown, the amount of money transferred to the gen- eral operating account has increased; how- ever, when figured as a percentage of the net value of the Reserve Fund, the amount transferred annually has remained relative- ly constant, fluctuating between 2.2 and 5.5% (Table 3). Each year, funds are transferred between the Reserve Fund and the society’s general operating account. Money transferred to the fund accrues principally from life member- ship payments. The average amount trans- ferred annually to the Reserve Fund in- creased from the 1930s through the 1970s but decreased slightly in the 1980s (Table 4). During the 1930s and 1940s the amount transferred annually to the Reserve Fund exceeded the amount received annually from the fund to support operations of the soci- ety, specifically publication of the Journal of Mammalogy; however, since then the amount transferred to the general operating account has exceeded the amount annually transferred to the Reserve Fund (Table 4). Throughout the past 60 years, the ratio of funds received from the Reserve Fund com- pared to money transferred from the general operating account to the Reserve Fund has increased steadily, so that in the 1980s more than five times as much was received from the Reserve Fund as was transferred to it (Table 4). 176 KIRKLAND AND SMITH TABLE 5.—Growth of the Future Mammalo- gists Fund, 1985-1992. Year Balance Year Balance 1985 $ 4,938 1989 $ 69,090 1986 34,720 1990 71,644 1987 51,468 199] 92,204 1988 60,637 1992 128,000 Davis (1969) prepared a comprehensive history of the Reserve Fund on the occasion of the society’s 50th anniversary. He ex- amined the growth of the “Permanent Fund” on a decade by decade basis and provided a more detailed analysis of the finances of the fund, including the composition of the fund’s portfolio by decade and strategies for investing the society’s funds in light of the prevailing economic climate. The American Society of Mammalogists has always been concerned about the sci- ence of mammalogy and about providing opportunities for its members. In 1985, this concern led the society to establish the Fu- ture Mammalogists Fund with the goal to raise a minimum of $100,000 for invest- ment. Interest from this investment will support young mammalogists who are just getting started professionally. The fund- raising efforts of the members and wise in- vestments by the trustees have been very successful. Reference to Table 5 shows that the fund began slowly with a balance of $4,938 in 1985, but has grown rapidly in recent years, surpassing the original goal be- tween 1991 and 1992. The 1992 balance, $128,000, constituted 13% of the society’s Reserve Fund. The proceeds are now being used to support young mammalogists from around the world. ASM Budgets Traditionally, the bulk of the society’s an- nual operating budget has been devoted to publishing the Journal of Mammalogy. The budgeted cost of publishing the Journal (in- cluding production costs, editorial expenses TABLE 6.— Comparison of the annual budgets of the American Society of Mammalogists and the costs of publishing the Journal of Mammalogy by decade. Mean annual Cost of cost of Journal as Mean annual producing % of Decade budget Journal* budget 1920s $ 2,741.50 $ 2,440.00 89.0% 1930s 3,080.56 2,155.56 89.4% 1940s 3,600.00 3,240.00 90.0% 1950s 11,817.86 9,800.00 83.0% 1960s 23,108.70 18,765.70 81.2% 1970s 76,306.80 65,222.40 85.5% 1980s 150,957.30 116,443.90 77.1% 1990s 161,693.33 119,133.33 73.7% * Includes costs of printing, distribution, editorial expenses, editorial honoraria, preparation of the index and Recent Literature in Mammalogy. and honoraria, and costs incurred by the bibliography and index committees) has ris- en from $1,600 in 1920 to $122,000 in 1992 (a 7,525% increase). During that period, dues increased from $3.00 to $23.00 (a 667% in- crease). The cost of publishing the Journal averaged about 90% of the society’s annual budgets during its first three decades (Table 6). In the 1950s annual budgets increased substantially (228%) compared to the pre- ceding decade, whereas the cost of publish- ing the Journal increased 202% (Table 6). This difference reflected increased costs of running the society’s executive office and a broader scope of society expenditures, in- cluding funds for graduate student hono- raria and dues to afhliate societies (e.g., membership in AIBS). As a consequence, in the 1950s expenditures for publishing the Journal averaged 83% of the annual budget. This percentage remained about the same in the 1960s (Table 6); however, the socie- ty’s budgets in the 1960s averaged about twice those of the preceding decade, as did costs of publishing the Journal of Mam- malogy (Table 6). In the 1970s, both av- erage annual budgets (230% increase) and costs of publishing the Journal (248% in- crease) more than doubled. As a conse- quence, the percentage of the annual budget MEMBERSHIP AND FINANCE 177 devoted to publishing the Journal during the 1970s increased to 85.5%. The first budget in excess of $100,000 was approved for 1977. There was less than a two-fold increase in budgets and costs of publishing the Journal in the 1980s with the percentage contribution of publishing the Journal declining to 77% (Table 6). During the first three years of the 1990s, budgets have increased little over those for the 1980s (Table 6). Summary Members of the American Society of Mammalogists can take singular pride in the financial history of their society. Today’s members benefit from the financial acumen and foresight of the society’s founding members. In terms of its finances, the ASM is a model for other scientific and profes- sional societies, who in the past have con- tacted the society’s executive office for ad- vice on financial matters. Members of the ASM not only belong to the oldest and larg- est scientific society devoted to the study of mammals, they are members of a society whose astute and prudent financial man- agement over the years has made it one of the “best buys” among professional soci- eties. Acknowledgments We thank staff members of the Smithsonian Archives, especially W. Cox, for facilitating ac- cess to the society’s historical files. We also thank W. C. Wozencraft for his assistance in locating ASM archival materials. Literature Cited Davis, W. D. 1969. The American Society of Mam- malogists permanent fund: a special report of the trustees. Pp. 33-40, in The American Society of Mammalogists 50th anniversary celebration. Pro- cessed by the American Museum of Natural History, New York, New York. 44 pp. TAYLOR, J. M., AND D. A. SCHLITTER. 1994. Award- ees. Pp. 71-109 in Seventy-five years of Mammalogy (1919-1994) (E. C. Birney and J. R. Choate, eds.). Special Publication, The American Society of Mam- malogists, 11: 1-433. PART II INTELLECTUAL DEVELOPMENT OF THE SCIENCE OF MAMMALOGY TAXONOMY MArkK D. ENGSTROM, JERRY R. CHOATE, AND HUGH H. GENOWAyYS Introduction i) Rares aden has been termed the “theory and practice of classifying organisms” (Mayr and Ashlock, 1991:2), whereas sys- tematics is the broader study of the history and diversity of life. In practice, in distinc- tion between these disciplines is often blurred. In this review, we focus on the role of taxonomy and taxonomists in the de- velopment of the discipline of mammalogy in North America over the past 75 years, although we occasionally will slip into broader discussions of systematics where it has influenced the philosophical underpin- nings of taxonomy. For purposes of discus- sion and in practice, taxonomy also can be divided conveniently into two levels: mi- crotaxonomy—the methods and principles by which species are recognized and delim- ited; and macrotaxonomy—the methods and principles by which recognized kinds of or- ganisms are Classified (Mayr, 1982). Historical Perspective Development of mammalian taxonomy in North American was a natural conse- quence of exploration of the continent. Many of the early descriptions of new mammals from the East were made by Linnaeus and 179 his contemporaries based on specimens re- turned to Europe from the American col- onies. Some of the most important taxo- nomic contributions by American authors were taxonomic catalogues (reviewed by Hoffmeister and Sterling, 1994). However, American naturalists were largely respon- sible for taxonomic investigations resulting from exploration of the West, beginning with the Lewis and Clark expedition and cul- minating with the expeditions of Major Ste- phen Long, Zebulon Pike, Thomas Say, Maximilian Prince of Wied-Neuweid, John C. Fremont, and numerous others. The tax- onomic products of those expeditions in- cluded such monumental catalogues as Baird’s (1857) report on the mammals of North America, Coues and Allen’s (1877) review of North American rodents, Elliot’s (1904) checklist of mammals of North America and the West Indies, and Mearns’ (1907) Mammals of the Mexican boundary of the United States. Most of the taxonomic collections made by naturalists of the 19th Century were re- turned to museums in the East, notably the Charleston Museum, Peale’s Museum in Philadelphia, Museum of Comparative Zo- ology at Harvard College, American Mu- seum of Natural History in New York, 180 United States National Museum, Chicago Academy of Sciences, and Field Museum of Natural History in Chicago. Taxonomists associated with those museums were among the leaders in development of the science of mammalogy, as were naturalists associ- ated with the most influential universities of the day: Harvard, Yale, Michigan, Cor- nell, California, and others. California was especially important because it was there that Joseph Grinnell had begun a dynasty of mammalogists that persists even today (Jones, 1991; Whitaker, 1994). However, the most productive group of North American mammalogists of the day by far were those associated with the Bureau of the Biological Survey, the progenitor of the U.S. Fish and Wildlife Service (de- scribed by Hoffmeister and Sterling, 1994). Authors of monographic revisions pub- lished by bureau employees in its North American Fauna series read like a who’s who of North American mammalogy in the years preceding the origin of the ASM: Vernon Bailey; Edward A. Goldman; Ned Hollister; A. Brazier Howell; Arthur H. Howell; Hartley H. T. Jackson; C. Hart Merriam; E. W. Nelson; Wilfred H. Osgood; Edward A. Prebel. Of the monographs pub- lished before 1919, Osgood’s (1909) revi- sion of the genus Peromyscus arguably has stood the test of time better, and has stim- ulated more taxonomic studies, than any other. The ASM came into being at a time when much of the work of North American mam- malogists was directed at understanding the diversity of mammals on the continent. Most of the founding fathers of ASM were thus taxonomists, and taxonomists subse- quently have had a greater influence on the society than have mammalogists of any oth- er subdiscipline. For North American taxonomists from the mid-1800s until about the turn of the century, the predominant species concept was typological—species were held to be nearly fixed entities that varied about a fi- nite number of types. By this concept, root- ed in the classical philosophy of European ENGSTROM ET AL. systematics, species were delimited subjec- tively based on relative degree of morpho- logical difference and consisted of aggrega- tions of individuals that agreed with the author’s diagnosis. There was little appre- ciation of the distinction between variation due to gender, age, or individual and geo- graphic differentiation. During this period, most new forms were described as species despite the fact that the category of subspe- cies was already in common use in orni- thology. Designation of morphologically distinct forms as species was understand- able in that most early collections consisted of specimens from widely separated local- ities and the concept of geographic variation was poorly understood. The extensive col- lections amassed under the auspices of the Bureau of the Biological Survey (among others), however, eventually demonstrated the pervasiveness of geographic variation and intergradation among many nominal “‘species.’’ Gradually, the practice of sorting apparently distinctive specimens into spe- cies was replaced by a broader view of spe- cies aS interrelated groups of populations united by reproductive ties. Taxoncmists shifted from describing and classifying ob- jects (specimens) to attempting to describe the living diversity of populations that those specimens represented. Perhaps the most notable early example of this shift was Os- good’s (1909) revision of Peromyscus. Os- good reduced the number of recognized spe- cies of deer mice from 130 to 43 (see review by Carleton, 1989) and, in one instance, combined 28 nominal species into the taxon he recognized as Peromyscus maniculatus. Many of the former species names were re- tained as formal subspecies, and the practice of recognizing polytypic species (consisting of two or more subspecies), in use since the late 1800s, thus became entrenched. Change from a typological or strict mor- phological concept of species to recognition of polytypic species composed of morpho- logically distinct, intergrading subspecies was gradual and was not universally ac- cepted by the time of formation of the ASM in 1919. For example, the first issue of the TAXONOMY 181 Journal of Mammalogy contains a staunch defense of a morphological species concept by Merriam (1919). He stated (p. 7) that “the criterion of intergradation is one of the most pernicious that has ever been intro- duced into the systematic study of animals and plants .. .” and, quoting a previous ar- ticle in Science (p. 9), “forms which differ only slightly should rank as subspecies even if known not to intergrade, while forms which differ in definite, constant and easily recognized characters should rank as species even if known to intergrade.”’ This philos- ophy, coupled with samples inadequate to demonstrate the full range of intra- and in- terpopulational variation, led him (Merri- am, 1918) to recognize two genera and 78 species of brown bears, all now considered to represent a single species (Hall, 1984). Interestingly, a rejoinder by Taverner (1920: 126) in the first volume of the Journal of Mammalogy advocated the essentials of what later would become known as the bi- ological species concept: “‘the species is a definite entity and its essential quality is its genetic isolation.” Many of the taxonomy publications of the 1920s were by employees of the Bureau of the Biological Survey; however, the most important taxonomic catalogue of the pe- riod was by Gerrit S. Miller, Jr. (1924), Cu- rator of Mammals at the U.S. National Mu- seum, who updated his earlier (Miller, 1912) list of North American mammals. Several taxonomic revisions were published during this decade, most notably those by A. B. Howell (1926, 1927), Jackson (1928), Miller and Allen (1928), and A. H. Howell (1929). Most of the taxonomic publications of the period were monographic in extent. Taxonomic work in the 1930s was dom- inated less than that of the previous decade by employees of the Bureau of the Biological Survey. An increasing number of mam- malogists at academic institutions and at museums other than the United States Na- tional Museum began to have an impact. One of the most important taxonomic re- visions of the period was the monograph on squirrels by A. H. Howell (1938). Other re- visionary studies emanated from the Field and American museums of Natural History and dealt largely with Latin American mammals (e.g., Sanborn, 1937; Tate, 1933). During this decade, there was an increasing tendency for taxonomic work to be less than monographic in extent and to focus on in- dividual species rather than genera or higher categories (e.g., Nelson and Goldman, 1933). Most North American mammalogists would agree that the taxonomic highlight of the 1940s was Simpson’s (1945) The Prin- ciples of Classification and a Classification of Mammals. Few generic revisions were published during the decade, as an increas- ing number of taxonomic studies focused on geographic variation within species (e.g., Hooper, 1943). The 1950s was a watershed decade for mammalian taxonomy in North America. An important taxonomic catalogue (North American Recent Mammals, by Miller and Kellogg, 1955) was published early in the decade only to be overshadowed by another (The Mammals of North America, by Hall and Kelson, 1959). Hall and Kelson’s mon- umental two-volume work quickly became a veritable landmark in mammalogy in that it summarized everything then known about the distribution and taxonomy of native mammals in North America. Much of the explosion of taxonomic research (especially on relationships within genera and geo- graphic variation within species—see dis- cussion of subspecies, beyond) was a direct result of studies leading to or stimulated by publication of this epic monograph. In place of faunal studies, numerous taxonomic re- visions were published during the 1950s. Some of the best known of those revisions were by Goldman (1950), Hall (1951), Hoff- meister (1951), Hooper (1952), Handley (1959), Moore (1959), and Van Gelder (1959). The number of studies of variation within species continued to climb, that by Findley (1955) serving as an example. The explosion of taxonomic literature on North American mammals that began in the 1950s continued in the 1960s. Taxo- nomic catalogues published during the de- 182 ENGSTROM ET AL. cade included those of Hershkovitz (1966) on living whales, and Anderson and Jones (1967) on mammals of the world. Taxo- nomic revisions continued to be numerous, a few examples being those of Lidicker (1960), Packard (1960), Russell (1968a, 19685), Davis (1968, 1969, 1970), Musser (1968), and Lawlor (1969). Increasingly, these revisions were of small genera and were less than monographic in length—a phenomenon possibly resulting in part from the increasing difficulty in finding outlets for lengthy, monographic manuscripts. The 1970s witnessed publication of few taxonomic catalogues (one example being Varona’s 1974 catalogue of Antillean mam- mals), but a large number of both “Mam- mals of ...’ books and taxonomic revi- sions. A sample of the many taxonomic revisions of the period includes those by Choate (1970), Findley and Traut (1970), Zimmerman (1970), Genoways and Jones (1971), Hooper (1972), Pine (1972), Smith (1972), Thaeler (1972), Birney (1973), Gardner (1973), Genoways (1973), Carle- ton (1977), Eger (1977), Hennings and Hoff- mann (1977), Yates and Schmidly (1977), Hoffmeister and Diersing (1978), Williams (1978), Carleton and Eshelman (1979), Haf- ner et al. (1979), Silva-Taboada (1979), and Williams and Genoways (1979). By the end of the decade, new techniques for taxonom- ic analysis (Baker and Hafner, 1994; Ho- neycutt and Yates, 1994) and changing pri- orities at academic institutions and funding agencies were beginning to take a toll on faunal studies and taxonomic revisions, of- ten relegating both to the category of long- term, low priority projects. The 1980s began with publication of Hall’s (1981) long-awaited update of The Mammals of North America. As noted by Jones (1982:718) in his review of this mon- umental taxonomic catalogue, “It is unlike- ly that any other American mammalogist would have undertaken, or will undertake again, such a gigantic task.” Another useful catalogue published during the decade was Anderson and Jones’ (1984) revised syn- opsis of mammals of the world. During the previous decade, an enthusiastic cadre of young mammalian taxonomists had begun developing in Mexico, and the 1980s were marked by the beginnings of taxonomic products from this group (e.g., Arita and Humphrey, 1988; Ceballos and Galindo, 1984; Ramirez-Pulido et al., 1986). It seems likely that a substantially greater percentage of the taxonomic papers on Latin American mammals will be authored by Latin Amer- ican mammalogists in decades to come. Fi- nally, the decade was marked by Koop- man’s (1984) classification of bats and a multitude of taxonomic reviews, many of the latter employing genetic techniques or focusing on species or species groups. A few examples were the studies by Carleton (1980), Huckaby (1980), Engstrom and Wil- son (1981), George et al. (1981), Patton and Smith (1981), Patton et al. (1981), Honey- cutt and Williams (1982), George et al. (1982), Grifhths (1982), Hafner (1982), Rogers and Schmidly (1982), Heaney and Timm (1983), Baker (1984), van Zyll de Jong (1984), Sullivan (1985), Sullivan et al. (1986), Webster and Handley (1986), Baker et al. (1988), George (1988), Robbins and Sarich (1988), Voss (1988), Baker et al. (1989), Carleton and Musser (1989), van Zyll de Jong and Kirkland (1989), and Woz- encraft (1989a, 1989b). The 1990s show promise of a continua- tion of the existing emphasis on microtax- onomic studies employing modern genetic methods plus development of a much great- er emphasis than in the past on macrotax- onomy. Early examples of the research that will characterize the decade include the studies by Patton and Smith (1990), Hafner (1991), Johnson and George (1991), Rogers and Engstrom (1992), and Wall et al. (1992). Biological Species Concept The empirical demonstration of species as natural aggregates of populations delin- eated from related species by reproductive TAXONOMY 183 MW Families 1! Genera Species () Subspecies 3000 + 2500 2000 1500 + 500 + Hall and Kelson, 1959 Hall, 1981 Miller and Rehn, 1902 Miller, 1924 Fic. 1.—Total number of families, genera, spe- cies, and subspecies of North American mam- mals recognized as valid in major taxonomic summaries of the 20th Century. gaps led to formulation of a biological spe- cies concept: ““Species are groups of inter- breeding natural populations that are re- productively isolated from other such groups” (Mayr, 1969:26). Viewing species as natural, objective entities rather than classes of objects had its genesis in the late 1700s and was accepted by ornithologists and ichthyologists by the turn of the cen- tury. Mammalogists were more conserva- tive, but the concept (with its common rec- ognition of polytypic species) had taken hold by the 1920s. Coupled with this philosoph- ical shift was the ascendancy of the neo- Darwinian school of “‘new systematics” (Huxley, 1940), led by R. A. Fisher, J. B. S. Haldane, S. Wright, T. Dobzhansky, E. Mayr, G. G. Simpson, V. Grant, and others from the 1930s through the 1960s. This phi- losophy reasserted the fundamental impor- tance of taxonomy and systematics. With its concern for microevolutionary processes underlying intraspecific genetic variation and the generation of diversity, this school focused on issues of population genetics, geographic variation, and speciation. Sev- eral classic generic revisions of mammals were written during this period, with an em- phasis on discerning patterns of geographic variation and taxonomic limits of species rather than on primary descriptions. Abandonment of a typological or strict morphological concept and recognition of geographically variable, polytypic species, led to a clarification and simplification of the classification of North American mam- mals at the species level. In the 35-year pe- riod between 1924 and 1959, the 1,441 spe- cies of North American mammals admitted by Miller (1924) were reduced to 1,003 (Hall and Kelson, 1959), despite the description of numerous new, valid species (Figs. 1 and 2). This led Hall and Kelson (1959:vi) to remark that “The decrease in number of species results from many of the named kinds having been reduced from specific to subspecific status in the past thirty years. Certainly the number of species listed in the present work is still too large, many geo- graphically adjacent pairs of nominal spe- cies will prove to be only subspecies of one and the same species when adequate spec- imens are studied from geographic areas be- tween the known areas of occurrence of the two kinds.’ Unfortunately, the descriptive efforts of some mammalian taxonomists soon were directed to the formal recognition of taxa below the level of species, and an explosion of new subspecies ensued (see fol- lowing section on subspecies). Conversely, from 1902 to 1924 the number of recog- nized genera and families increased by a factor of about one-half, due mostly to a less inclusive view of higher taxa; this num- ber has remained relatively stable since that time (Fig. 1). In the enthusiasm for polytypic species as a taxonomic device to address the problem wrought by the proclivity of some early tax- onomists to name every local variant as a species, application of the biological species concept sometimes was overly conserva- tive. In the never-ending search for real or inferred intergrades, several subtle but dis- tinct species were subsumed under the headings of single species. Thus, Merriam’s (1919:7) admonition rings true: “‘it [the cri- terion of intergradation to delimit species] has often resulted in bringing together forms between which intergradation has not only 184 ENGSTROM ET AL. not been demonstrated, but which in many cases never existed ...”’ Moreover, some authors came to view any evidence of hy- bridization as proof of intergradation and conspecificity (see discussion of Hall, 1981, in Patton and Smith, 1990). That the num- ber of distinct species of North American mammals currently is underestimated has become increasingly evident with the ap- plication of modern genetic and morpho- logical techniques to studies of geographic variation and speciation. Recent systematic studies often have revealed that many pur- portedly intergrading taxa actually repre- sent protected, reproductively isolated gene pools (Baker, 1984; Baker et al., 1985; Bir- ney, 1976; Carleton, 1989; Genoways and Choate, 1972; Patton and Smith, 1990; Schmidly et al., 1988; Zimmerman, 1970). The number of recognized species of North American mammals declined from 1,003 to 887 between 1959 and 1981 (Fig. 1), as pre- viously predicted by Hall and Kelson (1959). Between 1981 and 1993 the number de- creased again to 866 (Wilson and Reeder, 1993). Included in that total, however, is the long-awaited systematic review of brown bears (Hall, 1984), wherein the number of species was reduced from 78 to 1. Discount- ing the 77 species names belatedly placed in synonymy by Hall, the number of ad- mitted species actually rose by 56 during this period despite the fact that discovery of hitherto unknown species of mammals slowed to a trickle (Fig. 2). We anticipate that the number of recognized species will continue to rise as our view of species is refined, as more specimens become avail- able, as geographic coverage improves, and especially as multidisciplinary techniques are applied to studies of geographic varia- tion in a wider variety of taxa (see also Carleton, 1989). To the casual observer, these changes probably will appear to result from a frictionless pendulum perpetually swinging between “lumpers” and “‘split- ters.”” Instead, we would argue that these oscillations represent significant progress in our understanding of the composition and —— Subspecies --~-~- Species Fic. 2.—Number of species and subspecies of North American mammals described between 1900 and 1990. Data for 1900 to 1977 were com- piled from Hall (1981), and those for 1977 to 1990 were taken from The Zoological Record. distribution of North American mammals during the past 75 years. Although the biological species concept was, and continues to be, the dominant con- cept applied by North American mammal- ogists, it is by no means universally ac- cepted. Space precludes a full review of this ongoing debate, but a few comments may be pertinent. For operational reasons, phe- neticists dispute the idea that species are objective units bound by reproductive con- tinuity. Instead, they reiterate the nomi- nalist claim that the only objective unit in nature is the individual, and that all collec- tive higher categories (including species) are human constructs (Sokal and Crovello, 1970). This claim appears intuitively false when applied to sympatric species of sex- ually reproducing taxa, such as mammals or birds (Mayr, 1969). It does, however, highlight the difficulty of applying the bio- logical species concept to allopatric and al- lochronic populations where the potential for interbreeding and intergradation must be inferred, or in geographically contiguous populations among which gene flow is min- imal (Ehrlich and Raven, 1969). In these cases, biological species indeed are subjec- tive constructs, and the erection of polytyp- ic species as a taxonomic device runs the TAXONOMY 185 risk of underestimating or misrepresenting the number of independent evolutionary units. More recently, Wiley (1978, 1981) restated Simpson’s (1961) concept of evo- lutionary species. ““An evolutionary species as a single lineage of ancestor-descendant populations which maintains its identity from other such lineages and which has its own evolutionary tendencies and historical fate” (Wiley, 1981:25). This concept stress- es that species are bound by unique com- mon ancestry, whether or not reproductive continuity is evident, and adds the missing element of common evolutionary history to the biological species concept (Brooks and McLennan, 1991). This broader definition provides a conceptual means of delineating natural species, although operationally it sometimes is no less subjective than the bi- ological species concept. For example, faced with a monophyletic set of allopatric pop- ulations, the taxonomist must now decide if these populations represent a single evo- lutionary lineage, instead of deciding whether or not they potentially could inter- breed. Nonetheless, in our view, this theo- retical concept more closely approximates real species-level units (i.e., actual evolu- tionary units as manifested by the organ- isms themselves). Its application in mam- malogy portends a more realistic view of species-level taxonomy and the process of speciation (but see alternative view in Mayr and Ashlock, 1991). Operational variations on this theme, such as the phylogenetic spe- cies concept (Cracraft, 1983; Donoghue, 1985; McKitrick and Zink, 1988) also may prove useful but, strictly applied, run the risk of recognizing all apparently distinctive populations as species and a return to a ty- pological concept (for a recent application, see Engstrom et al., 1992). Subspecies Concept The history of the category of subspecies is closely tied to that of species. Subspecies came into regular use in North American mammalogy near the turn of the century, although the formal trinomen had been used by ornithologists since the mid- 1800s. Orig- inally conceived as a substitute for the am- biguous term variety (which had been used as a catch-all for a plethora of intra- and interpopulational miscreants), subspecies had the general connotation of geographic race (e.g., Osgood, 1909). As with species, they initially were viewed typologically and were defined on a morphological basis: a subspecies was a set of specimens that dif- fered from another set but not to the same degree as species. The general acceptance of polytypic species, and the potential for in- tergradation as a means of discerning spe- cies-limits, spurred use of the category as a means of characterizing morphologically distinct but intergrading sets of populations. Application of the trinomen initially was conservative and, until about 1920, about as many subspecies were named as new spe- cies (Fig. 2). With the onset of the “new systematics” in the 1930s and its focus on microevolutionary processes, considerable effort was expended by mammalogists in studying patterns of geographic variation, which were formally recognized using the trinomen. Unfortunately, rather than ex- amining the role of geographic differentia- tion in the generation of diversity, discovery of statistically distinct subspecies soon be- came a primary goal of some mammalian taxonomists and the “‘wild-goose chase”’ (Mayr, 1963:347) to find new subspecies was on. As a consequence, the rate of description of subspecies relative to species rose dra- matically during the period from 1930 to 1960 (Fig. 2). The number of recognized subspecies of North American mammals nearly doubled during this time, whereas the number of species decreased by about a third (Fig. 1). These changes reflected both increased acceptance of the utility of sub- species as a taxonomic device and conser- vative application of a biological species concept. During this period, different authors had different concepts of subspecies, ranging 186 ENGSTROM ET AL. from subjective geographic divisions of tax- onomic convenience to incipient species. For example, Mayr (1969) regarded subspecies as an arbitrary device to facilitate intraspe- cific classification and not as evolutionary entities, whereas Lidicker (1960) believed that the category should be reserved for phy- logenetically delimited subunits of species. Given that subspecies are subjective and at a point in a gradient between local popu- lations and species, the lower-limit of di- vergence at which they were recognized also varied greatly among authors. As noted by Lidicker (1960:161) “‘it is axiomatic that populations which consist of different in- dividuals are different. The ability to prove this difference statistically depends only on the size of the samples used and the per- ceptual ability of the investigator.”’ None- theless, some authors (Mayr et al., 1953; Simpson, 1961) advocated a 75% rule—if 75% of the individuals in one population could be distinguished from all individuals of an adjacent population, ensuring a sta- tistically significant difference, the two could be formally recognized as subspecies (pre- sumably based on even a single character). In some species, where localized patterns of geographic differentiation were pro- nounced, numerous microgeographic races were described. Hence, Setzer (1949) rec- ognized 35 subspecies of Ord’s kangaroo rat, Dipodomys ordii, many occupying small geographic areas. In perhaps the most in- famous example, 213 subspecies of the pocket gopher, Thomomys umbrinus, were admitted in Hall and Kelson (1959). This latter case prompted Simpson (1961:173) to remark critically “those who enjoy this game may go on until every little colony of these gophers sports its own Linnaean name.” As a mere device for cataloguing geographic variants based on a few or single characters, recognition of subspecies often has little bi- ological meaning and results in formal rec- ognition of rankless groups, with no predic- tive value relative to additional characters (Barrowclough, 1982). In our view, the larg- est abuses of the category were made by authors who described subspecies based on small samples from limited geographic ar- eas without a thorough analysis of variation within the entire species. By 1950, subspecies of North American mammals had become an amalgam of old names not relegated to full synonymy, lo- calized variants, arbitrarily partitioned sec- tions of geographic clines, polytopic and mi- crogeographic races, discrete evolutionary units and, in some instances, subtle but dis- tinct species. Not surprisingly, infraspecific taxonomy of vertebrates came under heavy criticism during a debate on the utility of the category that raged largely in the pages of Systematic Zoology for 10 years, sparked by Wilson and Brown (1953). They noted (p. 100), “‘the subspecies concept is the most critical and disorderly area of modern sys- tematic theory” and advocated that the cat- egory be abandoned. For North American mammalogists, among the most influential contributions to this debate were those of Lidicker (1960, 1962), who defined subspe- cies as (1962:169) “a relatively homoge- neous and genetically distinct portion of a species which represents a separately evolv- ing, or recently evolved, lineage with its own evolutionary tendencies, inhabits a definite geographic area, is usually at least partially isolated, and may intergrade gradually, al- though over a fairly narrow zone, with ad- jacent subspecies.” This restrictive defini- tion has been widely cited although it probably is no coincidence that its most suc- cessful applications have been with geo- myoid rodents (Genoways, 1973; Lidicker, 1960; Smith and Patton, 1988) in which gene flow among local populations often is restricted, pronounced local microgeo- graphic differentiation is commonplace, and geographic variation is partitioned hierar- chically. In other groups for which rates of gene flow are higher and geographic differ- entiation is less abrupt, taxa fitting the above definition most often would be regarded as distinct evolutionary species. After this debate, application of the sub- species category in mammalian taxonomy TAXONOMY 187 became much more conservative and the rate of description of new subspecies ap- proximated that of species, as it had prior to 1920 (Fig. 1). Thus, between 1959 and 1981, the number of recognized subspecies of North American mammals remained rel- atively stable (Fig. 2) owing to nearly equal rates of additions (new descriptions) and de- letions (relegation to synonymy of existing subspecies). Since 1981, the rate of descrip- tion of new subspecies of North American mammals has decreased to less than five per year, and there has been a tendency to attach less significance to the category (e.g., Wilson and Reeder, 1993). As an aside, critics of the subspecies category often have branded museum curators as the culprits who use subspecies aS a convenient device to aid them in arranging and subdividing groups of specimens in drawers. As curators who have spent many unproductive hours at- tempting to assign specimens to poorly de- fined, undiagnosable subspecies, which seem inevitably to be from geographically inter- mediate areas, we can assure the reader that arbitrarily defined infraspecific taxa are no boon to curatorial efficiency or order. The current state of the subspecies cate- gory in vertebrate taxonomy (and concom- itantly of recognized taxa at this level) is muddled. Some authors would abandon the category entirely (Cracraft, 1983; McKitrick and Zink, 1988), whereas several mam- malian systematists find a restricted concept useful in formally depicting discrete pat- terns of geographic variation (e.g., Patton and Smith, 1990). In our view, the real pur- pose of the trinomen is to describe formally patterns of geographic variation by calling attention to geographic discontinuities among distinctive, evolutionarily discrete subsets of populations. We anticipate that, as detailed multidisciplinary studies of geo- graphic variation are completed for more species, and as a conservative concept of subspecies is consistently employed, the number of recognized subspecies of North American mammals will decline substan- tially over the coming decades. Higher Level Taxonomy Schools of systematics and classifica- tion. —After the exploratory phase of tax- onomy of North American mammals in the late 19th and early 20th centuries, the focus of studies shifted more towards discerning systematic relationships among species. The new systematics emphasized studies at low- er taxonomic levels and down-played phy- logenetic research. Thus, during the period from 1930 to 1960 many comprehensive taxonomic studies of North American mammals focused on species and generic level revisions rather than on higher clas- sification. The guiding philosophical basis of this research was the somewhat intuitive school of evolutionary taxonomy champi- oned by E. Mayr, G. G. Simpson, and oth- ers. The goal was to discern genealogical relationships among taxa and then to rep- resent both genealogy and extent of phyletic divergence in the final classification. How these factors were to be weighed was up to the discretion of the investigator, and the process was said to be part art and part sci- ence (Simpson, 1961). Examples of this ap- proach include Simpson (1945) and Koop- man (1984). These classifications were meant to be inherently stable, utilitarian de- vices, consistent with what was known about evolutionary relationships and magnitude of evolutionary change. The seeming lack of objectivity of the evolutionary school triggered a change in systematic philosophy through develop- ment of the opposed phenetic and phylo- genetic schools of systematics in the 1950s and 1960s. These schools were largely re- sponsible for the revival of interest in mac- rotaxonomy that continues today. Early proponents of phenetics (or numerical tax- onomy) suggested that, because genealogies were difficult to reconstruct and phylogenies largely unknown, “natural” higher taxa were most objectively discerned by overall sim- ilarity (Sneath and Sokal, 1973; Sokal and Sneath, 1963). This operationalist (theory- free) school is concerned primarily with 188 ENGSTROM ET AL. multivariate, numerical methodologies for representing empirical phenetic relation- ships, typically weighting all characters equally. The method has its genetic exten- sion in DNA hybridization, where overall similarity between species is calculated from average melting temperatures of hybrid DNA molecules. Exemplary studies in North American mammalogy that employed these techniques (but did not necessarily adhere to a strict view of the philosophy) include those by Findley (1972), Schnell et al. (1978), Freeman (1981), Brownell (1983), Owen (1988), and Kirsch et al. (1993). Criticisms of the use of phenetics in classification in- clude: that overall similarity often gives a distorted view of phylogenetic relation- ships, especially when shared primitive, convergent, or uniquely derived character states predominate; and that the method, although repeatable using the same char- acters, produces inherently unstable classi- fications likely to be altered when new at- tributes are examined. Although phenetic philosophy for construction of classifica- tions has not been widely accepted in mam- malogy, numerical methodology for analyz- ing patterns of variation, particularly at the microtaxonomic level, has become an in- tegral part of the repertoire of techniques used by mammalian taxonomists. At about the same time as the develop- ment of phenetics, the school of phyloge- netic systematics (or cladistics) arose and has produced a revolution in macrotaxon- omy. Stimulated by the writings of Hennig (1950, 1966), phylogenetics aims to fulfill the goal set by Darwin to base classifications directly on genealogy. Phylogenetic rela- tionships are based on propinquity of de- scent determined from special similarity of homologous characters (shared derived character states) rather than unweighted, overall similarity. Reconstructed phyloge- nies subsequently are translated directly into classifications. Space precludes a review of the development of this school, but much of the debate concerning its methodology and philosophy (which is far from uniform) appears in the pages of Systematic Zoology from the 1970s to the present and is sum- marized in the texts by Wiley (1981) and Eldredge and Cracraft (1980) (see also the primer by Wiley et al., 1991). North Amer- ican mammalogists have been bit players in the development of phylogenetics, although arguably the most important recent ad- vances in higher classifications of mammals have employed this method (at least to re- construct cladistic branching sequences). In particular, molecular systematists working on North American mammals who initially used phenetic methods almost exclusively now routinely apply cladistic parsimony to discern relationships. One only need peruse the pages of the Journal of Mammalogy or Systematic Biology (formerly Systematic Zoology) for the past 10 years to see the predominant influence of this school on vertebrate taxonomy and systematics. Pub- lications on North American mammals em- ploying this methodology are too numerous to cite, but a few exemplary studies include: Greenbaum and Baker (1978); Carleton (1980); Smith and Madkour (1980); Grif- fiths (1982); Hood and Smith (1982); Rog- ers et al. (1984); Owen (1987); Voss (1988); Baker et al. (1989); Miyamoto et al. (1989); Wozencraft (1989a); Wyss (1989); Hafner (1991); Pacheco and Patterson (1991); Lim (1993). Continued dialogue (often acrimonious) among these three schools of systematics has resulted in considerable refinement of taxonomic methodology. By partitioning historical evolution (descent with modifi- cation) into the separate components of phenetic divergence and genealogy, classi- fications no longer need rest on intuition and authority; instead, they are based on empirical evidence of change in character states. Thus, as Hooper (1968:33) noted: “A classification is a tentative thing; it is not sacred.” This change has resulted in a re- kindled interest in macrotaxonomy in gen- eral, and in the higher classification of mam- mals, in particular. It also has sparked a new interest in using classifications to test hy- TAXONOMY 189 potheses about historical processes in bio- logical disciplines outside the field of sys- tematics (Brooks and McLennan, 1991). Higher classification. —The history of mammalian classification was reviewed by Gregory (1910), Simpson (1945), Szalay (1977), and Novacek (1982, 1990), and only a few highlights will be mentioned here. Since the turn of the century, much of the outstanding work by North Americans on classification of mammals has emanated from the Department of Vertebrate Pale- ontology of the American Museum of Nat- ural History. Before the formation of the ASM in 1919, the most comprehensive and influential mammalian classification was that of Gregory (1910: Table 1). Phyloge- netic in approach, Gregory was concerned with distinguishing between primitive and derived traits and with eliminating conver- gence (although these tenets were not always consistently followed in defining groups). Gregory’s classification was relatively high- ly resolved; an optimistic solution not shared by several later workers (including Simp- son, 1945), who more often regarded rela- tionships among most eutherian orders as an unresolved phylogenetic ““bush.”” Among several other groups, Gregory (1910) de- fined and defended the Archonta (including elephant shrews, tree shrews, bats, gliding lemurs, and primates), over which there has been much recent debate. Included in this synthesis (Gregory, 1910) is a fascinating historical review of mammalian classifica- tion that merits careful reading by anyone interested in the development of system- atics. Simpson (1945) later published what has been widely regarded as the standard clas- sification of mammals (Table 1). This work was more detailed than that of Gregory, in that all mammals were classified to genus. Until the last decade, the pervasive influ- ence of this monograph could be seen by touring the large museum and university collections of mammals in the United States, most of which were ‘“‘arranged according to Simpson (1945). Part of that influence stemmed from Simpson’s position as a lead- ing evolutionary theorist and his strong ad- vocation of intuitive, evolutionary taxon- omy. Many of his groups were based on his perception of phylogeny (e.g., recognition of the Ferungulata, including carnivores, un- gulates, and related orders to the exclusion of other mammals), although these groups were not justified by shared derived features and have not been well accepted. In fact, despite its comprehensiveness, there was little explicit discussion of characters on which the classification was based. For ex- ample, Simpson (1945:173) dismissed Gregory’s Archonta, without reference to characters or literature citations: “it is in- credible to me. . . that the primates are more closely related to bats than to the insecti- vores, and all recent research ... opposes that opinion.” Thirty years later, changes in systematic philosophy and discovery of new Mesozoic fossils led to a radical departure from Simp- son (McKenna, 1975; Table 1). This was the first major classification of mammals that used cladistic methodology to recon- struct phylogeny and it included explicit discussion of character state transforma- tions (especially dental homologies). Ini- tially, McKenna (1975) was criticized be- cause his classification was complex and because he erected a large number of new superordinal categories to reflect relative re- cency of common ancestry directly (Szalay, 1977). However, as noted by Novacek (1982), his departure from “traditional” systematics by providing explicit consid- erations of alternative phylogenetic hypoth- eses has not received due credit. Some of McKenna’s (1975) more important depar- tures from Simpson include (Table 1): early branching of the Edentata from the rest of the eutherian mammals; resurrection of Gregory’s Archonta (sans the elephant shrews— Macroscelidea); phylogenetic as- sociation of Macroscelidea and lagomorphs; arrangement of whales (Cetacea) within a superordinal group including ungulates and their relatives but excluding carnivores. AI- 190 TABLE |.— Selected 20th century, higher-level ENGSTROM ET AL. classifications of extant mammals. Gregory, 1910 Class Mammalia Subclass Prototheria Order Monotremata Subclass Theria Infraclass Metatheria Order Marsupialia Suborder Diprotodontia Suborder Paucituberculata Suborder Polyprotodontia Infraclass Eutheria Superorder Therictoidea Order Insectivora Suborder Lipotyphla Order Ferae Suborder Fissipedia Suborder Pinnipedia Superorder Archonta Order Menotyphla [includes Tupaidae, Macroscelidae] Order Dermoptera Order Chiroptera Order Primates Superorder Rodentia Order Glires Suborder Duplicidentata [Lagomorpha] Suborder Simplicidentata [Rodentia] Superorder Edentata Order Tubulidentata Order Pholidota Order Xenarthra Superorder Paraxonia Order Artiodactyla Superorder Ungulata Order Sirenia Order Hyraces Order Mesaxonia [includes Perissodactyla] Superorder Cetacea Order Odontoceti Order Mystacoceti Simpson, 1945 Class Mammalia Subclass Prototheria Order Monotremata Subclass Theria Infraclass Metatheria Order Marsupialia Infraclass Eutheria Cohort Unguiculata Order Insectivora [includes Lipotyphla, Macroscelidae] Order Dermoptera Order Chiroptera Order Primates TABLE |.— Continued. Order Edentata Order Pholidota Cohort Glires Order Lagomorpha Order Rodentia Cohort Mutica Order Cetacea Cohort Ferungulata Superorder Ferae Order Carnivora Suborder Fissipedia Suborder Pinnipedia Superorder Protungulata Order Tubulidentata Superorder Paenungulata Order Proboscidea Order Hyracoidea Order Sirenia Superorder Mesaxonia Order Perissodactyla Superorder Paraxonia Order Artiodactyla McKenna, 1975 Class Mammalia Subclass Prototheria Infraclass Ormithodelphia Order Monotremata Subclass Theria Infraclass Tribosphenida Supercohort Marsupialia Supercohort Eutheria Cohort Edentata Order Cingulata Order Pilosa Cohort Epitheria Magnorder Ernothena Order Macroscelidea Order Lagomorpha Magnorder Preptotheria Grandorder Ferae Order Carnivora Grandorder Insectivora Order Erinaceomorpha Order Soricomorpha Grandorder Archonta Order Scandentia Order Dermoptera Order Chiroptera Order Primates Grandorder Ungulata Mirorder Eparctocyona Order Tubulidentata Order Artiodactyla Mirorder Cete Order Cetacea TAXONOMY 191 TABLE |.— Continued. Suborder Odontoceti Suborder Mysticeti Mirorder Phenacodonta Order Perissodactyla Order Hyracoidea Mirorder Tethytheria Order Proboscidea Order Sirenia Magnorder Preptotheria, incertae sedis Order Pholidota Cohort Epitheria, incertae sedis Order Rodentia Eutherian Mammals (Novacek, 1986) Subclass Theria Infraclass Eutheria Cohort Edentata Order Xenarthra Order Pholidota Cohort Epitheria Superorder Insectivora Order Lipotyphla Superorder Volitantia Order Dermoptera Order Chiroptera Superorder Anagalida Order Macroscelidea Grandorder Glires Order Rodentia Order Lagomorpha Superorder Ungulata Order Artiodactyla Order Cetacea Order Perissodactyla Grandorder Paenungulata Order Hyracoidea Mirorder Tethytheria Order Proboscidea Order Sirenia Cohort Epitheria incertae sedis Order Tubulidentata Order Carnivora Order Primates Order Scandentia Metatherian Mammals (Marshall et al., 1990) Subclass Theria Infraclass Metatheria Supercohort Marsupialia Cohort Ameridelphia Order Didelphimorphia Order Paucituberculata Cohort Australidelphia Order Microbiotheria Order Dasyuromorphia Order Peramelina Order Notoryctemorphia Order Diprotodontia though subsequent authors (e.g., Szalay, 1977) have disagreed with some of Mc- Kenna’s (1975) interpretations of characters and methodology, this paper set the stage for a dynamic reinvestigation of higher-lev- el relationships in mammals. Szalay (1977) examined phylogeny of eu- therian mammals based on largely on tarsal morphology. His resulting classification was derived both from the proposed genealogy and his view of “‘adaptational history.”” He supported some of the same groups as Mc- Kenna (1975), such as the Archonta, the association of the Macroscelidea and Lago- morpha, and the existence of an ungulate supergroup, but was not convinced of the early derivation of edentates. A more recent phylogeny and classifica- tion of eutherian mammals was proposed by Novacek (1986; Table 1), reconstructed using a large suite of skeletal and soft ana- tomical characters (although his cladograms were based on characters of the skull). Al- though far from fully resolved, this is the most explicit statement and defense of eu- therian superordinal relationships to date. Therein (Table 1), he supported McKenna’s (1975) early derivation of edentates (in- cluding pangolins—Pholidota) from other eutherians, an ungulate superorder, and the association of Macroscelidea with lago- morphs and rodents. He was, however, un- able to find support for Gregory’s (1910) Archonta (tentative justification for this group based on penial morphology and structure of the tarsus is given in Novacek and Wyss, 1986; Novacek et al., 1988, but see comments in Novacek, 1993). Perhaps the most radical recent change in the higher classification of mammals is the subdivision of marsupials into several or- ders (Aplin and Archer 1987; Marshall et al., 1990; Ride, 1964; Szalay, 1982; Table 1). In particular, the recognition of the South American Microbiotheridae as a member of the Australidelphia clade (Aplin and Ar- cher, 1987; Kirsch et al., 1991; Marshall et al., 1990; Szalay, 1982) is novel. The past 20 years have witnessed a re- 192 ENGSTROM ET AL. markable improvement in the state of our knowledge concerning higher classification of mammals, aided immeasurably by the for- mulation of explicit, falsifiable hypotheses of monophyly and evolution of character states. Thus, the statement by Ammerman and Hillis (1992:230) that, ““Mammalogists to- day have less confidence in the branching order of the 18 orders of mammals than they did 100 years ago” is overly pessimis- tic. Analyses of molecular data hold con- siderable promise in the resolution of sev- eral of the seemingly intractable problems of mammalian phylogeny and interordinal relationships (Czelusniak et al., 1990; Ho- neycutt and Yates, 1994; Miyamoto and Goodman, 1986). Examination of congru- ence (or the lack thereof) among molecular and morphological data sets, however, sug- gests that this promise has yet to be fully realized (Novacek, 1989, 1990; Novacek et al., 1988; Wyss et al., 1987). We cautiously agree with McKenna (1987:82), referring to the congruence of amino acid sequences and morphology: “As with all information, there is a mixture of signal and noise, ..., but the situation seems to be getting quieter [italics ours].” Faunal Surveys One of the natural outgrowths of taxo- nomic work on mammals has been pro- duction of catalogues of mammals occur- ring in circumscribed geographic areas. The best of these catalogues have been written by practicing taxonomists. For the most part, these catalogues were not compiled within a “biodiversity” framework; however, they form the basis of our knowledge of mam- malian diversity and geographic distribu- tion. Mammalian faunal surveys have deep roots reaching back to the 19th Century to such classics as Harlan’s (1825) Fauna Americana, Richardson’s (1829) Fauna Bo- reali-Americana, DeKay’s (1842) Zoology of New- York, and Audubon and Bachman’s (1846 to 1854) The Viviparous Quadrupeds of North America. The monumental classic of the era was Baird’s (1857) review of mammals of North America. This publi- cation preceded by 100 years the classic of the next century, The Mammals of North America, by Hall and Kelson (1959). Both monographs stimulated considerable addi- tional taxonomic studies and faunal sur- veys. Faunal studies in the 10 years following the establishment of the ASM included those of Goldman (1920) for Panama, Howell (1921) for Alabama, and Bailey (1926) for North Dakota. The number of “Mammals of...’ monographs showed a marked in- crease during the 1930s, the most notable by Bailey (1932, 1936) for New Mexico and Oregon, Grinnell (1933) for California, and Goodwin (1935) for Connecticut. However, a sign of things to come was the publication of the first faunal studies by two of Grin- nell’s professional progeny (Burt, 1938, So- nora; Davis, 1939, Idaho). The 1940s, like the 1930s, were characterized by publica- tion of an increasing number of faunal stud- ies, a few of the best known being those of Bole and Moulthrop (1942) for Ohio, Ham- ilton (1943) for the eastern U.S., Anderson (1947) for Canada, Burt (1948) for Michi- gan, and Dalquest (1948) for Washington. Also published during this period was Hall’s (1946) Mammals of Nevada, which set the standard for subsequent mammalian sur- veys. Relatively few faunal studies were pub- lished in the 1950s, the most important be- ing the classic Biological Investigations in Mexico, by Goldman (1951). Additional ex- amples were the state faunas and regional surveys by Cockrum (1952) for Kansas, Durrant (1952) for Utah, Dalquest (1953) for San Luis Potosi, Baker (1956) for Coa- huila, and Bee and Hall (1956) for northern Alaska. Noteworthy faunal studies during the 1960s were those of Jackson (1961) for Wisconsin, Baker and Greer (1962) for Du- rango, Alvarez (1963) for Tamaulipas, Hall and Dalquest (1963) for Veracruz, Jones (1964) for Nebraska, Long (1965) for Wy- oming, Peterson (1966) for eastern Canada, TAXONOMY EOS Villa-R. (1967) for Mexico, and Goodwin (1969) for Oaxaca. Some of the more im- portant of the large number of ““Mammals of ...” books produced during the 1970s were those of Armstrong (1972) for Colo- rado, Anderson (1972) for Chihuahua, Ban- field (1974) for Canada, Lowery (1974) for Louisiana, Findley et al. (1975) for New Mexico, Youngman (1975) for the Yukon Territory, and Schmidly (1977) for Trans- Pecos Texas. Faunal studies published dur- ing the 1980s included those of Mumford and Whitaker (1982) for Indiana, Baker (1983) for Michigan, Jones et al. (1983) for the Great Plains, Schmidly (1983) for east- ern Texas, Hoffmeister (1986, 1989) for Ar- izona and Illinois, Caire et al. (1989) for Oklahoma, and Merritt (1987) for Penn- sylvania. Coincident with the formation of the Mexican Society of Mammalogy (AM- MAC), there has been an increasing trend for locally produced faunal surveys and identification guides in Mexico over the last decade, a few examples of which include Ceballos and Galindo (1984) for the valley of México, Ceballos and Miranda (1986) for Chamela, Jalisco, Ramirez-Pulido et al. (1986) for Mexico, Aranda and March (1987) for Chiapas, Coates-Estrada and Es- trada (1986) for Los Tuxtlas, Veracruz, and Alvarez-Castaneda and Alvarez (1991) for Chiapas. These studies herald the burgeon- ing local interest and expertise in the region of highest diversity of mammals in North America, and we anticipate an increasing number of faunal surveys in Mexico over the coming decades. Acknowledgments We thank B. K. Lim for his assistance in com- piling historical data and producing the figures. Literature Cited ALVAREZ, T. 1963. 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LILLEGRAVEN Introduction Ne differences between neo- and pa- leomammalogy already existed as early as 1919, primarily because of the na- ture of the materials researched and the technologies that could be utilized. Even so, paleomammalogists have made major ad- vances toward a better understanding of mammalogy since the founding of the so- ciety. These contributions can be consid- ered under four areas: general, geological, biological, and a blending of the latter two. General advances include a significant in- crease in the number of individuals and in- stitutions working in paleomammalogy; a tremendous increase in the size of collec- tions, especially of smaller taxa, due to the development and modification of screen washing techniques; a better understanding of the fossilization process through tapho- nomic studies; and development of a com- prehensive bibliography. Geologically ori- ented advances include the use of improved biostratigraphic techniques, together with radiometric dating and magnetostratigra- phy, to increase our understanding of the sequential occurrence of mammalian fau- nas and decipher the complex geology of the highly deformed ranges and intermontane basins in the American West; and use of the plate tectonics model to explain biogeo- graphic distributions and patterns. Biolog- ically oriented advances include major im- provements in our understanding of the reptile-mammal transition and the defini- tion of ‘““mammal’’; important systematic studies of many mammalian taxa, using various taxonomic philosophies; and mul- titudinous studies of form, function, and phylogenetic relationships of particular groups of Cenozoic mammals. These have all been blended into important studies con- sidering the issues of tempo and mode in evolution and the cause of extinctions. Compartmentalization of Mammalogy By 1919, the discipline of mammalogy already had become compartmentalized into neo- and paleomammalogy. Osborn (1921), in the first article of Volume 2 of the Journal of Mammalogy, pointed out that paleo- mammalogists were constrained to dealing only with hard parts and, therefore, the types of studies that were undertaken usually were different from those of neomammalogists. 200 PALEOMAMMALOGY 201 However, he further suggested that there should be more standardization of terms and approaches to research problems in mammalogy, as well as cooperative studies between neo- and paleomammalogists for their mutual benefit. He cited, as an ex- ample, the work on rodents by Miller and Gidley (1918). Unfortunately, such collab- orations have been infrequent (e.g., Carle- ton and Eshelman, 1979; White and Keller, 1984). A classic exception is the work of the late John E. Guilday who, perhaps as well as anyone in this century, fused mammal- ogy and paleomammalogy (e.g., Guilday, 1971). The less-than-expected level of in- terchange between paleo- and neomam- malogists probably relates to a perception that the former still are constrained to studying only hard parts in a geological con- text, whereas the latter have even more av- enues and methods of study available to them now than existed 75 years ago. Also, geophysical advances of the 20th Century that are critically important to geologically oriented paleomammalogists often have ap- peared scientifically irrelevant to neomam- malogists. Perhaps advances in specialized technology themselves have led to wider gulfs between subdisciplines of mammalo- gy. Be that as it may, paleomammalogists have made major contributions to the gen- eral field of mammalogy, and a small sam- pling of these is considered below. Analogous to the dichotomy between neo- and paleomammalogists, there exists sig- nificant compartmentalization among pa- leomammalogists. The splits result, in part, from interest and training, but also stem from the use of fossils in approaching geo- logical versus biological problems. Some paleontologists (who might prefer to be called mammalian biostratigraphers) study fossil mammals principally to determine the age of enclosing sediments to solve strati- graphic or structural problems; paleomam- malogists sensu stricto, like neomammal- ogists, typically are more interested in anatomical and functional problems and evolutionary implications associated with fossils. Many paleontologists, however, have attempted to work in both areas. Before considering contributions made in these two areas, we briefly examine impor- tant developments of a general nature that have led to enormous benefit both within geologically and biologically oriented paleo- mammalogy. These include an increase in the number of paleomammalogists, tech- niques in collecting fossils, understanding how particular associations of fossils come to be, and the development of a compre- hensive bibliography. General Advancements A Slow Start for American Paleomammalogy When the ASM was founded in New York on 3 April 1919, there were only two major centers of mammalian paleontology in the United States. One at the American Mu- seum of Natural History, led by Henry Fair- field Osborn, William Diller Matthew, and Childs Frick, the other at the University of California, Berkeley, where John C. Mer- riam had built a program. About the time the ASM was founded, Merriam became president of the Carnegie Institution of Washington. He was among the charter members of the society, together with col- leagues from New York and the Smithson- ian Institution. Merriam and Matthew were two of the first council members of the so- ciety. Merriam also served on the first Anat- omy and Physiology Committee, together with William King Gregory of Columbia University and Alexander Wetmore and James W. Gidley of the Smithsonian Insti- tution. Matthew served as President of the society in 1926, the only paleomammalogist to have done so. Why there were so few centers of mam- malian paleontology as late as 1919 is not clear. Perhaps it was, in part, a legacy from the days of Cope and Marsh, when the 1m- 202 ZAKRZEWSKI AND LILLEGRAVEN petus was for the collection of large reptiles from Mesozoic deposits of the American West. This tendency extended into early parts of the 20th Century with collections made by Earl Douglass for the Carnegie Mu- seum in Pittsburgh and the Sternbergs for various Canadian institutions. Many of the paleontologists in the first quarter of the 20th Century were interested principally in lower vertebrates rather than mammals. In marked contrast, there exist today in North America about 120 institutions in which individuals perform research on fossil mammals; esti- mating conservatively, at least 20 of these research centers must be considered major. Such increase in interest since 1919 must, in itself, be considered a huge advance in American paleomammalogy. Finding the Tiny Philip D. Gingerich (1986), in lamenting the demise of the paleontology program at his alma mater, aptly showed that theoret- ically oriented paleontology depends upon extensive personal experience based, in turn, upon a solid data base. For all paleontolog- ical endeavors, the fundamental objective elements of data are the fossils themselves, set within geological contexts. Early collec- tors of fossil mammals, perhaps influenced by their predecessors’ searches for dino- saurs, selectively looked for sites with ac- cumulations of large mammals. Although small mammals certainly were not inten- tionally ignored, quarrying techniques em- ployed by many early collectors were not conducive to discovery of minuscule fossils. A “fossil” to many of these individuals had to be at least six inches long, preferably bearing teeth. A change in attitude began about a decade after the founding of the ASM. In 1928, Claude W. Hibbard (a future director of the ASM) was hired as cook and camp caretaker for a field party from the University of Kan- sas led by Handel Tong Martin. The crew was returning to Edson Quarry (late Mio- cene, Sherman County, Kansas) for another summer of collecting. During the previous summer, Martin had found some fossil sal- amander bones and was asked to collect ad- ditional remains by an anatomist who was interested in studying the group. When Hib- bard went to the quarry, after finishing camp chores, Martin greeted him with a pair of tweezers and told him to collect all the small bone he could find on the spoil pile. Hibbard soon decided to expedite matters. Obtaining some window screen from the local rancher, he attached the screen to a wooden frame to produce a little box. Loose sediment from the spoil pile passed easily through the screen and the fossil bone was trapped by it and picked out. Hibbard thought he might hurry the process even more by the use of water. Thus, he took the sediment and his box to a nearby buffalo wallow and proceeded to agitate the box in the water. Within a few days, he had enough small material to fill a large matchbox. When Hibbard showed the material to Martin, the latter stated that there were enough small specimens in the box to keep paleontologists occupied for years. De- spite the innovation, Hibbard spent the re- mainder of the summer in the quarry, help- ing Martin collect “real” (1.e., large) fossils. Subsequently, Hibbard (1949) expanded on the washing technique and used it to accumulate tens of thousands of specimens from southwestern Kansas and northwest- ern Oklahoma. Thereby, he was able to doc- ument a sequence of faunas that reflected both phylogenetic and climatic change (Bayne, 1976; Zakrzewski, 1975). Subse- quent workers (e.g., McKenna, 1962) have modified the technique for massive collec- tion of fossils from other areas and ages. An example of the importance of widespread use of screen-washing techniques is the in- crease in our knowledge of Mesozoic mam- mals. When George Gaylord Simpson (1928, 1929) published his comprehensive sum- mary of known Mesozoic mammals (based, in part, on his Ph.D. thesis), he worked with PALEOMAMMALOGY 203 fewer than a thousand specimens, collected by standard quarrying from around the world. When William A. Clemens, Jr. (1963, 1966, 1973) and Jason A. Lillegraven (1969) published their Ph.D. theses on latest Cre- taceous mammals, their specimens from only two local faunas numbered well into the thousands. Mammalian paleontology in North America, especially dealing with the Mesozoic, was never quite the same again. As Simpson (1971) stated, it “would not be possible now, as it was in 1871, 1888, and 1928-1929 for one person to treat all avail- able material on Mesozoic mammals... .” Grasping the “How” of Fossil Accumulations Most workers are painfully aware of im- portant biases in the fossil record. Before useful scientific inferences can be drawn from paleontological data, one needs to know how the fossils themselves accumu- lated. Although inadequacies and biases in the fossil record have been appreciated for many years (e.g., Darwin, 1859), it has been only relatively recently that formal study of the process of fossilization (i.e., taphonomy) has been undertaken on a large scale. The majority of early taphonomic work was by the Russians, applied to faunas of lower ver- tebrates (Olson, 1980). Perhaps the seminal work in North America for explaining the occurrences of accumulations of large mam- mals is that of Michael R. Voorhies (1969) on the Verdigre Quarry in northeastern Ne- braska. Subsequent work by Anna K. Beh- rensmeyer and her colleagues (e.g., Beh- rensmeyer and Hill, 1980) have added much to the understanding of how deposits of fos- sil mammals might accumulate. James S. Mellett (1974) demonstrated that many mi- cromammal accumulations result from owl predation, a mechanism suggested earlier by Hibbard (1941). Subsequently, problems of origin of microvertebrate fossils have been addressed by various workers, such as Dod- son and Wexlar (1979) and Korth (1979). The subdiscipline of taphonomy is only in its infancy relative to understanding asso- ciations of fossil mammals. Unique Research Tool The development of a unique biblio- graphic research tool cannot be omitted from discussion of 20th Century progress in pa- leomammalogy; we refer to the Bibliogra- phy of Fossil Vertebrates (BFV) (Gregory et al., 1989, plus predecessor volumes involv- ing various editors, including Charles L. Camp). The BFV is published by the Society of Vertebrate Paleontology (which shares a large membership with the ASM), and pro- vides unparalleled, annual access to the breadth of world literature on fossil mam- mals. Geologically Directed Paleomammalogy Toward a More Useful Time Scale Original versions of the geologic time scale were developed using the law of superpo- sition in combination with the stage of evo- lution of marine invertebrates, mostly in- volving European rock sequences. Some of the sequences could be correlated with those in North America using marine inverte- brates. Where American continental and marine deposits interfingered, there was lit- tle problem in placing the terrestrial units into a scheme of relative chronology. How- ever, as workers moved on to the High Plains and into the structurally isolated intermon- tane basins of the American West, many mammal-bearing nonmarine stratigraphic units could not be placed easily into context within the standard time scale. As mam- mals often were the most abundant fossils in these strata, early workers sometimes named deposits after the most common 204 ZAKRZEWSKI AND LILLEGRAVEN kinds. Names such as the Equus beds of Kansas and the Titanotherium and Oreodon beds of South Dakota were established. These ill-defined units were assigned to Eu- ropean-based Tertiary epochs through com- parative estimation of the stage of evolution of contained mammals. This procedure of- ten involved litthe more than guesswork, however, and it ultimately led to wide- spread misconceptions in correlation. All but one of the standard Tertiary epochs were based on marine fossils, and few North American continental deposits could be su- perpositionally related to marine strata. Clearly, a new method for dating and correlating the North American mammal- bearing continental units had to be devel- oped, independent of the standard Euro- pean marine sequence. Eventually, a committee was established to devise such a time scale independent of the marine standard. Work of the ‘““Wood Committee” led to the development of the North American Land-Mammal Ages (NALMAs; Wood et al., 1941), as reviewed by Hesse (1941). NALMAs were defined principally on the first occurrence of certain genera and the unique occurrences or con- sistent associations of others. Although last occurrences also were considered, these usually were given less weight because of potential complications to correlation re- sulting from relictual taxa. The original NALMAs applied only to Tertiary time. Subsequent to work by the Wood Com- mittee, Savage (1951) established the Ir- vingtonian and Rancholabrean NALMAs for the Pleistocene. Although all NALMAs originally were intended to be independent of the Lyellian, European-based Tertiary epochs, NALMAs inevitably became al- most synonymized with Lyellian epochs in the minds of geologists and paleontologists alike. Such mental linkages (e.g., Bridgerian = middle Eocene; Chadronian = early Oli- gocene; etc.) have proven highly unfortu- nate in the history of North American geo- logical research, being a source of much confusion in temporal correlation between vertebrate paleontologists and traditional geologists. Gradually, however, expanded use and reliability of radioisotopic dating techniques (starting most importantly with the pioneering work of Evernden et al., 1964), in conjunction with data from fossil mammals has increased markedly the reli- ability of temporal correlation between North American nonmarine sequences and other parts of the world (see Savage and Russell, 1983). In 1973, asymposium on Vertebrate Pa- leontology and Geochronology was held in Dallas at the annual meeting of the Geo- logical Society of America. One outcome of the symposium was re-establishment of committees to refine the various NALMAs. After much trial, tribulation, and delay, their work resulted in publication of Cenozoic Mammals of North America, Geochronol- ogy and Biostratigraphy (edited by Wood- burne, 1987). The use of mammals for biostratigraphic purposes reached its acme in the decipher- ing of the complex Cenozoic history of mountain ranges and intermontane basins in western North America. Beginning late in the Cretaceous and continuing to the present time, most of this area has been subjected to major tectonism. Large seg- ments of the continental crust experienced important displacement, both horizontally and vertically. Erosion of zones of defor- mation provided sediments that accumu- lated to prodigious thicknesses 1n the inter- montane basins. Mammalian assemblages, involving all Cenozoic NALMAs, have proven to be of outstanding utility in the relative dating of structural and deposition- al histories of western North America. Per- haps there exist no better examples of the marriage between paleomammalogy and historical geology than the various works of Galusha and Blick (1971), Dorr et al. (1977), Skinner et al. (1977), and Wilson (1978). Mobile Continents and Oceanic Basins The advent of plate tectonics in the late 1960s had a profound effect upon American PALEOMAMMALOGY 205 paleomammalogy of the 20th Century. As imaginatively summarized by McKenna (1973, 1983), general recognition that major plates across the surface of the earth were mobile (and, by way of seafloor spreading, subduction, and collision, could change in shape and size through geologic time) rev- olutionized the discipline of historical bio- geography. The geological impact of plate tectonics upon historical biogeography can, without exaggeration, be compared to the importance of Darwinism within the bio- logical sciences. It is certainly true that the two editions (1915, 1939) of Matthew’s Climate and Evolution established the foundations of modern historical biogeography. Significant additional refinements in principles were provided by Simpson (e.g., 1952, 1953a). Further, influences on evolutionary thought of continental stabilist biogeographic view- points issuing from these two eminent American paleomammalogists were pro- found. Both workers had developed con- vincing biogeographical interpretations (principally involving fossil mammals) that seemingly did not require mobilized con- tinents, especially for geologic intervals as young as the Cenozoic. In essence, it took independent devel- opment and observational application of new techniques in geophysics (especially pa- leomagnetism) to shake the American com- munity of geoscientists into accepting the reality of highly mobile continents (and ac- tively evolving oceanic basins). Interesting- ly, much of the European community of paleontologists had accepted various forms of continental drift far in advance of most Americans, even though all proposed phys- ical mechanisms seemed inadequate for purposes of explanation. Once geophysical- ly established, however, American paleo- mammalogists jumped solidly onto the plate-tectonic bandwagon, and continental mobilism has been a fundamental compo- nent of their training and research ever since. Further, it has been accepted that plate tec- tonics is highly relevant in explaining dis- tributional patterns of particular groups of Cenozoic mammals, such as marsupials (e.g., Tedford, 1974; Woodburne and Zins- meister, 1984), and even of wholesale con- tinental exchanges (e.g., Dawson, 1980; Webb, 1985). Along with acceptance of a continental mobilistic perspective came appreciation of a whole series of new possible mechanisms (in supplement of Simpsonian corridors, fil- ter bridges, and sweepstakes routes) for ex- planation of geographic distributions of suites of fossils. Some processes involved passive transport of already-fossilized as- semblages (e.g., the “grounded Viking fu- neral ships” of McKenna, 1983), but most were pertinent to ancient groups of organ- isms at times during which they were still alive (e.g., continental ““Noah’s arks”’ of Mc- Kenna, 1973: ‘‘escalator counterflow,”’ ‘hopscotch on the escalator,” and ““voyages to nowhere and return” of McKenna, 1983). As occurs all too often in the case of real progress in scientific understanding, recog- nition of the possibility of several of these cited mechanisms also has served to com- plicate interpretations of historical bioge- ography, especially in situations involving archipelagos. Biologically Directed Paleomammalogy So What Is a Mammal? If one studies only modern-day elements of earth’s biota, mammals can be differen- tiated easily from all other vertebrate groups. As one traces the paleontological history of Mammalia back into the middle Mesozoic, however, one-by-one the usual features used to define what a mammal /s appear in more and more primitive stages, becoming blurred to generally non-mammalian in therapsid ancestors. As a result, paleomammalogists, much more than neomammalogists, have given attention to definition of the Mam- malia, and to questions of phylogenetic re- lationships within the class. One result of such effort is an interesting paradox. On the 206 ZAKRZEWSKI AND LILLEGRAVEN one hand, the reptile-mammal (or perhaps better, the therapsid-mammal or cyno- dont—mammal) transformation is better un- derstood anatomically than any other in- terclass transition within the Vertebrata. But, in contrast, and in large part because of the deadly combination of great Triassic diver- sity, extensive parallel evolution in many features, and a generally spotty Mesozoic fossil record, the phylogenetic path(s) from therapsids toward mammals is (are) ex- ceedingly uncertain (compare results, for example, among Crompton and Sun, 1985; Hopson and Barghusen, 1986; Miao, 1991; Rowe, 1988). Paleomammalogy and Systematics Most of the early paleomammalogists were typologists. Each morphological vari- ant seemed to demand at least a new specific (if not generic) name. Likewise, it seemed that scientific reputation and prestige for some workers was directly proportional to the number of taxa described and named. A classic example of this situation was pro- vided by E. D. Cope when he named the arvicoline genera Anaptogonia and Sycium. Anaptogonia, originally considered a sub- genus of Arvicola (Cope, 1871), was based primarily upon mls of the taxon, whereas Sycium was based on upper teeth (Cope, 1899). Subsequently, Hibbard (1947) dem- onstrated that these two taxa were junior synonyms for the modern muskrat, Ondat- ra. Fortunately, a major advance within pa- leomammalogy during the 20th Century has been to step away from typological ap- proaches to science. As the flood of newly discovered fossils accumulated in museums, and as masses of data became available from new and di- verse fields of biological science (e.g., pop- ulation genetics), workers in the 1930s and 1940s tried to integrate all aspects of the study of life, as dubbed the ‘“‘new synthesis.” Particularly important parts of this integra- tion were publication by Simpson of Tempo and Mode in Evolution (1944) and The Ma- jor Features of Evolution (1953b). The sem- inal paper on mammalian interrelation- ships 1s The Principles of Classification and a Classification of Mammals by Simpson (1945). Compiled before WW II, Simpson’s classification dealt with every mammalian genus known to him, taxonomically utiliz- ing the philosophy of the new synthesis. A rationale of his approach to the classifica- tion of mammals was presented at the 24th annual meeting of ASM at the American Museum of National History, and the work was reviewed in the Journal of Mammalogy by E. Raymond Hall (1946). Although in many places outdated, Simpson’s work re- mains an invaluable taxonomic reference; a more detailed compendium has yet to be published. Toward that end, however, McKenna (1975) has updated information for a com- prehensive revision of mammalian taxon- omy, with development of elaborately an- notated computer files. McKenna (1975) provided a first approximation of this mon- umental work, using cladistic philosophy as developed by Willi Hennig (1966). Mc- Kenna’s tentative classification remained above the level of family, and involved many new taxonomic terms that have not been readily accepted by the professional com- munity. Cladistics as a taxonomic philosophy is being used increasingly by paleomammal- ogists as seen in a recent special volume by the Systematics Association edited by Ben- ton (1988). A more detailed discussion of the cladistic method can be found in Eng- strom et al. (1994). Additional synthesis by attempting to combine morphological and molecular studies in the phylogeny of mam- mals can be found in the volumes edited by Szalay et al. (1993). Knowledge of the First Two-thirds of Mammalian History Tremendous strides have been made dur- ing the 20th Century in documentation of Mesozoic mammals. Because few Mesozoic mammals have yet proven their potential PALEOMAMMALOGY 207 worth as biostratigraphic tools, most re- search on them has been taxonomic or of generally biologic nature. Published re- search on systematic paleontology of Me- sozoic taxa 1S expanding at an astounding rate (e.g., Cifelli, 1990; Clemens, 1973; Fox, 1989), to the point that necessity for taxo- nomic and stratigraphic specialization in study of Mesozoic mammals has become a reality, as has long been the case for Ce- nozoic forms. Additionally, major features in the origin of tribosphenic molars have been worked out (e.g., Crompton, 1971): serious attempts have been made at deter- mining origins of mammalian metabolic pathways (e.g., McNab, 1978); and even study of major steps in Mesozoic mam- malian reproduction (e.g., Blackburn et al., 1988) have been approached. Cladistic methodology has figured importantly with- in comparative studies of detailed anatomy of Mesozoic mammals (e.g., Wible and Hopson, 1993), largely in pursuit of phy- logenetic analysis. Diverse forms of re- search (biological and geological) on Me- sozoic Mammalia hold promise for an unusually bright future. Unparalleled Expansion of New Biological Information on Cenozoic Mammals The extent of increased knowledge made available since 1919 on comparative anat- omy, biological function, paleogeographical distribution, and evolutionary relationships among Cenozoic mammals is no less than astounding. Whole new disciplines of pa- leobiological research, such as paleoneurol- ogy (e.g., Edinger, 1948; Jerison, 1973; Ra- dinsky, 1981), have come into existence. Major paleogeographic surprises, such as the discovery of North American pangolins (Emry, 1970), have occurred. Documenta- tion of highly specialized adaptive realms for mammalian life, such as origin of pow- ered flight (e.g., Jepsen, 1970; Novacek, 1987) or entry into the sea (e.g., Barnes et al., 1985; Domning et al., 1986; Kellogg, 1936; Repenning et al., 1979) has become available. Functional studies, varying from mech- anisms of mastication (e.g., Krause, 1982) to origins of arborealism (e.g., Jenkins, 1974) to recognition of the importance of body size in ancient mammals (e.g., Damuth and MacFadden, 1990), have burgeoned. Fi- nally, at least rough phylogenetic frame- works have been established for most mam- malian orders (e.g., Gazin, 1953; Novacek, 1990; Prothero and Schoch, 1989; Schoch, 1986; Simons and Kay, 1983; Wilson, 1986; Wood, 1955). Unquestionably, the greatest diversity and absolute volume of research in 20th Century paleomammalogy has been in the documentation of form, function, and phylogenetic relationships of particular Ce- nozoic taxa. The Blending of Geologically and Biologically Directed Paleomammalogy Tempo and Mode in Evolution Paleomammalogy can provide unique in- formation that is of key importance to the research of neomammalogists. Obvious ex- amples include paleobiogeographic histo- ries and minimum dates of evolutionary di- vergence of particular taxa. Potential for such useful applications has been recog- nized since the origin of paleontology as a science. More recently, however, new kinds of evolutionary inquiry have resulted from the blending of procedural advances de- rived jointly from the geological and bio- logical sciences. A few examples follow. Rates and mechanisms of evolutionary change involve questions that have in- trigued scientists since the appearance of Charles Darwin’s (1859) The Origin of Spe- cies. For nearly a century after its publica- tion, however, most questions remained vaguely posed, with little real progress being made toward understanding the detailed na- ture of evolutionary modification. Principal 208 ZAKRZEWSKI AND LILLEGRAVEN underlying reasons involved an inadequate- ly documented fossil record combined with infancy of the science of genetics. Both areas were strengthened during the first 40 years of the 20th Century, setting the stage for the ‘new synthesis.” It was in large part the greatly improved fossil record of mammals, developed through literally centuries of man- years of field and laboratory effort, and ex- ploited by Simpson (1944, 19535), that allowed integration of paleontological knowledge with paradigms derived from advances in population genetics. Better doc- umentation of morphological change through geologic time, as based on detailed studies of fossil mammals, allowed greater scientific focus on tempos of evolution. Simpson demonstrated, for example, that rates of mammalian evolution varied with- in and among taxa. He also noticed that paleontologically recognizable change oc- curred in spurts and starts, separated by what appeared to be extensive intervals of mor- phological stability. Simpson was a firm be- liever, however, in the essential gradualness of evolutionary change, and attributed much of the apparent irregularity in rates to strati- graphic and geographic imperfections and biases within the fossil record. More recently, questions of tempo and mode in evolution have been reconsidered by Eldredge and Gould (1972), using a more literal interpretation of the fossil record. They suggested that the apparent stasis within species, and the paucity of transi- tional forms between species, are real, and represent ways in which the allopatric mod- el of speciation would be expected to be reflected in the fossil record. Because of the apparent sudden appearance of new species in local stratigraphic columns above long sections of morphological stasis, they coined the term “‘punctuated equilibrium”’ for their concept. Although their suggestion origi- nally attempted to reconcile the fossil record with the concept of allopatric speciation, they expanded it subsequently to include other features as well, such as the restriction of virtually all evolutionary change to the process of speciation (Gould, 1985; Gould and Eldredge, 1977). The punctuated equil- ibrists have been opposed by many neo- Darwinists (e.g., Bown and Rose, 1987; Gingerich, 1985), who demonstrated strat- igraphically controlled gradual change be- tween mammalian species in the fossil rec- ord; such workers have come to be known as phyletic gradualists. Yet a third group reached a compromise position, suggesting that both patterns have operated, as already had been suggested in some cases by earlier workers (see Newman et al., 1985). Issues involved in the debate cited above were summarized by Barnosky (1987), who examined results of various studies on Qua- ternary mammals. He pointed out that the Quaternary should be an ideal geologic in- terval for the testing of competing models because both time- and species-resolution are highly determinable, at least compared to the Mesozoic or Tertiary. Case-histories cited by Barnosky (1987) demonstrate that some species transitions appear to follow patterns of punctuated equilibrium, where- as others seem to fit more closely models of phyletic gradualism. No matter where the truth eventually may be shown to lie, all of these highly focused studies have depended upon elevated standards of detailed, strat- igraphically documented collections made in the field at levels of thoroughness only imagined even when the new synthesis was being developed. The Spectre of Heterochrony in Homotaxy Huxley (1870) recognized the spectre of heterochrony [i.e., “temporal overlap of as- semblages assigned to successive, presumed non-overlapping ages, or assemblages as- signed to the same age being time trans- gressive or not precisely time-equivalent” (Flynn et al., 1984)]. Huxley (1870) also ap- preciated that the possibility of heterochro- PALEOMAMMALOGY 209 ny cannot be eliminated through applica- tion of standard paleontological techniques alone. Wisely, he suspected that fully ho- motaxic faunas (i.e., taxonomically identi- cal assemblages), even when using the most closely spaced, stratigraphically controlled fossil collections, in reality, might be asyn- chronous. Therefore, it is possible that when comparing identically changing taxonomic assemblages between geographically sepa- rated areas, the usual assumption of syn- chrony of the assemblages may be incorrect. Instead, the geographically separated but homotaxic faunas may, for example, have been tracking, through time, shifting eco- logical regimes. Needless to say, anyone en- deavoring to study the tempo and mode of evolutionary change must be able to rec- ognize absolutely that no significant asyn- chrony exists between geographically sep- arated, homotaxic faunal assemblages. As discussed by Flynn et al. (1984), two recent advances from the geological sciences pro- vide capabilities, not available in the days of Huxley, to better evaluate the possibili- ties of heterochrony. One advance involves detailed study of the record of polarity reversals of earth’s magnetic field through orientation of fer- romagnetic minerals in individual fossil lo- calities (e.g., Lindsay et al., 1981). When polarity data are used in combination with other, independent dating techniques, it 1s often possible to identify particular brief in- tervals of earth’s magnetic polarity history. The other advancement has been with ra- dioisotopic dating, of which a multiplicity of suitable isotopes and variations in tech- niques is now known to exist. One particular variant that is especially promising for ap- plication to pre-Pleistocene, mammal-bear- ing units is the single-crystal, laser-fusion method, involving isotopes of argon (Swisher and Prothero, 1990). Through combination of detailed paleontology, mag- netostratigraphy, and high-resolution ra- dioisotopic dating, it is possible (Flynn et al., 1984) to recognize the existence of geo- graphic migration of ‘“‘age-defining” taxa through geologically significant intervals of time; however, no entire land-mammal fau- na has yet been shown to be heterochronic. The Nature of Extinction The phenomenon of extinction has in- trigued scientists since its possibility was first proposed by Hooke in the 1670s (Dott and Batten, 1971). Although extinctions have occurred throughout the history of life, the times of major (or mass) extinctions, reputedly concentrated at major geologic boundaries, have received the most atten- tion. Most of the recent study on extinctions by North American paleomammalogists has been on those in the proximity of the Cre- taceous/Tertiary (K/T) and Pleistocene/ Holocene (P/H) boundaries. In both cases, the majority of paleomammalogists has fa- vored a conservative (i.e., rather gradual- istic) point of view in explaining the ex- tinctions; others, however, have suggested more dramatic scenarios. A catastrophic perspective for the K/T boundary was presented initially by Alvarez et al. (1980), involving a presumed impact with earth of a major extraterrestrial body, probably an asteroid. Over the following de- cade, a variety of independent geological and paleontological evidence has been mar- shalled in support of the impact theory (see Izett, 1990). In simplest terms, the putative impact led to a kind of “nuclear winter” caused by fine-grained debris hurled into the atmosphere, initiating a complex series of events that essentially ended, through ex- tensive marine and terrestrial extinctions, the unique biota that was characteristic of late Cretaceous time. Most vertebrate paleontologists, in con- trast, have been unconvinced. Archibald and Bryant (1990), for example, have examined the entirety of the extensive vertebrate fau- nas (including aquatic, semiaquatic, and terrestrial species) as stratigraphically rep- 210 resented below, at, and above the presumed K/T boundary of northeastern Montana. This is the world’s only nonmarine section at which a detailed analysis of faunal change across the K/T boundary has been com- pleted. Observed faunal changes across the boundary not only run contrary to ecolog- ical predictions for the effects of a nuclear winter but, according to Archibald and Bry- ant, are not even necessarily consistent with environmental catastrophy. They suggest the possibility of a more protracted interval (in- volving various extinctions and replace- ments). Such change could have been allied, for example, to alteration of habitat across the broad, latest Cretaceous coastal plain, resulting from retreat from North America of the Western Interior Seaway. One suggested explanation of extinctions near the P/H boundary is that of overkill by invading humans (e.g., Martin, 1984). Chief evidence, at least in the Americas, involves the correlation, supported by ra- diometric dates, of extinctions of large un- gulates (and their contemporaneous pred- ators) with the first appearances of Man. Many archaeological sites across Eurasia and North America unequivocally document the prowess of late Pleistocene Man as a hunter, even of the largest contemporary mammals. The idea of Man as the principal culprit in P/H extinctions has not, however, en- joyed unanimous acceptance, and all inter- gradations of viewpoints exist. Some work- ers have been willing to accept certain limited extinctions as having resulted from human overkill (principally through habitat destruction), particularly on oceanic is- lands. Widespread avian extinctions, for ex- ample, are well documented in the Hawai- ian Islands (James et al., 1987) in association with arrival of the original Polynesians and their various commensals. Other workers (see Martin, 1967 for citations), in contrast, simply have found it difficult to accept the demise of vast herds of North American Pleistocene mammals at the hands of Man. This is especially true in light of the long coexistence of Man and mammalian mega- ZAKRZEWSKI AND LILLEGRAVEN faunas across Eurasia and Africa during all of Quaternary time. As presumed for the K/T boundary, many workers have suggested that habitat changes were responsible for extinction of the latest Pleistocene megafaunas. Although evidence associated with local habitat (or global cli- matic) change may not be obvious for the latest Pleistocene, it is clear that climates became cooler overall and more seasonal in the interior through the latter half of the Cenozoic. Such changes caused dramatic shifts in distributions and types of plant communities. For example, Webb (1983) demonstrated changes in dominance of North American ungulates from browsing to grazing forms during late Miocene time. Workers such as Guthrie (1984) suggested that climatic changes accounting for the Miocene shift continued into Plio—Pleisto- cene time, thereby ultimately decreasing the net annual quality and quantity of food re- sources available to the megafauna. Gra- ham and Lundelius (1984) suggested biotic disequilibrium as a possible reason for late Pleistocene extinctions. In any case, no matter how the physical evidence itself may be interpreted, mar- riages among detailed biostratigraphy, mag- netostratigraphy, radioisotopic dating, and even archaeology have led to greatly im- proved levels of focused inquiry associated with questions of causation in extinction. At least for the late Pleistocene and early Holocene, the levels of precision in dating made possible by '*C-technology have reached levels that make such age deter- minations of true relevance of biological considerations of extinction. Epilogue We have summarized what we consider to be a broad sampling of major contribu- tions by paleomammalogists to the field of mammalogy since the founding of the ASM 75 years ago. Many of these advancements PALEOMAMMALOGY 2a have occurred in the last 25 years as new technologies, philosophies, and more work- ers have entered the field. As technologies continue to improve, philosophies mature, and information expands, we look forward to the spectacular additional progress that surely will be documented in the Centennial Volume of the society. Acknowledgments We thank B. H. Breithaupt, J.-P. Cavigelli, R. W. Graham, L. E. Lillegraven, and R. W. Wilson for their help in the preparation of this manu- script. We thank W. A. Clemens, Jr. and M. R. Voorhies for their critical reviews. Literature Cited ALVAREZ, L. W., W. ALVAREZ, F. ASARO, AND H. V. MicHEL. 1980. Extraterrestrial cause for the Cre- taceous-Tertiary extinction. Science, 208:1095-1108. ARCHIBALD, J. D., AND L. J. 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Hibbard Memorial Volume 3), 143 pp. BIOGEOGRAPHY SYDNEY ANDERSON AND BRUCE D. PATTERSON Introduction | Beary the study of the distribu- tion of life, seeks to comprehend an immense range and diversity of phenome- na. Most broadly conceived, the field ranges from the domain of astrophysics (the dis- tribution of matter in the universe and the physical laws of radiation, gravitation, and others which affect this) to ecological and behavioral interactions that govern the spa- tial distribution of individuals within local demes. For the purposes of this brief his- torical review, and in parallel with editorial opinion in biogeographic journals (see Blondel, 1987), however, we consider bio- geographic patterns and processes ranging from global climates and drifting continents on the one hand to local communities and species responses at distributional limits on the other (e.g., Reichman, 1984). Concep- tually, at least, our coverage transcends the fields now known as historical biogeography and landscape and geographical ecology, al- though space limitations preclude detailed treatment of all aspects. Biogeographic patterns and processes are sensitive to variations in time, space, and biological organization. These patterns and processes may be categorized according to the scales of these crucial factors. ““Ecolog- ical’’ time-periods may be contrasted with 215 a x on : ” an oS At a Bee ar @ 4 ie “evolutionary” ones—the former denotes the years, decades, and centuries over which ecological processes, such as dispersal, suc- cession, altered resource-use patterns, and others take place. Evolutionary time peri- ods may involve different types of organ- ismal responses, including changing gene frequencies, local adaptation and genetic drift, and speciation. In similar fashion, processes that operate over local spatial scales differ from those involved in larger (regional or continental) patterns. Finally, the processes of environmental stimulus and organismal response are mediated in fun- damentally different ways by species pop- ulations (through the genetics of reproduc- tion and adaptation) and biotas (through competition, predation, and other com- munity-level processes). We attempt here to chronicle the devel- opment of mammalian biogeography over the last 75 years. After considering some trends that generally apply to all biogeo- graphic subdisciplines, we use the different scales of time, space, and biological orga- nization to organize our discussion of var- ious topics. We first treat studies of species over ecological time, proceeding then to those on biotas (but emphasizing mam- malian faunas) over ecological time, species 216 ANDERSON AND PATTERSON over evolutionary time, and faunas over evolutionary time. Within each unit, we have attempted to arrange patterns and pro- cesses in order of increasing spatial scope. Historical Trends By 1919 the discipline of biogeography was already vigorous and well established. That different plants and animals lived in different places was known in classical times, but elaboration and formalization of that recognition increased dramatically in the three centuries before the founding of the American Society of Mammalogists. Im- portant contributions were made by early 19th Century workers, including von Hum- boldt and Bonpland, de Candolle, and Lyell (see Nelson, 1978). Sclater’s (1858) classi- fication of the world’s avifauna into bio- geographic regions and subregions ranks as a major biogeographic development of the 19th Century. This work, and the burgeon- ing inventories of worldwide faunas assem- bled by imperial Europe, permitted Lydek- ker (1986) to develop a strikingly accurate discussion of regionalism in mammalian faunas. The life-zone concept of Merriam (1890) was another major event, at least for understanding the ecological factors that af- fect the distribution of North American mammals. In addition, under Merriam’s leadership, the U.S. Biological Survey had produced a growing series of taxonomic re- visions and regional faunal accounts that were published mainly in the North Amer- ican Fauna series—43 numbers had been published by 1919. Based on copious col- lections, many of these accounts included detailed distribution maps of species, veg- etation types, and finally formal “life zones.” Moreover, they contributed importantly to the developing polytypic species concept, with its explicit recognition of geographic variation, and thence eventually to the *““modern synthesis” of evolutionary theory. Just before the founding of the society, Mat- thew’s (1915) Climate and Evolution was published, postulating the northern origin and southward dispersal of many mammalian groups; Matthew’s thesis emphasized the im- portance of history in interpreting biogeo- graphic patterns. This paper had consider- able influence on mammalian biogeography, in significant part through the work of his student G. G. Simpson. However, some of the details and major assumptions in Mat- thew’s five-point thesis have required mod- ification. A more enduring contribution to this field was Wegener’s hypothesis of drifting con- tinents, originally presented in 1912. This revolutionary hypothesis was soundly re- jected by Matthew and many other mam- malogists, and its revival required the pas- sage of half a century and the discovery of a geophysical mechanism, plate tectonics, to allow drift. Since the founding of the ASM, a number of trends are discernable in the development of biogeography. Simple, general patterns were dissected to reveal more complex ones. Emphases shifted from purely descriptive accounts to increasingly quantitative and predictive ones. Models of biogeographic processes were developed, initially static and then increasingly more dynamic in char- acter. Some of these trends have long been evident—in a mid-century appraisal, Hubbs (1958:470) noted “‘a shift from the classical, purely descriptive biogeography to a kinetic approach, which is more concerned with processes and explanations than with the classification of the earth into a hierarchy of biogeographical regions.” As biogeography matured, gains in ana- lytical rigor have been achieved, sometimes at the expense of flexibility and breadth. In its infancy, biogeography had spanned all or most of natural history, but as it matured, rival schools developed around narrower concepts (e.g., island biogeography) or ap- proaches (e.g., numerical biogeography). Biogeographers were themselves classified as champions of dispersal or vicariance, or devotees of equilibrium or historical schools. Even finer distinctions were thought nec- essary to reflect philosophical differences BIOGEOGRAPHY 217, within these categories (e.g., vicariance bio- geography, phylogenetic biogeography, and panbiogeography). For the most part, bio- geographic discords reflected parallel acri- mony in the sister disciplines of systematics and ecology, which also experienced philo- sophical and technological revolutions dur- ing the 1960s and 1970s (Hull, 1988; Mc- Intosh, 1985). Perhaps because extended critical discussion has exposed the short- comings of each approach, biogeography to- day is best carried out under a banner of pluralism (McIntosh, 1987). Species Over Ecological Time Periods How is the distribution of a species re- lated to its abundance? This relationship was explored, mostly from an ecological per- spective, by Andrewartha and Birch (1954). The thesis of the book is that “distribution and abundance are but two aspects of one phenomenon.” The book is replete with biogeographical implications. They showed that common species may be rare in mar- ginal parts of their ranges and that there is no fundamental distinction between the ex- tinction of a local population and the ex- tinction of a species except that, in the latter case, the population becoming extinct hap- pens to be the last one of the species. How is the distribution of a species lim- ited? Trying to understand those limits be- gan simply enough with concepts such as Liebig’s “‘law of the minimum” proposed for the limits to growth in plants (discussed by Hesse et al., 1937:21). This interesting question continues to attract speculation and investigation. A wholesale shift in distri- bution of a local fauna of mammals accom- panying changes in local climates in the Pleistocene was described by Guilday et al. (1964). The dynamic nature of species limits on a shorter time scale is indicated by numer- ous documented cases in which boundaries of individual species have expanded or con- tracted recently in North America over a relatively few years of time. For example, Dasypus novemcinctus (Fitch et al., 1952; Smith and Lawlor, 1964), Baiomys taylori (Baccus et al., 1971), and Sigmodon hispi- dus (Genoways and Schlitter, 1967), ex- tended their ranges northward; Marmota monax extended westward in Kansas (Choate and Reed, 1986); Lepus californicus extended eastward in Texas (Packard, 1963); Spermophilus richardsoni (Hansen, 1962) extended southward in Colorado; and since 1960 Sorex cinereus, Microtus pennsylvani- cus, Mustela nivalis, and Zapus hudsonius have extended southward in Kansas (Frey, 1992). It is more difficult to demonstrate retractions in ranges, but surely these have been occurring as well. The retractions in ranges of many larger mammals, such as grizzly bears, mountain lions, gray wolves, and wapiti in North America, need no fur- ther documentation here. Another recent mammalian example is the correlation of hours of darkness (about 7.3 hours in this case) needed for feeding with the northern limit of an Asian porcupine (Alkon and Saltz, 1988). In 1957, Darlington’s book Zoogeogra- phy: the Geographical Distribution of Ani- mals summarized distribution of the major groups of terrestrial vertebrates. Questions posed (p. vii) were: (1) What is the main pattern of animal distributions? (2) How has the pattern been formed? (3) Why has the pattern been formed? and, (4) What does animal distribution tell about ancient lands and climates? The answers (Darlington, 1957:618) were: (1) The main pattern is a “‘concentration of the largest, most diverse, least-limited fau- nas in the main tropical regions of the Old World; limitation caused by climate north of the tropics; and limitation and differen- tiation caused by barriers in South America and Australia.” (2) The pattern has been formed by spread of successive dominant groups from the Old World tropics over much or all of the world, followed by zo- nation and differentiation according to cli- 218 ANDERSON AND PATTERSON mate and ocean barriers, and by retreat and replacement of old groups as new ones spread.”’ (3) The pattern has been formed ‘‘because evolution has tended to produce the most dominant animals in the largest and most favorable areas, which for most vertebrates are in the main regions of the Old World tropics” (see Darlington, 1957: 569 for brief comments on probabilities and dominance). (4) Animal distribution tells us that ‘‘as far back as can be seen clearly, the main pattern of continents and climates seems to have been the same as now.”’ From a slightly skeptical point of view, we may now judge that the compilation of sum- maries of distributions of different groups may have been a greater contribution than the set of answers or conclusions. A hypothesis that dominant animals usu- ally move to gain advantages rather than to escape disadvantages is repeatedly asserted in various contexts (e.g., Darlington, 1957: 620, 637, and ranging from major groups of vertebrates to races of humans). The con- cept lacks clear definition and has a teleo- logical implication that is, at best, mislead- ing. An interesting exchange on the application of the concept to human races was published in the Journal of Mammal- ogy (Hall, 1946; Hill, 1947). In The Mammals of North America (Hall and Kelson, 1959) was a chapter (of 8 pages) on zoogeography (by Hall). The questions posed were: ““What patterns emerge from the 500 maps showing the geographic dis- tribution of North American mammals? What factors account for these patterns?” and, ‘““Why are there fewer kinds of mam- mals in one area than in another?” The ma- jor patterns discussed are: (1) the distinction of three major regions with largely different faunas, namely boreal, temperate, and trop- ical; (2) the presence of more temperate than boreal species, and more tropical than tem- perate; (3) the presence of zonation within each of the major regions; (4) the presence in North America of more species thought to have come from Asia than vice versa, and the presence in South America of more species from North America than the re- verse; and (5) the presence of an unusually large number of subspecies in the South- west. The major factors said to account for these patterns are: (1) temperature was regarded as a major factor in determining mamma- lian distributions from north to south; (2) the number of different habitats that are available is positively correlated with the number of species, both on the large spatial scale of regions and on the smaller scale of zones and local areas within zones; (3) the greater vigor of ““mammals of a large land area [which] more often than not prevail over their counterparts of a small land area when the two are brought into competition” (p. xx1x); and (4) advances and recessions of glaciation and accompanying aridity in areas from west to east within the temperate zone. The relevance of paleontological his- tory was mentioned briefly. Hall (1981) shortened the original eight-page discussion of zoogeography to one page and included no basically different interpretations. Nei- ther the patterns nor their explanations dif- fered greatly from what could be found in earlier literature. Returning to the hypothesis that animals from a greater land mass are more vigorous, we note that Hall in Hall and Kelson (1959) incidentally presented two other and con- trary hypotheses. A probabilistic explana- tion appears in a footnote on p. xxvi, relat- ing to the relative contributions of the South American and Central American tropics. Elsewhere (p. xxv) he noted that ‘North America and Eurasia might properly be thought of as one continuous region—the Holarctic region,”’ which has only recently been broken by the barrier of the Bering Sea. In current terminology this is simply a vi- cariant event and the original hypothesis about different areas of different sizes and about vigor seems irrelevant, at least as it relates to Asia and North America. A prob- abilistic model was discussed by Horton (1974), basically as a null hypothesis, and the conclusion was reached that it is not BIOGEOGRAPHY 219. necessary to invoke the concept of relative species dominance as a determinant of the direction of species movement in many cases. Frequently the term “dominance” has been used in the literature somewhat in- consistently and without careful definition, with resulting confusion. A few years after the publication of Hall and Kelson (1959), Eduardo Rapoport came to the Department of Mammalogy at the American Museum of Natural History and asked one of us (Anderson) what similar works might exist for the mammals of other continents. Unfortunately, the answer was none. Since then a set of maps for Australian species has become available (Strahan, 1983) and has been the subject for biogeographical analysis from the standpoint of areography (Anderson and Marcus, 1992). A three vol- ume work on South American mammals when completed will provide maps (two volumes have been published, Eisenberg, 1989, and Redford and Eisenberg, 1992). Another three-volume work with maps for South American mammals has been in preparation for many years (to be edited by S. Anderson, A. L. Gardner, and J. L. Pat- ton). There is no comparable compilation with maps for Africa. Most of Eurasia lies in the Palaearctic Region, for which a set of maps was published by Corbet (1978), and the remainder lies within the Oriental or Indomalayan Region, recently treated by Corbet and Hill (1992) and including a set of maps. No subsequent biogeographical or areographic analyses based on these two sets of maps has been published yet. Inciden- tally, faunal lists, whether regional or on some more local scale, even when not ac- companied by maps, have traditionally been basic sources for biogeographic data and their importance needs to be acknowledged here. The set of maps for North American mammals in Hall and Kelson (1959) was used as the source of data in subsequent analyses by several authors. The question of how many species occur in different areas was addressed by Simpson (1964), who tal- lied numbers of species postulated (on the basis of the published range maps) to occur in each of the squares of a 150-mile grid. These sources were used in a more detailed examination of the relative contributions of different groups of mammals to the latitu- dinal gradient in species numbers by Wilson (1974). He noted ‘“‘the lack of increase in species density” toward the tropics when quadrupedal mammals are considered alone, the major contributors to the latitudinal ef- fect being the bats. He considered also the possible effect of the lesser amount of space available in Central America. Wilson’s studies provided a much “finer grained” look than the tallies by three major regions in Halls’ (1981) analysis. Even finer detail is worthy of analysis (but there is a limit to the ability of progressively smaller units of space to yield meaningful geographic infor- mation, as was discussed by Anderson, 1972). Willig and Sandlin (1991) compared the effects of quadrat and latitudinal band methodologies on detection of latitudinal gradients in species richness. What is the frequency distribution of sizes of geographic ranges among all possible ranges for species of North American mam- mals? This question was addressed by An- derson (1977), using the same set of maps, and he noted that “‘it is clear that the species are not spread evenly, but that they are about an order of magnitude (10 times) less ‘con- centrated’ in each successively larger order of magnitude of range” (Fig. 1). Various analyses have focused on areas of distributions. For example, Armstrong (1972:354) noted that ‘““Areographic anal- ysis is of interest because it enables the pro- visional segregation of faunal elements of possible historical integrity from assem- blages with compatible and complementa- ry, yet coincidental ecology.” The areo- graphic analysis referred to was the sorting of species into groups with respect to the locations of their geographic ranges. Thus, in Colorado, Armstrong recognized nine ‘“‘faunal elements” such as Cordilleran, Chi- huahuan, Neotropical, and Great Basin. 220 ANDERSON AND PATTERSON 10 +1 10-4 NUMBER OF SPECIES PER 100 KM? INCREMENT IN SIZE OF AREA 10' 2 3 4 5 6 10’ AREA IN KM? Fic. 1.—Graph for North American terrestrial mammals showing the number of species (averaged for each succeeding order of magnitude) having ranges of any given size. Counts are grouped in 100 km? increments. The negative values on the ordinate are powers of 10, thus 10~* or 0.0001 species per 100 km? increment for a range of 10° (1,000,000) km? means that there are so few species with ranges of this size that most increments or size-classes of 100 km? are unoccupied and, and on the average, there is about one species for each 10,000 size-classes (Anderson, 1977:12). It may be reasonably inferred from these data that at any range size a species has a greater probability of losing range than of increasing its range. Most publications in mammalogy, or in biogeography, fit an existing mold. Al- though they contain new information, test an existing theory, or otherwise contribute to knowledge, they seem basically familiar as to topic, concept, assumptions, empha- sis, and methodology. Occasionally a pub- lication breaks new intellectual ground. Ar- eography (Rapoport, 1982; an earlier Spanish edition, published in 1975, was not widely distributed) was such a publication. Clearly the author was thinking along new lines, developing new methods, and asking new questions. Let us briefly consider some of these. Do North American species of mammals belonging to different orders and families have geographic ranges of different sizes (Rapoport, 1982:7)? Mean ranges were giv- en for 9 orders and 14 families. Arithmetic means were used and differences noted. For example, the mean for Carnivora, the order BIOGEOGRAPHY 224 with the largest ranges, was about eight times that of the Rodentia. Graphs of range size distributions for six orders were published by Anderson (1977:10). Rapoport used ‘“‘square megametres”’ as his unit of mea- surement and defined a megametre (Mm) as 100 km. The prefix mega is usually used for million rather than 100 thousand, so these discrepant usages need to be taken into account when comparing data in Ander- son’s paper with those in Rapoport’s. One square megameter as used by Rapoport is equal to 1 x 104 km? as used by Anderson, and Anderson used geometric means in- stead of arithmetic means. What are the mean geographic ranges of bats with different feeding habits (Rapoport, 1982:9)? Those that eat animal food are more widespread than those that eat plant food. Whether this would remain true if their entire ranges are included, rather than just the parts of ranges within North America, remains to be tested. What is the frequency distribution of the sizes of ranges of species among all possible sizes (Rapoport, 1982:13)? This question was investigated at about the same time, but independently of Anderson’s work, which was published in 1972. Both authors point- ed out the logarithmic or “hollow curve” distribution. How are the ranges of subspecies distrib- uted in space and in size relative to each other (Rapoport, 1982:27)? Various aspects of this were discussed and it was noted that “There is a tendency to increase the perim- eter of the irregularity of the species’ exter- nal frontiers when the number of subspecies increases.” How are numbers of subspecies with ranges surrounded by the ranges of other subspecies correlated with the total number of subspecies recognized within the species (Rapoport, 1982:31)? The correlation of in- ternal subspecies and total number of sub- species in the species is +0.979. Do the ranges of subspecies relative to each other differ among taxonomic groups (Rapoport, 1982:35)? The relative numbers that are considered to be contiguous, in- cluded, disjunct, and superimposed, differ some among the species of different orders, but the significance, both statistically and biologically, is unclear. Does the size of the range of the most widespread subspecies agree with an equi- table model or a random model (Rapoport, 1982:41)? A broken stick model was dis- cussed and it was concluded that the divi- sion of lands among subspecies “‘seems to be a stochastic process” rather than an eq- uitable one. This question was considered in some detail and with the same conclusion by Anderson and Evensen (1978). Does the total size of the range ofa species affect the way it is divided into subspecies (Rapoport, 1982:42)? “It seems that in the very widespread species the bigger land- owners (sspp.) have a better chance of de- veloping into very big landowners,” and that as the size of a subspecies’ range decreases it becomes less likely to fragment into two parts. As a result there is greater equitability among the ranges of smaller subspecies. The author noted that this poses more questions than it answers. [In a way this is more stim- ulating than the common procedure in which an author concludes that we now have “‘ex- plained”’ something or other. ] The focus of areography on the areas of distribution or ranges of species, and on the sizes, shapes, and locations in space and time of these ranges, leads to other types of questions and answers. For example, An- derson (1977:11) was led to conclude that species “‘are about an order of magnitude (10 times) less ‘concentrated’ in each suc- cessively larger order of magnitude of range”’ (Fig. 1). This led Anderson (1985) to the conclusion that ‘“‘the geographic range of a species, regardless of its size, is more likely to decrease than to increase.”” The former ‘““conclusion’”’ summarizes an observed pat- tern at one time, whereas the latter is an inference from that pattern and from the- oretical assumptions and considerations and may well be true over time spans of different duration. These two conclusions seem to ype ANDERSON AND PATTERSON 180° 120° 60° 60° 0° 0° 120° 180° LLL TAS SS <6 TOA SEE AEE ag E77 LT La SS ° Pet AN ag Turcee sae aaeae 60° RES om 1 = coy ie / a = rapetai area Z s tp HA mma + [AEH Ae | SR4abaN®): 6Aw) ° ! i ag, Ug aenet se La RGN TY AG. ROT . Nearctic . Palearctic . Neotropical . Argentine 100 articles) by Benedict on the subject. In 1922, at meetings of the American Phys- iological Society, F. G. Banting and C. H. Best presented their Nobel-winning re- search on the role of insulin in regulation of blood sugar. Work on the definition, role, and function of endocrine glands flourished. Most of the studies on such systems con- sisted of removing the gland to observe re- sults and infer function from the resulting change in function. In the physiological literature there was little emphasis on comparative physiology or using forms other than humans or ani- mals as models for humans. Because there was so little emphasis on comparative as- pects of physiology, very little work was re- ported on wild vertebrates in journals such as Journal of Mammalogy. In the Journal there are only about eight papers in the 1920s that could be defined generally as physio- logical, and five of those were on reproduc- tion. Most of the work on reproduction em- phasized description of reproductive cycles PAY STOLOGY 261 and timing of reproduction, which might be considered population biology today. Things expanded somewhat in the 1930s with ca. 35-40 papers appearing in the Journal. Most (16) of these concerned food habits with a little work on the actual physiology (digest- ibility) of digestion, but most simply listed food habits. Reproduction was still a strong field with 10 papers. Many articles de- scribed reproduction cycles, but a few pur- sued questions related to development. Be- nedict’s study on the physiology of the elephant appeared in 1938, and there was early work on the role of the pineal in pho- toperiodic mechanisms. F. G. Hall’s early work on adaptations to altitude was pub- lished in 1937, and there were ca. five pa- pers on respiration in porpoises, as inves- tigators pushed them as a novel system to understand respiration. Early work describ- ing electrical activity and effects of shock on brains of beaver and kangaroo rats ap- peared. Studies of temperature regulation patterns and metabolism in humans were expanding due to interests in nutrition fol- lowing World War I, and four papers on temperature regulation patterns and novel mechanisms (e.g., torpor) were published in the Journal of Mammalogy. Two of the pa- pers were descriptions of low body temper- atures in sloths by R. K. Enders from Swarthmore and one paper was on hiber- nation. As early as 1935, A. Brazier Howell and I. Gersh wrote a short paper indicating that kangaroo rats (given as Dipodomys mo- havensis) could exist without free drinking water and speculated on the role of succu- lent vegetation and metabolic water in their adaptations. They even performed histo- logical studies on the kidneys and speculat- ed about reabsorption. 1940s The subject of comparative physiology expanded greatly in the 1940s. The early part of the decade saw a focus of physiology on national needs associated with the war efforts of World War II. This single event greatly expanded opportunity, support, and questions about physiology more than any other factor up to this time. With the de- velopment of aviation, new questions about adjustment to altitude arose. With more emphasis on submarine warfare, the Navy (through the Office of Naval Research) be- came interested in torpor (hence hiberna- tion) as a possible way of maintaining crews underwater for long periods of time. The “off-duty” crew would use less oxygen in a reduced metabolic state, allowing subma- rines to remain under the sea for longer times. Thus, money became available for studies of metabolism, temperature regu- lation, and water balance (how could troops better adjust to desert or jungle condi- tions?). The standard topics of nutrition, di- gestion, circulation (especially hemody- namic shock), endocrine function, and neural control flourished with new and bet- ter equipment and support. These latter ar- eas took on a more mechanistic flavor fol- lowing the earlier descriptive work. Two groups greatly spurred the work in comparative physiology. Laurence Irving was trying to build a program at Swarth- more and brought to the U.S. several stu- dents of the renowned Danish physiologist, August Krogh. In 1939, he helped Per Scho- lander obtain a Fulbright Fellowship and persuaded him to come to Swarthmore (Scholander, 1978). In 1946 Irving brought Bodil (Krogh’s daughter) and Knut Schmidt- Nielsen to Swarthmore. Here, Scholander, always clever at designing and building equipment, developed the “‘Scholander sy- ringe,”’ which allowed gas analysis in very small samples of fluid (a “micro” Van Slyke apparatus). In 1947 Irving suggested that the group go to southern Arizona to study water metabolism in kangaroo rats. From that experience Bodil Schmidt-Nielsen went on to a distinguished career studying the physiology of the kidney and its role (along with other excretory organs) in regulating osmolality and volume of extra- and intra- cellular compartments. She served as Pres- 262 WUNDER AND FLORANT ident of the American Physiology Society from 1975 to 1976 (Brobeck, 1987). Knut Schmidt-Nielsen continued his outstanding career working on adaptations of a variety of animals to aridity focusing on tempera- ture regulation and water balance. Irving himself founded and was the first Director of the Institute of Arctic Biology at the Uni- versity of Alaska following a career focused on study of adaptations of mammals and birds to Arctic conditions. He became in- terested in the Arctic at the urging of Scho- lander, who previously had worked in Greenland doing botanical studies as a stu- dent. Scholander later became interested in questions related to diving physiology, which is what led him to Irving’s lab (Scho- lander, 1978). These collaborations resulted in the early classical papers describing how Arctic birds and mammals are better insulated than tropical forms, yet their patterns of metab- olism and temperature regulation are sim- ilar (Scholander et al., 1950a, 1950 5, 1950c). At this time such studies consisted primar- ily of exposing animals to different ambient temperatures and measuring their body temperatures. However, Scholander also developed an experimental way to measure insulation via heat flow through skins using a hot plate as heat source. Metabolism was tediously measured using a spirometer and taking gas samples periodically for analysis with the Scholander syringe or Haldane ap- paratus. The primary focus was the use of comparative material to ask questions about how animals might be best adapted to par- ticular, stressful environmental conditions. About this same time (1945-1948), a group at Harvard consisting of O. P. Pear- son, George Bartholomew, Peter Morrison, and G. E. Folk, Jr. was finishing their Ph.D.s and developed similar interests in asking questions about how animals were adapted to specific environmental stressors. Togeth- er with the Swarthmore group (Morrison went to Swarthmore before moving to the University of Wisconsin) they and their stu- dents were a dominant force in comparative physiology (especially mammals) for the next 30-40 years. Morrison began studying temperature regulation of Central American mammals in the 1940s and went to Swarthmore where he interacted some with R. K. Enders. He quickly moved to the University of Wis- consin and later went to Alaska where he became Director of the Institute of Arctic Biology following Larry Irving in the late 1960s. In the 1940s, the emphasis was still upon measurement of temperature response patterns to varying environmental temper- atures. Some labs began to look at mecha- nisms by which heat was conserved or lost (see Scholander et al., 1950a, 1950, 1950c), but the methods were difficult and tedious. Pearson published some of the earliest pa- pers on metabolism and temperature reg- ulation of shrews, as did Morrison. Both were intrigued with the observation that the animals were reported to eat prodigious quantities and, hence, should have high me- tabolism. With small size they should have a large surface area for heat loss relative to their mass for active metabolism. Moving to southern California (UCLA), Bartholo- mew began work on desert forms using both birds and mammals, but emphasizing birds for his early work. However, in the 1950s he made trips to Alaska to study marine mammals. After some early reports on tem- perature and respiratory rates in these forms he emphasized study of behavior, a then emerging field. His mammal work, together with that of his students, focused on water balance and temperature regulation with at- tention to torpor as an energy-saving ad- aptation. The field of temperature regulation was changing in the physiological arena also. In the early 1940s, the Annual Review of Phys- iology had a section entitled ““Temperature Regulation,” but starting in 1943 it was changed to “Heat and Cold” and in 1948 an entire paper on factors influencing sweat- ing was published. Most of the studies then looked at factors that influenced body tem- perature, such as ambient temperature, ra- PHYSIOLOGY 263 % OF TOTAL ev oe ye epee nn er-. se Sate eve scaessetrasss Spemcs tems eles Cle em ca Ss Mol lacy a Sear seat rocvt fens 3 (o) setts 42SESSF=SZECE toe = 5s 2c 3 br S oc 2) o.8 0 me Ws 2 > Oe lt stgz eo oI WM Ueese ac a 4 ego & a N ae = E a oo 26 Ay My eo OU oo mm i=) Fic. 1.—Percentage of papers published on various topics in the Annual Review of Physiol- ogy comparing the decades of the 1940s, 1950s, and 1960s. diant heat loads, and effects of different clothing and activity levels on body tem- perature. These, of course, were in response to needs associated with World War II. The mid-1940s also produced papers on applied aviation medicine and anoxia in aviation. 1950s The impetus in comparative physiology begun in the 1940s continued into the 1950s. Much comparative work was done on water balance and thermoregulation of wild forms emphasizing Arctic and desert forms, with some studies on adaptation to high altitude. The general paradigm was to study an an- imal best adapted to deal with a particular environmental stressor. This work was a spin-off from the interest in stress physiol- ogy brought on by World War II and the available funding associated with that. In the “‘mechanistic”’ physiological literature there was a subtle shift in areas of emphasis. Figure | shows the relative percentage of papers in different subject areas published in the Annual Review of Physiology for the period 1940-1960 by decade. Temperature regulation made up ca. 5% of the literature in the 1940s and 1950s, then declined, while water balance (including ion balance) in- creased from 2% to 5% of the literature. The big increases were in work on endocrine sys- tems and shifts to cellular approaches to mechanism. The dramatic change in en- docrine coverage was a shift to specific gland function, their hormones, and mode of ac- tion versus “the endocrine system” dis- cussed in earlier reviews. Early papers fo- cused on the pituitary and its role in reproduction, along with thyroid and effects on growth and metabolism. These presaged the work on cellular mode of action that later were emphasized in the 1960s. The comparative approach shows dra- matically in the number and sorts of reviews written from the mid-1950s. Before this time, most studies emphasized the rat or humans, but in 1953 many papers with a comparative theme appeared in Annual Re- view. Starting in 1953, there was an article on comparative physiology of invertebrate muscle. From then to 1960 each issue had at least one paper with a definite compar- ative approach (e.g., sense organs, respira- tion in invertebrates, nutrition and feeding in vertebrates) with a comprehensive re- view by F. E. J. Fry on temperature com- pensation mechanisms for metabolism in poikilotherms in 1958. This followed a re- view on energetics in 1956 by Max Kleiber. In 1957 Kayser, who had worked on the subject since the 1930s, presented a defin- itive review on hibernation. Most of the work on hibernation to that point was de- scriptive regarding torpor patterns and body temperature shifts. Some early workers (e.g., Benedict and Lee, 1938; Lyman, 1948) had looked at metabolism in hibernators, but it was not until the 1950s and the develop- ment of the paramagnetic oxygen analyzer that such studies increased greatly in num- ber. Charles P. Lyman and others reported on studies of nerve conduction, electrical activity of the cerebral cortex, circulation, and function of endocrine glands of hiber- nators. 264 The early work on water balance was ex- panded to include wild forms and total wa- ter budgets during the 1950s. Early work had focused on movement of water through skin, sweating mechanisms, and amounts of water needed by animals (Adolph and Dill, 1938: Dill et al., 1933; Tennent, 1946; Vor- hies, 1945), and on structure and concen- trating capacity of the kidney (Sperber, 1944). Although Howell and Gersh (1935 and see above) early pointed out that kan- garoo rats needed little or no water, and the Schmidt-Nielsens expanded upon that in the late 1940s, 1t was not until the 1950s that studies focused on compartmentalizing wa- ter balance. Bodil and Knut Schmidt-Niel- sen (see review 1n 1952) presented a ““com- plete’’ account of water balance for “‘the” kangaroo rat and reported a value for pul- monary water loss (actually evaporative wa- ter loss). Later in the decade, Robert M. Chew expanded the work and included many other desert rodents, as did Bartholomew and his students (Dawson, Hudson, MacMillen). 1960s The comparative trend begun in the late 1940s expanded even more in the 1960s. Throughout the decade each volume of the Annual Review of Physiology had at least one article with a comparative approach, starting with Clyde Manwell’s paper on blood pigments in 1960. An article by Don Farner on photoperiodic mechanisms in birds appeared in 1961 along with Florey’s paper on comparative transmitter sub- stances in neurophysiology (always a large topic for review). Vernberg reviewed what was known about adjustment to different geographic regions with a 1962 paper on latitudinal effects on physiological proper- ties of populations (most of his work was on marine invertebrates, but it stimulated interest in vertebrates, including mammals) and it introduced a new technique—trans- plantation, which was used later in the de- WUNDER AND FLORANT % OF TOTAL co Ce sv Es QeevesB®soostsecugys 2 -— SS =< = = 2 So 2 ie Soir ao = 2925 5 = So Soa = SRE is) sos 3S ok se a > } --} “ao lkse ec = = wm 2 5 ares ‘Sone ee . avnZz Ss S25 2 = & i 2 > 2 a~ S =a 2 & r. ~ P = as <3) fe = = = EG = = es) os a2 E = eo = =D = = a Fic. 2.—Percentage of papers published on various topics in the Annual Review of Physiol- ogy comparing the decades of the 1960s, 1970s, and 1980s. cade by Ray Hock and others to study ad- aptation to altitude in deer mice. Articles on navigation by animals, comparative physiology of nutrition of vertebrates and invertebrates, and hormones in fish (by Hoar) added to J. Aschoff’s classic paper on diurnal rhythms. Water and ion balance be- came more important topics than in the past. Bodil Schmidt-Nielsen reviewed mecha- nisms by which invertebrates dilute urine in the Annual Review of Physiology in 1963, a comparative paper on invertebrate excre- tory organs appeared in 1967, and G. Parry reviewed osmotic and ionic regulation (sys- tem level studies) in 1968. In 1961 Max Kleiber again reviewed energetics, empha- sizing cellular energy transfer and metabolic control mechanisms over organismal met- abolic rates, size, and ties to temperature regulation and food as in his 1956 review. Studies of thermoregulatory patterns and mechanisms of thermoregulation under stress conditions for wild animals became more common. H. T. Hammel reviewed this topic in a 1968 paper in Annual Review of Physiology. In 1964 the first, and only, Handbook of Physiology: Adaptation to the Environment was published by the Ameri- PHYSIOLOGY 265 % OF TOTAL Hy i Hi i i i t ' z ' ig 3 Fy i g i = 7) = =) Energetic: ae Blood/Heart = Water Balance —xaaeessmen Temp. Regulation -==essssessssnmnsenss A i fe i o.2 eon GH Ge ww won Ya ou ee eS oe cwo wo a=, =| = Sacto Saou? sa oc sls eSg5Sfeetsessi = be “Ms Eas ete o Qerosag oes 2 ove Zs cate = = CO 1a, 3s 4 {ao} MuUYE ES a =& oo _ N a ial a7 + v0 oD i= 4 i=) Fic. 3.—Percentage of papers published on various topics in Physiological Zoology compar- ing the decades of the 1960s, 1970s, and 1980s. can Physiological Society giving a state-of- the-art coverage for comparative physiol- ogy and human adjustment to stress brought on by environmental variables. In 1962 the first International Symposium of Hiberna- tion and Cold Physiology was held in As- pen, Colorado (the 9th meeting was held in 1993 at Crested Butte, Colorado). Fig. 1 suggests that this topic of thermoregulation declined in coverage from the 1940s to the 1960s. Generally that is true with a reduc- tion in human “stress” work after World War II, but Fig. 2 shows an increase in the 1970s and an increase in studies of ener- getics. The increase in 1970 reflects more papers on comparative topics (more wild species) and the increase in papers on en- ergetics reflects an increase in papers inves- tigating the mechanisms of thermoregula- tion and the role of metabolism in those. As noted, frequently it was difficult to sep- arate a paper into one or the other category of thermoregulation or energetics. In the 1940s and early 1950s that was not so dif- ficult because energetics papers usually re- lated to total energy turnover, or need, and related more to nutrition and body size ef- fects than to mechanisms of thermoregu- % OF PHYSIOLOGY Energetics Ssh Lipids Ss Blood/Heart BSSSsss Other SSS 4% A ee) ie 4 | e ec o > & > na oD ° } = o © &® © = i] = = Se ae oo Oa a) 3 a a = SZ ses 6 ¥ Go =] -_ GI be 3 jee} ~ S E aM 6 £ 5 ec a cr) > fo & } a S 2 - ec a yy pe = = mo — Se ot > ° a s = pa a -. wm Dv ve : = =) oc @ a a= a w a i= 7) oO v a i-4 Digestion/Nutrition PSS Sieve Fic. 4.—Percentage of papers published on various topics in physiology among the total pa- pers on physiology published in the Journal of Mammalogy comparing the decades of the 1960s, 1970s, and 1980s. lation. Also many new journals appeared during this decade allowing more places for authors to submit work on these topics (e.g., Journal of Comparative Biochemistry and Physiology, Journal of Thermal Biology) and coverage of these topics in journals such as Physiological Zoology (Fig. 3) increased. The increased coverage was reflected in the Journal of Mammalogy (Fig. 4). Over 20% of the papers in physiology concerned thermoregulation. Papers on energetics in- creased from 5% of all physiological cov- erage in the 1960s to 12% in the 1970s and 20% in the 1980s. During the 1960s inves- tigators revived the paradigm of Justus von Leibig (from the 1800s) that physiology sets limits to distribution patterns. Thus, com- parative physiology evolved into the fields of comparative (mechanistic) physiology, which selected organisms because they might best show the mechanisms at work in an organ system under stress, and physiologi- cal ecology, a new field developed to inves- tigate how animal function and distribution might be restricted through physiological limitation to the environment. Thus, in 1963 Brian McNab’s (a student of Peter Morri- 266 WUNDER AND FLORANT son) paper on the relation between home range and energy needs of mammals ap- peared. In the Journal of Mammalogy many papers published during this decade took on the emphasis of the interaction between physiology and “limitations.” We find E. W. Jameson, Jr., writing about body mass effects and hibernation (how fat must in- dividuals be before they can enter torpor?) and L. Getz investigating salt tolerance and aridity tolerance in voles and their relation to competition and habitat use and selec- tion. Negus and Pinter published one of their first papers of a 15—20-year search for plant compounds that affect reproduction in voles (Negus was later joined by Berger in this work, which culminated in a 1981 paper in Science [Berger et al.] identifying the com- pound and a 1987 review of the topic). Fur- ther, Christian and Davis wrote about ad- renal function, reproduction, stress, and vole cycles in Microtus pennsylvanicus. No mat- ter what the physiological system (water balance-kidney; stress-adrenal; reproduc- tion-endocrine/gonads), the paradigm for questions in this decade became limitation on some ecological parameter. 1970s As was the case in earlier decades, the strong topics for coverage in the physiolog- ical literature during the 1970s were endo- crinology, circulation and respiration, and topics in neurobiology. The urinary system and kidney received less coverage than be- fore. A look at Fig. 2 suggests that cell phys- iology received less attention in the 1970s than in the 1960s. However, that is mis- leading because much of the approach in endocrinology and neurobiology was mo- lecular and cellular, with work on hormone receptors and mode of receptor function re- ceiving much attention. In neurobiology, our understanding of impulse transmission and the cellular basis of nerve synapses and nerve/muscle interaction was being eluci- dated. In comparative physiology there was a continuation of the ecological emphasis be- gun in the 1960s. Thermoregulation (in- cluding hibernation), energetics, water bal- ance and kidney function, and reproduction continued strong or increased in coverage. At this time more papers on vertebrates in general, and mammals in particular, ap- peared in Physiological Zoology. Prior to 1960 much of the coverage in this journal was on invertebrates. As can be seen in Fig. 3, the topics listed above increased during the 1970s, just as they did among physiol- ogy papers published in the Journal of Mam- malogy (Fig. 4). Thermoregulation, ener- getics, and water balance were all topics that expanded in coverage during this decade (Fig. 4). However, there were changes in approach and paradigms within which these physiological data were interpreted. Within the field of thermoregulation and energetics, papers took on a new level of sophistication. Instead of just documenting more species for patterns of ability to ther- moregulate in extreme environments (e.g., hot or cold, dry or wet), or evaluating the effects of body mass, there was a shift to- ward studying effects of, and cost for, var- ious activities such as locomotion or repro- duction, and an incorporation of broader factors influencing thermoregulation. The field of biophysics came of age following publication of David Gates’ Energy Ex- change in the Biosphere a decade earlier (Gates, 1962). Aaron Moen applied these techniques to deer and Heller and Gates used them to describe thermal physiology as a factor influencing chipmunk distribu- tion along an altitudinal gradient on the eastern slope of the Sierra Nevada moun- tains in California. Here was use of physi- ology coupled with behavior to describe mechanisms of competitive exclusion for these distribution patterns. There was also increased emphasis on mechanisms of ther- moregulation. Work on brown adipose tis- sue as a means of warming small mammals (first described as a heat generating tissue by Smith and Horwitz in 1969) took on PHYSIOLOGY 267 more importance and was investigated by Heldmaier in Germany and Lynch and Wunder in the U.S. The role of various structures and mechanisms to modulate en- ergy exchange with the environment (using biophysics and heat transfer concepts and equations) became more in vogue for study (e.g., Cena and Clark, 1973; Heller, 1972). Energetics studies were applied more at a population level (following the lead of McNab, 1963) in an attempt to explain a variety of processes (e.g., home range sizes, reproductive costs, population growth). En- ergy became a currency to be used for de- scribing behavior and to try to predict the consequences of population processes. The Polish school, led by Ladd Grodzinski, was quite active during this time writing on en- ergetics, and reproduction and population growth in a variety of mammals varying in size from voles to roe deer. Grodzinski and Wunder (1975) reviewed the topic of en- ergetics in small mammals. McNab contin- ued in the vein of his 1960s work using energetics to discuss the distribution of vampire bats and other mammals. He then went on to develop ideas about how life history traits, such as food habits and body mass, might influence energetics in mam- mals. There was also a shift during this decade to study energetics of animals in the field. While mechanistic studies still used meta- bolic rates measured as steady states during rest or some specific activity with oxygen analyzers in the lab, there was a new isotopic technique introduced to study integrated metabolism in the field. Much of the con- ceptual development and early validation work on these techniques to study metab- olism and water turnover was done by Lif- son in the 1950s and 1960s. However, the technique was expensive and required spe- cial equipment. Thus, few studies were un- dertaken until Ken Nagy, at UCLA, ac- quired access to the expensive isotopes and equipment to measure them. Much collab- orative work was done, culminating in his review paper a decade later (Nagy, 1987) summarizing and scaling the allometric re- lationships of field metabolism in birds and mammals. During this decade it was also realized that energy, per se, may not be the only limitation or major currency for evaluating performance of mammals in the field, and nutritional ecology took on a new impor- tance. George Batzli became a dominant fig- ure studying small herbivores. Realizing that energy is important to the lives of animals, these studies suggest that certain secondary chemicals in food may influence energy availability to mammals and some energy sources may have limited availability. For that reason most of the studies focused on herbivores, because they eat a high energy density food (plants) in which the energy is not readily available to mammals because it is tied up as cellulose and hemicellulose and vertebrates lack the enzymes necessary to break these down. Thus, digestion and digestive processes become critical to make these foods available for herbivores. There was a tremendous literature available from animal science where such processes had been studied for decades to enhance food production (e.g., Kleiber, Baldwin, Van Soest), but, with few exceptions, most stud- ies of wild forms did not reference this lit- erature to any great extent. Studies of water balance still focused pri- marily upon animals living in arid regions (work by MacMillen and Hinds). Like the studies on energetics, however, there was a new push to learn how animals were truly challenged in the wild and, hence, radioiso- topes were introduced to study water turn- over in the field (see papers in the Journal of Mammalogy by Nagy and by Bradford). In the latter part of the decade and into the early 1980s, Christian (1979, 1980) inves- tigated the role of water in reproduction, demographics, and habitat use by small des- ert rodents. Previously there was specula- tion that moisture may be important in these processes, but no one had sorted out mois- ture from energetics despite the fact that most desert forms obtain their moisture 268 WUNDER AND FLORANT from their food. Christian simply intro- duced small watering stations in the field and found that the reproductive season was prolonged for some species, some actually showed numerical population increases, and there were habitat shifts to use of drier, more open habitat if moisture was present. Inter- estingly, little has been done with this tech- nique in application to other species or hab- itats. Overall during this decade there was a strong emphasis on environment factors and attempts to see how animals actually per- formed in the field. Tied to this was an in- terest in how performance of mammals shifts seasonally, regardless of whether one was studying temperature regulation, en- ergetics, water balance, or reproduction. 1980s In the general physiological literature this was a time when many new, specialty jour- nals were started or expanded having been initiated during the 1970s. Thus, papers in many fields were being shifted to these spe- cialty journals and we found analysis of trends in a discipline harder to document using the standard review journals that we had used up to this decade. Endocrinology continued as a strong field with much more emphasis on molecular mechanism and ties to genetic control than had been the case earlier. Cardiac and circulatory function re- mained a strong area of research, with ca. 25% of the papers in Physiological Review being published in this area (Fig. 2). Most topics had molecular and cellular orienta- tion and the general topic itself increased in coverage in Physiological Review from <10% to >15% of total papers. Physiological Zoology changed editors in the 1970s from T. Park, who had been in- volved with the journal since its early days, to C. L. Prosser and J. E. Heath. Thus, many more papers on vertebrates, and mammals in particular, were published in the 1980s. The area of emphasis was energetics and, secondarily, thermoregulation (Fig. 3). Within thermoregulation there was a resur- gence of interest in hibernation and torpor. This was a very topical subject in the 1950s and early 1960s, but seemed to lack focus in the late 1960s to late 1970s, except for papers on cellular mechanisms and tissue tolerance to cold. However, in the late 1970s there was renewed interest at the organismal level stimulated by work showing that the sorts of fuels burned during torpor may in- fluence lengths of torpor bouts and that dif- ferent kinds of fats (saturated versus poly- unsaturated) might be used differentially during torpor periods. Thus, mammals may need to seek certain nutrients prior to hi- bernation. Kenagy and Geiser, Florant, and later Frank added to this area. French de- veloped insight into the effects of body size on torpor bout lengths and optimal tem- peratures for torpidity. Many of the ener- getics papers of the decade relate to other aspects of a species’ biology, such as pop- ulation processes and costs for various be- haviors or reproduction, adding to the in- formation started in the 1970s. This was also a time when the field shifted to examine how body size (mass) influenced energetics and many other functions of organisms. Three major books on allometry were pub- lished emphasizing how body mass con- strains and allows organisms (mammals in particular) to function (Calder, 1984; Pe- ters, 1983; Schmidt-Nielsen, 1984). Water balance of mammals became a top- ic of less emphasis, but some fine work on total water budgets and their significance for distribution limits or function was pub- lished by MacMillen, and MacMillen and Hinds. This work grew from the early stud- ies of Bartholomew and Chew first pub- lished in the 1950s and 1960s. In these papers the relationship of water to ther- moregulation was stressed as much as the use of water for general life processes and as a means of effecting ion balance. Within the Journal of Mammalogy, pa- pers on thermoregulation remained strong PHYSIOLOGY 269 at >15% of the total papers in physiology published (Fig. 4). Energetics received re- newed interest for investigation, increasing from around 10% to over 20% of the total physiology papers published. Reproduction remained steady at ca. 12%. The topic that truly took on a new interest was digestive biology and nutrition (Fig. 4). Many inves- tigators began to study how the process of digestion might limit energy acquisition by mammals, especially small herbivores, and how nutrition might influence herbivore- plant interactions and animal performance. Those studying thermoregulation contin- ued the trends of the 1970s, applying this theme to limits on distribution and perfor- mance in mammals. Many studies linked thermoregulation to energetics so the shift to more energetics papers was, in part, a slightly different emphasis on thermoregu- lation. Many studies had, as part of their focus, adjustment to different seasons (work by Wunder and Merritt and colleagues), and mechanisms for those shifts (work by Hill, Kenagy, MacMillen, Wunder, French, Har- low, Dertin, McNab, and Cranford). As mentioned above, along with these studies of energetics and the theme of limits to distribution and performance, many in- vestigators began to study how energy sources and allocation pathways were fueled by animals. That is, what were their foods and how were nutrients obtained? George Batzli and his students had studied such questions for about two decades and, in the 1980s, began to look more closely at the role of secondary chemicals in food, in addition to rate processes and digestive efficiencies. Wunder and students showed that small herbivores (e.g., voles) could change gut size to better or more quickly process food, and many related papers followed. Two major texts on the topics of nutrition appeared, in addition to many symposia volumes, es- pecially on ruminant herbivores. Peter Van Soest’s book, Nutritional Ecology of the Ru- minant (1982), set the stage for Charlie Robbins’ book, Wildlife Feeding and Nu- trition (1983). Both are used as a basis for posing questions about how various mam- mals adjust to novel foods or environments compared to more studied forms. Recent work is beginning to focus on limits to en- ergy processing and the trade-off of the roles of digestion and assimilation with tissue uti- lization of substrates, or behavior of feed- ing. Over the next decade, we hope there will be a more complete understanding of how mammals, especially herbivores, uti- lize the myriad of plants available to them, and how plant—animal interactions are in- fluenced by physical and biological factors such as thermoregulation, energy needs, and nutrient needs for reproduction. Epilogue We have attempted to give a brief over- view of how physiology in general, but es- pecially comparative physiology of wild mammals, has shifted, waxed, and waned over the past 75 years as the ASM has grown. We suspect that the recent fervor for cell and molecular approaches will stimulate an understanding of not only mechanisms of process, but also how those processes relate to the fundamental biology (life histories) of the wild mammals possessing them. Such knowledge will be useful not only for un- derstanding ourselves and our functions, but also how mammals function in ecosystems, and how they might adjust to changes in those ecosystems as we witness climatic and other environmental changes. Literature Cited Apo pH, E. F. 1987. Physiology flourishes in Amer- ica. Pp. 1-10, in History of the American Physio- logical Society (J. R. Brobeck, O. E. Reynolds, and T. A. Appel, eds.). Waverly Press, Baltimore, Mary- land, 533 pp. Apo pH, E. F., AND D. B. Ditt. 1938. Observations on water metabolism in the desert. American Journal of Physiology, 123:369-372. AppeL, T. A. 1987a. Founding. Pp. 11-29, in History of the American Physiological Society (J. R. Bro- beck, O. E. Reynolds, and T. A. Appel, eds.). Waver- ly Press, Baltimore, Maryland, 533 pp. 270 WUNDER AND FLORANT . 19876. First quarter century, 1887-1912. Pp. 31-62, in History of the American Physiological So- ciety (J. R. Brobeck, O. E. Reynolds, and T. A. Ap- pel, eds.). Waverly Press, Baltimore, Maryland, 533 . 1987c. Second quarter century, 1913-1937. Pp. 63-96, in History of the American Physiological Society (J. R. Brobeck, O. E. Reynolds, and T. A. Appel, eds.). Waverly Press, Baltimore, Maryland, 533 pp. BENEDICT, F. G., AND R. C. LEE. 1938. Hibernation and marmot physiology. Carnegie Institution of Washington Publication, 497:1-239. BERGER, P. J., N. C. NEGus, E. H. SANDERS, AND P. D. GARDNER. 1981. Chemical triggering of reproduc- tion in Microtus montanus. Science, 214:69-70. Broseck, J.R. 1987. Presidents, 1963-1987. Pp. 177- 280, in History of the American Physiological So- ciety (J. R. Brobeck, O. E. Reynolds, and T. A. Ap- pel, eds.). Waverly Press, Baltimore, Maryland, 533 BROBECK, J. R., O E. REYNoLps, AND T. A. APPEL (EDs.). 1987. History of the American Physiological Society. Waverly Press, Baltimore, Maryland, 533 pp. CALDER, W. A., III. 1984. Size, function, and life history. Harvard University Press, Cambridge, Mas- sachusetts, 431 pp. Cena, K., AND J. A. CLARK. 1973. Thermographic measurements of surface temperatures of animals. Journal of Mammalogy, 54:1003-1007. CHRISTIAN, D. P. 1979. Comparative demography of three namib desert rodents: responses to the provi- sion of supplementary water. Journal of Mammal- ogy, 60:679-690. 1980. Vegetative cover, water resources, and microdistributional patterns in a desert rodent com- munity. Journal of Animal Ecology, 49:807-8 16. Dit, D. B., A. V. Bock, AND H. T. Epwarps. 1933. Mechanisms for dissipating heat in man and dog. American Journal of Physiology, 104:36-43. Gates, D. M. 1962. Energy exchange in the bio- sphere. Harper and Row Publishers, New York, 151 GRODZINSKI, W., AND B. A. WUNDER. 1975. Ecolog- ical energetics of small mammals. Pp. 173-204, in Small mammals: their productivity and population dynamics (F. B. Golley, K. Petrusewicz, and L. Rysz- kowski, eds.). 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Cambridge University Press, Cambridge, Great Britain, 328 pp. Rossins, C. T. 1983. Wildlife feeding and nutrition. Academic Press, New York, 343 pp. ROTHSCHUH, K. 1973. History of physiology (Trans- lated and edited by G. B. Risse). Robert E. Kriegen Publishing Co., Huntington, New York, 379 pp. SCHMIDT-NIELSEN, K. 1984. Scaling: why is animal size sO important? Cambridge University Press, Cambridge, Great Britain, 241 pp. SCHMIDT-NIELSEN, K., AND B. SCHMIDT-NIELSEN. 1952. Water metabolism of desert mammals. Physiological Reviews, 32:135-166. SCHOLANDER, P. F. 1978. Rhapsody in science. An- nual Review of Physiology, 40:1-17. SCHOLANDER, P. F., V. WALTERS, R. Hock, AND L. IRvING. 1950. Body insulation of some arctic and tropical mammals and birds. Biological Bulletin, 99: 225-236. SCHOLANDER, P. F., R. Hock, V. WALTERS, F. JOHNSON, AND L. IRvING. 1950. Heat regulation in some arc- tic and tropical mammals and birds. Biological Bul- letin, 99:237-258. SCHOLANDER, P. F., R. Hock, V. WALTERS, AND L. IrvinG. 1950. Adaptation to cold in arctic and tropical mammals and birds in relation to body tem- perature, insulation, and basal metabolic rate. Bio- logical Bulletin: 99:259-271. Smitu, R. E., AND B. A. Horwitz. 1969. Brown fat and thermogenesis. Physiological Review, 49:330- 425. SPERBER, I. 1944. Studies on the mammalian kidney. Zool. Bidrag Fran Uppsala, 22:249-431. TENNENT, D. M. 1946. A study of the water losses through the skin in the rat. American Journal of Physiology, 145:436-440. Van Sosst, P. J. 1982. Nutritional ecology of the ruminant. Comstock Publishing Associates, Cornell University Press, Ithaca, New York, 373 pp. Voruies, C. T. 1945. Water requirements of desert animals in the southwest. University of Arizona Ag- ricultural Experiment Station Technical Bulletin, 107: 487-525. REPRODUCTION OLIVER P. PEARSON AND G. J. KENAGY Introduction W: find ourselves in the early 1990s enriched by fascinating accounts of the reproductive biology of hundreds of kinds of mammals. We believe that we have a sophisticated understanding of the ways in which various reproductive mechanisms and strategies represent fitness. Almost all of this knowledge has been gained in the last 100 years. When the ASM was founded in 1919, de- tailed information about reproductive pat- terns and mechanisms was available for only a handful of domesticated and wild animals, as well as for humans. Further understand- ing was severely handicapped by the prim- itive state of the science of endocrinology and the absence of yet-to-be-discovered in- sights in cell and molecular biology. In the years immediately following the founding of ASM, anatomists, physiologists, geneti- cists, psychologists, medical researchers, and biochemists all began contributing ideas and data to the emerging discipline of mam- malian reproductive biology (Fig. 1). To illustrate the relative collective effort that mammalogists have directed into stud- ies of reproduction, we tallied all the articles published in every fifth volume of the Jour- nal of Mammalogy from 1920 through 1990. Pa { Le ay ip = ~ J 1 ak / / ! Sa { { segame cs w= (Bim, \ Vas SSS et 0° SarKtocs (| Wy \) “&@e PomeSqure \ [ WY ene \ Nf ok vont? \ \ KY /\y mh | GS | y | A\ iM (de \ (A Wy Ae Overall, 8% of the 1,846 papers dealt with reproduction. The percentage increased, however, during this 70-year interval. For the first 25 years only ca. 4% of the articles dealt with reproduction, but this increased to ca. 11% in the last 30 years (Fig. 2). The development of our knowledge of the reproductive biology of mammals resulted from the vision of a few pioneers whose discoveries and teachings spread and mul- tiplied while passing through a variety of institutions. The favorable climate for this flowering was found within institutions that drew their support from medical interests, agricultural and livestock interests, labora- tory-animal needs, entrepreneurs who saw commercial opportunities, and surely, from the traditional “‘pure”’ scientists— those who could not rest until they found out whether some exotic species was an induced ovu- lator or why some other species had such a long gestation. We shall focus on only a few of the institutions and people who played important roles during the early decades of the 20th-Century flowering of reproductive biology. By mid-century, when the number of participating scientists became so nu- merous, we shall call attention to new ideas and approaches that have been shaped by No ~I i) 120 100 80 60 40 Number of Papers 20 O D 1880 1890 1900 Marshall, 1910 1910 PEARSON AND KENAGY NN oO oO ie m ® ge re) < 335 o— £ 9 bo Ais E= 1920 1930 1940 Year of Citation Fic. 1.—The growth of research on mammalian reproduction. Dates of appearance of 1,362 papers cited by Asdell (1946). Five significant publications or events are noted, as discussed in the text. more recent generations of innovative peo- ple. In the more recent time period we have, for simplicity, been highly selective and general, indicating ideas of importance rath- er than describing them in detail, and we have not generally presented these modern trends in terms of specific people. More time will tell which recent approaches will have the most enduring value in the history of mammalian reproductive biology. EARLY 20TH CENTURY The Cambridge Legacy The flowering of interest in mammalian reproduction reflected in Figure 1 can be traced to Great Britain, where a founding figure was Walter Heape. After a late start in science, Heape found himself teaching anatomy at Cambridge, where he co-au- thored a textbook of embryology. He soon obtained grant support and thereafter de- voted himself full time to research. Working at a time when even the sex-determination mechanism of mammals was unknown, he successfully transplanted fertilized ova from one rabbit to another in the early 1890s, developed artificial insemination in 1897, and in 1901 published an impressive sum- mary and synthesis (Heape, 1901). He fitted humans and dozens of species of wild and domesticated mammals into a common framework of reproductive categories using now-familiar terms (British spellings) such as oestrus, pro-oestrum, metoestrum, dioestrum, polyoestrous, and monoestrous. Had he remained longer in teaching, he no doubt would have become the leader of a “‘school’’; but, his impact seems to have been mostly through his publications. Heape’s work inspired F. H. A. Marshall, a lecturer at the School of Agriculture in Cambridge, to publish his influential book on physiology of reproduction (1910). In the introduction, Marshall acknowledged, “I take this opportunity of recording my in- REPRODUCTION 273 n=1847 O N a Frequency (percent) Oo NO 1920 1930 1940 Oo 1950 1960 1970 1980 1990 Year of Publication Fic. 2.—Increase in relative frequency of articles on reproduction appearing in the Journal of Mammalogy. Frequency distribution is shown for articles containing important information on re- production (7 = 1,847), sampled every fifth year from 1920 through 1990. debtedness to Mr. Walter Heape, through whose influence I was first led to realise the importance of generative physiology both in its purely scientific and in its practical aspects.” Marshall’s book was a wide-ranging ac- cumulation of information on breeding sea- sons, estrous cycles, uterine cycles, ovarian changes, spermatogenesis, the testes and ovaries as endocrine organs, the placenta, and other topics, all with reference to hu- mans, laboratory animals, livestock, and wild animals. The 1910 and 1922 editions of this book became the “bible” to a gen- eration of biologists who were to outline the diversity of reproductive strategies in mam- mals. A second book by Marshall on reproduc- tive physiology appeared in 1925. It ap- peared in time to influence the people, mostly British, who published reproductive studies in the 1930s and 1940s. The closing paragraphs of this second book call atten- tion to global population concerns, Mal- thus, contraception, and eugenics. Reading those paragraphs two generations later brings one face to face with the fact that during the intervening 70 years we have not resolved those old yet vital ethical concerns. Fur- thermore, still newer discoveries have cre- ated yet more concerns undreamed of by Marshall. Even before Marshall’s books, British bi- ologists were otherwise prepared for a flow- ering of reproductive studies. W. H. Cald- well, a Cambridge scholar on an expedition in 1884 to one of the colonies (Australia), sent the famous cable ““Monotremes ovip- arous, Ovum meroblastic” not to Great Brit- ain or “the Continent,” but to another out- post of the United Kingdom, Canada and the city of Montreal, where the British As- sociation for the Advancement of Science was holding its annual meeting (Burrell, 274 1927). In this geographically widespread and receptive climate, Marshall’s books provid- ed a foundation on which subsequent gen- erations could build. The pages of the Pro- ceedings of the Zoological Society of London, the Philosophical Transactions of the Royal Society of London, and other prestigious publications are forever enriched by im- portant reproductive studies by other lu- minaries such as E. C. Amoroso, J. R. Ba- ker, F. W. R. Brambell, R. Deanesly, J. Hammond, J. P. Hill, L. H. Matthews, A. S. Parkes, I. W. Rowlands, and Sir Solly Zuckerman. Within little more than a de- cade in the 1930s and early 1940s they de- scribed the intricacies and novelties in the reproductive cycles of shrews and bats, hedgehogs and hyaenas, kangaroos and fer- rets, wildcats and moles, and gibbons and rabbits. In the coming decades these re- searchers were followed by P. H. Leslie, J. L. Davies, B. Weir, and many others. A third edition of Marshall’s book, delayed by World War II and published as three vol- umes with many chapter authors, appeared between 1952 and 1966 under the editor- ship of A. S. Parkes. Marshall had died in 1949, but he had contributed to many of the chapters. A fourth edition appeared in 1984, edited by G. E. Lamming. The Zoological Society of London under the presidency of Sir Solly Zuckerman be- came one of the institutions that had a great impact on the development of studies of reproduction. In 1963, with support from industry (the Wellcome Trust), a research center was established, with an emphasis on studies of mammalian reproduction—I. W. Rowlands was its first director. Perhaps the ultimate fruition of the Cam- bridge rootstock came in 1960, when the Society for the Study of Fertility, with sup- port from the Wellcome Trust, founded the Journal of Reproduction and Fertility. C. R. Austin was editor and A. S. Parkes Chair of the Editorial Board. In the first issue, Parkes pointed out that the “‘output of lit- erature on reproduction and fertility is mounting rapidly owing to the increasing number of scientifically based clinical stud- PEARSON AND KENAGY ies, the greater importance attached to pro- ductivity in farm animals, the extension of field and laboratory studies to additional species, and the growing realization of the urgent need for finding means of controlling fertility in man.” For three decades this journal has advanced in a distinguished manner the research interests of reproduc- tive biologists. The first issue of volume 1 contains Hilda Bruce’s description of a pheromonal influence on reproduction that came to be known as the Bruce Effect (Bruce, 1960). A recent number (1988, no. 1), ed- ited in Cambridge by Barbara Weir, with E. J. C. Polge as Chair of the Executive Com- mittee, contains articles on the reproduc- tion of no less than 16 genera of mammals. The Johns Hopkins Legacy Returning to 19th-Century North Amer- ica, the Johns Hopkins University was es- tablished in Baltimore, Maryland, in 1876. The goal of the biology program was to pro- vide students with hands-on, laboratory- oriented research training rather than the traditional lecture-til-full system; this suc- cessful model was eventually adopted by many North American universities (Ben- son, 1987). Thomas Huxley had been con- sulted extensively during the planning of the curriculum, and he recommended one of his proteges from Cambridge, H. Newell Mar- tin, a physiologist, to be the first professor in the new Biology Department. The ap- pointment of W. K. Brooks, a morphologist, followed immediately. The department subsequently produced an impressive array of scholars including E. B. Wilson, T. H. Morgan, E. G. Conklin, and R. G. Harrison, who all made a great impact on biology. The great influence of biology at Johns Hop- kins on the discipline of mammalian repro- duction was accomplished through a variety of the university’s satellite programs, 1n- cluding the Medical School, the School of Hygiene and Public Health, the Institute for Biological Research, and, beyond the uni- versity itself, the Department of Embryol- REPRODUCTION 21D ogy of the Carnegie Institution of Washing- ton. The Medical School opened in 1893. It was headed by Franklin Mall, who had been head of the Anatomy Department at the University of Chicago, an institution that had been modelled after Johns Hopkins. Many of the movers and shakers in the dis- cipline of reproductive biology, such as Os- car Riddle, B. Bartelmez, Carl Moore, W. C. Young, Karl Lashley, and Frank Beach, were eventually trained at Johns Hopkins. Mall served as Professor of Anatomy at the Hopkins Medical School and encouraged development of at least 20 future professors ofanatomy; three of them are especially per- tinent to this review: George Wislocki, Her- bert Evans, and George Corner. Of these three, anatomist-histologist George Wislocki went from Johns Hopkins to the Medical School at Harvard Univer- sity. He and his colleagues and students, such as Roy Greep, E. B. Astwood, E. W. Dempsey, Don Fawcett, Helen Deane, and William Wimsatt, spread the base of species studied to even more remote corners of the Class Mammalia. Herbert Evans moved from Johns Hop- kins to the Medical School of the University of California in Berkeley, where he founded the Institute of Experimental Biology. Dur- ing nearly four decades he and members of the Institute accomplished a remarkable amount of important research. One of the first achievements was the 1922 monograph on the estrous cycle in the rat, coauthored by zoology professor Joseph Long (Long and Evans, 1922). They had created the Long- Evans strain of laboratory rat and, using the newly discovered vaginal smear technique, revealed the formerly unknown details of the estrous cycle of this laboratory animal. As pointed out by A. S. Parkes (1969), one has only to review the 10 abstracts by Long and Evans in the 1920 Anatomical Record, followed by 13 abstracts in the 1921 Ana- tomical Record by Evans and his associates, to be awed by the sweep of Evans’ early contributions to reproductive anatomy and physiology. This was only a beginning, and was followed in 1931 by a monograph on reproduction in the dog (with H. H. Cole of the Department of Animal Sciences of the University of California at Davis), dem- onstrations of the pituitary gland as an en- docrine organ, description of the growth hormone, and discovery of vitamin E and its role in reproduction (Parkes, 1969). The third of this trio, George Corner, went to the Medical School at the University of Rochester, where he became widely known for his studies of the menstrual cycle of monkeys, the role of the corpus luteum as an endocrine organ and, with Willard Allen, the purification of the hormone progester- one. In 1940, Corner returned to Johns Hopkins and became Director of the De- partment of Embryology of the Carnegie In- stitution of Washington. His former pro- fessor, Mall, had been the first Director (1914), and two of his Hopkins teachers, Florence Sabin and Warren Lewis, also had distinguished careers at Carnegie. The greatest impact of Johns Hopkins on the discipline of mammalian reproduction was through the Department of Embryology of the Carnegie Institution. It became the most important center of reproductive stud- ies in the United States. At one time or another it included important anatomists and physiologists such as Warren Lewis, George Streeter, Oscar Riddle, Chester Heuser, Arthur Hertig, John Rock, Carl Hartman, George Bartelmez, Sam Reyn- olds, George Corner, Robert Enders, and Harland Mossman (Fig. 3). Two other administrative units that add- ed strength to the Johns Hopkins University were the School of Hygiene and Public Health, created in 1918, and its offshoot, the Institute of Biological Research. The lat- ter was headed by Raymond Pearl and then was absorbed by the School of Hygiene and Public Health after Pearl’s death in 1940. Pearl was a biometrician. He applied sta- tistics to the birth, life, and death rates of populations, especially humans. He had wide-ranging influence through the two journals that he founded: Human Biology and Quarterly Review of Biology. 276 PEARSON AND KENAGY a ro c oxy ot TT e i . al ig ee o- ‘ = * as >. gag é 4 oe a, & . J a5 4 Fic. 3.—Photograph at the Carnegie Institution of Washington, Department of Embryology, Bal- timore, 1931. Left to right: George Streeter, Robert Enders, Chester Heuser, Josephine Ball, Carl Hartman, P. Mihalic, Warren Lewis, Sam Reynolds. The Carnegie group became known for exquisite studies of the embryology of hu- mans, rhesus monkeys, and other mam- mals, published in the Contributions to Em- bryology of the Carnegie Institution. Many of the studies were beautifully illustrated by the noted medical illustrator James Di- dusch. Indeed, the first paper in volume 1 is by Mall himself (Mall, 1915). The Car- negie group moved inevitably into endo- crine studies at a time when the exciting interplay of hormones produced by gonads, pituitary, and placenta was just being dem- onstrated. Other Legacies The significant role played by anatomists at medical schools during the development of our understanding of mammalian repro- duction is illustrated also by research and teaching at many such institutions. Much of the research was directed not at human problems but at a truly comparative un- derstanding. While teaching at Cornell Medical College, Stockard and Papanico- laou (1917) discovered the utility of the vaginal smear in guinea pigs and in humans (the Pap smear). Harland Mossman, after a brief stay at Carnegie, had a long career of teaching and research at the Medical School at the University of Wisconsin, and pub- lished several influential books on human embryology (Hamilton et al., 1945, 1962); comparative morphology of the mamma- lian ovary (Mossman and Duke, 1973); and fetal membranes of vertebrates (Mossman, 1987). The potential of academic institu- tions was demonstrated by this small nu- cleus at Wisconsin; when an international symposium on the comparative biology of reproduction in mammals was convened in 1964 in London, eight of the 30 contribu- REPRODUCTION 217 tors held advanced degrees from the Uni- versity of Wisconsin. Further aspects of the development of North American reproduc- tive physiology in the early 20th Century are presented by Clarke (1987). Another radiation directly traceable to the Carnegie group was into a government- sponsored program to understand the re- productive performance of commercially important fur-bearing mammals. This pro- gram was led by Frank Ashbrook in the Division of Fur Resources, U.S. Depart- ment of Agriculture (later Fish and Wildlife Service of the Department of Interior). Studies were conducted on the reproduction of fur seals, martens, minks, foxes, nutrias, and muskrats. Some of these studies were carried out at Swarthmore College near Philadelphia under the leadership of Robert Enders, who had spent a stimulating post- doctoral period at the Carnegie Institution. In addition to his own research on the mink and other fur-bearing animals, he used this major project, beginning in the 1940s, to introduce numerous students to research on mammalian reproduction. Some of them, chronologically, were David Bishop (sperm physiology), David Davis (rat populations, stress), Oliver Pearson (reproductive cy- cles), Bent Boving (implantation), Hewson Swift (Sertoli cells), Duncan Chiquoine (germ cells), Allen Enders (implantation), William Tietz (embryogenesis), Edward Wallach (ovarian physiology), Phil Myers (rodent and bat reproduction), and Anne Hirschfield (dynamics of ovarian follicles). Many of these students and more recently their own students continue searching for insights into reproductive biology. Further Notable Publications North American researchers were influ- enced by the excitement over reproductive biology at Cambridge and other European sources in two ways—by reading the Eu- ropean literature and by direct contact with researchers in North America who had been exposed earlier to the ideas and approaches in Europe. For example, workers such as Asdell, Bissonnette, Chang, and Pincus spent early parts of their careers at Cambridge. Meanwhile, North Americans published most of their own work in American jour- nals. Three journals of great importance to reproductive biology were the American Journal of Anatomy (founded 1901), the An- atomical Record (1908), and The Journal of Experimental Zoology (1904). All three were managed by the Wistar Institute in Phila- delphia. A book of undoubted importance in the development of reproductive biology ap- peared in 1932, with a second edition in 1939. Professor Edgar Allen at the Univer- sity of Missouri, who had published on the early embryology of humans in the Carnegie Institution Contributions to Embryology, assembled a collection of coherent reviews by 21 distinguished collaborators that was published under the title of ““Sex and Inter- nal Secretions.” It was dedicated to A. D. Mead, one of the members of the staff in anatomy at the University of Chicago in its early days. This book enabled a new gen- eration of students to approach reproduc- tive studies with a more solid foundation in the new science of endocrinology than was available to the generation weaned on Marshall’s book. W. C. Young edited a third edition in 1961. Studies of reproduction in farm livestock were conducted largely by federal agencies and by universities with an agricultural em- phasis, both in Europe and the United States. A milestone of this radiation, which dem- onstrated the coming-of-age of comparative reproductive biology, was the appearance in 1946 of “Patterns of Mammalian Repro- duction” by S. A. Asdell. Asdell came as a postdoc from England to Corner’s labora- tory at the University of Rochester Medical School, and later became a professor in the Department of Animal Husbandry at Cor- nell University. Asdell realized that “a beneficial purpose would be served if the available information on mammalian re- 120 100 10.¢] Oo 122) © a © Number of Papers Marshall, 1910 Marshall, 1922 NO O 1880 Marshall, 1925 PEARSON AND KENAGY Asdell, 1946 1980 1940 1960 Year of Citation Fic. 4.—A century of research on mammalian reproduction. Dates of appearance of 2,346 papers cited by Mossman (1987). Significant publications or events are noted, as in Figure 1. production were brought together, species by species... .”” After paying tribute to his great predecessor at Cambridge, F. H. A. Marshall, Asdell displayed the fruits of the labors of hundreds of authors who had stud- ied the reproduction of about 382 genera and 850 species of mammals. In those pages one could find information ranging from the unilateral functioning of platypus ovaries (page 37) to the number of spermatozoa in the ejaculate of the donkey (page 405). An expanded version of Asdell’s book has ap- peared recently (Hayssen et al., 1993). We have compiled a distribution of the dates of 1,362 literature citations in Asdell’s 1946 book (Fig. 1), covering the late 19th and first half of the 20th centuries. Studies in mammalian reproduction clearly blos- somed beginning in the 1920s. The dates of Marshall’s books, of the founding of the ASM, and of Allen’s book on sex and in- ternal secretions are indicated as reference points. The decrease in number of citations in the mid-1940s is partially the result of World War II, in addition to the decline expected for bibliographic truncation at the approach of the publication date of Asdell’s book. Figure 4 illustrates further prolifera- tion of work in the 1960s and 1970s, fol- lowing three-quarters of a century over which the early historical background was built. Another serial, Biology of Reproduction, was Started in the United States in 1969, edited by H. H. Cole. It too continues to publish scores of papers each year in com- parative reproductive anatomy and physi- ology. With growing audiences of university stu- dents, in addition to the research specialists, a parade of text books in reproductive bi- ology arrived on the scene in the 1960s, 70s, and 80s. These books, mostly dealing with all vertebrates, rather than exclusively with mammals, are general and broad enough to be useful as texts for undergraduate zoology courses in reproduction, yet most of them also contain sufficient synthesis and over- REPRODUCTION 219 view along with the observational detail to make them useful in a personal research library. Sadleir’s book (1969) on mammals emphasizes reproductive ecology, breeding patterns, and responses to environmental conditions; his later book (1973) on verte- brates is much broader in scope and surveys general reproductive patterns and compar- ative anatomy and physiology. Nalban- dov’s book (three editions: 1958, 1964, and 1976) emphasizes the reproductive physi- ology and anatomy of mammals and birds. Van Tienhoven (1968, 1983) treats the physiology and anatomy of all vertebrates. Two of the most recent books on vertebrate reproduction (Bliim, 1986; Jameson, 1988) are organized thematically, rather than tax- onomically and, in addition to the usual information on reproductive patterns, anat- omy, and physiology, provide a greater comparative and evolutionary perspective and greater integration of behavioral themes with all these areas. Finally, and with exclusive attention to mammals, several well-produced text sources are available. Austin and Short (1972-1986, eight books, two editions) have produced a series of booklets that cover pretty much the full range of topics in mam- malian reproductive biology, with well il- lustrated examples of research results along with the conceptual developments. Bron- son’s (1989) single-volume book offers an extensive and well laid out analysis of the regulatory processes that comprise mam- malian reproductive physiology set in an environmental context. Flowerdew (1987) provides a useful blend of fundamentals of reproductive physiology with the biology of free-living mammalian populations. Clear- ly, and without our being able to mention all such existing books, a great variety of general reading has become available on mammalian reproductive biology. Proba- bly one of the strongest recent areas of in- tegrative bridging in the field of reproduc- tive biology has been between physiology and behavior (see Eisenberg and Wolff, 1994), Perhaps the most impressive evidence of the growth and vigor of reproductive biol- ogy as a general discipline is the appearance in 1963 and subsequent growth of the Bib- liography of Reproduction. It is published monthly in Cambridge, England, by a con- sortium of reproductive societies in Great Britain, the United States, and Australia. The editors estimated that the annual pro- duction of papers (in 1990) on the repro- ductive biology and clinical sciences of ver- tebrates including humans may be on the order of 20,000. In view of such a torrent of research, the impact of a relatively few institutions and individuals (as we have selected), along with their academic offspring, on the early de- velopment of the discipline of mammalian reproduction becomes quickly lost in the distal branches of the family trees. While emphasizing, and even exaggerating, the roles of only a few individuals, we have omitted untold other early researchers and teachers, many of whom worked in other countries. Thus we admit that it would be impossible to trace a balanced and objective presentation of all the research schools and their modern ramifications in a short article such as this. The rest of our review will thus simply identify the appearance of a selected series of what we believe to be important research trends in reproduction that have developed during the final third of the 20th Century. LATE 20TH CENTURY We find ourselves at the end of the 20th Century in a stream of fast-moving devel- opments and continued new discoveries in reproductive biology as we mark the 75th anniversary of the founding of the ASM. The most comprehensive new treatise on mammalian reproduction (Knobil and Neill, 1988) in the latter part of the century has appeared in two volumes, 2,413 pages, and 60 contributed chapters, each containing from several hundred to a thousand refer- 280 PEARSON AND KENAGY ences. This new work, inspired by Allen’s (1932) original “Sex and Internal Secre- tions,’ was edited and produced in the United States, with most of the authors from North America and many from elsewhere around the world. It provides a strong focus on cells, tissues, and neuroendocrine phys- iology, yet extends as far as reproductive behavior. Our breadth of understanding of repro- ductive physiology and behavior in an evo- lutionary context can only continue to im- prove and become more meaningful. For the entire first century after Darwin’s writ- ings, challenges in the form of important questions in evolutionary theory resulted in important refinements and a maturity in our current view. Therefore, the potential rel- evance of integrative and evolutionary thinking at present is greater than ever. The tendency of so many scientists to specialize SO narrowly offers a new challenge: to over- come narrow specialization by seeking breadth of understanding in the context of evolutionary biology. As an example, a seemingly simple ques- tion remains of interest: why is reproduc- tion typically sexual, rather than asexual, and why are there two, rather than some other number, of sexes (Short, 1994)? Ideas concerning this theoretical and evolution- ary question can lead us in our search for the still unresolved issues of the mecha- anisms of sex determination and sexual dif- ferentiation, which lie at the level of the molecular biology of gene function (Mc- Laren, 1991). Reproduction, Neuroendocrinology, and Molecular Biology Mammalian reproduction is comprised of a great array of processes: gamete pro- duction and release, mating behaviors, fer- tilization, implantation, development, pla- cental function, parturition, lactation, and parental care. Our understanding of each of these processes has developed strongly in conjunction with the identification of hor- mones that control them (Knobil and Neill, 1988). Study of hormones has been a major paradigm of reproductive physiology since the middle of the century, with the advent of radioimmunoassays for measuring hor- mone concentrations and the perfection of biochemical techniques for characterizing hormone structure and function. Under- standing the integration of nervous system output, including secretion by neurons of small peptide hormones that stimulate fur- ther hormonal signals that enter the blood stream, has provided the challenge to elu- cidate the role of the brain, hypothalamus, and pituitary in neuroendocrine regulation (Everett, 1988). Despite the general appli- cability of the neuroendocrine paradigm, it should also be useful in elucidating excep- tional patterns and modes of reproduction. For example, the arrest and later reactiva- tion of embryonic development occurs in special cases (“delayed implantation” and ““embryonic diapause’’) where the delay may be associated with either lactation for earlier young that precede the arrested embryo(s), or with environmental factors that allow birth to occur at an appropriate time (Ren- free and Calaby, 1981). Through the extensive series of neuroen- docrine regulatory schemes that have been unveiled by research on mammalian repro- duction, the general field has served as a model for study of neuroendocrinology. One of the newest directions for this research has been the molecular neuroendocrinology of gene expression, i.e., identifying and quan- tifying the first gene products associated with hormone production. This new research trend amounts to another dimension in in- tegrative reproductive biology, namely elu- cidating functional (physiological) aspects of molecular biology. Environmental Physiology and Regulatory Processes Use of environmental information and environmental stimulation or inhibition of reproductive function represents one of the REPRODUCTION 281 most popular themes in reproductive re- search. We will mention only a few high- lights of our current understanding of this area, for which Bronson’s (1989) book pro- vides a useful view. The time course over which seasonally breeding mammals respond and the cues used differ between the sexes and according to different stages in the overall reproduc- tive program, beginning with activation of the gonads and extending through final as- pects of postnatal care and termination of breeding condition (Wingfield and Kenagy, 1991). An enormous literature on the initial predictive effects of day length in stimulat- ing gonadal recrudescence and thus prepar- ing mammals for the onset of breeding (Bronson, 1989; Farner, 1985; Wingfield and Kenagy, 1991) has probably lead to an over- impression of the importance of ‘“‘photo- period”’ in breeding, at least in part because the effect is so consistent, easily obtainable, and the first to occur in a series of steps. Actually, not all mammals are “photope- riodic,” 1.e., capable of differential response to long versus short days. A small number of species (most notably ground squirrels and their relatives in the tribe Marmotini of the squirrel family Sciuridae) show per- sistent endogenous cycles of reproductive function in the experimental absence of sea- sonal changes in day length (Gwinner, 1986). The mammalian mechanism of photo- reception that drives the initial response of the reproductive system begins with the eyes and then a connection through the retino- hypothalamic tract, a neural circuit from the retina to the brain that is distinct from the visual pathway (Rusak and Morin, 1976; Stetson and Watson-Whitmyre, 1976). The information on day length is processed in the suprachiasmatic nuclei of the hypo- thalamus, and signals are then sent through the brainstem and a spinal ganglion and back to another site in the brain, the pineal gland. Finally the daily rhythmic secretion of mel- atonin by the pineal plays an important role in the regulation of reproduction in re- sponse to changes in day length (Binkley, 1988; Hoffmann, 1981; Reiter, 1984). Some of the earliest pioneering work with the pi- neal was that of Wilbur Quay (1956), who studied seasonal and sexual variation in the pineal of Peromyscus. Many aspects of environmental infor- mation besides day length, including the so- cial context of an animal in its population, provide supplementary stimuli that syn- chronize, integrate, and modify the repro- ductive responses at all stages of the breed- ing cycle (Wingfield and Kenagy, 1991). Manipulations of simulated environmental conditions have been conducted to observe these responses, often including hormonal measurements, to environmental factors such as food supply (quantity and quality), water availability, temperature, and the so- cial setting and attendant cues (Bronson, 1989; Wingfield and Kenagy, 1991). Some of the most useful research has involved species that can be studied both in the field, for correlative analysis, and in the labora- tory, where simulation and manipulation can be carried out. Comparative field in- vestigation of multiple species has illustrat- ed that diverse patterns of breeding occur even in the same environment, and that body size, phylogeny, and specific adapta- tions of species account for the differences in timing and intensity of reproduction (Kenagy and Bartholomew, 1985). Such field observations have indicated the potential for each species to utilize different cues and to respond with different sensitivities to the entire range of environmental factors. One of the most obvious and direct phys- iological responses that involves regulation of reproductive function is the availability of appropriate amounts and quality of nu- trients and energy. Nutritional plane and energy balance act directly on the animal’s metabolism and the assessment of body condition (I’Anson et al., 1991). Research in this area involves integration of data on general metabolism and metabolic hor- mones, as well as relevant organs such as the thyroid and adrenals, with the neuroen- docrinology of the hypothalamic-pituitary- gonadal axis. The mammal’s assessment of its nutritive plane and energy balance ap- 282 pears to play a direct day-by-day role in the onset and maintenance of reproductive function. A mechanism of reproductive stimula- tion in mammalian herbivores that has re- mained an attractive research subject is the possibility that fresh green food contains a gonadotropic chemical signal (Friedman and Friedman, 1939). A natural plant com- pound, 6-methoxy-2 benzooxazolinone (6- MBOA), has more recently been identified and shown experimentally to stimulate re- productive function (Berger et al., 1981). Since the initial demonstration of this effect, similar results have been obtained in several rodent species. However, much remains to be learned about this effect, the extent of its occurrence among rodents, and the strength of interactions between the effect of 6-MBOA and other environmental factors that promote reproductive responses. It could be argued, for example, that because food is available already at the time it is being consumed, there would be no need for a predictive cue. The fact that a com- pound of interest has been identified has opened the door to new research possibili- ties. Reproductive Energy Expenditures The study of energy relations in repro- duction has continued to develop in pop- ularity (Loudon and Racey, 1987). Energy is a meaningful reflection of allocation to reproduction and the relative functional sig- nificance of both physiological and behav- ioral work; it is often considered to be a currency that might represent fitness. The reproductive energy allocations of small mammals are of particular interest because of the extreme maternal intake and expen- diture that must be required to support a litter whose requirements eventually far ex- ceed those of the mother herself (Pearson, 1944). Considerable impetus to the analysis of energy use in animals came from the ef- forts of two researchers in American agri- cultural university settings at the middle of PEARSON AND KENAGY the 20th Century. Both S. Brody (1945) of the University of Missouri and Max Kleiber (1961) of the University of California at Da- vis produced important books that present the usefulness of energy analysis. Attention recently focused on measuring the energy allocated to reproduction and growth in the context of life histories of free- living animals. It is clear that for many spe- cies the peak of all energy expenditures is reached by females during lactation (Ofte- dal, 1984). Some of the earlier attention to “reproductive energetics’ that addressed only the basal, nonreproductive rates of en- ergy expenditure will not remain as useful as newer, more explicit approaches (Loudon and Racey, 1987). A more direct approach that seeks to quantify reproductive energy expenditure and intake as they approach peaks may allow us to understand energetic bottlenecks associated with reproduction and even thereby the impact of reproduc- tive expenditures on fitness costs (Daan et al., 1991; Kenagy et al., 1990). Olfaction and Regulation of Reproduction Mammals generally rely to a much greater extent on the use of air-borne chemical in- formation concerning their environment and their conspecifics than do most other ver- tebrates. Olfactory sensation and “‘phero- mones” are particularly important in repro- ductive behavior and physiology, which has made mammals the most important re- search model for the study of olfaction (Booth and Signoret, 1992; Marchlewska- Koj, 1984; Vandenbergh, 1988). Next to research on mammalian olfaction, that on insects is far greater than on all the other vertebrate classes. The function of air-borne chemicals (pheromones) to prime other in- dividuals by influencing their physiology and behavior probably extends across most mammalian orders; pheromones play a role not only in priming the initial (puberty or recrudescence) and mating stages of repro- duction, but extend through the time of lac- REPRODUCTION 283 tation and mother-young relations, and be- yond that to the level of recognizing the identity of individuals within a population (Booth and Signoret, 1992). Substantial documentation is available for pheromonal influences such as the cancel- lation of pregnancy due to the odors of a strange male (the classical “‘Bruce Effect’; Bruce, 1960), the accelerated onset of pu- berty in females due to the odors of males, and the inhibition of onset of female repro- duction by the odors of other females or family (Vandenbergh, 1988). The impact of this field of research has been substantiated by study of these kinds of processes in the field, which represents an important con- tribution to population biology and behav- ior. Behavior and Neuroendocrinology During the last quarter of the 20th Cen- tury the contributions of studies of neu- roendocrine mechanisms to the under- standing of reproductive behavior have become extremely important. The popular- ity of such research derives from its ability to address ecological and evolutionary questions with the approaches of neuro- biology and molecular biology (Crews, 1992). Such a potential for integrative ex- ploration with a focus at the organismal lev- el reflects back to a view that prevailed at the founding of the ASM in 1919. It is grat- ifying, in light of the enormity and diversity of the modern biological research enter- prise, that modern mammalogists have the opportunity to foster interest in the per- spective of mammals as organisms. Research on the diversity of reproductive patterns and their mechanisms of neuroen- docrine control has produced valuable evo- lutionary insights. For example, certain bats have temporally dissociated the time of mating from the time of gametogenesis by allowing hibernation to intervene; the gen- eration of neural and endocrine signals that direct this program modification illustrates the adaptive adjustments that can evolve within the constraints of the mammalian system (Crews, 1992). As another example, we have accumulated information on over 50 species of primates alone concerning var- ious patterns of neuroendocrine regulation that sustain the diversity of sexual behavior strategies within this group (Dixson, 1983). An area of mammalian reproductive bi- ology that has relied on integration of phys- iological and neuroendocrine analyses going back to the middle of this century, and even earlier, is represented by the classic rodent population studies of Christian and Davis (1956). The potential interaction of the ad- renal glands (and glucocorticoid hormones) with somatic and reproductive condition became apparent with the advent of the “stress” concept by Selye (1936). Neuroen- docrine mechanisms of reproductive func- tion and the interaction of this with stress physiology have thus been a long-standing aspect of research on small-mammal pop- ulation regulation (Lee and McDonald, 1985). The most recent research has dem- onstrated the action of glucocorticoids in establishing a behavioral basis for differ- ences among individuals within popula- tions (Sapolsky, 1992). Marsupials Mammalian diversity has provided a ba- sis for comparative functional studies as well as evolutionary analysis. In this regard the marsupials represent a most remarkable payload of fascinating subject matter. J. P. Hill, C. G. Hartman, and G. B. Sharman were the earlier pioneers of marsupial re- productive biology. Since their time, re- search has been conducted by many others, especially in Australia, both at the univer- sities and at other institutions, particularly the Commonwealth Scientific and Indus- trial Research Organization (CSIRO) and its Division of Wildlife and Ecology, known earlier by other names. ‘“‘Reproductive Physiology of Marsupials” (Tyndale-Biscoe and Renfree, 1987) is an excellent mono- graphic review of this research, answering 284 PEARSON AND KENAGY many earlier questions concerning patterns and mechanisms, and raising new questions for future research. Many of the most re- markable contributions to marsupial repro- ductive endocrinology involve the process of embryonic diapause, originally identified by G. B. Sharman (1955). This process has since been shown in macropod marsupials to include simultaneous maintenance of two or three young of different ages by a mother and the production of milk of two different types out of different teats to support young of different ages (Tyndale-Biscoe and Ren- free, 1987). The evolutionary question as to why mar- supials quickly pass through uterine embry- onic life and then so greatly prolong lacta- tion, as the major avenue of matrotrophy for development, remains open. One idea, now dispelled by recent immunological research (Rodger et al., 1985), was that mar- supial mothers have a short gestation be- cause the trophoblast lacks the immuno- suppressive capability that would allow it to remain in the uterus without being re- jected by the mother as “foreign”? tissue. Fetal immunosuppression had already been recognized as a basis for eutherian maternal recognition of pregnancy and retention of young in the uterus, and was only demon- strated recently in marsupials (Rodger et al., 1985). New arguments for the evolutionary predilection of marsupials for lactation over placentation must be developed and sup- ported. It is clear that the marsupial mode of reproduction is adaptive and should not be considered “‘primitive”’ or “inferior” — which was an inappropriate notion that dates back to the earliest discoveries of the pouch mode of nurturing extremely immature newborn. Reproductive Technologies Experimental reproductive biology has both agricultural and medical applications. Manipulations of hormones, cells, and tis- sues were underway by the mid 20th Cen- tury, whereas genetic (transgenic) manipu- lation did not arise in the applied context until the 1980s. Many aspects of reproduction have been manipulated to increase production by farm animals (Betteridge, 1986). These include artificial insemination, induction of estrus, synchronization of estrus or ovulation in groups, embryo transfer and manipulation, and in vitro fertilization; development of diagnostic tests has improved the usefulness of all these techniques. Genetic engineering, the insertion of specialized hormone-pro- ducing genes in transgenic animals, is being tested actively for applications such as en- hancement of milk and meat production by growth hormone (Pursel et al., 1989). Other manipulations of mammalian re- production are being developed in wildlife conservation or management and in pest control. Captive breeding programs, which often include artificial insemination or em- bryo transfer, have been the only apparent alternative for maintaining some rare spe- cies, either in zoos or wildlife sanctuaries. On the other hand, explorations are being made of means to curb female reproduction, for example, in elephant populations that are overcrowded due to habitat destruction; in this case the antigestagenic steroid RU486 has been proposed as an abortion agent (Short, 1992). Finally, artificial steroid hor- mones that produce infertility or disturb normal function have recently been pro- posed to control pest populations of wild rodents (Gao and Short, 1993). Human reproductive technology ad- dressed birth control as a first priority and achieved this in the 1950s; control of the human population had been established as a goal of public planning (Austin and Short, 1986). Recently, immunological techniques have been applied to fertility control in the form of the “pregnancy vaccine” (Wang and Heap, 1992). Enhancement of fertility rep- resents a growing enterprise of the 1980s and 1990s, with in vitro fertilization and manipulations of embryos becoming more important bases of attempted therapies. Fi- REPRODUCTION 285 nally, and with even greater ethical reser- vations, we are moving in the 1990s in the direction of genetic manipulations, gender manipulations, and transgenic innovation. Clearly the creativity of scientists and the demands of at least some members of so- ciety will drive us further. In this realm our ethical and legal systems have much catch- ing up to do, as we struggle to deal with ‘‘what science has wrought.” Natural History and the Future Certainly scientific cleverness and crea- tivity will spur us on to new vistas in re- productive biology. Approaching the end of the century, we are well equipped with tech- nological potential to make new discover- ies. It is reassuring to know that natural his- tory and biodiversity remain part of the stuff from which we can extract discoveries. For example, this 75th anniversary year of the ASM we will learn of something that seems to violate a simple generality of mammalian parental care standards, and it was discov- ered serendipitously by unsuspecting inves- tigators in Malaysia, who had set up mist nets for birds (Francis et al., 1994). The discovery was a population of fruit bats (Dy- acopterus spadiceus) with males that had actively lactating mammary glands, yet also, later discovered, actively spermatogenic testes. Nature will certainly continue to sur- prise us and teach us, even as we enter the 21st Century. We hope that the present historical syn- opsis of some of the highlights of mam- malian reproductive biology over the past 75 years will offer some insights to mam- malogists both young and old. From the standpoint of the ASM, some aspects of the early beginnings were provincially North American in scientific character. Another important trend in the history of science, along with the modernization of travel and communication, has been the internation- alization of science. As modern scientists we have much available in the way of sci- entific resources to enhance our future pur- suits and a whole world in which to do so, yet as mammalogists we also have our an- imals. Being oriented to the biology of the Class Mammalia, we can distinguish our- selves by continuing to seek the insights that will come from continued attention to these animals and their natural history and di- versity. Acknowledgments We thank K. Benson and M. Wake for histor- ical references and A. Enders for providing Fig- ure 3: Literature Cited ALLEN, E. 1932. Sex and internal secretions. First ed. Williams and Wilkins, Baltimore, 951 pp. . 1939. Sex and internal secretions. Second ed. 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Oxford Reviews of Reproductive Biology, 14:303-370. WINGFIELD, J. C., AND G. J. KENAGy. 1991. Natural regulation of reproductive cycles. Vertebrate Endo- crinology: Fundamentals and Biomedical Implica- tions, 4(B):181-241. Youna, W. C., (ED.) 1961. Sex and internal secre- tions. Third ed. Williams and Wilkins, Baltimore, 2 volumes, 1,609 pp. MOLECULAR SYSTEMATICS RopDNEY L. HONEYCUTT AND TERRY L. YATES Introduction Be the founding of the American So- ciety of Mammalogists in 1919, Nut- tall (1904) wrote a paper on the use of blood immunology in comparative studies of an- imals. This paper was the prelude to later comparative serological papers (see Boy- den, 1942). By 1953 the molecular structure of DNA had been discovered (Watson and Crick, 1953), yet it was not until much later that systematists and evolutionary biolo- gists capitalized on this discovery and the earlier serological findings. Molecular sys- tematics is a young field that the founders of the ASM probably never imagined. Nev- ertheless, from the beginning, research on mammals played an important role in the development of the field of molecular sys- tematics, and in many cases mammalian taxa were used to investigate the patterns and processes of molecular evolution. It was not until the middle to late 1970s, however, that mammalogists began to use cladistic methodology and molecular characters in phylogeny reconstruction and the study of evolutionary processes. Once the applica- tion of these techniques began, the field of molecular mammalian systematics explod- ed and has been rapidly growing as a result of increased access to molecular techniques and computer technologies. The purpose of this chapter is to provide an historical account of mammalian mo- lecular systematics. We present this infor- mation in three parts. First, we describe sev- eral molecular techniques and discuss how these have been used in mammalian sys- tematics. Second, we discuss how mammals have been used to study the molecular evo- lutionary process, especially as it relates to the derivation of a molecular clock. Finally, we provide an overview of emerging issues and future directions in mammalian mo- lecular systematics. Molecular Techniques in Mammalian Systematics Protein Electrophoresis For the past 30 years, protein electropho- resis has been the most extensively used method by those interested in patterns of genetic variation within and between pop- ulations and species. The method allows for the recognition and quantification of allo- zyme differences for both enzymatic and nonenzymatic proteins. These differences are observed as changes in migration of pro- teins across an electric field, primarily as a MOLECULAR SYSTEMATICS 289 consequence of changes in net charge (size and shape are minor factors as well) of the protein. These changes are genetically based and reflect underlying changes in amino acid sequence between products of alleles at the same locus. As a result, genetic variation at multiple loci can be examined and used as characters in comparative studies. The application of protein electrophoresis in evolutionary studies has been enhanced by a continual refinement of electrophoretic techniques (Harris and Hopkinson, 1976; Hunter and Markert, 1957; Murphy et al., 1990; Selander et al., 1971; Shaw and Pra- sad, 1970). Two early technique papers, Harris and Hopkinson (1976) on humans and Selander et al. (1971) on Peromyscus polionotus, have continued to be important contributions to mammalogy because they provided the detailed conditions (e.g., stains and buffers) for examination of electropho- retic variation at many loci in mammalian species. Michael H. Smith was a coauthor on the Selander et al. (1971) paper, and he has continued to promote protein electro- phoresis by training and collaborating with a large number of mammalian systematists and evolutionary biologists. Most electrophoretic studies during the 1960s and 1970s consisted of an examina- tion of genetic variation within populations and species, with an emphasis on popula- tion genetics and the selectionist versus neu- tralist controversy (Harris, 1966; Hubby and Lewontin, 1966; Hubby and Throckmor- ton, 1965). As indicated by Selander and Whittam (1983), the neutral theory provid- ed a null hypothesis for those interested in levels of diversity in structural genes. As a result, many of the earlier studies of allo- zyme variation attempted to interpret the observed levels of genetic heterozygosity and polymorphism found in species in light of neutral models as well as differences in se- lection pressures and life history strategies (Allendorf and Leary, 1986; Hedrick et al., 1976; Lewontin, 1974: Nei and Graur, 1984; Nevo, 1978; Selander, 1977; Selander and Kaufman, 1973). Research on genetic vari- ation in mammals, using electrophoretic techniques, began in the middle 1960s and paralleled similar studies on other organ- isms. This research can be subdivided into: 1) microevolutionary studies and studies of geographic variation; and 2) macroevolu- tionary studies. Microevolutionary studies. —The primary emphasis of early microevolutionary stud- ies ON mammals was on levels of genetic diversity within and between populations and the microevolutionary processes re- sponsible for the variation observed (e.g., random genetic drift, migration, population bottlenecks, selection). One of the more in- teresting debates pertaining to mammals re- lated to an interpretation of genetic varia- tion within and between populations and species, especially in fossorial mammals (Baccus et al., 1983; Kilpatrick and Crowell, 1985; Nevo, 1985; Nevo and Shaw, 1972; Patton and Yang, 1977; Penny and Zim- merman, 1976; Sage et al., 1986; Schnell and Selander, 1981; Selander et al., 1974; Straney et al., 1976, 1979; Yates, 1983). Ev- itar Nevo and colleagues (Nevo, 1978, 1985; Nevo and Shaw, 1972; Nevo et al., 1974) found a correlation between biotic factors associated with the environment and allo- zyme polymorphism and heterozygosity in mammalian species, suggesting “‘adaptive relationships between genetic variability and spatial environmental heterogeneity.’ The low levels of genetic variation seen in fos- sorial mammals was interpreted as selection for homozygosity in a narrow subterranean niche. Other electrophoretic studies on pri- marily fossorial mammals disagreed with Nevo’s interpretations (Patton and Yang, 1977; Penny and Zimmerman, 1976; Sage et al., 1986; Schnell and Selander, 1981; Selander et al., 1974). These studies re- vealed no positive relationship between “niche-width” and genetic variability in fossorial and non-fossorial mammals, sup- porting a more important role for historical factors related to fluctuating population size, founder events, and random drift. The data ZOU on this topic are still equivocal and little consensus has been achieved. Some of the more interesting studies of microgeographic variation in mammals us- ing electrophoresis have utilized genetic markers to examine both interactions be- tween hybridizing species or chromosome races (Baker et al., 1989a; Cothran and Zimmerman, 1985; Gentz and Yates, 1986: Greenbaum, 1981; Greenbaum and Baker, 1976; Hafner et al., 1983; Heaney and Timm, 1985; Herd and Fenton, 1983; Nel- son et al., 1987; Patton et al., 1972, 1979a, 19795; Smith and Patton, 1984; Sullivan et al., 1986) and the structure of mammalian populations as a result of social organization and dispersal patterns (Chesser, 1983; Gaines and Krebs, 1971; McCracken and Bradbury, 1977, 1981; Scribner et al., 1983; Smith et al., 1983; Wilkinson, 1985). The most extensive research on mammalian hy- brid zones has been conducted on hybrid- izing chromosomal races of Peromyscus leu- copus (Adkins et al., 1991; Baker et al., 1983: Nelson et al., 1987; Stangl, 1986), Uroder- ma bilobatum (Baker, 1981: Greenbaum, 1981), and Geomys bursarius (Baker et al., 1989a; Bradley et al., 1991a, 1991). These studies have characterized gene flow across hybrid zones using a combination of chro- mosomal and gene markers (both nuclear and mitochondrial) and have demonstrated that the dynamics of mammalian hybrid zones differ with respect to the origin of variation, the distribution of that variation, and the survival of hybrid individuals. Finally, patterns of both microgeographic and macrogeographic variation have been used in studies of threatened and endan- gered species of mammals (Bonnell and Se- lander, 1974; Chesser et al., 1980; Dragoo et al., 1990; Forman et al., 1986; Hafner and Yates, 1983; Hamilton et al., 1987; Kil- patrick et al., 1986; Newman et al., 1985; Sullivan and Yates, in press; Wayne et al., 1986, 1991; Wayne and Jenks, 1991). Some of this research has focused on the overall level of genetic variation within species of mammals as a consequence of past popu- HONEYCUTT AND YATES lation bottlenecks and other demographic features, and other studies have attempted to discuss conservation issues (e.g., identi- fication of unique genetic stocks and deter- mination of population status) in light of observed levels of genetic variation. The classic studies by Stephen J. O’Brien and colleagues on genetic variation in the chee- tah (Newman et al., 1985; O’Brien et al., 1983; 1985, 19874) and other felid species (O’Brien et al., 1986, 1987a, 1990: Packer et al., 1991; Roelke et al., 1993) have con- tributed greatly to our understanding of population bottlenecks and how genetics can be used in the conservation of mammalian species. These studies helped pave the way for a more routine use of genetic techniques and theory in conservation and manage- ment. Geographic variation.—Protein electro- phoresis also has been used to examine pat- terns of geographic variation in mammals, with the majority of the studies pertaining to patterns of variation in rodents. These geographic studies have focused on issues pertaining to the biogeographic history of relict populations (Hafner and Geluso, 1983; Smith et al., 1973), species such as pocket gophers that demonstrate fragmented pop- ulations and reduced gene flow (Hafner and Geluso, 1983; Hafner et al., 1987; Patton and Yang, 1977; Patton et al., 19795; Smith et al., 1983), species demonstrating a mon- tane distribution (Sullivan, 1985), the bio- geography of species that have a more ex- tended distribution (Nadler et al., 1973; Svoboda et al., 1985), and an examination of speciation patterns within a genus (Nevo et al., 1974; Patton, 1985). In more recent years, electrophoretic data have been com- bined with other genetic, morphologic, and ecologic data in an effort to identify recent or historical factors responsible for ob- served patterns of geographic variation (Av- ise et al., 1979c; Nelson et al., 1987; Nevo et al., 1993: Smith and Patton, 1988). Allozyme variation has been used to compare differences in the overall level of genetic variation between island and main- MOLECULAR SYSTEMATICS Pie land populations of the same species as well as taxa endemic to islands (Aquadro and Kilpatrick, 1981; Avise et al., 19744; Berry, 1964; Kilpatrick, 1981; Patton, 1984). Again, most of these studies have involved rodent populations and, as indicted by Kil- patrick (1981), the overall pattern of vari- ation is one whereby insular populations are more monomorphic than mainland popu- lations. These results suggest that the level of variation on islands is related to the re- cency of colonization, the number of colo- nizations, the immigration rate between the island and mainland, and the effects of founder events and genetic drift. These con- clusions may also hold true for insular pop- ulations on continental land masses as well. Macroevolutionary studies.—As indicat- ed by Avise (1974) and Buth (1984), protein electrophoresis is a valuable tool for ad- dressing taxonomic issues in mammals and determining the relationships among taxa. A large number of electrophoretic studies have been used to identify species bound- aries, identify cryptic species, compare sib- ling species, and determine the taxonomic status of particular species (some of which are threatened or endangered; Dragoo et al., 1990). For instance, Peter Baverstock and colleagues (Adams et al., 1982, 1987; Bav- erstock et al., 1977, 1983, 1984) have used protein electrophoresis to identify cryptic species of bats, rodents, and marsupials in Australia. Similar studies have been con- ducted on Nearctic mammal genera includ- ing Lasiurus (Baker et al., 1988), Geomys (Burns et al., 1985), Spermophilus (Cothran etal., 1977; Hafner and Yates, 1983; Nadler etal., 1982), Blarina (Tolliver and Robbins, 1987), and insectivores in general (Tolliver et al., 1985). Some studies, such as those on Peromyscus comanche (Johnson and Pack- ard, 1974), Peromyscus hooperi (Schmidly etal., 1985), Peromyscus maniculatus/Pero- myscus melanotis (Bowers et al., 1973), and arid-land foxes (Dragoo et al., 1990) were taxonomically focused with the primary role being the determination of the taxonomic status of a particular population or race. Some of the earliest systematic studies employing protein electrophoresis per- tained to the derivation of phylogenetic re- lationships among mammalian taxa. The rodent genus Peromyscus has received con- siderable attention over the years (Avise et al., 1974a, 1974b, 1979c; Bowers et al., 1973; Kilpatrick and Zimmerman, 1975; Patton et al., 1981; Rennert and Kilpatrick, 1986; Robbins et al., 1985; Schmidly et al., 1985; Zimmerman et al., 1975, 1978), and elec- trophoresis has helped resolve many taxo- nomic problems within this diverse genus. Robert Baker and colleagues (Arnold et al., 1982, 1983a; Baker et al., 1981; Koop and Baker, 1983) have conducted a large num- ber of electrophoretic studies on phyllos- tomoid bats, both within and among genera. These studies are significant because they incorporated a cladistic approach (outgroup approach of Baverstock et al., 1979; Patton and Avise, 1983; Patton et al., 1981) to the analysis of allozyme data. In addition, these studies examined phylogenetic hypotheses using multiple data sets and discussed issues of taxonomic congruence (see Mickevich and Johnson, 1976). These studies, in com- bination with immunological, chromosom- al, and morphological data, resulted in a revised phylogenetic classification for the bat family Phyllostomidae (Baker et al., 19895). Phylogenetic studies also have been con- ducted on a large number of other mam- malian taxa, including rodents (Arnold et al., 1983; Best et al., 1986; Cook and Yates, in press; Hafner, 1982; Hafner et al., 1981; Honeycutt and Williams, 1982; Janecek et al., 1992; Johnson and Selander, 1971; Nel- son et al., 1984; Woods, 1982; Zimmerman and Nejtek, 1977), insectivores (George, 1986; Yates and Greenbaum, 1982; Yates and Moore, 1990), and carnivores (Wayne and O’Brien, 1987). Although these studies vary in the analytical approach chosen, the resultant phylogenies have been used to ad- dress hypotheses related to the biogeogra- phy and speciation. In this regard, studies designed to examine coevolution among 292 HONEYCUTT AND YATES mammalian hosts and their parasites are some of the more innovative in terms of using molecular phylogenies to examine evolutionary processes (Gardner, 1991; Hafner and Nadler, 1988, 1990: Reduker et al., 1987). Concluding remarks concerning electro- phoresis. — Protein electrophoresis is still the most cost-effective and rapid approach for assessing patterns of genetic variation, and it is very important in areas where little is known about the taxonomy of specific groups. In short, if one is interested in vari- ation within a genus, electrophoresis has been and will continue to be the best starting point for the assessment of genetic variation and species-level differences. Having said this, we must add that the analysis of allo- zyme data has changed significantly over the past 20 years. Phenetic analyses utilizing distance estimates (Nei, 1972; Rogers, 1972) and clustering approaches that assume rate constancy have been shown to be inappro- priate (Buth, 1984; Farris, 1972, 1985; Mi- yamoto and Cracraft, 1991; Swofford and Berlocher, 1987; Swofford and Olsen, 1990). Today, allozyme data can be analyzed more objectively using either distance approaches that do not assume rate constancy (Farris, 1972; Felsenstein, 1982, 1990; Fitch and Margoliash, 1967) or cladistic approaches (Farris, 1988; Patton et al., 1981; Swofford, 1990; Swofford and Berlocher, 1987; Swof- ford and Olsen, 1990) that treat loci (or al- leles) as character states. If one peruses the papers that have been published on mam- mals over the past 20 years, the trend to- ward a cladistic approach in phylogeny re- construction is apparent. Finally, one of the major contributions that an interest in allozyme variation con- tributed to mammalogy is the formation of frozen tissue collections at several major museums including: 1) Texas Cooperative Wildlife Collection, Texas A&M Univer- sity; 2) Museum of Vertebrate Zoology, University of California at Berkeley; 3) Mu- seum of Southwestern Biology, University of New Mexico; 4) The Museum, Texas Tech University; 5) San Diego Zoo; 6) Section of Mammals, Carnegie Museum of Natural History; and 7) Natural History Museum, Louisiana State University. In addition, there are a large number of laboratories that have considerable frozen tissue holdings. One can affirm that frozen tissue collections are today an important resource to the mammalogical community (Dessauer et al., 1990) and more curatorial research, such as that conducted by Moore and Yates (1983), is needed. In addition, all those involved in studies that include collection of specimens, such as surveys and inventories, should be encouraged to collect tissue samples. Not only are resources limited and these speci- mens are valuable to continued molecular systematic efforts, but those values that ap- ply to long term storage and maintenance of more traditional museum specimens ap- ply to these specimens as well. Immunology One of the oldest molecular techniques for evaluating relationships among mam- malian taxa is comparative immunology (Boyden, 1942; Gerber and Leone, 1971; Goodman, 1963; Leone and Wiens, 1956; Levine and Moody, 1939; Nuttall, 1904), and this technique was perfected by Allan Wilson and Vincent Sarich at the University of California at Berkeley. Wilson, Sarich, and colleagues published a considerable number of papers on the rates of protein evolution and the relationships among mammals and other vertebrates (Carlson et al., 1978; Cronin and Sarich, 1975; Hafner, 1982: Honeycutt and Sarich, 1987a, 1987b; Honeycutt et al., 1981; Maxson et al., 1975; Pierson et al., 1986; Sarich, 1969a, 19695, 1973, 1977, 1985; Sarich and Cronin, 1976; Sarich and Wilson, 1967a, 1967b; Wilson and Sarich, 1969). Most of these studies dealt with intraordinal relationships among mammalian genera and families and em- ployed primarily the immunological tech- niques of precipitin and microcomplement MOLECULAR SYSTEMATICS fixation (MC’F). The two major molecules examined in these studies were albumin and transferrin, and an immunological distance, depicting the amount of amino acid differ- ence between molecules from different taxa, was determined. This quantitative estimate of immunological distance was determined by the degree of reactivity between anti- bodies and antigens from different species based on comparisons of homologous and heterologous reactions (Maxson and Max- son, 1990). In many cases both albumin and trans- ferrin were shown to evolve in a clocklike manner within mammalian orders, and the early studies on primates employed this clock in estimating divergence times for specific taxa such as the hominoid primates (Sarich and Wilson, 1967a, 1967b; Wilson and Sarich, 1969). One exception to the al- bumin clock was found by Arnold et al. (1982) and Honeycutt and Sarich (1987a) for phyllostomoid bats, with considerable rate heterogeneity observed among lineages. Although immunological distance data have been criticized (Farris, 1985), the overall usefulness of these data to mammalian sys- tematics has been verified, with phylogenies from albumin and transferrin being congru- ent, in most cases, with other molecular and non-molecular data (Arnold et al., 1982; Baker etal., 1989a; Dene et al., 1978; Prager and Wilson, in press; Sarich, 1985, in press; Sarich and Cronin, 1976). In at least two cases (Baker et al., 19895; Kirsch, 1977), the phylogenetic trees shown by immuno- logical data were used in combination with other data to revise the classification of mammalian groups. Amino Acid Sequences The most thorough molecular studies of interordinal relationships in mammals have been conducted by Morris Goodman, Jaap Beintema, Wilfried De Jong, and colleagues using amino acid sequence data from ap- proximately 10 polypeptides (Beintema et 209 al., 1973, 1991; Beintema and Lenstra, 1982: Czelusniak et al., 1990; De Jong, 1982; De Jong et al., 1977, 1981; Dene et al., 1982; Goodman, 1976a, 1976b; Goodman et al., 1982, 1985, 1987; Miyamoto and Good- man, 1986; Romero-Herrera et al., 1978). One of the major strengths of amino acid sequences is that the data can be analyzed cladistically. A maximum parsimony pro- cedure was introduced by Moore et al. (1973) to find ancestral codons which minimize the number of mutations over a given network of species. This approach operates on the principle that the genetic code is redundant and, therefore, the number of possible co- dons at a particular node in a network will be minimized. The procedure works back- wards from a derived network and deter- mines ancestral codons for particular nodes. The overall objective of this procedure is to obtain a network or phylogeny of sequences that minimizes the total number of nucle- otide replacements (NR score). Goodman and colleagues have used this procedure for years to examine the relationships of eu- therian mammals and primate taxa. There have been criticisms of the maxi- mum parsimony approach used by Good- man (Kimura, 1981), as well as the resultant trees derived from this approach or amino acid sequence data in general (Wyss et al., 1987). Goodman (1981) addressed some of Kimura’s original criticisms. Issues raised by Wyss et al. (1987), concerning incongru- ence among phylogenies derived from dif- ferent polypeptide sequences and between sequence phylogenies and those derived from morphological characters, are some- what harder to address. As indicated by Honeycutt and Adkins (1993), one critical problem with amino acid sequence data 1s that the numbers and kinds of taxa repre- sented by different genes vary. In addition, some genes are more conservative than oth- ers in terms of the overall amount of amino acid sequence differences between taxa, an observation related to functional con- straints on the molecule. Both of these fac- 294 HONEYCUTT AND YATES tors may contribute to a certain amount of incongruence. More recent studies (Graur et al., 1991; Lietal., 1990, 1992) of relationships among eutherian orders still rely on amino acid se- quence data. In one case, the issue of rodent monophyly has been challenged (Graur et al., 1991; Li et al., 1992). Honeycutt and Adkins (1993) discussed these data at length and suggested that in all of these recent stud- ies the results are equivocal. Nucleotide Sequences Most recent studies on the molecular sys- tematics of mammals have focused on pat- terns of nucleotide sequence divergence in both the nuclear and mitochondrial ge- nomes, and advances in molecular tech- nology have made these studies consider- ably easier. These comparisons can be divided into two major categories, those us- ing indirect estimates of nucleotide se- quence divergence and those employing a direct sequencing method. DNA/DNA hybridization provides a quantitative estimate of sequence differ- ences between single copy nuclear DNAs from two or more taxa. This indirect esti- mate of sequence divergence is based on differences between the melting tempera- tures of a hybrid duplex DNA (heterodu- plex) and DNA from a single species (homo- duplex). The methodology used is based on earlier studies of reassociation kinetics (Britten and Kohne, 1968; Kohne et al., 1972), and in recent years this method has been employed extensively in studies of bird phylogenies (Sibley and Ahlquist, 1981). In fact, Sibley and Ahlquist have published nu- merous papers on avian systematics and have even provided a classification of birds based upon their findings (Sibley et al., 1988). The results and interpretations of DNA/ DNA hybridization studies have been chal- lenged by several individuals (Cracraft, 1987; Sarich et al., 1989). Some of these criticisms arose in direct response to the findings of Sibley and Ahlquist (1984) on hominoid primate relationships. These crit- icisms pertained to the appropriateness of estimates of divergence based on T;)H, a measure of melting differences that includes the non-hybridizing portion of the melting profile. Although many of the issues raised by these criticisms have not been complete- ly answered, DNA/DNA hybridization studies have been conducted on mammals (Arnason and Widegren, 1986; Brownell, 1983; Catzeflis et al., 1987; Kirsch et al., 1990a, 19906, 1991, 1993; Springer and Kirsch, 1989, 1991; Springer and Krajews- ki, 1989). By far the most extensive research on mammals has been conducted by John Kirsch and colleagues at the University of Wisconsin on marsupials, and these studies have provided an excellent assessment of earlier criticisms and potential problems with the technique. Another indirect method of estimating nucleotide sequence divergence involves an examination of restriction site variation in mitochondrial genomes and nuclear genes (for details, see Melnick et al., 1992). In this technique, DNA is digested with restriction endonucleases that specify combinations of primarily four and six base pair sequences. These restriction endonucleases cleave at specific sites and, when digested, the DNA is separated by gel electrophoresis and ei- ther labelled directly in the case of mito- chondrial DNA (mtDNA) or probed with specific cloned DNA fragments. These re- sultant fragment patterns can be used di- rectly to estimate sequence divergence or converted to restriction site maps, making the estimate of sequence divergence more straightforward (for more details see Li and Graur, 1991; Melnick et al., 1992). The analysis of restriction fragment or site variation among mtDNAs has been the most popular approach in most studies involving mammals, and it is impossible to do justice in this review to the many studies that have been done. As indicated by several research- ers (Avise et al., 1984; Brown, 1983, 1985; MOLECULAR SYSTEMATICS 295 Brown et al., 1979, 1982), mammalian mtDNA is maternally inherited and evolves, on average, much faster than nuclear genes. These features have made this molecule ex- ceedingly useful in studies of geographic variation and the biogeography of mam- mals (Avise et al., 1979a, 1979b, 1987; Cann etal., 1987; Patton and Smith, 1992; Riddle et al., 1993; Riddle and Honeycutt, 1990; Wayne et al., 1992), patterns of speciation (Nevo et al., 1993), interactions among hy- bridizing taxa (Baker et al., 1989a; Carr et al., 1986; Nelson et al., 1984), and phylo- genetic studies (Ferris et al., 1981, 1983; George and Ryder, 1986; Honeycutt et al., 1987). Although Allan Wilson, Wesley Brown, Robert Lansman, and John Avise introduced the technique of restriction en- zyme analysis of mtDNA to evolutionary biologists, today there are laboratories all over the world involved in this type of re- search. Restriction site analysis of mammalian nuclear DNA has not been as extensive, with most studies focusing on the ribosomal DNA (rDNA) repeat (see Hillis and Dixon, 1991, for a review). In terms of mammalian stud- ies, two recent studies involving the higher level systematics of bats (Baker et al., 1991) and relationships among rodent taxa (AI- lard and Honeycutt, 1991) have been con- ducted. In both these studies, restriction site variation at the rDNA repeat provided little resolution, with most variation restricted to the nontranscribed spacer region. Direct sequencing of mammalian mito- chondrial and nuclear genes is fast becom- ing the method of choice for those interested in relationships at higher taxonomic levels (see review by Honeycutt and Adkins, 1993). By far, the bulk of data is from the mito- chondrial cytochrome c oxidase subunit II gene (Adkins and Honeycutt, 1991, in press; Disotell et al., 1992; Ruvolo et al., 1991), the cytochrome b gene (Irwin et al., 1991; Sudman and Hafner, 1992), the ND4 and NDS genes (Brown et al., 1982; Hayasaka etal., 1988), and the 12S and 16S ribosomal RNA genes (Allard and Honeycutt, 1992; Allard et al., 1991b, 1992: Hixson and Brown, 1986; Kraus and Miyamoto, 1991; Mindell et al., 1991; Miyamoto and Boyle, 1989; Miyamoto et al., 1989, 1990). These data have been used to address questions pertaining to relationships among taxa within primarily the orders Primates, Ar- tiodactyla, and Rodentia, and in several cases issues pertaining to interordinal rela- tionships were addressed. Two of the more interesting debates concerning ordinal level relationships involved the question of chi- ropteran monophyly and relationships among orders in the superorder Archonta, and in these studies both nuclear and mi- tochondrial gene sequences were used to test conflicting hypotheses (Adkins and Honey- cutt, 1991; Ammerman and Hillis, 1992; Bailey et al., 1992; Honeycutt and Adkins, 1993; Mindell et al., 1991; Stanhope et al., 1992). Research in molecular systematics on mammals using nuclear gene sequences has lagged behind studies of mitochondrial gene sequences. The most extensive data exist for rDNA genes, and these data have consid- erable potential for higher level questions (Hillis and Dixon, 1991; Mindell and Hon- eycutt, 1990). One exception to the more extensive rDNA studies has been the con- sistent research efforts of Morris Goodman and colleagues with respect to determining the relationships among eutherian mam- malian orders using single copy genes or pseudogenes (Bailey et al., 1992; Koop and Goodman, 1988; Koop et al., 1986; Stan- hope et al., 1992). As indicated by Honey- cutt and Adkins (1993), morphology has not been able to resolve the relationships among eutherian orders (Novacek, 1992; Shoshani, 1986; Simpson, 1945) and, if nucleotide se- quence data are to contribute to this issue, considerably more information is needed. Molecular Clock Concept The analysis of morphological change in mammals has revealed irregularity in the 296 HONEYCUPY AND YATES evolutionary process, with different lineages demonstrating mosaic evolution in terms of the overall rate of morphological evolution. This mosaic evolution reflects the overall adaptive radiation observed for mammals, especially in terms of the diversity in form and function seen for higher categories. In contrast to phenotypic evolution, molecules (both proteins and nucleic acids) of mam- mals and other organisms presumably evolve in a neutral fashion, demonstrating a rather constant rate of change through evolutionary time and across diverse tax- onomic groups (Brown et al., 1982; Easteal, 1985, 1990; Kimura, 1983; Sarich and Wil- son, 1967a, 1967b; Wilson et al., 1977; Zu- kerkandl and Pauling, 1965). Some of the principles of the neutral theory were derived to distinguish between evolution at the mor- phological and molecular level. These prin- ciples relate to both the elimination of del- eterious mutations and fixation of variation through selective neutrality as opposed to positive Darwinian selection and the over- all rate of evolution observed for particular molecules as a consequence of the level of structural and functional constraints placed on these molecules. An outgrowth of the neutral theory is the idea of a molecular clock, which sees the evolutionary process at the molecular level as arandom process with a constant average rate of change (Fitch and Langley, 1976; Kimura, 1983; Li and Graur, 1991; Wilson et al., 1977; Zukerkandl and Pauling, 1965). In fact, one might say that the observation of a molecular clock has provided support for the neutral theory. By necessity, the mo- lecular clock is a statistical clock, and it as- sumes a linear relationship between time since evolutionary divergence and molec- ular divergence. Obviously, the best test for a clock is one that evaluates the regularity of overall rates of divergence through time, and this test is best applied in a phylogenetic context (Fitch and Langley, 1976). When evaluating rates of molecular evo- lution, several analytical approaches can be applied. One approach, the relative rate test, first introduced by Sarich and Wilson (1967a, 1967b) and expanded upon by oth- ers (Li and Graur, 1991; Li et al., 1987; Mindell and Honeycutt, 1990; Wu and Li, 1985), is a test for rate uniformity. It re- quires no knowledge of divergence times be- tween species but does presuppose branch- ing order in that an outside reference species or outgroup is required for the examination of lineages sharing a common point of di- vergence. The test is actually a comparison of the magnitude of change along two lin- eages subsequent to divergence from a com- mon ancestor. It has been suggested that more than one outside reference species be used to minimize the effects of back mu- tations and convergent substitutions (Bev- erley and Wilson, 1984). The effects of such homoplasy increase over evolutionary time, thus the need for several calibration points (Gingerich, 1986). Another method, the star phylogeny ap- proach (Kimura, 1983), is a test that con- siders a case where all species diverge at the same point in time from a common ancestor and compares the observed and expected variances in rate under the Poisson process. This approach might be valid for mam- malian orders but the estimates are proba- bly minimal as a result of dichotomous branching (Nei, 1987). Gillespie (1986) has modified this approach to take into account branching. Langley and Fitch (1974) introduced a third procedure that requires knowing the branching order. In this procedure expected branch lengths are calculated using maxi- mum likelihood, and then a test for rate heterogeneity is employed using chi-square analysis. Finally, the absolute rate can be estimated by calculating substitutions along each branch length in a phylogeny and calibrating the evolutionary rate based on dates from either the fossil record or biogeography (Beverly and Wilson, 1984; Maxson et al., 1975; Sarich and Wilson, 1967a, 1967b). What is the evidence for a molecular clock? First, the evolutionary rate of diver- gence in amino acid sequence has been shown to be linear with time. This has been MOLECULAR SYSTEMATICS 207 demonstrated for many proteins in mam- mals, including globins (Kimura, 1983; Li et al., 1985; Zukerkandl and Pauling, 1965). Although the overall rates between proteins may differ, this difference can be explained in terms of functional constraints and is consistent with the neutral theory (Kimura, 1983). Second, a large body of data on al- bumin immunology in mammals has re- vealed an overall relationship between rate of divergence and time (Carlson et al., 1978; Sarich, 1977), and this albumin/transferrin clock has been used extensively in compar- isons of times of mammalian divergence. Finally, at the level of nucleotide sequence in both mitochondrial and nuclear genes, certain types of substitutions demonstrate clock-like behavior in terms of their diver- gence over time (Brown et al., 1982; Bulmer et al., 1991; Easteal, 1985, 1990; Hasegawa et al., 1985; Kimura, 1983; Mindell and Honeycutt, 1990; Miyamoto and Boyle, 1989: Vawter and Brown, 1986). In mam- mals there also is evidence of clock-like be- havior of estimates of divergence derived from DNA/DNA hybridization (Catzeflis et al., 1987; Sibley and Ahlquist, 1984). Although there is some confirmation of rates of amino acid and nucleotide substi- tutions being linear with time, there are many exceptions that challenge the gener- ality of a molecular clock. First, differential rates of evolution have been observed for both nuclear and mitochondrial genes (Ad- kins and Honeycutt, 1991; Bajaj et al., 1984; Britten, 1986; Gillespie, 1991; Goodman et al., 1975; Holmes, 1991; Liand Graur, 1991; Li et al., 1985, 1987; Romero-Herrera et al., 1978; Wu and Li, 1985). Second, both distance estimates from DNA/DNA hy- bridization and synonymous substitution rates in genes suggest a generation time ef- fect for mammals and other animals in terms of overall rates of divergence at the level of nucleotide substitutions (Britten, 1986; Li and Graur, 1991; Li et al., 1985; Wu and Li, 1985). Recently, a relationship between substitution rate differences, body size, and metabolic rates in mammals and other or- ganisms has been found (Martin and Pal- umbi, 1993). Finally, in the case of an elec- trophoretic clock (Nei, 1971; Sarich, 1977; Smith and Coss, 1984), rates calculated from the same overall genetic distances from dif- ferent mammals and other organisms vary as much as 20-fold (Avise and Aquadro, 1982). Therefore, the idea of using an al- bumin clock to set the electrophoretic clock is clearly suspect (Sarich, 1977). As Hills and Moritz (19905) pointed out, molecular divergence and time are corre- lated to an extent. The question, however, pertains to the amount of error associated with any time estimate derived from the magnitude of divergence separating taxa and the various means of clock calibration. In terms of the latter, paleontological and bio- geographical estimates of time since diver- gence have associated errors and, in addi- tion, using a calibrated rate from one set of taxa (e.g., between the rodent taxa Mus and Rattus) to determine time since divergence in an unrelated set of taxa (e.g., another or- der of mammals) can clearly create error if the overall rate or pattern of divergence dif- fers for the same gene between the two un- related groups. Although the error associ- ated with an estimate of absolute time can be great, assessments of relative rates of mo- lecular divergence are very useful to those interested in the processes of molecular evo- lution and the use of molecular characters in phylogeny reconstruction. Clearly, mam- mals provide an excellent model for study- ing either of these two aspects of evolution. Emerging Issues and Future Directions Several major developments over the past three decades have had a profound impact on systematic and evolutionary biology. First, cladistic analysis has become the pri- mary methodological approach used in phy- logeny reconstruction, and it has provided an objective framework for deriving clas- sifications, studying biogeography, and in- vestigating speciation, cospeciation, and 298 HONEYCUTT AND YATES other evolutionary processes (Baker et al., 1989a; Brooks and McLennan, 1991; El- dredge and Cracraft, 1980; Hafner and Nad- ler, 1988, 1990; McKenna, 1975; Riddle and Honeycutt, 1990). Second, the ability to test hypotheses pertaining to the patterns and processes of evolution have been enhanced by the development of more sophisticated analytical procedures and more accessible computer software and hardware (Farris, 1988; Felsenstein, 1990; Miyamoto and Cracraft, 1991; Swofford, 1990; Swofford and Olsen, 1990). Third, genetics and mo- lecular biology have provided information that has broadened our view as to the role of selection and neutrality in the evolution- ary process (Gillespie, 1991; Kimura, 1983; Li and Graur, 1991; Nei, 1987). Finally, variation at the level of genes, gene prod- ucts, and nucleotide sequences has provided a suite of literally thousands of indepen- dently evolving characters that can be used to examine diversity within populations, species, and higher taxa (Hillis and Moritz, 1990a; Honeycutt and Adkins, 1993). All of the above events have contributed di- rectly to the ever increasing use of molecular characters in systematic and evolutionary studies, and today molecular systematics and molecular evolution are two of the fastest growing areas of research in systematic and evolutionary biology. Recent advances in molecular biology have provided an easy-to-use set of tools for mammalogists interested in the origin and diversification of mammalian taxa. The polymerase chain reaction (Allard et al., 1991a; Higuchi and Ochman, 1989; Kocher etal., 1989; Saiki et al., 1988) and improved methods for obtaining nucleotide sequence information (Maxam and Gilbert, 1980; Sanger et al., 1977) are revolutionizing the fields of molecular evolutionary biology and systematics. Literally thousands of molec- ular characters can be used to address ques- tions of higher level relationships among mammalian families and orders and, in combination with morphological data, one can begin to unravel the secret of the mam- malian radiations. One of the most exciting areas of research is the use of ancient DNA, extracted from museum specimens and fos- sils, to provide a historical perspective on the genetics of populations and the rela- tionships among extinct and extant forms of mammals (Higuchi et al., 1984; Paabo, 1989; Paabo et al., 1988, 1989; Shoshani et al., 1985; Thomas et al., 1990). As these techniques become more refined, we may one day be able to address questions per- taining to the early origin of mammals. A major challenge to all mammalogists interested in molecular systematics pertains to data analysis, as can be seen by recent publications on the subject (Felsenstein, 1981, 1984, 1988; Miyamoto and Cracraft, 1991; Swofford and Olsen, 1990). This issue will become even more important as the amount of sequence data increases, and sev- eral questions pertaining to molecular data and the analysis of those data must be ad- dressed. Some of these questions are (for a more detailed discussion on mammalian molecular systematics see Honeycutt and Adkins, 1993): 1) What criteria should be used in selecting the correct molecule and experimental approach? 2) Should one use equal or unequal weighting schemes in an analysis of molecular data? 3) How impor- tant is the selection of an outgroup, and what criteria should be used in selecting out- groups? 4) Which methodological approach to estimating evolutionary trees should be used, and are there situations when one par- ticular method might be superior to the more accepted method? 5) How does one evaluate the reliability of trees derived from molec- ular sequences, and what factors can influ- ence the accuracy of a cladogram? and 6) How does one consider total evidence when evaluating phylogenetic hypotheses, and what are some explanations for incongru- ence among trees derived from different molecular and non-molecular characters? Finally, questions pertaining to the evo- lutionary process are being addressed using a phylogenetic framework (Brooks and McLennan, 1991). For instance, the orga- MOLECULAR SYSTEMATICS nization and evolution of communities are being examined using a combination of bio- geography, phylogenetics, and molecular characters (Avise et al., 1987; Riddle and Honeycutt, 1990; Riddle et al., 1993). As indicated earlier, the process of cospeciation is being studied by comparing the phylog- enies of both the mammalian hosts and their parasites (Hafner and Nadler, 1988, 1990; Reduker et al., 1987). Phylogenies also offer a means of evaluating the evolution of com- plex behavior in mammals (Honeycutt, 1992). Aside from questions pertaining to organismal evolution, gene trees derived from mammals offer a means of examining convergent evolution at the molecular level (Stewart and Wilson, 1987) and the mech- anisms responsible for producing variation (Bradley et al., 1993). 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Biochemical genetics of truei and boylei groups CYTOGENETICS ROBERT J. BAKER AND MARK S. HAFNER Introduction hen we were invited to prepare a re- view of the field of cytogenetics for the 75th anniversary of the ASM we had several discussions on the breadth and na- ture of the subject. This sent us scurrying to A Dictionary of Genetics (King and Stans- field, 1990:98) to determine the exact def- inition of the word cytogenetics: cytogenet- ics—the science that combines the methods and findings of cytology and genetics. This definition failed to provide us with the res- olution that we desired. Pertaining to the field of mammalogy, the word cytogenetics is a synonym for karyology, chromosomal evolution, or chromosome biology. Chromosomes, or collectively, the karyo- type, are subcellular morphological entities, and this chapter on cytogenetics is the only such chapter devoted to a single cellular or- ganelle. Why then is the karyotype accorded such an important position in mammalogy? Several books have been written on this subject, of which two of the best are M. J. D. White’s Animal Cytology and Evolution (1973) and Modes of Speciation (1978b). This organelle (the chromosome) has been implicated in many biological phenome- na including speciation (Baker and Bick- ham, 1986; Bush et al., 1977; White, 1968, 1978a), rapid morphological change (Wil- 310 son et al., 1974), gene duplication (White, 19785), and sex determination (Bull, 1983; Ohno, 1967). However, there may even be more basic reasons that the karyotype has been important to mammalogy. Before the advent of molecular biology, there were few easily quantified characters that provided systematic resolution among closely related species. The karyotype represents such a character. In addition, most karyological techniques are adaptable to field conditions and require minimal expense; therefore, it is not surprising that a number of mam- malogists have chosen to specialize in this area. As is the case with many other sub- disciplines, the field of cytogenetics extends far beyond the classical limits of mammal- ogy. For example, cytogenetics has impor- tant implications in the fields of carcino- genesis, mutagenesis, and medicine. Herein, however, we restrict our report to cytoge- netics as related to the science of mam- malogy. Conceptual Development of the Field The field of cytogenetics was essentially nonexistent prior to 1919. Until the 1950s, CYTOGENETICS ell no reliable methods were available to de- termine diploid number or morphology of chromosomes. Although the theory that he- redity was chromosomally based was de- veloped in the 1890s, this discovery had little immediate impact on the field of mam- malogy. A brief review of the history of our understanding of the karyotype of the hu- man provides insight into the state of the methods available during this time. In the early 1920s, the diploid number for Homo sapiens was commonly described as 24. In 1923, T. S. Painter reported the diploid number was 48 with an XX/XY sex-deter- mining system (Painter, 1923). Not until 1956 (Tjio and Levan, 1956) was the correct diploid number (46) determined. The sig- nificance of the difficulty in documenting the human karyotype is that early methods were tedious, subjective, and labor inten- sive, and they could not be adapted easily to the type of survey work that mammal- ogists usually conduct. Nevertheless, by 1951, two significant lists of chromosomal data had been generated that together de- scribed the diploid or haploid numbers of approximately 175 species of mammals (Makino, 1951; Matthey, 1950). As verified by more recent studies, the majority of these descriptions were reasonably accurate. Even though technical aspects of the field of cytogenetics were rather primitive until the mid-1950s, some theoretical and con- ceptual aspects of the field were remarkably current as early as the 1920s. The following quote is from Painter (1925:407—408): “In the present paper a good deal of atten- tion has been given to chromosome num- bers, yet at the same time it has been fully realized that numbers per se are of second- ary importance. The significant point is that as far as we can gauge it, the total amount of chromatin in the different mammalian groups 1s about the same, and there has been a remarkabie stability in the chromosome associations. Inferentially, we may surmise that the total number of genes is about the same in all groups. In their chromosome constitution, the mammals have shown themselves, so far at least, comparable to an order of insects. If my general conclusion is a valid one, then we may expect that the plotting of chromosome maps in the eutheria will go forward with comparative rapidity, because linkage values established in one group or species can be applied to other forms... . Transverse fragmentation or end to end fu- sion will occasionally upset these relations, but on the whole they should prove the same in different forms, and enable us eventually to plot the chromosome maps of the euth- Cilawe Painter’s (1925) insights into chromo- somal evolution and the future of mam- malian cytogenetics were remarkably pre- scient, especially considering the dearth of actual data that existed in the field of cy- togenetics in the mid-1920s. We encourage the student of cytogenetics to review Pain- ter’s article in its entirety. In the 1960s, there was a burst of activity in the field of cytogenetics that produced accurate diploid numbers and descriptions of karyotypes for a wide variety of mam- malian taxa. Interpretation of these new data was influenced strongly by prevailing views of chromosome evolution in the 1950s and 1960s. For example, it was widely held that most or all chromosome rearrangements re- duced fertility (i.e., fitness); hence, karyo- typic differences were generally viewed as indicators of species distinctiveness. For this reason, the first examples of chromosomal polymorphism discovered within taxa that behaved otherwise as biological species (Ford et al., 1957) received considerable at- tention. Of course there are several exam- ples where numerous chromosomal poly- morphisms exist in naturally occurring populations and these demonstrate rather conclusively that fitness reduction in het- erozygotes can be minimal if not nonexis- tent (Koop et al., 1983; Nachman, 1992a, piZ BAKER AND HAFNER 1992b; Nachman and Myers, 1989; Stangl, 1986). Most mammalian cytogeneticists of the 1960s also assumed that karyotypes iden- tical in gross morphology were also identical at the level of gene order. Of course G-band- ing has shown that similar nonbanded kar- yotypes may underestimate amounts of chromosomal evolution by several orders of magnitude (Baker and Bickham, 1980; Haiduk et al., 1981). Breakage points in chromosomes were assumed to be stochas- tic, such that the independent occurrence of the same rearrangement in separate lineages was considered highly improbable and con- vergent evolution would not be a problem in cytogenetics. The significance of this con- clusion is that when two taxa shared a chro- mosomal rearrangement identified by G-bands, its usefulness as a synapomorphy was almost beyond question. This too has been shown to be inaccurate by several ex- amples, including chromosome 6 in 30 spe- cies of Peromyscus, which may have been rearranged as many as seven times (Stangl and Baker, 1984). The strongest evidence that the same chromosomal rearrangement can occur repeatedly comes from studies of human families that have unusual rear- rangements (such as the 11q;22q; Fraccaro et al., 1980) that have arisen independently in many families from widely separated geo- graphic origins. Chromosomal evolution was thought to be a highly ordered and time- dependent process (John and Lewis, 1966; for review see Baker et al., 1987). Therefore, taxa distinguished by a large number of chromosomal differences were thought to be distantly related. Examples such as the fol- lowing two document that little time or ge- netic distance is required in some cases where extensive chromosomal evolution has occurred. 1) Despite the karyotypic differ- ences between the species of Muntiacus (one with 2n = 6, 7 and the other with 2n = 46), viable offspring are produced by interspe- cific crosses of the two (Wurster and Be- nirschke, 1970). 2) Reithrodontomys mega- lotisand R. zacatacae have widely divergent karyotypes distinguished by over 30 rear- rangements, but the two are not distin- guished by any differences in allozymes at 30 loci (Hood et al., 1984; Nelson et al., 1984). In the 1960s, chromosomes were be- lieved to be stable structures and exchanges between nonhomologous chromosomes were thought to be rare. Barbara Mc- Clintock’s Nobel Prize-winning work (1978) provided the first insights into an excep- tionally dynamic process of exchange among nonhomologous chromosomes. Although the syntenic groups shared by various or- ders of mammals (O’Brien et al., 1985) in- dicate a measure of stability in the karyo- type, nonetheless it is widely documented that the exchange of transposable elements, heterochromatin, and other pieces of DNA, such as ribosomal genes, between nonho- mologous chromosomes is a common pro- cess (Arnheim et al., 1980; Dover, 1982; Hamilton et al., 1990, 1992; Wichman et al., 1991, 1992). Concepts about chromo- somal evolution and the forces that result in chromosomal conservatism in some lin- eages and rapid change in others are being revised continually (Baker et al., 1987; Bradley and Wichman, in press; Grapho- datsky, 1989; Patton and Sherwood, 1983; Wichman et al., 1991, 1992). The primary focus at this time reflects recent technolog- ical advances associated with molecular bi- ology, which has permitted more sophisti- cated experiments and testing of the molecular based hypotheses associated with cytogenetics. Technological Advances Although the microscope was invented in 1590 by Hans and Zacharias Janssen in Holland (King and Stansfield, 1990), in- struments powerful enough to observe chro- mosomes were not designed until the 1800s. It was not until 1888 that the term chro- mosome was introduced by Wilhelm Wal- deyer. The X chromosome was documented in 1891 by Henking, who also described its meiotic behavior. Henking (1891) used the CYTOGENETICS eB: term ““X”’ because the function of the chro- mosome was unknown. The concept of the X chromosome’s involvement in sex deter- mination was developed by McClung (1901, 1902). The Y chromosome was first de- scribed by Wilson (1909). In 1901, Mont- gomery associated maternal and paternal chromosomes into pairs (homologous chro- mosomes) and related this to Mendel’s ge- netic laws. By 1903 the role of the chro- mosome in heredity was demonstrated conclusively by Sutton (1902, 1903). One technical difficulty in examining chromosome morphology and number stems from the fact that the cellular space is small and the methods used to examine chromosomes before 1960 involved squashing cells between a microscope slide and a coverslip (Hsu, 1979). The end result of this procedure was poorly spread masses of chromosomes whose depth extended be- yond the normal field of focus for light mi- croscopes. Therefore, chromosomal counts were made by following within the mass of chromosomes an individual chromosome through several focal lengths. Needless to say, this process was exceedingly tedious and often inaccurate. A technical breakthrough that was of par- amount importance in determining chro- mosomal morphology was the hypotonic pretreatment of cells to enlarge the cells and aid in the ability to see each chromosome of the karyotype as an independent unit in a single field of focus. Hsu (1979) calls this the hypotonic miracle in his well-written documentation of this discovery. Although the effects of hypotonic treatment of cells were described by Slifer in 1934, the sig- nificance of her discovery to the field of cy- togenetics went unnoticed for almost two decades. In 1952, three papers (Hsu, 1952; Hughes, 1952; Makino and Nishimura, 1952) were published describing the hypo- tonic pretreatment phenomenon. Ultimate- ly, hypotonic pretreatment was combined with another methodological breakthrough, the blaze-dry method (Scherz, 1962), to spread the chromosomes effectively from a single cell into a broader field for easier viewing of chromosomal detail. Students of cytogenetics who are interested in the his- tory and development of this field should read Hsu’s (1979) account. Another major methodological break- through in the field of cytogenetics was Krishnan’s (1968) discovery that mitotic in- hibitors such as Colchicine and vinblastine sulfate (Velban) arrest cell division at the metaphase plate. Mitotic inhibitors had been used commonly in plant genetics long be- fore they were applied to mammalian cy- togenetics. For example, Blakeslee and Avery demonstrated as early as 1937 that Colchicine induced polyploidy in plants. Techniques for preferential staining of particular regions of chromosomes (col- lectively called ‘“‘banding’’ techniques) stemmed from work by Caspersson et al. (1968, 1970) and Pardue and Gall (1970). Those generally acknowledged as producing the first Q-bands are Caspersson et al. (1968, 1970), and production of the first C-bands is credited to Pardue and Gall (1970) and Arrighi and Hsu (1971). G-bands were first documented by Seabright (1971) and Sum- ner et al. (1971), R-bands were developed by Dutrillaux and Lejeune (1971), and stains specific for nucleolar organizing regions (NORs) are credited to Matsui and Sasaki (1973). Modern techniques for in situ hy- bridization stemmed from work by Gall and Pardue (1969) and John et al. (1969). In situ hybridization techniques advanced even further with the introduction of nonradioac- tive antibody probes visualized with en- zymes or fluorescent dyes (Frommer et al., 1988; Langer et al., 1981; Manuelidis et al., 1982; Pinkel et al., 1986). A modern review of chromosome banding and other cytoge- netic methods was provided by Sumner (1990). Cytogenetic Studies: Insights from the Journal of Mammalogy There are more than 9,000 scientific jour- nals that deal with the biological sciences. 314 BAKER AND HAFNER In 1992 alone, nearly 7,000 articles in the field of cytogenetics were published in no fewer than 627 different journals (Macgre- gor, 1993). Because of the revolution in mo- lecular biology, the scope of cytogenetics is ever expanding. We feel that valuable in- sights into the nature of the science of mam- malogy can be gained by examination of publications in the Journal of Mammalogy that appeared during this period of expan- sion of the science of cytogenetics. Approx- imately 130 studies emphasizing chro- mosomes or using cytogenetic data or tech- niques have been published in the Journal of Mammalogy since its inception. Included in these studies are the first descriptions of karyotypes of roughly 284 species of mam- mals, including the first karyotypes reported for many mammalian genera and several families. As the following account will doc- ument, the Journal of Mammalogy played only a minor role in the early history of the field of cytogenetics. However, in 1967 it was thrust into the mainstream of mammal cytogenetic research, largely due to the im- provement of karyotyping techniques such as use of mitotic inhibitors and blaze-dry methods that improved the spreading of chromosomes. Since 1966 (Nadler, 1966; Nadler and Hughes, 1966; Singh and Mc- Millan, 1966), the Journal of Mammalogy has played an important role in the field of mammal cytogenetics, especially in the sub- fields of cytotaxonomy and cytosystematics. Readers of the Journal of Mammalogy were introduced to the nascent field of cy- togenetics in L. C. Dunn’s (1921) study of coat-color inheritance in rodents. This study, which also introduced many mammalogists to Mendelian genetics, reported that diploid numbers were known at that time for only four species of rodents: the mouse (Mus); the rat (Rattus); the guinea pig (Cavia); and the Old World rabbit (Oryctolagus; rabbits were then classified as rodents). Based on this fragmentary evidence, Dunn (1921:139) made a remarkably insightful speculation, ““... there is some slight evidence that in the evolution of rodents a fractionation of chromosomes may have occurred, for the mice and rats have 19 (haploid) while the guinea-pigs have 28.’ This comment was all the more remarkable considering that the entire concept of organic evolution was open to question when Dunn published this work. With reference to the haploid-number sim- ilarity between Mus and Rattus, Dunn (1921: 139) commented: “Whether this is due to a community of descent in the terms of cur- rent evolutionary theory or to relationship through some other cause is one of the ques- tions which genetics, aided by the chro- mosome notation, may be expected at some time to answer.” Seventy-two years later Science published a genome issue showing a genetic linkage map of Mus (Copeland et al., 1993) docu- menting exactly the kinds of results pre- dicted by Dunn (1921). Copeland et al. (1993) calculated that based on linkage maps, the mouse and the human have un- dergone approximately 150 chromosomal rearrangements since they last shared a common ancestor (Nadeau and Taylor, 1984). The first figure of chromosomes pub- lished in the Journal of Mammalogy was a camera lucida drawing of meiotic prophase tetrads of the house mouse, Mus musculus (Hoy and Berkowitz, 1931). Although this article described a relatively simple method for fixation and preservation of chromo- somes in the field, it did not catalyze the intense interest in mammalian chromo- somes anticipated by its authors. To the contrary, this article was followed by a hi- atus of almost 30 years, during which time no cytogenetic paper was published in the Journal of Mammalogy. As noted above, two landmark books were published during this time in the rapidly expanding field of cytogenetics: Matthey’s (1950) Les Chromosomes des Vertebres, and Makino’s (1951) An Atlas of the Chromo- some Numbers in Animals. Although these books were primarily compendia of diploid and fundamental numbers known at that time, Matthey (1950) speculated on the po- CYTOGENETICS 315 tential systematic value of chromosomes in the Mammalia. Johnson and Ostenson (1959) were the first to publish a paper in the Journal of Mammalogy that empha- sized the potential usefulness of chromo- somes as taxonomic characters. Their study was primarily a review of taxonomic meth- ods available in 1959, and they reported no new mammalian karyotypes. However, Johnson and Ostenson (1959:573) referred to Matthey’s (1952) pioneering studies of microtine chromosomes and stated: “Such a fundamental difference as in chromo- somes [between two voles, Microtus agrestis and M. pennsylvanicus| must be regarded as strong evidence of species difference.” This was the first of many such statements to appear in the Journal of Mammalogy sig- naling the taxonomic importance of cyto- genetic characters. The first figure of a mitotic-metaphase karyotype to be published in the Journal of Mammalogy appeared in volume 47 (Nad- ler and Hughes, 1966). This karyotype of a ground squirrel (Spermophilus spilosoma) was remarkably clear and showed in con- siderable detail individual chromosomal el- ements. The same year, Nadler (1966) pub- lished the first diagram to appear in the Journal showing hypothetical chromosom- al changes that occurred during the evolu- tionary history of a mammalian lineage (in this case, the ground squirrel subgenus Sper- mophilus). Nadler’s (1966) paper was among the first to bring cytogenetic evidence to bear on higher-order questions in the field of mammalian systematics, a field that, before that time, had been dominated by morpho- logical and paleontological studies. Before 1967, articles on mammalian cy- togenetics were published in a wide variety of outlets including The American Natu- ralist, Anatomical Record, Chromosoma, Experientia, Journal of Genetics, Journal of Morphology, Proceedings of the Society of Experimental Biology and Medicine, and a myriad of other books, journals, proceed- ings, and reports. In an effort to organize the rapidly expanding literature in this field, Hsu and Benirschke published in 1967 their important compendium titled, 4n Atlas of Mammalian Chromosomes. Methodological breakthroughs in the field of cytogenetics in 1967 triggered a major thrust in this research area worldwide. In- strumental in development of these new methods was James L. Patton, then a grad- uate student at the University of Arizona. The University of Arizona was a nucleus for this type of activity at this time with Patton and Robert J. Baker focusing on mammalian cytogenetics. Fortunately, Pat- ton and Baker chose to publish many of their earliest cytogenetic studies in the Jour- nal of Mammalogy (e.g., Baker and Patton, 1967; Patton, 1967; Patton and Hsu, 1967), which in concert with others (Nadler, 1966; Nadler and Hughes, 1966; Singh and Mc- Millan, 1966) brought the Journal into the mainstream of cytogenetics research. Baker and Patton’s seminal contributions to the field of mammalian cytogenetics and, in particular, their development of convenient techniques for use in the field (e.g., Baker, 1970; Patton, 1967), are still widely cited in the cytogenetics literature. An analysis of the rate of publication of cytogenetic studies in the Journal of Mam- malogy from the time of the journal’s in- ception (1920) to the present (Fig. 1) illus- trates the enormous surge in this field that began in the 1960s. For example, no cyto- genetic studies appeared in the Journal be- tween 1961 and 1965; in contrast, 22 such articles appeared for the time period of 1966 to 1970. Similarly, no new karyotypes were described in the Journal during the first half of the 1960s, whereas the karyotypes of 85 species of mammals were reported there for the first time between 1966 and 1970. Most cytogenetic studies published in the Journal of Mammalogy in the late 1960s and early 1970s were descriptive in nature, and most authors linked—explicitly or im- plicitly—chromosomal differentiation with taxonomic distinctness. For example, Shell- hammer (1967:549) stated (with respect to two species of harvest mice, Reithrodonto- 316 BAKER AND HAFNER mys) that: “the karyotypes... are different enough to suggest that the two are in the terminal stages of speciation.’’ However, as the karyotypes of more and more species of mammals were reported in the Journal and elsewhere, it became apparent that chro- mosomal variation in mammals was not necessarily linked to the process of specia- tion and that chromosomal variation, in general, was much more complex than had been envisioned by earlier workers in the field. In a study that described the karyo- types of 32 species of vespertilionid bats, Baker and Patton (1967:283) stated: ““From the few studies of mammalian karyotypes that have thus far been made, it appears obvious that the degree of karyotypic vari- ation encountered at a given taxonomic lev- el. ..1is in itself highly variable from mam- malian group to group.” Thus began a period of intensive surveys of chromosomal variation in mammals, which was the subject of several articles published in the Journal beginning in 1968 (e.g., Blanks and Shellhammer, 1968; Lee and Zimmerman, 1969; Nelson-Rees et al., 1968). Although intraspecific chromosomal polymorphism had been known since Ford et al.’s (1957) classic study of shrews (Sorex araneus), the genetic consequences and evo- lutionary significance of chromosomal polymorphism were only poorly under- stood even a decade later. For example, Blanks and Shellhammer (1968:729), whose article in the Journal of Mammalogy was the first report of supernumerary chromo- somes in mammals, stated candidly: ““We do not understand the mode of inheritance of the small chromosomes... .”” Not sur- prisingly, this period of intensive karyolog- ical surveys (1966-1970) generated a large gap between data and theory in the field of mammalian cytogenetics. This, in turn, led to a certain amount of disillusionment on the part of workers attempting to solve tax- onomic problems using chromosomal evi- dence. For example, Sutton and Nadler (1969:534) stated: ““Chromosomes are of limited value for the solution of taxonomic 35 > N Number of Karyotypes Described ai s Number of Cytogenetics Publications—_{, oN Number of Publications Number of Karyotypes 0 T T T —- 1925 1930 1935 1940 1945 1950 1955 1960 1965 1970 1975 1980 1985 1990 Year Fic. 1.—Number of cytogenetics publications and number of new karyotypes described in the Journal of Mammalogy from 1919 to 1990. The axes are scaled differently to show that the rate of publication of cytogenetics research increased throughout the 1970s, whereas the rate of pub- lication of new karyotypes has declined consis- tently since 1970. problems and they are of little help in es- tablishing relationships between species and subspecies of the genus Eutamias [chip- munks].”’ As the number of studies reporting intra- specific chromosomal variation in mam- mals increased, there was growing confu- sion in the literature with respect to the terms ‘“‘seographic variation’ and “‘polymor- phism.”’ Fortunately, Lee and Zimmer- man’s (1969) chromosomal study of cotton rats (Sigmodon) stemmed the tide of grow- ing confusion by carefully distinguishing be- tween geographic variation (“‘. . . differences in karyotype between [presumably conspe- cific] organisms from different localities ...’) and chromosomal polymorphism (““... variation within a geographically lo- calized, panmictic population.’’) (Lee and Zimmerman, 1969:335-—336). Patton and Dingman’s (1968) cytogenetic study of natural hybridization between the CYTOGENETICS od7 pocket gophers Thomomys bottae and T. umbrinus was published in volume 49 of the Journal of Mammalogy. Although their taxonomic conclusion (that 7. bottae and T. umbrinus are distinct species) was contro- versial and was rejected by certain leading mammalogists of the time (e.g., Hall, 1981: 469), they demonstrated for the first time the value of chromosomes in analyses of genetic introgression in mammals. Patton and Dingman’s (1968) taxonomic conclu- sion was bolstered 5 years later by a detailed analysis of meiosis in bottae x umbrinus hybrids (Patton, 1973). This work set the standard for cytogenetic studies of mammal hybrid zones for many years. From 1967 through 1972, most major publications in the field of mammalian cy- togenetics and reports of significant meth- odological and conceptual breakthroughs in the field were published in the journals Chromosoma, Cytogenetics, Experientia, Science, and Nature. During the same pe- riod, most studies describing the karyotypes of mammal species were published in Mam- malian Chromosomes Newsletter. Perhaps as a result, the number of karyotypes de- scribed in the Journal of Mammalogy began to decline in the early 1970s (from its peak in the late 1960s) and has continued to de- cline (Fig. 1). However, as more and more chromosomal data accumulated in the early 1970s making large-scale syntheses possi- ble, noteworthy publications in the field of mammalian cytogenetics began to appear with increasing frequency in the journals Evolution, Hereditas, Systematic Zoology, and Journal of Mammalogy (Fig. 1). One particularly important contribution that ap- peared in the Journal of Mammalogy during this period was Nadler et al.’s (1971) study of prairie dog (Cynomys) evolution; this was the first of many studies published in the Journal that used combined chromosomal and biochemical evidence to address a sys- tematic problem. The early 1970s witnessed a renaissance in the field of cytogenetics that was cata- lyzed by the development of techniques for banding chromosomes that increased dra- matically the taxonomic usefulness of kar- yotypes. In his chromosomal study of kan- garoo rats (Dipodomys), Stock (1974) published the first figure of a metaphase karyotype stained for constitutive hetero- chromatin (““C-bands’’) and the first figure of a Geimsa-banded karyotype (““G-bands’’) to appear in the Journal. Stock’s contribu- tion was followed soon thereafter by a study that used banded karyotypes to document chromosomal conservatism in rodents (Mascarello et al., 1974a), and another that used banded karyotypes to confirm the role of Robertsonian mechanisms in the origin of chromosomal diversity in woodrats (Ne- otoma; Mascarello et al., 19745). Four years later, Mascarello (1978) introduced readers of the Journal of Mammalogy to yet another staining procedure (Ag-As silver staining), which was used to visualize nucleolus or- ganizing regions on individual chromo- somes. Development of these new staining pro- cedures in the mid-1970s triggered a burst of activity on the part of mammalian cy- tosystematists, and as a result the number of cytogenetic studies published in the Jour- nal of Mammalogy peaked between 1976 and 1980 (Fig. 1). During this period, Greenbaum and Baker (1978) published the first article in the Journal that used C- and G-banded karyotypes to deduce the prim- itive karyotype for a group of mammals (in this case, white-footed mice of the genus Peromyscus). This was among the first stud- ies published anywhere in which a cytoge- netic analysis was viewed in the context of phylogenetic systematics. Bickham’s (1979) study of the chromosomal variation in ves- pertilionid bats used cladistic methods to produce a phylogeny of these taxa using G-banded karyotypes. The frequency of appearance of cytoge- netic publications in the Journal of Mam- malogy declined steadily during the 1980s and continues to decline today (Fig. 1). This trend probably reflects the general shift away from morphological and cytogenetic meth- 318 BAKER AND HAFNER ods toward use of molecular methods by large numbers of mammalian biologists. This decline in frequency of cytogenetic studies during the 1980s has occurred de- spite the recent introduction of new and promising cytogenetic techniques. Notable among these new techniques are fluores- cent-banding procedures (Bickham, 1987) and flow cytometric studies of nuclear-DNA content (Burton and Bickham, 1989). The first color photo published in the Journal of Mammalogy appeared in an article by Ba- ker et al. (1992) that documented the num- ber of ribosomal gene sites in bats using fluorescent in situ hybridization. Although these new developments have failed, thus far, to reinvigorate the field of mammalian cytogenetics within the pages of the Journal of Mammalogy, there is little doubt that the next generation of mammalogists will re- discover the value of cytogenetic characters for genetic and systematic inquiry. Geographic and taxonomic coverage. — Published literature in the Journal of Mam- malogy shows a strong emphasis on North American species. This geographic bias is likewise reflected in the set of 130 studies categorized herein as cytogenetic research. For example, 102 of the 130 studies (78%) published between 1920 and 1990 in the field of cytogenetics have dealt exclusively with North American species. Of the re- maining 35 studies, 22 (17%) have involved Central or South American species, 6 (5%) have focused on African species, 5 (4%) on Asian species, and 2 (2%) on Australian or New Zealand species. All 79 karyotypes published in the Jour- nal of Mammalogy during its initial 50 years of existence (1920-1969) were from either rodents (14 studies/45 species) or bats (three studies/34 species). This trend was broken in 1970 when Holden and Eabry published the karyotypes of two species of rabbits (Sy/- vilagus). The first cetacean (Kulu et al., 1971) and artiodactyl (Nadler, 1971) karyotypes were published in volume 52, and the first carnivore karyotype appeared a year later (Wurster-Hill, 1973). Yates and Schmidly 80 Taxonomic Representation for Major Orders of Mammals O Percentage of all mammal species 604 ll Percentage of all karyotypes published in Journal of Mammalogy Percentage Fic. 2.—Taxonomic bias in the cytogenetics literature published in the Journal of Mammal- ogy. For each of the nine orders of mammals listed, the bar on the left represents the percent- age of all extant mammalian species that belong to that order and the bar on the right indicates the percentage of all karyotypes published in the Journal of Mammalogy relating to species of that order. Note that rodents are over-represented in the cytogenetics literature, whereas all other groups, except bats, are under-represented rela- tive to their species abundance. (1975) reported the first insectivore karyo- type, and the first marsupial karyotype ap- peared almost a decade later (Seluja et al., 1984). Surprisingly, no other mammalian order is represented by karyotypes pub- lished in the Journal. Considering that bat species (Chiroptera) comprise approximately 22% of all living species of mammals (Anderson and Jones, 1984), it seems appropriate that roughly 22% of all karyotypes that have appeared in the Journal of Mammalogy are from species of bats (Fig. 2). In contrast, rodents comprise approximately 42% of extant mammal spe- cies, yet nearly 70% of all karyotypes re- ported in the Journal are of rodents. This striking taxonomic bias in favor of rodents CYTOGENETICS 319 is probably a consequence of the fact that most rodents are small and easily captured and karyotyped. Summary and Conclusions The field of cytogenetics was in its infancy when the ASM was founded in 1919. Per- haps in part because the Journal of Mam- malogy was not yet widely known in inter- national circles, early workers in the field of mammalian cytogenetics chose to publish results of their studies in journals with wider readership; hence the Journal played only a minor role in the early development of the field. In the 1960s, methodological advanc- es developed by several mammalogists, in- cluding Charles F. Nadler, James L. Patton, and Robert J. Baker, finally brought the Journal of Mammalogy into the main- stream of cytogenetics research. The future of cytogenetic studies is es- pecially promising. Recent advances in chromosome painting (Lengauer et al., 1990, 1991), which can provide resolution to ho- mologous chromosomal regions among dis- tantly related taxa, should permit survey type work among various groups of mam- mals. Polymerase chain reaction amplifi- cation of chromosomal loci with conserved primers (Koch et al., 1991; Terkelsen et al., 1993) should also be readily adaptable to the types of investigations that are valuable to the science of mammalogy. The use of multi-color in situ hybridizations (Reid et al., 1992; Scherthan et al., 1992) will permit examination of the order of genes on a chro- mosome during a single experiment. Chro- mosomal banding through computerized images using fluorescent dyes (K. L. Bowers, pers. comm.; Volpi and Baldini, 1993; Ward et al., 1991) will greatly facilitate identifi- cation of chromosomes without the nu- merous replications required by the old trypsin methods. The development of in situ probes from DNA libraries should provide countless loci to be mapped. These ad- vances indicate that we are only beginning to see the methodological improvements that will aid in cytogenetic analyses. 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Indian muntjac, .Wuntiacus muntijak: a deer with a low dip- loid chromosome number. Science, 168:1364-1366. WuourstTer-Hit, D. 1973. Chromosomes of eight spe- cies from five families of Carnivora. Journal of Mammalogy, 54:753-760. Yates, T. L.. AND D. J. ScHMIDLy. 1975. Karyotype of the eastern mole (Sca/opus aquaticus), with com- ments on the karyology of the family Talpidae. Jour- nal of Mammalogy, 56:902-905. POPULATION ECOLOGY WILLIAM Z. LIDICKER, JR. Introduction he term “‘population” traces its roots to “people” (Latin populus), which is a collection of human beings. Later it took on the meaning of collections of (usually sim- ilar) things. In biology it defines a group of individuals of the same species (kind). Of- ten such groups live in a prescribed place and can be distinguished operationally from other similar groups by partial or complete discontinuities 1n space or time or both. It is important, however, to recognize that such “natural” groupings are not essential to the “concept” of population; any arbitrarily designated group of individuals of the same species is sufficient. Once a population is designated, it is then possible to investigate whether it can also be defined by spatial or temporal discontinuities. Much confusion results from confounding these two objec- tives. Increasingly, biologists find it useful to view the living world (the biosphere) as be- ing organized on different levels of com- plexity that can be hierarchically arranged. Such a holistic perspective is by no means universally accepted as useful, and in fact this view has progressed rather slowly and fitfully over the past century. The history of population ecology as an intellectual disci- 3235 pline is inextricably connected to that de- velopment (Allen and Starr, 1982; MclIn- tosh, 1985; O’Neill et al., 1986). The concept population fits into the hi- erarchy of biotic complexity above the level of the individual organism and below that of the community. The concept community is biotically much more complex than pop- ulation because it concerns a universe (sys- tem) that includes more than one species (kind) of living organism. It is often difficult to distinguish studies at the population and community levels because populations al- most universally live with and interact with other kinds of living organisms. Neverthe- less, a distinction can generally be made on the basis of whether the study 1s focused on a single species or more than one. This is the same distinction made by the old terms “‘autecology”’ and “synecology.”’ Moreover, populations can be viewed conceptually in isolation even if this is rarely realistic, and one can certainly focus attention on one spe- cies at a time. A bacterial culture in a test tube is an example of the former and a study of the causes of mortality in a population of deer is an example of the latter. The con- cept population also fits into a hierarchy of evolutionary units (Brandon and Burian, 324 LIDICKER 1984; Eldridge, 1985; Lewontin, 1970; Salthe, 1985; Vrba and Eldridge, 1984). This chapter reviews how research on mammals over the last 75 years has influ- enced population ecology and considers how developments in ecology generally have im- pacted mammalogy. One of the central is- sues 1n population ecology is that of pop- ulation regulation, and this will therefore constitute a major thread through this chap- ter. A second theme will concern matura- tion of the concept “‘population”’ along with the recognition of population processes as being real biological phenomena above the level of the individual organism. I use the metaphor of a tree to organize this chapter. First I discuss the historical underpinnings (roots: pre-1930), followed by a review of the early research on population processes in mammals (trunk: 1930-1070). Next is an overview of modern foci in the field (branches: 1970 forward), and finally, I give brief comments on future perspectives (buds). Note that flowers and fruit are left for the future. In the context of this book, the emphasis has been on North American contributions, although I fully acknowledge the immense importance of others to this history. Roots: Initial Thoughts The question of what regulates the num- bers of organisms all began of course with a focus on a mammal, Homo sapiens. Thomas Malthus (1798) pointed out that populations have the capacity to increase exponentially but, except for brief episodes, do not do so. Therefore, negative forces (checks and balances) must operate on pop- ulations so as to counter the tendency to increase toward infinity. This insight was critical to the ontogeny of Charles Darwin’s thinking about evolution, and an essential ingredient in the development of our un- derstanding of evolution by natural selec- tion. In ecology, however, Malthus’ pio- neering contribution to the analysis of population processes languished until early in the 20th Century when ecology really started to blossom as a discipline (McIn- tosh, 1985). Like the roots of a majestic chestnut, the origins of mammalian population ecology are deep, intricate, numerous, and nourish- ing. Formal discussions of population birth, death, and growth rates were published in the first few years of this century (Lotka, 1907, and references therein). One influ- ential paper that is often credited with the beginning of modern population theory (at least in North America) was published in 1911 by two economic entomologists work- ing on gypsy moths (Howard and Fiske, 1911). They clearly defined density equilib- rium and attributed its achievement to “‘fac- ultative agents” that increased proportion- ally in their suppressing effects as density increased. Thus, it was an interest in eco- nomically important insects and their con- trol that was the impetus for quantitative thinking about population growth. Ento- mologists were soon joined by mathemati- cal theorists in the development of quan- titative models for population processes (Lotka, 1925; Pearl, 1927; Volterra; 1926; 1931), but these efforts were slow to influ- ence ecologists generally and mammalogists in particular. Early ecology texts hardly mentioned population regulation at all (Chapman, 1931; Shelford, 1913, 1929). In the early part of this century, mam- malogists were preoccupied with faunal sur- veys and documenting the occurrences and - distribution of species and subspecies of mammals (Hamilton, 1955; Miller, 1929). Population-level thinking was not much in evidence, and in fact most systematists har- bored a typological philosophy. A common view was that if a specimen were demon- strably different from “‘typical’’ individuals, it should be given a formal scientific name so that the fact of its uniqueness would not be lost to the scientific community. As in- _ formation accumulated on geographic vari- ation within species and within popula- tions, these views were gradually replaced by the realization that populations are not collections of identical individuals, and that POPULATIONS 325 these assemblages of individuals also have features beyond those of the individuals that make them up. Mammalogists also gradually became more interested in ecological questions, es- pecially as information on life histories was acquired. In this they were encouraged by several leaders including Cabrera (1922), Seton (1929), Hamilton (1939), and Bour- liére (1951). Wildlife managers also played a critical role in this transition, because they were interested in questions of population regulation and control. Their approach, however, was normally to identify impor- tant mortality factors, and not to view pop- ulations in any quantitative way (Leopold, 1933; Trippensee, 1948). They also popu- larized the notion of ‘‘optimal density,” not only as an ideal of management technology, but also as a natural state of some popula- tions (Bates, 1950; Dasmann, 1964; Elton, ~ 1927; Howard, 1965; Leopold, 1933). The idea was that densities stabilized below a subsistence level so that body size, health, growth, and fecundity would be maximal. There was no recognition of the difficulties such idealism posed for natural selection at the individual level, although professional managers could strive for such a goal. Another root of critical importance to fu- ture population ecology was the gradual de- velopment of holistic philosophy. The name and formal description date from Smuts (1926), but the roots are deep and pervasive (Forbes, 1880; Semper, 1881), and include Forbes’ “‘microcosm” (1887) and the infa- mous “‘vitalism”’ of earlier times. Also ho- listic philosophy has been a dominant thread in many Eastern cultures for at least 2,500 years (Barnett, 1982; Konishi and Ito, 1973; Lidicker, 1988). A few well-known early ecologists struggled with holistic notions (Clements and Shelford, 1939; Elton, 1930: 30; Friederichs, 1927, 1930; Gause, 1934: 2; Thienemann, 1939), but were largely un- successful because of a combination of the difficulty of the idea, lack of formal termi- nology for systems concepts, lack of a data base for population and community pro- cesses, and the spectacular successes of re- ductionist approaches to research (Lidicker, 1978). One example will illustrate this sit- uation. When Clements (1905, 1916) and especially Clements and Shelford (1939) used the metaphor of “‘complex organism” to express the idea that communities rep- resented a higher order of biological orga- nization than that of individuals, the idea was received with hostility. Today we rec- ognize their supra-organism as an expedient metaphor for an idea almost all ecologists now accept, but only in the suitable format of modern jargon. E. P. Odum deserves con- siderable credit for encouraging holistic thinking, especially through his influential ecology texts beginning in 1953 (Odum, 1953). The final major “root” to be mentioned is that of genetics and evolution. These two disciplines developed independently of ecology until recent decades. Of course, there were notable exceptions such as Charles El- ton, who was very much an evolutionary biologist as well as an ecologist (Crowcroft, 1991: McIntosh, 1985). For the most part mammalogists thought about evolution in terms of phylogenies and adaptations, but not much about population-level processes. With the ““modern synthesis” in the 1940s, evolution and genetics (especially popula- tion genetics) were brought together and provided a more appropriate framework for synthesis with ecology (Brown and Wilson, 1994). Still, the entrenched notion that eco- logical time frames are very much shorter than evolutionary time is still hampering us today. In 1969, I started to teach a lecture course in genetic ecology for graduate stu- dents, and remember well that for a number of years I spent the first lecture explaining and justifying such a radical interdisciplin- ary notion. The Trunk: Early Research on Population Processes Early research (1930s and 1940s) on mammalian population ecology emerged 326 LIDICKER from research on life histories and on wild- life and forest management. Hamilton (1955), in his review of American mam- malogy, pointed out how important the in- vention and widespread use of the snap-trap was in encouraging life history studies and in making possible large collections of spec- imens. Still, populations were not viewed as entities with growth rates, birth rates, and the like. In Hamilton’s (1939) classic trea- tise on American mammals, only one brief chapter is devoted to populations. In this he debunked the “balance of nature’ as a fiction pointing to the ubiquitous variability in species numbers. Most of the chapter is devoted to cycles and mass outbreaks. Twelve years later, Gabrielson (1951) sim- ilarly allocated only one chapter to “pop- ulation controls” in his wildlife manage- ment text. He also attacked the balance of nature ideal, especially where human influ- ences are present, and briefly discussed in- terspecific competition, predation, damage to crops and habitat by wildlife, and the control of introduced plants. Trippensee’s text (1948) mainly discussed individual game species, followed by a section called ‘‘Miscellaneous Wildlife Relationships,” with a chapter on “‘variations in numbers of wild animals” and one on “predator-prey relationships.” Toward the end of this period, main- stream ecologists at least were clear on the components of the population growth equa- tion (Allee et al., 1949; Cole, 1948; Park, 1946). However, no coherent concept of populations being regulated by the quanti- tative interplay of births, deaths, and dis- persal rates was generally expressed. Trip- pensee (1948:386), for example, seems to have been unaware that an unrestrained positive biotic potential will produce ex- ponential growth toward infinity. Of course, any concept of community processes was even more vaguely perceived. While inter- specific competition, predation, and dis- eases were clearly thought important, no interacting network of interspecific inter- actions was envisioned. Trippensee (1948: 398), nonetheless, did warn readers that “Predator relationships are complex and cannot be dealt with as simple phenomena,” and then illustrated the prevailing simpli- fied viewpoint with a table from Mendall (1944) classifying species of predators into four categories from ‘“‘distinctly beneficial” to “primarily detrimental.”’ It is interesting that “cycles” played such a prominent role in discussions of popula- tions even before Elton’s (1942) classic work on this subject. Hamilton’s (1939) analysis of multi-annual cycles is particularly thor- ough. He gives most space to sunspots as the causal agent, but in the end finds the evidence inadequate. Paraphrasing his views at that time, cyclic increases seemed to be the result of “abnormal” reproduction, and declines were caused by disease. In Trip- pensee’s (1948) chapter on variations in numbers, four out of 19 references cited have sunspots in the title, and he gives serious support to “cosmic factors’? as causative agents. Surprisingly, food was not consid- ered a critical factor at that time, except for lynx (Lynx canadensis) during crashes in snowshoe hares (Lepus americanus). Gen- erally the feeling was that population growth usually was checked far short of subsistence limitations (McAtee, 1936), a view that was consistent with the prevalent notion of ‘“‘op- timal densities.” Hamilton (1939:253) did, however, speculate that the “‘“abnormal” re- production that led to rodent outbreaks may have been abetted by a vitamin. The importance given to predation and disease as significant mortality agents went through an interesting transition at that time. Early wildlife biologists (e.g., Leopold, 1933) generally accepted predation and disease as major mortality agents. In this they were supported by the prevailing opinion among insect ecologists that parasites (including parasitoids) were the most important biotic mortality agents. A major shift in thinking can be attributed to the classical work of Errington (1946), whose primary research was on muskrats (Ondatra zibethicus). He professed that predators generally took only surplus prey, and therefore had no influence on density levels. This view of benign pre- POPULATIONS a2f dation gained rapid popularity, possibly fu- eled by a reaction to the vehement anti- predator stance of ranchers and government agencies. It reached an extreme form in the Cartwright Principle, which proclaimed that predators could save gallinaceous birds from extinction because when first nests were de- stroyed, birds re-nested at a more favorable time of the year and hence were more pro- ductive (Trippensee, 1948:392). This Er- ringtonian principle dominated thinking about predation among mammalian ecol- ogists almost to the present day, although, as I will point out, in recent decades im- portant modifications have been advanced. While mammalogical ecologists were thus occupied, insect ecologists were moving rapidly toward more rigorous and quanti- tative approaches to population regulation (Lidicker, 1978). Strongly influenced by the mathematical theorists active early in the century, they sought to fit environmental complexities into the relatively simple pop- ulation models that were being developed. They thus began to think clearly about how various factors can interact quantitatively to bring about changes in population num- bers. Some early and spectacular successes in biological control abetted this approach (Dunlap, 1981:31-35). The inherent risk in this path was that simple models led to sim- ple concepts of reality, and investigators were seduced into looking for single factor explanations of population changes. Tre- mendous advances in experimental biology made possible by reductionist approaches to research made the search for general and elegant explanations of biological phenom- ena especially tantalizing (Lidicker, 1988)). Mammalogists were, of course, not com- pletely isolated from this ferment. Hamil- ton (1939), for example, quotes the ento- mologist Uvarov (1931) at length regarding the balance of nature idea, and by the 1950s vertebrate ecologists generally had joined the fray. The Bureau of Population at Ox- ford under Charles Elton’s leadership was one of the centers of ferment and excitement that contributed to the developing synthesis (Crowcroft, 1991). As changes in numbers were seen increas- ingly clearly as the product of rate changes in the influences of various environmental “factors,” controversies quickly developed. It became widely appreciated in the 1930s that control of numbers required that neg- ative processes (environmental resistance) be positively related to population densi- ties. Some, however, were convinced that the relevant forces were abiotic factors and others were just as sure that they had to be biotic (Lidicker, 1978). On the one side were those most impressed with climate, weath- er, habitat, fire, and the like as determining numbers, with biotic factors being inciden- tal. Others were sure that biotic factors such as intra-specific competition, food, para- sites, and predators were all important, with the abiotic environment simply setting the stage for their actions. Advocates of the for- mer tended to view population densities as strongly variable, even stochastic, with local extinctions common. Champions of biotic control usually saw densities as carefully regulated about an equilibrium that, while not constant, was not random. Because of the association between abi- otic factors and failure to establish a fairly constant equilibrium density, and the cor- responding association between biotic fac- tors and density regulation, the term “‘den- sity independent factor’’ came to be applied to the abiotic and ‘“‘density dependent fac- tor’ to biotic influences. These terms were introduced by Smith (1935) and quickly be- came widely used. Unfortunately, they took on so many shades of meaning and innu- endo that semantic problems have plagued the subject ever since (Lidicker, 1978; Sol- omon, 1958). To summarize briefly, density dependence sometimes meant biotic fac- tors, sometimes density regulating, some- times simply that the factor’s effect changed with density, sometimes positively, some- times negatively, sometimes absolutely and sometimes proportionately, and sometimes it meant that the factor itself (not its effect) changed with density (responsiveness). Similarly, density independence meant whatever density dependence did not: abi- 328 LIDICKER otic factors, non-regulating effects, effects that were unrelated to density, were con- stant numerically or proportionately, or were factors that were simply unresponsive themselves to density changes. Valiant ef- forts by leading ecologists failed to untangle this muddle (Schwertfeger, 1941; Solomon, 1949; Thompson, 1939). Clarifying data were slow to accumulate. Because the questions were semantically mired, so were the answers. This was after all before the era of field experiments and hypothesis testing. Excellent laboratory studies were reported that clearly estab- lished that both biotic and abiotic factors could regulate numbers, but such infor- mation was easily dismissed by field ecol- ogists as irrelevant. Field researchers were generally searching for evidence to support their particular biases and almost always they succeeded. This situation led to a lot of argument and excitement, but little prog- ress toward clarifying the issues of the rel- ative importance of abiotic and biotic in- fluences, how they interacted, and how decimating effects changed quantitatively with density in field populations. A second circumstance that strongly in- fluenced the way that research on popula- tions was done in this era, and how ecolo- gists thought about the issues was the predominance of reductionist approaches. Not that very many ecologists thought ex- plicitly about what they were doing in these terms but, as already alluded to, holistic thinking was still embryonic and quite dif- ficult. Reductionism was achieving fantastic successes in cell and molecular biology, as well as physiology and medicine. All science students were taught that in good science one asks only “how” something works and not “why” it works the way it does. Natu- rally, ecologists wanted to be good scientists too. The emphasis on reductionism had sev- eral beneficial effects. It led to many good field and laboratory experiments and it en- couraged the practice of carefully studying the effects of various factors on a subject population one by one. This was, and re- mains, a powerful protocol. To suggest that it had its limitations remains controversial indeed (Gaines et al., 1991; Lidicker, 1991). In my view, however, the single-minded re- ductionist approach, without a complemen- tary systems (holistic) framework to guide it, ultimately limits understanding (Lidick- er, 1988a, 1988h; Macfadyen, 1975; Odum, 1977). For the time and subject under dis- cussion, the important effect was to en- courage investigators to expect simple mechanisms for density regulation to be found. Not only were single key factors reg- ulating densities sought, but it was opti- mistically hoped that the answer once found could be extrapolated across time, across populations to the entire species, and then across species and even larger taxonomic groupings. After all, general properties of cells, biotic molecules, and genetic codes, were being reported regularly. In retrospect, we now know that this approach failed be- cause density regulation machinery turned out to be generally not simple, and single factor hypotheses are not amenable to this discovery (Hilborn and Stearns, 1982; Lid- icker, 1978:133; Smith, 1952). It is analo- gous to the futile search for the cause of cancer. With various investigators focusing on different aspects of density regulation, new controversies emerged. An important one that is only just now fading is whether ex- trinsic or intrinsic factors were most im- portant. That is, some argued that factors in the environment directly imposed regu- lation on the subject population, while oth- ers felt that changes in the organisms that constitute the population were the essential variables. It is surprising that ecologists could be so oblivious to the basic paradigm of their discipline, namely the organism- environment interaction system, and to the truism that both the properties of the or- ganisms and the environment change over space and time. Thus, while the intrinsic versus extrinsic argument was ultimately sterile, it did call attention to the impor- POPULATIONS 329 tance of looking at the properties of both organism and environment in trying to un- derstand population processes (Lidicker, 1978). Another development in the 1940s to which mammalogists made critical contri- butions was the acceptance of the life table concept in population ecology (Deevey, 1947). It was, of course, introduced much earlier (Pearl, 1922), but failed to make much of an impact on vertebrate ecologists, prob- ably because the required data were too dif- ficult to acquire with existing technologies. Life tables served to focus attention on the attributes of various age and sex groups within populations, and eventually led to an appreciation for the age and sex structure of populations. The Leslie Matrix (Leslie, 1945) for calculation of population growth is a familiar manifestation of this devel- opment. Thus intra-population demo- graphic variation was added to the increas- ing appreciation for genetic variation within populations to generate an increasingly re- alistic image of population phenomena. Modern population modelers continue to invoke structured populations in their mod- els (Boyce, 1977; Lomnicki, 1980; Schaffer, 1974). One negative aspect of the enthusi- asm for life tables was the easy assumption that a particular life table characterized each species. In strict terms, a life table applies to a particular cohort of individuals born over a specified, and usually quite limited, . time and space. Confusion on this point continues. In the 1950s and 1960s, proponents of various classes of density-regulating factors tended to be viewed as “schools of thought.” The climatic school was not very popular among vertebrate ecologists (once sunspots were abandoned), but it was sometimes conceded that climatic factors could be crit- ical on the edges of species’ ranges. The availability of cover and nest sites were ad- mittedly part of what determined a species’ habitat, but were not often considered in determination of densities. Predation and parasitism had their champions, but mam- malian ecologists generally seemed to have lost interest in disease and the Erringtonian Principle diminished faith in the efficacy of predators (Errington, 1963; Howard, 1953). The extrinsic factor with the most wide- spread support was that of food. Lack (1954, 1966) had eloquently argued for food lim- itation being the primary regulating factor. It was logical (all organisms required nutri- tion), and it fit into the emerging synthesis of evolutionary thinking in ecology (organ- isms should evolve so as to maximally use their food supplies). Detractors, however, pointed to contradictory evidence in spe- cific cases, to the potential (and frequently to evidence as well) for regulation by non- food factors, and to the necessity that con- sistent regulation by food requires optimal tracking by a population of its food re- sources. The food theory also became more sophisticated. While food quantity was stressed at first, nutrients later became rec- ognized as potentially limiting (Pitelka and Schultz, 1964). Other researchers turned their attention to intrinsic mechanisms. For some, self-reg- ulation made sense in that organisms would seem to be better off if they were not always at the point of exhausting their resources (e.g., Wynne-Edwards, 1962, 1965). Pru- dence demanded some measure of self con- trol. Others were disappointed that no ex- trinsic factor was found that fulfilled the hope of a general regulating factor. A tech- nique that became widely utilized at this time was to grow populations of small mammals in laboratory or outdoor enclo- sures. In this way a bridge between the lab- oratory and field was forged, and population processes could be studied in a circum- stance such that either intrinsic or extrinsic factors could be manipulated individually. One class of intrinsic factors that was studied extensively was that of physiologi- cal change associated with varying densi- ties. An early hypothesis of Chitty (1952, 1955, 1958) that high densities led to phys- iological damage that increased mortality rates and moreover could be passed on to 590 LIDICKER offspring during gestation or lactation was later abandoned by him (Chitty, 1960, 1967). Christian (1950) introduced the intriguing idea that exhaustion of the ad- reno-pituitary system may be involved in population declines. High densities would feature a variety of stressors, he suggested, and hence the proximate causes of mortality would be non-specific. Later (Christian, 1955a, 1955b, 1959, 1961; Christian and Davis, 1955) he expanded the model to sug- gest that high densities activated the stress resistance mechanisms of the body, even- tually resulting in their exhaustion. Re- duced reproductive competence and death soon followed. A related phenomenon was the “‘shock disease”’ widely associated with population crashes in snowshoe hares. As this was known to involve hypoglycemia and non-specific mortality agents, it could easily be fitted into the stress hypothesis. Trippensee (1948:392), however, thought shock disease was caused by a lack of min- erals in the diet. Many researchers pursued these ideas, and by the end of the 1960s the situation could be summarized as follows (Lidicker, 1978): the stress syndrome was real in laboratory situations, but was not found to be generally applicable to field pop- ulations. A second class of intrinsic factors to be proposed was that of behavioral changes with density. Territoriality, fighting, dis- persal, and cannibalism all could change with density and may be expected to have demographic consequences. Wynne-Ed- wards (1962, 1965, 1986) proposed that “‘epideictic displays’’ were a mechanism by which individuals communicated their den- sity circumstances to each other. As such, this notion was criticized for not making sense in the context of individual selection, but could be defended by involving group selection mechanisms (Wynne-Edwards, 1986). The use of enclosed populations led to the discovery of behaviorally-mediated reproductive inhibition (Calhoun, 1949, 1962: Crowcroft and Rowe, 1957; Davis, 1949: Lidicker, 1965; Petrusewicz, 1957; Southwick, 1955). In fact, Petrusewicz (1957) startled ecologists with his evidence that in laboratory colonies of house mice (Mus musculus), a socially-inhibited group can be induced to resume reproduction sim- ply by moving it to a new cage, even a small- er one. Otherwise, phenotypic behavioral changes with density were mainly studied in more recent decades. Genotypic shifts in populations with den- sity changes were the third class of intrinsic factors contemplated seriously as regulating mechanisms. Led by Chitty (1960, 1967) and Krebs (1964, 1971), the stimulating idea was proposed that selective pressures vary- ing with density favored different genotypes at high versus low densities, and the cor- responding shifts in gene frequencies led to predictable demographic consequences. Such ideas had been suggested earlier for insect populations (Turner, 1960; Welling- ton, 1960; Wilbert, 1963), but Chitty and Krebs applied them specifically to density cycles of microtine rodents and suggested that aggressive versus docile behavior was the relevant behavior being selected. Later they hypothesized that, instead of aggres- sion, the behavior being selected was spac- ing behavior including dispersal (Krebs, 1979a; Krebs et al., 1973). These ideas were so important that they strongly influenced the character and direction of research on small-mammal populations in subsequent decades. Over the roughly four decades covered in this section (1930s through 1960s), some general trends in the relative importance of mortality, natality, and movements in and out of populations (immigration and emi- gration, respectively; Lidicker, 1975) can be discerned. Of course, early in this period, mammalian researchers did not usually think of these processes as interacting vari- ables in a growth equation. Early emphasis was on mortality; reproduction was thought to be almost always “normal,” i.e., non- varying. In fact, Smith (1935), in his sem- POPULATIONS pol inal paper defining density dependence and independence, referred to density depen- dent factors as mortality agents only. Even Dasmann (1964) discussed density depen- dence only in terms of mortality. Gradually, the importance of reproduction gained ap- preciation, especially as data accumulated showing that it too could vary with density. At first, “abnormally” good reproduction was thought to produce population out- breaks (Hamilton, 1939:274), but then it became apparent that reproduction often declines with increasing density as well (see Howell, 1923, for a pioneering example). This new focus on reproduction reaches an extreme with demographers who tend to view human population growth rates as mainly influenced by birth rates and hardly at all by mortality, a tradition going back at least to Pearl (1925). Movements in and out of populations were not given much attention (but see Hamilton, 1953). Early on, dispersal was viewed as destabilizing because individuals were visualized as moving about in search of favorable circumstances, thus increasing the variability of local densities. Then, as growth equations entered the arena, growth rates were defined as birth rates minus death rates (r). This dogma swept through the text books and assured that immigration and emigration would not be considered seri- ously. When they were mentioned at all, they were dismissed as trivial or balanced between imports and exports and therefore ignorable. If significant emigration was ac- knowledged, it was lumped with mortality under the rubric “‘gross mortality.” Except for the paper by Howard (1960) postulating that both “genetic” and “environmental” dispersal may occur, and my own paper (Lidicker, 1962) suggesting that emigration should be examined for its possible effects in density regulation, the fervor of interest in dispersal came in later decades. I end this section with a caveat and men- tion of two exceptional individuals. For the four decades covered here, I have tried to portray major themes of intellectual devel- opment. As time progressed through the pe- riod, it becomes increasingly difficult to fol- low one thread. Our disciplinary “trunk” forms major branches and many more re- searchers are involved. Moreover, the av- erage intellect that one tries to describe is a statistical artifact drawn from a fairly small sample size. Each individual investigator is of course exceptional in at least some re- spects. An important exception to this av- erage intellect was Charles Elton, who some consider the father of mammalian popula- tion ecology (Berry, 1987). Not only was he an early architect of community concepts (e.g., Eltonian pyramids), but he was an ad- vocate of incorporating evolutionary think- ing in ecology long before this was routine. As early as 1930, he expressed the holistic view that a whole biological community could act as a unit of selection (Elton, 1930: 30), and warned that “*. . . the modern ecol- ogist runs a risk of ... falling back upon a severely mechanistic view... based on the laws of physics and chemistry, solid in themselves, but unsatisfactory as a com- plete explanation of the life and mind of animals” (1930:9). Secondly, for the mam- malian ecologist, Elton’s treatise on voles, mice, and lemmings (1942) was where it all began. His Bureau of Population at Oxford was, moreover, the gestation site for nota- bles such as Dennis Chitty, Peter Crowcroft, Richard Miller, and Mick (H. M.) Southern, and also strongly influenced long-term vis- itors like Frank Pitelka (see also Crowcroft, 1991). A second exceptional individual in this formative era was Kazimierz Petrusewicz (Lidicker, 1984). He established in 1952, in the rubble of World War II, a Department of Ecology within the Polish Academy of Sciences, which was elevated in 1971 to the status of an Institute. Petrusewicz was di- rector from 1956 to 1973, during which time Polish ecology became an internationally recognized center of excellence, with im- portant work on mammals. Mammalian re- 932 LIDICKER search extended from the analysis of pop- ulation processes in laboratory settings to energetics, production, population regula- tion, dispersal, social behavior, and wildlife management. Petrusewicz himself was in- tensely interested in relating evolution to ecological processes, had a sophisticated ho- listic philosophy, and contemporaneously with Elton was writing papers on concepts of community structure. His influence on population ecology in Poland, eastern Eu- rope, and the world community was pro- found and long lasting (Lidicker, 1984). He was elected an Honorary Member of the American Society of Mammalogists in 1975 (Taylor and Schlitter, 1994). The Modern Era: The Last Two Dozen Years Alluding to our botanical metaphor, we have now reached the stage in the devel- opment of our subject where we have branches, lots of branches, both major sup- ports, and idiosyncratic twigs. No longer can we imagine that there is but a single path or even a few major paths of intellectual ontogeny, and it becomes increasingly dif- ficult to review intellectual history by trac- ing the origin and transmission of key ideas and the influence of especially significant leaders in the process. Of course, there were these, but the abbreviated hindsight of his- tory and the huge dimensions and the es- tablishment make these leaders seem for now more like extenders of intellectual pseudopodia than creaters of new para- digms. Mammalian population ecology had in this period not only joined the mainstream (I should say maelstrom) of population ecol- ogy, but was providing a leading voice. It was and is vigorous, diverse, incredibly in- terdisciplinary, and has nurtured the ger- mination of new subdisciplines such as evo- lutionary ecology, behavioral ecology, community ecology, landscape ecology, and conservation biology. Still our enthusiasm cannot quite match that of R. J. Berry who wrote (1987:1) that “... the proper study of biology inevitably involves an investi- gation of the processes which affect popu- lations.” ASM programs.—The increasing atten- tion given to populations and community level phenomena, as well as the expanding diversity of subdisciplines in this field, are reflected in the programs of the annual meetings of the ASM. These programs allow us to monitor and assess the prevailing par- adigms over time among working mam- malogists, and thus to measure the net pro- gressions of the field (Also see Gill and Wozencraft, 1994). For this purpose, I classified all the papers in 16 programs covering 1926 to 1991. The classification was subjective and used 10 major categories plus a number of subcat- egories. There were, or course, a few am- biguous or cryptic titles, and some papers could be placed into more than one cate- gory. Because of the scope of this chapter, I focused particularly on papers that seemed to reflect a population or community con- cept. Ecological papers judged to be at the organismal level were assigned to a “general life history” or “physiology and morphol- ogy’ category. The few titles with a land- scape perspective were lumped with com- munity ecology. A category of “behavioral ecology”’ was also recognized to include pa- pers that related behavior to ecological pro- cesses and that included group behavior such as mating systems or other social behavior. This scheme of categorization allows for the monitoring of research activities at the pop- ulation or higher levels, which is the subject of this chapter. Otherwise, the plethora of papers in general life history phenomena would obscure these patterns. The percentage of papers in ecology at the population or higher level is plotted over a 66-year period (Fig. 1). There were no pa- pers in this category in 1926 and only two in 1938. These first in our sample were an address by Joseph Grinnell on “Effects of a wet year On mammalian populations,” and one by W. P. Taylor on “Significance of numbers in mammalian ecology.” There was POPULATIONS b Jee No. of papers 47 62 276 44 39 33 38 39 58 76 104 112 203 227 247 270 Percent Population Community Behavioral 1920 1930 1940 1950 1960 1970 1980 1990, Year Fic. 1. Percentages of papers on ecological subjects presented at annual meetings of the ASM, based on 16 programs from 1926 to 1991. Eco- logical papers are allocated to behavioral, pop- ulation, and community categories based on their primary conceptual level. The dashed line for 1947 indicates the percent of papers in popula- tion ecology when six papers in a symposium on populations are omitted. an increase to nine papers in 1947, but this was almost entirely the result of a sympo- sium on “Population, home range, and ter- ritories in mammals.” Interestingly, five out of the nine papers were on techniques and another (by Durward L. Allen) was titled “Purposes of population studies.” If these six are subtracted, the percentage of ecology papers drops from 30.3 to 12.1% (Fig. 1). This symposium and one at the society’s 1950 meeting on the dynamics of mam- malian populations mark the beginning of a steady increase in the proportion of papers given on these topics, which reached a peak of 31.3% in 1981 and declined moderately after that. Papers recognizable as community-level started in the 1954 program and increased rapidly after 1969. One paper was assigned to behavioral ecology in 1947, but the next one was not until 1961, and the third was in 1974. After 1947, the proportion of pop- ulation-level papers varied hardly at all (6.5- 18.3%), with changes in the ecological of- ferings being due to the addition of com- munity and behavioral ecology contribu- tions (Fig. 1). Importance of new techniques.—An im- portant contributor to the success of pop- ulation research in this period was the ar- rival of new and powerful techniques. Whereas the snaptrap and livetrap were the technical “work horses” of the previous era, they were soon supplemented by an im- pressive list of innovations. Following World War II, radioactive isotopes became readily available and were used to follow individuals, determine pedigrees, reveal movements, and measure various demo- graphic parameters (Stenseth and Lidicker, 1992a). Because of health hazards to the investigators as well as to the research sub- jects and their environments, however, such isotopes are less commonly used now. A second technique was that of radio- tracking (Amlaner and MacDonald, 1980; McShea and Madison, 1992). At first this approach was restricted to large mammals, but with the increasing miniaturization of transmitters, radios with batteries have shrunk to where even mice can carry them successfully. Telemetry has provided a wonderful opportunity to follow the move- ments and activities of individual mam- mals, even through the guts of predators. When numerous individuals in the same population are being followed simulta- neously, it is also possible to reveal social interactions, and thereby to understand why certain movements are occurring in addi- tion to describing them. A more recent development is the use of fluorescent powders to track movements of nocturnal species (Kaufman, 1989). Under favorable circumstances these powders can reveal paths of movement by reflection of ultra-violet light. They have also been used to determine social bonds such as mother- juvenile and adult male-female relation- ships by detection of the transfer of small amounts of the powder between individuals (Ribble and Salvioni, 1990). Critically important has been the devel- opment of various biochemical techniques. Electrophoresis of blood and tissue proteins and enzymes has been used widely since the late 1960s, and has been an effective tool in 334 LIDICKER assessing the genetic architecture of popu- lations and in measuring relatedness among groups. The analysis of mitochondrial DNA restriction enzyme fragments has also been useful for measuring relationships over a shorter time span than is usually possible with the allozymic variants coded by nu- clear DNA. This is because the mutation rate, and hence biochemical drift, is faster with certain sections of mitochondrial DNA than with nuclear. As of this writing, the most exciting new development is that of DNA-fingerprinting. Although a more dif- ficult and laborious technique, it has the potential for unequivocal individual iden- tification as well as for parental exclusion analysis. Thus it has tremendous promise in investigations requiring individual rec- ognition and knowledge of pedigrees. An- other new development with great promise is the polymerization chain reaction (PCR), which allows for amplification (multipli- cation) of small sections of DNA so that such fragments can be sequenced, com- pared, and relatedness judged. It has also opened up the possibility of using small amounts of DNA surviving in museum specimens and near-fossils to assess rela- tionships among taxa, and perhaps more relevant to the ecologist, is the possibility of charting genetic change in populations over relatively short periods of time. PCR techniques utilizing dinucleotide repeats called ‘“‘microsatellites” that are widely dis- tributed throughout the mammalian ge- nome may be rich sources of polymor- phisms and hence information on re- latedness among individuals because of their extensive and presumably neutral variabil- ity. New developments useful to the pop- ulation biologist can be predicted confi- dently. Finally, it is appropriate to call attention to the vast improvement in quantitative techniques available to the population bi- ologists. These include powerful computer software packages for organizing and ana- lyzing data, using multivariate statistics, clustering techniques, and the like. Even field methodologies for gathering demographic and other data are greatly improved (Ham- mond, 1987; Hiby and Jeffery, 1987; Mont- gomery, 1987; Smith et al., 1975; Ward et al., 1987). Mathematical modeling, both analytical and computer simulation, has benefited our understanding of population processes (Conley and Nichols, 1978; Dek- ker, 1975; Hestbeck, 1988; Stenseth, 1981, 1983, 1986; Stenseth and Lidicker, 19925), and undoubtedly will play a large role in the future. It helps us to think clearly, to test the quantitative consequences of our ideas, and allows us to synthesize quantities of facts and relationships that would otherwise push beyond the limits of our mental capacities. Modeling only threatens progress when we view mathematical expressions as tem- plates of reality, or as substitutes for data, or confuse mathematical proof with careful testing of hypotheses. Intellectual foci.—1 have divided the in- tellectual history of our subject in the mod- ern era into six interconnected and over- lapping foci or themes. A single branch of inquiry is no longer realistic, and, more- over, the order in which I discuss them is completely arbitrary. These vignettes are in no way attempts to review these topics, each of which is a vast subject in itself. The most I can do here is attempt to connect each theme with the previous historical period, and to suggest major intellectual trends. As I have been a participant in this process, the risks of personal biases creeping into the analysis are greater than for the earlier pe- riods. My intention, nevertheless, is to be as objective as possible. One major area omitted here is that of life history evolution (Boyce, 1988). This is because I think of this field as more at the organismal than population level of analysis. Clearly, how- ever, the study of life history extends into the population level especially where gender differences in life history strategy or other polymorphisms occur. 1) Spatial structuring of populations. As mentioned, population ecologists were gen- erally aware of the importance of age and sex structure within populations, continued POPULATIONS 6 o)5) to gather data on this, constructed life ta- bles, and increasingly emphasized cohort analysis rather than extrapolation over time or to species as a whole. Appreciation of spatial structure, however, was slower in coming. Contrary to common sense, populations of organisms were, at the beginning of this modern period, conceptualized as infinite in size and generally panmictic. Such ap- proximations were consistent with the the- ory of population genetics and evolution then prevailing and with the ubiquitous maps of species’ ranges. Although mam- malian ecologists generally realized that these simplifications were unrealistic, they did not, I think, appreciate that it mattered very much. In the summer of 1967, P. K. Anderson traveled extensively in the Soviet Union, and learned first hand about the views of several leading Soviet ecologists (particularly B. K. Fenyuk, T. V. Koshkina, N. P. Naumov, P. A. Panteleyev, I. Ya Pol- yakov, and S. S. Shvarts) concerning the spatial structuring of mammalian popula- tions and the ecological and genetic impor- tance attributed to this structuring. Inspired by these insights (as well as recent research on Mus musculus), Anderson (1970) wrote an important review on ecological structure and gene flow in small mammals in which he proposed that genetic and social frag- mentation was indeed the rule for species of small mammals and that this implied a dramatic change in the way we should view population biology. Shortly thereafter, Shvarts’ book (1969) on the evolutionary ecology of animals was translated into En- glish by A. E. Gill (Shvarts, 1977), and Hansson (1977) wrote his influential paper on the importance of heterogeneous land- scapes in the ecology of small mammals. It is important that these contributions ap- peared in an intellectual environment in which notions of environmental grain (Lev- ins, 1968) were being widely discussed, at least by evolutionary theorists. In 1978, a symposium on mammalian population genetics was held in conjunction with the annual meetings of the ASM. In reviewing the published volume from this symposium (Smith and Joule, 1981), it is apparent that even at this time, most atten- tion was given to temporal variation in ge- netic constitution of populations (e.g., Gaines, 1981) and the causes and signifi- cance of genetic variation within popula- tions (e.g., Schnell and Selander, 1981). Only one paper gave significant attention to spatial variation on the scale of habitat patches (Massey and Joule, 1981). Subsequently, the importance of spatial structuring became increasingly recognized as a critical demographic and genetic influ- ence. Currently, it is an extremely fashion- able topic of investigation (Hansson and Stenseth, 1988). Even models of density cy- cles of microtines now are incorporating habitat heterogeneity as a relevant variable (Bondrup-Nielsen and Ims, 1988; Gaines et al., 1991; Lidicker, 1985a, 1988a, 1991; Ostfeld et al., 1985). The culmination of this trend is the emer- gence of the subdiscipline of landscape ecol- ogy (Forman and Godron, 1986; Lidicker, 19885), and its application to mammalian ecology (Bauchau and LeBoulengé, 1991; Lidicker et al., 1991; Merriam, 1990, 1991: Szacki and Liro, 1991; Wegner and Merri- am, 1990; Wolff, 1980). At this level of bi- ological complexity, systems composed of two or more habitat patches (community- types) are the subject of inquiry. Thus, the role of patch size, edge-to-area ratios, con- nectedness, and inter-patch fluxes are ex- plicitly investigated. Many new demo- graphic and evolutionary insights can be anticipated as a result of this advance. 2) Dispersal. As pointed out, interest in dispersal was almost non-existent at the beginning of this modern era. Currently, it is one of the most vigorous areas of inquiry in mammalian ecology, marking a devel- opment that is clearly one of the most dra- matic of this period. Apart from some early signals (Andrzejewski et al., 1963; Howard, 1960; Kalela, 1961; Lidicker, 1962), a bur- geoning interest developed in the late 1960s and 1970s (see Fenton and Thomas, 1985; Lidicker, 1975, 1985b; McCullough, 1985 336 LIDICKER for early reviews). In January 1992, the BIo- sis electronic data base listed 7,240 refer- ences (Zoological Record, Online, 1978 to 1991) indexed by the descriptor “‘dispers- ale Basically, what happened were two crit- ical intellectual breakthroughs: 1) the real- ization that movements into and out of pop- ulations (immigration and emigration, respectively) are critical components, along with births and deaths, of population dy- namics; and 2) the realization that if pop- ulations were not always panmictic and in- finite (see previous section), subpopulations must be connected genetically, demograph- ically, and behaviorally by dispersal. Thus, the study of dispersal became a critical in- gredient in questions ranging over physi- ology, behavior, evolution, epidemiology, and conservation biology as well as all levels of complexity in ecology (Stenseth and Lid- icker, 1992c). One important factor that helped start this avalanche of research on dispersal was the extensive use of confined populations (en- closures, islands) giving meaning to the fence-effect concept. Thus it was that the study of populations in which dispersal was absent helped us realize how important it was in unconfined situations (Lidicker, 1979a). These studies, as well as a growing number on unenclosed populations, led to the explicit recognition that dispersal often occurred before conditions in the home habitat became economically desperate (“pre-saturation dispersal,’ Lidicker, 1975) and hence at least some dispersal was fa- vored by natural selection (“‘adaptive,” Stenseth, 1983); see Lidicker and Stenseth (1992) for summary of the factors motivat- ing dispersal. A second important element was the in- corporation of dispersal in models of mi- crotine rodent multi-annual cycles. Early papers (Krebs et al., 1973; Lidicker, 1973; Stenseth, 1978; Tamarin, 1978) led to widespread attention to dispersal by micro- tine ecologists and inspired numerous in- vestigations, empirical and theoretical, as to the role of dispersal in these cycles. 3) Coactions. I use the term “‘coaction”’ as a brief equivalent to “interspecific inter- action” (Clements, 1916; Clements and Shelford, 1939; Haskell, 1949; Leary, 1985; Lidicker, 19796). Such community-level processes are appropriately reviewed in an- other chapter (Mares and Cameron, 1994), but it is important to comment here, albeit briefly, on several paradigm shifts occurring in recent decades. In the last section, I pointed out how the Erringtonian or benign predation view had become the prevailing one. This trend reached an extreme form in Howard’s (1965) extension of the Cartright Principle to mammalian predators. He advocated the view that in management of rodent pests, predators were a hindrance rather than a help because they stimulated rodent popu- lations to increase reproductive effort. Two other shifts in the way predation was viewed were more generally accepted. The first was that in spite of usually lower re- productive rates (than their prey), predators could reduce prey densities through func- tional rather than numerical responses to prey numbers (Keith and Windberg, 1978; Weaver, 1979). The second change was the realization that predators sometimes made their greatest impact, not on increasing prey populations, but on declining ones. Thus, they have an increasing effect as density falls (anti-regulating, de-stabilizing) and can drive prey densities to extremely low levels (Lid- icker, 1975, 1988a; MacLean et al., 1974; Maher, 1967: Newsome and Corbett, 1975; Pearson, 1966, 1971, 1985; Wagner and Stoddart, 1972). In the case of ungulates, well-documented examples of predator reg- ulation became available (Caughley, 1970; McCullough, 1979; Peterson and Page, 1983). All of these developments reestab- lished predation as a potentially important influence in population regulation. The importance of parasitism in the pop- ulation biology of mammals went, as ex- plained, from the early assumption that it POPULATIONS 337 was important to almost complete neglect. In recent decades a renewed interest is emerging. Partly this was fueled by theo- reticians (Anderson and May, 1979; Dietz and Schenzle, 1985; May and Anderson, 1979; Mollison, 1977, 1987), who drew at- tention to the potential for demographic im- pact that parasites and disease can have. A second factor was the slowly increasing em- pirical evidence that parasites can regulate mammalian populations (Anderson, 1982; Anderson et al., 1981; Fenner, 1976; Greg- ory, 1991; Plowright, 1982; Ross, 1982; Scott, 1988). In my view, this is one area ripe for exploitation by interdisciplinary teams of investigators. The extent to which species of mammals enter into competitive coactions with each other and with non-mammals began to be explored vigorously by the beginning of this modern period. Early leaders were Rosen- zweig (Rosenzweig, 1966, 1973; Schroder and Rosenzweig, 1975), Grant (Grant, 1969, 1972, 1978: Morris and Grant, 1972) and Brown (Brown, 1971; Brown and Davidson, 1977; Brown et al., 1979; Davidson and Brown, 1980; Munger and Brown, 1981). The potentially exciting arena of coopera- tive coactions (mutualisms) remains to be explored in the future. 4) Social behavior. Although a topic that is discussed more fully in another chapter (Eisenberg and Wolff, 1994), it is important to mention here that studies of social be- havior are an increasingly important part of mammalian population biology. Behavior has always been of interest to mammalo- gists, but until recently it was viewed simply as one element in the description of a spe- cies’ life history. In recent years social be- havior has been studied as a group process impacting in important ways and in turn being influenced by various aspects of evo- lutionary and ecological dynamics (Armi- tage, 1988; Berger, 1986, 1988; Cockburn, 1988; Krebs and Davies, 1984; Mech, 1987: Sherman et al., 1991; Slobodchikoff, 1988; Smith and Ivens, 1984; Tamarin et al., 1990). It is this view of behavior that I have included in “behavioral ecology.” It began as a serious trend in mammalian ecology about 1970 (Fig. 1). Examples of a few early contributors include King (1955), Eisenberg (1967), Hamilton (1971), Trivers (1971), Kleiman and Eisenberg (1973), Alexander (1974), and Barash (1974). Wilson’s (1975) influential opus on sociobiology stands as a monument to this critically important de- velopment. Important current themes in behavioral ecology include: 1) social signaling with spe- cial emphasis on the olfactory mode; 2) mating systems; 3) kin recognition and as- sociated cooperative behaviors; 4) plasticity versus tight genetic control of social behav- ior; 5) effects on demography (e.g., spacing behavior, dispersal, density dependent ag- gression); and 6) relationships between so- cial structure and genetic structure of pop- ulations. Based on a 1980 conference, the ASM published an influential review of mammalian behavioral research (Eisenberg and Kleiman, 1983). 5) Density regulation. The subject of how population densities are regulated continues to be an important, exciting, and contro- versial area up to the present time. Past de- bates about “density dependent” versus “density independent” factors and intrinsic versus extrinsic regulation have abated. It is now widely appreciated that densities are influenced by a variety of factors operating in a variety of ways, but that eventually there must be a net increase in the rate at which negative forces act as density increas- es (regulation) or the Earth would be filled with infinite populations. Such negative forces impose either an upper limit for den- sity or result in an equilibrium level (K) toward which densities tend. Similarly, the intrinsic-extrinsic dichotomy is now gen- erally accepted as a non-issue. The density regulating machinery consists of the organ- ism-environment axis, and not with either component alone (Lidicker, 1978). Prop- erties of the organism and properties of its environment interact to result in a given density with the relative contribution of each 338 LIDICKER varying, but with both being always in- volved. With these contentious issues behind us, much of importance remains. What is the actual regulating mechanism for a given population? How much does this vary spa- tially and temporally? Are there general pat- terns for certain taxonomic groups, habitat assemblages, trophic levels, and life styles? Moreover, we need to discover if one or a few factors are consistently of overriding importance for specific populations, with other forces being clearly secondary or con- tributing only to the variance of densities. How important are time lags and age-sex structure? Finally, can we learn to predict population trajectories accurately, and if not, why not? A surprising development has been the emergence of sex ratios as important de- mographic variables. Not only can they vary greatly by microhabitat (Ostfeld et al., 1985), be biased by dispersal (Lidicker and Sten- seth, 1992), and influenced by density (Clut- ton-Brock, 1991; Fredga et al., 1977; van Schaik and Hrdy, 1991), but in some cir- cumstances can be influenced by litter size and maternal social status and condition (Austad and Sunquist, 1986; Clutton-Brock and Albon, 1982; Clutton-Brock and Iason, 1986; Clutton-Brock et al., 1977, 1982: Cockburn et al., 1985; Frank, 1992; Sy- mington, 1987; Verme, 1969). I expect fur- ther significant discoveries in this area. One important trend has been the redis- covery of multi-factorial models of popu- lation regulation. In the early part of this century, ecologists and wildlife biologists routinely accepted that populations were subject to a multiplicity of positive and neg- ative forces. Then, as the field became more quantitative, along with the success of re- ductionist and experimental approaches to research, pressures became intense for find- ing general and simple explanations for how things worked. Complex and especially id- losyncratic explanations were viewed sus- piciously as non-scientific. In recent de- cades, ecologists have become more comfortable with holistic views and partic- ularly with a research protocol that balances reductionist and holistic aspects (Lidicker, 19885, 1991; Macfadyen, 1975, 1978; Mc- Intosh, 1980; Odum, 1977). This new per- spective has encouraged viewing density regulation in a systems context with nu- merous intrinsic and extrinsic factors inter- acting together, a multi-factor perspective (Finerty, 1980; Lidicker, 197359978 1988a). Such a perspective is only the start- ing point, however, as the quantitative re- lationships among the factors remains to be determined. We need to know the temporal and spatial stability of the patterns ob- served, and finally we must search for gen- eralities in pattern. This knowledge will al- low us to manipulate (manage) population numbers effectively and to make predic- tions of future density changes, or at least to know when predictions are reliable and when they are not. It will also give us the data to look afresh at some old questions such as the extent to which carrying capac- ities of habitats and equilibrium densities (K) coincide. With such a huge agenda ahead of us, it is encouraging that some mammalian ecol- ogists are exploring effectively the realities of this complex world. Pioneering research based on multi-factorial hypotheses has been reported by Wagner and Stoddart (1972), Keith and Windberg (1978), Taitt and Krebs (1983), Sinclair (1986), Hansson and Hen- tonnen (1988), Desy and Batzli (1989), and others. The approach remains controver- sial, however (Gaines et al., 1991; Krebs, 1979b; Tamarin, 1978a); and the future is as unpredictable for this field as it is for many mammalian population densities. 6) Conservation. Conservation biology is the extension of wildlife management from concern for economically important species to the biota as a whole. As such, it was for many decades a legitimate part of biology. Then in the rush and push for ““modern sci- ence” that swept through biology in the 1960s, conservation became relegated to its political and moral aspects, and was shunned POPULATIONS 339 by the scientific establishment. However, with the accelerating deterioration of the Earth in the 1980s, along with the prospects for massive losses in biodiversity, and with the help of significant pressure from uni- versity students, conservation biology re- emerged as an important field of scientific inquiry. Even staid academic units began to offer courses, and even major programs, in this area. Helping to legitimatize the field was the establishment of two high quality journals, Biological Conservation in 1968 and Conservation Biology in 1987. Coinci- dent with the latter event was the initiation of the Society for Conservation Biology, which was an instant success. Now conservation biologists are applying frontline basic research in population, com- munity, and landscape ecology, as well as evolutionary biology and population genet- ics to address the mega-threats to humanity caused by losses of biodiversity and the un- controlled growth of our own species. As they operate from an increasingly firm foun- dation in basic science, they can and are moving with confidence to embrace politi- cal, social, and even moral aspects of the human predicament. Thus, the realistically interdisciplinary nature of the problems are being acknowledged and addressed, but this time, hopefully, without losing a solid foot- ing in the basic sciences. At this writing, society at large is beginning to show a glim- mer of recognition for where it is headed, but support for research in the relevant ar- eas remains a tiny fraction of that provided for activities that tend to exacerbate the problems. Whether or not human society at large recognizes its dilemma in time to deal with it humanely is the mega-question for the future. Future Perspectives Even a cursory overview of how popu- lation ecology has changed during the past 75 years reveals a dramatic ontogeny. Lan- guage has changed, new concepts have ap- peared, and the empirical base and number of scientists have grown enormously. All these facts signal that the field has not yet reached maturity, and so should have a long future. A seedling has indeed grown into a young tree. In this development, mammal- ogists have played critical and constructive roles. Setting aside this developmental meta- phor, one can predict with confidence that mammalian population ecology will not fade away. Just as the structure and function of organisms and of cells is fundamental to any overview of biology, so too is the structure and function of populations. Populations, moreover, are the parts (holons) for com- munities and landscapes that in turn cannot be understood without knowledge of these constituents. Besides, as outlined in the six preceding vignettes about the current status of subdisciplines within population ecology, there is much to be learned at this level as well. Trying to be as subjective as possible, I suggest that the following topics will receive increasing attention in the near future: 1. Relating genetic structure to demograph- ic and social structure, giving new in- sights to all three areas, and tending to blur the traditional distinction between ecological and evolutionary time scales; Focusing on landscape-level issues, both for their intrinsic interest and because community-types are being increasingly fragmented; 3. Understanding of dispersal as critical in- puts and outputs to population systems and a major connector and information link within meta-populations; 4. Recognizing parasitic and cooperative coactions as important community or- ganizers; 5. Exploring the interplay of social behav- ior and other aspects of population bi- ology, with the emphasis being on mu- tual effects, and on a comparative approach; N 340 LIDICKER 6. Appreciating the local complexity and global simplicity of density regulating mechanisms, and reconciling this ap- parent paradox through multi-factor models; and 7. Giving all the support we can to arresting the decline in our life-support system through conservation biology and relat- ed efforts. Where do mammals and mammalogists fit into all of this relating, focusing, under- standing, recognizing, exploring, appreci- ating, and giving? Right at the front lines. Mammals are among the more complex in- habitants of this planet; so if we can un- derstand them, we can provide guidelines for the rest. Also, being larger and cleverer than most creatures, they often represent keystone species (strong interactors) in their communities. As such, they often can serve as indicator species for the status and sta- bility of intractably complex chunks of the biosphere. Finally, mammals include the species Homo sapiens. Thus for us, mam- mals are our closest kin, and no wonder many are loved, feared, admired, or reviled. When we study life, we learn about our planet and ourselves, but when we study mammals we come even closer to intimate understanding. Acknowledgments History abhors any attempt to define bound- aries around those who can be credited or blamed for any effort at reconstruction. All one’s expe- riences contribute in intangible ways. Neverthe- less, I gratefully acknowledge R. H. Tamarin who contributed to early discussions regarding the scope and content of this chapter, C. W. Wozen- craft who kindly trusted me with seven programs of ASM annual meetings from the society’s ar- chives, E. P. Odum for helpful discussions, and the editors of this volume for choosing me for this assignment. Both Tamarin and an anony- mous reviewer made many helpful suggestions for improving the manuscript. L. N. Lidicker gave logistic and other support throughout the project. Literature Cited ALEXANDER, R. D. 1974. The evolution of social be- havior. Annual Review of Ecology and Systematics, 5:325-383. ALLEE, W. C., A. E. EMERSON, O. PARK, T. PARK, AND K. P. ScHmipt. 1949. Principles of animal ecology. W.B. 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Self-regulating systems in populations logical Monographs, 50:111-130. of animals. Science, 147:1543-1548. Wynn_e-Epwarps, V. C. 1962. Animal dispersal in 1986. Evolution through group selection. relation to social behaviour. Hafner Publishing Blackwell Scientific Publishers, Oxford, 386 pp. Company, New York, 653 pp. COMMUNITY AND ECOSYSTEM ECOLOGY MICHAEL A. MARES AND Guy N. CAMERON Introduction biotic community is defined by Odum (1971:140) as “*. . . any assemblage of populations living in a prescribed area or physical habitat; it is an organized unit to the extent that it has characteristics addi- tional to its individual and population com- ponents.” Organisms forming a community interact in some manner with one another, whether through coevolutionary adapta- tions, as links in food chains, or any of in- numerable other potential biotic nexuses. Thus, a community may include all of the tree species in a particular forest, or all of the trees plus their associated plant and an- imal species, including detritus-feeding or- ganisms. Ecosystems, on the other hand, in- clude all of the organisms composing a community plus the abiotic components of the environment. Organization and inter- action among trophic levels, in addition to energy flow or nutrient cycling between the living and non-living parts of the system, 1s implied in this definition. While inclusion of several trophic levels within a single community is common, re- search on mammals seldom deals with an entire community. It is important to un- derstand these terms as they were classically employed because they are frequently mis- used. For example, Jaksic (1981) cited sev- 348 eral studies of mammals that ostensibly dealt with communities, but actually dealt either with a partial guild [e.g., a guild being (Root, 1967:335) “a group of species that exploit the same class of environmental resources in a similar way ... without regard to tax- onomic positions’] or with simple taxo- nomic assemblages. An example of the for- mer might be the seed-eating rodents in a desert, which are a part of the granivore guild—the complete guild would include birds, ants, and other consumers of seeds. An example of the latter is research con- ducted on a “rodent community,” when in fact a study may have been done at the pop- ulation level—the community would in- clude all of the mammals and other organ- isms that interact in some important manner within a particular habitat or defined region (see, for example, the discussion of Slobod- kin, 1987). As May (1984:15) stated: °... any attempt to elucidate patterns of com- munity structure must deal with the ques- tion of how to delimit the community. Much academic research restricts itself to a par- ticular taxonomic group . . . instead of first consciously deciding which groups of spe- cies comprise a coherent and irreducible community.” In this context, however, it is important to emphasize that entire com- COMMUNITIES AND ECOSYSTEMS 349 munities do not have to be studied in a community ecology study as long as inves- tigations are undertaken within a commu- nity-based framework. Our goal in this chapter is to examine how research on mammals has influenced, or has been influenced by, ideas of community and ecosystem organization. Mammals perform important functions at and above the com- munity level, whether through pathways of energy flow (e.g., mammals are trophically diverse and may be primary, secondary, or tertiary consumers), through widespread coevolutionary adaptations with plants and other organisms (e.g., pollination activities of tropical bats or dispersal of seeds by trop- ical rodents and ungulates), by affecting standing biomass and production, or by dramatic impacts on a particular habitat, such as elephants and ungulates in the Af- rican savanna community. The effects of mammals on each other and on other or- ganisms, as well as on the abiotic portions of the ecosystem, are extensive. A good deal of effort has been dedicated to understand- ing interactions at levels of biological or- ganization above the individual and the population. It is this area of investigation — research examining the place and the im- portance of mammals in biological com- munities and ecosystems—that will be re- viewed in this chapter. When the ASM was founded in 1919, in- formation on community and ecosystem re- lationships of mammals was negligible. Re- search at this time focused on questions dealing with individual and population ecology, championed by such giants as Jo- seph Grinnell; however, many of the guid- ing principles in community and ecosystem ecology were being formed (see below for work by Merriam, Shelford, and Elton) and were rapidly incorporated into studies deal- ing with mammals. Historical Overview Background research on communities and ecosystems.—Odum (1971:Chapters 1-2) and Kendeigh (1974) reviewed the history of the conceptualization of the terms “‘eco- system” and “community,” and McIntosh (1985) provided an overview of the history of ecology. The idea that plants and animals occur together in some type of non-random pattern is quite old. Kendeigh (1974), for example, mentioned a reference to species assemblages by Theophrastus at the time of Aristotle in the 4th century BC (see McIn- tosh, 1985; Ramalay, 1940). As early as 1807, Humboldt and Bonpland referred to plant associations which could be identified by physiognomy and which were related to both latitudinal and vertical zonation. In 1815, Humboldt devised a grid system for recording presence or absence of plant spe- cies between different landscapes (MclIn- tosh, 1985). The German botanist, A. Grisebach, in 1838, described animals and plants occurring together in interrelated as- sociations. Seventy years after Humboldt’s ground-breaking work, in 1877, another German, Karl Md6bius, discussed oyster communities on a coral reef; M6bius used the term biocoenosis, which subsequently became the European term for biotic com- munities. When Mobius’ work was trans- lated into English in 1883, biocoenosis be- came community (e.g., Allee et al., 1949). C. SchrGter, a Swiss botanist, working 1n the late 1800s and early 1900s, was one of the first biologists to use the concept of plant community consistently for describing veg- etation (Gigon et al., 1981). S. A. Forbes (1887) also used the term community in his classic work on lake ecol- ogy, and it became the term generally used in North America to describe interrelated biotic associations. Forbes, who has been called the complete ecologist (e.g., McIn- tosh, 1985), was curator of the Illinois Nat- ural History Museum and director of the State Laboratory of Natural History (=Il- linois Biological Survey). As McIntosh (1985) noted, Forbes’ influence on ecology was enormous, with his 1887 paper found- ing the science of limnology and other pa- pers anticipating such modern ecological concepts as competitive exclusion. Cur- 350 MARES AND CAMERON ously, competitive exclusion was first more specifically defined, if in a qualitative man- ner, by two mammalogists, Joseph Grinnell (1904, 1908), the father of academic mam- malogy in North America (Jones, 1991), a charter member of ASM and president of the society in 1937, and Angel Cabrera (1932), a Spaniard, who was named an hon- orary member of the ASM (see Hutchinson, 1978). One of the first animal ecologists, Victor Shelford, wrote that ecology was the science of communities (Shelford, 1913). Com- munity theory primarily developed by plant ecologists (e.g., A. G. Tansley, F. E. Clem- ents, H. C. Cowles) in the early part of this century initially was exemplified by the or- ganismic dynamic theory of Clements that predicted a stable, climax stage. This early view, widely accepted by plant ecologists and more or less by animal ecologists, was challenged from the 1930s to the 1950s by plant ecologists espousing an individua- listic theory (Gleason, 1917, 1939; McIn- tosh, 1975, 1980; Whittaker, 1951). Where- as these studies challenged the idea of the plant community, animal ecologists adopt- ed the concept of the community as an en- tity composed of species at equilibrium. Such an idea, associated with the work of Robert MacArthur, derived largely from the belief that many patterns in nature were a consequence of competition to promote niche separation (Cody and Diamond, 1975; Connell, 1980; Diamond, 1978). Mammal- ogists contributed substantially to uncov- ering the role of competition in structuring natural communities (see below). However, another mammalogist (Brown, 1981) ar- gued that theoretical population ecology largely failed to produce a quantitative the- ory applicable to community ecology. The largest oversight, he argued, was a failure to emphasize energy flow as a coalescing pat- tern (see also Hall et al., 1992). The idea of the ecosystem is more recent than that of the community. A botanist, A. G. Tansley (1935), in a review of botanical concepts, coined the term ecosystem, which expanded the concept of the biotic com- munity to include the interactions of the organisms comprising the community with the abiotic parts of the environment. The term biocoenosis was enlarged to geobio- coenosis by a Russian, V. N. Sukachev (Odum, 1971; see Sukachev, 1958), thus be- coming the equivalent of ecosystem. Al- though the terminology used in the New and Old World differed, and different underly- ing ecological philosophies influenced re- search within these two regions (e.g., Gigon et al., 1981), there was a general apprecia- tion of supra-individual and supra-popu- lation effects in ecology, especially in con- tributing to community stability and system cohesiveness. Inherent in the work of some ecologists was the idea that communities, and later, ecosystems, were superorganisms, respond- ing as unified units to experimental and evo- jutionary perturbations (e.g., Clements, 1905, 1916; Semper, 1881). Tansley (1935), however, argued strongly that neither the community nor the ecosystem should be viewed as some type of superorganism. The concept of the ecosystem as a super entity largely has been discounted by most ecol- ogists. However, the idea has arisen again in recent years under the guise of a bio- spheric entity called Gaia (see Barlow, 1991). This mystical super life form is almost sen- tiently responsive to deviations from “‘nor- mal’? environmental parameters that are conducive to maintaining the life to which it (Gaia) 1s presently adapted. Mammalogists, communities, and eco- systems. —Despite the long history of Eu- ropean botanists and invertebrate biologists who developed community-based studies, a number of North American biologists, who also conducted important research on mammals, were intimately involved with the foundations of community and ecosys- tem ecology. As early as the late nineteenth century, C. Hart Merriam, the father of modern mammalogy (e.g., Osgood, 1943; Sterling, 1977), was the first North Ameri- can to develop research interests relating to communities and ecosystems. Merriam de- veloped the team method of conducting sur- COMMUNITIES AND ECOSYSTEMS eeu vey research in particular regions. This in- volved sending groups of researchers into the field to study botany, geology, and most aspects of vertebrate biology (systematics, distribution, natural history, and ecology of both birds and mammals), either for specific localities or for broader regions (e.g., Mer- riam, 1890, 1892, 1894, 1898). Merriam was among the earliest propo- nents in North America of a unified view of natural communities. The biological sur- veys that were conducted in a broad-based manner across taxa, and that included ex- tensive geological investigations and data on climate, amassed a great deal of infor- mation on how the biota of a region reflect- ed abiotic factors in the environment. In examining such data for the San Francisco Mountains region of northern Arizona, Merriam formulated the concept of life zones (Merriam, 1894, 1898). The life zone con- cept was the first attempt to include dom- inant animals in a community classification scheme. This concept warrants additional discussion because it led to early consider- ation of the interactions among taxonomi- cally diverse organisms (i.e., community in- teractions) and with their abiotic environment (i.e., ecosystems). Merriam attempted to explain the distri- bution of animals in relation to life zones that were themselves defined by tempera- ture laws that he formulated. The resultant zones formed altitudinal and _ latitudinal bands that stretched across the North American continent. The life zone concept worked effectively in the mountainous areas of the western United States where it was derived, partially because the temperature limits defining the faunal zones coincided with vegetation regions. There was a good deal of criticism of Merriam’s life zones (see Odum, 1945, for a review), and the sugges- tion that there were definable life zones was replaced by the biome concept (see below) which is still widely used today. Merriam’s revolutionary techniques of field research and broadly based field sur- veys assisted in the development of a ho- listic view of entire biotas as organized and interrelated units responding to abiotic in- fluences. Subsequently, several other mam- malogists helped lay the foundations of modern community and ecosystem ecology. Charles C. Adams, for example, who ini- tially worked for S. A. Forbes in the Illinois Natural History Survey, published some of the earliest work in community ecology when he described a number of animal com- munities while conducting a biological sur- vey of Michigan (Adams, 1905, 1909; see Kendeigh, 1974; and McIntosh, 1985). Ad- ams was a charter member of ASM, was nominated by president Merriam to chair the ASM Committee on Life Histories of Mammals (Hollister, 1920), and published the first manual on animal ecology (Adams, 1915). Another landmark in the development of community ecology was also produced by a mammalian ecologist in North America. The first book ever published on animal or plant communities was by Victor Shelford (1913), who was the first president of the Ecological Society of America (in 1915) and who joined ASM in 1923. Some of his work had a physiological orientation and led to initial ideas about how environmental ex- tremes limited species (and community) ranges. Although he did not formalize the concept, Shelford’s work outlined food chains and made initial conceptual linkages between communities and ecosystems, de- scribing them as dynamic units responding to changing environmental parameters. [Ideas concerning food chains and the con- cept of the pyramid of numbers were first set forth by K. Semper, a North American zoologist, who published a book on animals and their relationship to their natural en- vironments (Semper, 1881, see McIntosh, 1985). Semper’s work was an early zoology text that applied Darwin’s ideas of natural selection to a wide array of organisms and included discussion of such topics as cryp- sis, warning coloration, and competition be- tween similar species.] Shelford realized the importance of biological surveys (e.g., Shel- ford, 1926) and conducted detailed research on lemming populations (e.g., Shelford and jDZ MARES AND CAMERON Twomey, 1941). Shelford’s landmark work was the development of the biome concept in conjunction with the plant ecologist, F. Clements (Clements and Shelford, 1939). Shortly after these contributions of North American ecologists were published, semi- nal research on how organisms functioned was conducted in Great Britain. Perhaps the preeminent work contributing to the de- velopment of community and ecosystem theory (and to the development of ecology in general) was that of the mammalian ecol- ogist, Charles Elton (Elton joined the ASM in 1931), who formulated or developed in detail four important ecological concepts: the niche; differences in food particle size as a mechanism to reduce competition; the food web; and the pyramid of numbers (Duff and Lowe, 1981; Elton, 1927, 1933). These ideas became paradigms of ecological the- ory and contributed greatly to an appreci- ation of the functional relationships of or- ganisms in communities and ecosystems. Elton’s work, which built directly upon the research of Adams and Shelford, was fundamental to understanding the com- plexities of nature. With the pyramid of numbers, Elton showed that there was a structure to nature—organisms in a com- munity were not randomly organized so far as their abundance was concerned; rather, different trophic levels showed specific nu- merical relationships to one another (e.g., herbivores were more abundant than car- nivores). Similarly, pyramids of biomass and energy illustrated non-random organiza- tions with both biomass and energy content decreasing in a pyramidal fashion toward higher trophic levels. Even though we now know that only the pyramid of energy can- not be inverted, these descriptions of nat- ural communities were pivotal to the de- velopment of the modern underpinnings of ecosystem research. With the description of food chains and webs, Elton clearly showed how energy linked component species in an ecosystem in often unexpectedly complex pathways. This was a profound description of nature that continues to impact current ideas of community structure (e.g., Pimm et al., 1991). Elton was also responsible for quantitative research on mammal popula- tion ecology, particularly with his bench- mark publication on 10-year population cy- cles of the lynx (Elton and Nicholson, 1942), his classic book on population ecology of mice, lemmings, and voles (Elton, 1942), and other contributions (e.g., Elton, 1958, 1966). Although the original concept of niche was not necessarily associated with com- munity studies, it has had an important im- pact on modern ecological theory (e.g., Ehr- lich and Roughgarden, 1987). It is worth noting that Grinnell (1914, 1917a, 19175) was among the earliest individuals to de- velop the idea of the niche. Indeed, until Gaffney (1973) reviewed the history of the niche concept and found that it was coined by Robert Johnson in 1910, the origin of the term had been attributed to Grinnell (Cox, 1980). Clearly, Adams, Shelford, Grinnell, and Elton utilized their ecological expertise, es- pecially that developed from working on mammals, to influence the foundations of ecology, particularly at the higher levels of biological organization. By the early 20th Century, mammalogists were among the leading ecologists in conducting studies and developing theories bearing on the devel- opment of community and ecosystem ecol- ogy. Their work, along with the burgeoning disciplines of limnology and plant com- munity ecology, helped drive the field into the modern age. Mammalogists have con- tinued to play a role in the development of community and ecosystem studies, not only in the field and the laboratory but, at least in the case of modern ecosystem research, in the biopolitical arena as well. Approaches to Community and Ecosystem Ecology Early studies in mammalian ecology mir- rored the natural history approach exem- plified by Grinnell’s work. This descriptive approach was reflected in biotic surveys that COMMUNITIES AND ECOSYSTEMS 353 encompassed a variety of techniques to sample both plants and animals through the 1940s in the United States (i.e., Fautin, 1946). The 1940s and 1950s were a period during which studies were designed to de- scribe community processes, in particular trophic dynamics and energy flow (Linde- man, 1942; Odum, 1957; Teal, 1957). Ini- tial emphasis was on aquatic habitats, but subsequent studies in terrestrial ecosystems included small mammals as major consum- ers (e.g., Golley, 1960). The International Biological Program (1969-1974; IBP) was an important factor in the development of community and eco- system ecology because it bridged the earlier descriptive approach and the current em- phasis on empiricism. One thrust of IBP was to organize groups of specialists to study major terrestrial biomes and to integrate the findings with models used as predictive tools. This international effort at under- standing the structure and function of eco- systems on a global scale was in large part developed and administered by another mammalogist, W. Frank Blair. Many mam- malogists active today participated in IBP (IBP will be discussed in detail below). One of the criticisms about IBP was the lack of hypothesis testing. Ecological studies since the mid-1970s have become increas- ingly grounded in the scientific method, thus completing the transition from the descrip- tive approach that was begun at the turn of the century. To facilitate experimental stud- ies at appropriate ecological scales (both spatial and temporal), a variety of ecological research areas have been established, in- cluding Biosphere Reserves, Experimental Ecological Reserves, and Long-term Ex- perimental Research areas (Franklin et al., 1990). Ecological experiments are conduct- ed in the laboratory and field, use natural or experimentally controlled perturbations, and consider factors that influence organ- isms over the short- or long-term (Dia- mond, 1986). Mammalogists have been at the forefront of development of empirical studies conducted in the field (see citations below) and have argued for the develop- ment of facilities where long-term experi- mental research could be undertaken. Mammalogists also have argued that nat- ural history should continue to play a crit- ical role in empirical studies by providing the crucial knowledge to design appropriate experiments (Bartholomew, 1986; Brown, 1986; Mares and Braun, 1986). Finally, mammalogists have played a role in devel- oping methods to conduct and analyze field experiments, such as taking into account the effect of scale, both spatial (J. S. Brown, 1989: Morris, 1987, 1989; Price and Kra- mer, 1984) and temporal (Brown and Heske, 1990; Brown and Kurzius, 1989). Community Ecology The concept of niche. —The development of the concept of the niche began with sev- eral mammalogists. Joseph Grinnell wrote that ‘“‘As with zones and faunas, associa- tions are often capable of subdivision; in fact such splitting may be carried logically to the point where but one species occupies each its own niche” (Grinnell and Swarth, 1913:218), and “A concurrent axiom 1s that if associational analysis 1s carried far enough, no two species of birds or mammals will be found to occupy precisely the same ecologic niche, although they may apparently do so where their respective associations are rep- resented fragmentarily and in intermixture” (Grinnell, 1914:91). Grinnell defined the niche as “the concept of the ultimate dis- tributional unit, within which each species is held by its structural and instinctive limitations...” (Grinnell, 1928/1943:192- 194). This view of the niche as a distribu- tional entity was complemented by Charles Elton’s (1927:64) idea that the ‘“‘niche of an animal means its place in the biotic envi- ronment, its relations to food and ene- mies’’—the so-called functional niche. Dice (1952) suggested that the niche represented a coalescence of both functional and distri- butional attributes of a species. The current concept of the niche was for- malized mathematically as an n-dimen- 354 MARES AND CAMERON sional hyperspace by an aquatic biologist, G. Evelyn Hutchinson (1957). Mammalo- gists have contributed to refining the niche concept. For example, MacMahon et al. (1981) discussed how the niche reflects the actual or potential state of an organism at an instant in time. They concluded that an organism’s niche is bounded by tolerance limits set by heredity, maturity, and accli- matization, and that changes in tolerances during an organism’s life cycle create on- togenetic bottlenecks in the niche. Mammalogists have contributed to our knowledge of the niche concept with re- search measuring niche parameters (Carnes and Slade, 1982; Churchfield, 1991; Dueser and Shugart, 1979, 1982; Montgomery, 1989: Slobodchikoff and Schultz, 1980; Smartt, 1978; Van Horne and Ford, 1982). In addition, mammalogists have conducted empirical studies that illustrated increases in niche breadth with intraspecific compe- tition (Smartt and Lemen, 1980; Van Horne and Ford, 1982), variation in genetic and morphological measurements with niche breadth (i.e., the niche variation hypothesis; Smith, 1981), a correlation of niche breadth with species abundance (Brown, 1984; Sea- gle and McCraken, 1986), body size (Bar- clay and Brigham, 1991; Willig and Moul- ton, 1989), and partitioning of resources (Brown, 1973, 1975; Cameron, 1971; Em- mons, 1980; Mares and Williams, 1977; McKenzie and Start, 1989; M’Closkey, 1980; Meserve, 1981; Owen-Smith, 1989; Price et al., 1991; Willig et al., 1993). Interspecific interactions. —In addition to the niche concept, mammalogists have con- tributed substantially to another basic con- cept of community and ecosystem ecology, that of interspecific interactions, including competition, predation, and mutualism. Again, Joseph Grinnell laid the framework for this concept when he wrote “‘these var- ious circumstances, which emphasize de- pendence upon cover, and adaptation in physical structure and temperament there- to, go to demonstrate the nature of the ul- timate associational niche occupied by the California thrasher. ... It is, of course, ax- iomatic that no two species regularly estab- lished in a singie fauna have precisely the same niche relationships” (Grinnell, 1917a: 433), and that “‘no two species in the same general territory can occupy for long iden- tically the same ecological niche ... com- petitive displacement of one of the species by the other is bound to take place” (Grin- nell, 1928/1943:192-194). The great Span- ish mammalogist, A. Cabrera, who spent most of his professional life in Argentina and was the preeminent force in the history of South American mammalogy, also pub- lished an important paper on competitive exclusion that described the concept as a biological law (Cabrera, 1932). Interspecific competition was first de- scribed mathematically by Lotka and Vol- terra (see Slobodkin, 1961). Over the years, mammalogists have contributed to the modification of these models to overcome some of the limiting assumptions (Fryxell et al., 1991). Mammalogists have also de- vised statistical methods to measure com- petition in the field (Hallett and Pimm, 1970; Rosenzweig et al., 1984). Other mammal- ogists were instrumental in beginning the classification of this process into what is now known as interference and exploitation competition (Elton and Miller, 1954; Mil- ler, 1967) and in describing the relative im- portance of these processes (King and Moors, 1979). Mammalogists have com- pleted numerous other studies on the pro- cess of interspecific competition (e.g., Brown, 1971; Brown et al., 1979; Dickman, 1989: Fox, 1989; Holbrook, 1979; Kirk- land, 1991; Pulliam and Brand, 1975; Ro- senzweig, 1966; Smith and Balda, 1979; Willig and Moulton, 1989; see below for role of competition in community struc- ture), but data gathered across entire mam- mal faunas to clarify competitive or other mechanisms that are important in structur- ing temperate and tropical faunas are still rudimentary (Lacher and Mares, 1986; Wil- lig, 1986). The niche overlap hypothesis states that maximum tolerable niche overlap decreases as the intensity of competition increases COMMUNITIES AND ECOSYSTEMS bey) (Pianka, 1974). Studies on several mam- malian systems offer support for this hy- pothesis (Fox, 1981; Lacher and Alho, 1989; M’Closkey, 1978; Porter and Dueser, 1981; but the multivariate technique used by Por- ter and Dueser has been questioned by Carnes and Slade, 1982). However, Brown (1975) found that niche overlap increased when number of species increased for North American desert rodents. He attributed this response to the fact that the Mohave desert communities he studied may be composed of more generalist species than those ex- amined in the other studies. A second interspecific interaction to which mammalogists have contributed is the pro- cess of predation. As with competition, ba- sic models for this process were developed by Lotka and Volterra. Mammalogists were instrumental in refining these models (Ro- senzweilg, 1969, 1973; Rosenzweig and MacArthur, 1963). Much of the subsequent development of this aspect of community ecology relied on studies of mammals; for example, functional and numerical re- sponses were described with responses be- tween Sorex, Blarina, and Peromyscus and their sawfly larva prey (Holling, 1959), and differences in susceptibility of age groups to predation were described in the moose-wolf system (Mech, 1966). Mammalogists have conducted many studies on the basic nature of predator-prey relations (e.g., Hornocker, 1970; Pearson, 1971; Schnell, 1968; Wagner and Stoddart, 1972). Two views on the role of predators arose earlier in this century. One, champi- oned by the mammalogist Paul Errington (1946), held that predators only took sur- plus prey above the carrying capacity, a view without current support. The other view arose in the entomological literature and concluded that predators regulated their prey. Demonstration of this phenomenon has been elusive largely because of the myr- iad of definitions given to this process (Var- ley, 1975); population regulation, however, is a density-dependent feedback of either increasing mortality or decreasing fecundity proportional with increasing predation. Er- linge and his colleagues (Erlinge et al., 1983, 1984) analyzed population density of field voles and rabbits, as well as food habits of their major avian and mammalian preda- tors, in Sweden. They recorded both func- tional and numerical responses by predators to changes in prey numbers and concluded that the functional response, combined with switching by predators from voles to rabbits and vice versa when numbers of prey be- came low, produced a density-dependent ef- fect during the period of highest vole density (autumn). These findings were challenged by Kidd and Lewis (1987), who argued that Erlinge and his colleagues had not demon- strated density-dependent predation; Er- linge et al. (1988) responded that predator switching among alternative prey affected regulation. Korpimaki (1993), however, presented evidence that Microtus sp. in Fin- land are regulated by density-dependent avian predation and delayed density-depen- dent mammalian predation. Sinclair et al. (1990) concluded that house mice in Aus- tralia were regulated by delayed density-de- pendent predation at low-moderate mouse densities, but by inverse density-depen- dence at high mouse densities. Trostel et al. (1987) found that avian and mammalian predators may affect the 10-year cycle of snowshoe hares in a delayed density-depen- dent fashion. Mutualism has been studied much less intensively than either competition or pre- dation, but research on mammals has again provided perspectives on the mechanics and pervasiveness of this process. Mutualism can be a direct or indirect process. Mammal- plant interactions, such as seed dispersal (Carpenter, 1978; Sazima and Sazima, 1978; Simpson and Neff, 1981; Sussman and Ra- ven, 1978) or pollination (Fleming, 1981; Howe, 1980; Smith, 1970; Stapanian and Smith, 1978) are direct processes. In indi- rect mutualism, a positive interaction is achieved even though there is no direct con- tact between the species. For example, al- though Thompson gazelles, zebras, and wil- debeests eat different foods on the Serengeti, the gazelles prefer to feed in areas where 356 MARES AND CAMERON wildebeests have grazed a month earlier, since such areas contain greater plant bio- mass (McNaughton, 1976). Brown et al. (1986), building upon an evolutionary hy- pothesis developed by Mares and Rosen- zwelg (1978), demonstrated that rodents in the Mohave desert eat large seeds, whereas ants prefer smaller seeds. When rodents were removed, large-seeded plants increased in abundance, reduced the abundance of small- seeded plants and, consequently, the small seed resources of ants. Thus, rodents acted as indirect mutualists on ants (Davidson et al., 1984). Other examples of indirect mutualism in- clude the observation that the progress of plant succession may be positively affected when pocket gophers alter soil characteris- tics and thereby affect the resultant plant species composition (Andersen and Mac- Mahon, 1985; Huntly and Inouye, 1988; Tilman, 1983). In a similar fashion, food availability for granivorous birds is affected positively by desert rodents that forage pref- erentially upon those plant species that compete with plant species eaten by the birds and that maintain areas of bare soil which serve as germination sites for those plants eaten by the birds (Mitchell et al., 1990). Coppock et al. (19835) also discovered that bison preferentially grazed in areas where prairie dogs had reduced the occurrence of less preferred plants, thereby allowing growth of more preferred plants. Finally, dispersal of seeds from parent plants re- duced seed predation by desert rodents and thereby enhanced seed germination (O’Dowd and Hay, 1980). Community structure. —Structure within a community is determined by both com- position and relative abundance of species. Many studies have addressed Elton’s (1927) concept of limited membership: Why is it that what does occur together constitutes a limited subset of what might occur together? One avenue of research has been to inves- tigate whether structure exists for subsets of a community [i.e., within community struc- ture, termed guild structure by Root (1967) to refer to groups of species exploiting re- sources in a similar way; the multiple mean- ings of guild, however, have been discussed by Hawkins and MacMahon (1989) and Simberloff and Dayan (1991)]. Most of this work has centered on insects and lower ver- tebrates. In one of the few studies with mammals, MacMahon (1976) concluded that similarities in guild structure of small mammals among sites in the deserts of the western United States resulted from inter- actions of evolutionary events and site char- acteristics. Fox (1989) and others (e.g., Findley, 1989; Humphrey et al., 1983; McKenzie and Start, 1989; Rosenzweig, 1989; Smythe, 1986; Willig and Moulton, 1989) have also examined the mechanisms affecting community (or guild) assembly in mammals. Fox (1989) used a taxonomical- ly-based rule for species assembly of small mammals in Australian heathlands that stipulated there was a higher probability that species comprising a community will have been drawn from a genus, guild, or taxo- nomically-related group of species with similar diets. Fox and Brown (1993) applied an assembly rule based upon functional groups to suggest that interspecific compe- tition was an important mechanism struc- turing desert rodent communities in North America. Willig and Moulton (1989), on the other hand, found that ecomorphology in bat communities was not different from that expected by a stochastic model; Willig et al. (1993) reported that dietary differences among Brazilian bats did not order com- munity structure, but suggested that com- petition for some other resource could be more important. Other research has centered on the role of competition in determining community structure. This research can be divided into observational and empirical evidence. Here again, mammalogists have played promi- nent roles. Several sorts of observational ev- idence have been used to conclude that in- terspecific competition has been important in determining community structure. Re- source partitioning, comparative species COMMUNITIES AND ECOSYSTEMS Sey) distributions, and character displacement will be considered. Resource partitioning, the subdivision of resources by two or more species, is one outcome of the Lotka-Volterra model of competition, whereby niche dimensions of competing species are modified such that niche overlap decreases (see reviews by Schoener, 1974, 1986a). Numerous studies have demonstrated resource partitioning in mammals (e.g., Belk et al., 1989; Brown, 1989; Dueser and Hallett, 1980; Fleming et al., 1972; Hallett et al., 1983; Heithaus et al., 1975; McNab, 1971; McNaughton and Georgiadis, 1986; Meserve, 1981). The negative correlation between spatial distributions of species is another way that the effect of competition on community structure has been inferred. There are many examples of this effect from the literature on mammals. For example, mammalogists have noted such spatial partitioning be- tween Sigmodon hispidus, S. fulviventer, and S. ochrognathus in Durango, Mexico (Pe- tersen, 1970, 1973); Sigmodon leucotis and Microtus mexicanus in Durango, Mexico (Baker, 1969); among seven species of Mi- crotus in western North America (Ander- son, 1959); and among desert rodents in the southwestern United States (Whitford and Steinberger, 1989). Similarly, the northward withdrawal of Microtus coinci- dent with a gradual northward advance of S. hispidus is also viewed as an indication of competition (Baker, 1969). Other mam- malogists have devised methods of detect- ing the effects of competition by analysis of captures at trap stations (Hallett and Pimm, 1970; Rosenzweig et al., 1984). Character displacement is the change un- der natural selection of morphological, physiological, or behavioral characteristics in one or more ecologically similar species whose ranges overlap in sympatry. Such evolved differences reduce competition. Malmquist (1985) demonstrated that Sorex minutus had significantly smaller jaws when it occurred in sympatry with S. araneus (Sweden) than when it occurred allopatri- cally (Ireland). Similarly, Dayan et al. (1989, 1990) analyzed cranial characteristics of weasels in North America and Israel, and feline carnivores in Israel, and concluded that past competition for food led to pres- ent-day cranial differences. Although these studies suggest an impor- tant role for competition in community structure, they are not conclusive. Empirical evidence demonstrating a change in niche breadth in response to a change in abun- dance of a potential competitor is necessary. Such evidence can be gathered from natural experiments or from perturbation experi- ments. Natural experiments involve com- paring an area where a species 1s allopatric with a similar area where it occurs sympat- rically with a potential competitor; differ- ences in niche dimensions between the two areas are taken to indicate the effect of com- petition. For example, Glass and Slade (1980) reported that when S. hispidus de- clined locally in Kansas, Microtus ochro- gaster expanded its spacial use of habitats; there was spatial separation when both spe- cies were present. The greatest problem with such natural experiments is that the sites compared may differ in ways other than the presence or absence of the species under consideration. A perturbation experiment is arguably the best way to demonstrate whether compe- tition affects community structure. This type of experiment, where one species is re- moved or reduced in density by the inves- tigator, and the effect upon the remaining species 1s documented, avoids problems of possible differences between study sites. Such field experiments have demonstrated that interspecific competition affects com- munity structure in a wide variety of sys- tems (Busch and Kravetz, 1992; Connell, 1983; Schoener, 1983, 1985; Underwood, 1986). The inclusion in these general re- views of certain field experiments on mam- mals in which experimental flaws had been detected were criticized (i.e., enclosures smaller than home ranges; Galindo and Krebs, 1986; Schoener, 19866). However, 358 MARES AND CAMERON Dueser et al. (1989) reaffirmed the role of competition in structuring rodent commu- nities. Details of these effects can be found in the numerous studies cited in the above reviews, such as Grant (1972), Crowell and Pimm (1976), and Dickman (1988). One of the major criticisms to the con- clusion that competition affects community structure was that many empirical studies were biased and that null models (1.e., mod- els assuming no biological effects) could ex- plain observed patterns of community structure (see Harvey et al., 1983; Strong et al., 1984). Community patterns of neotrop- ical bats seem to be affected by factors other than simple competitive interactions (e.g., Willig and Mares, 1989). While problems certainly existed with empirical studies, analyses and reanalyses of data with null models have reconfirmed the importance of competition in general, and among mam- mals in particular, in structuring some com- munities (Bowers and Brown, 1982; Brown and Bowers, 1984; Dayan et al., 1990; Find- ley, 1989). However, Owen-Smith (1989), studying African ungulates in savanna grasslands, concluded that competition had little effect on community structure. Simi- larly, Findley (1993), in a comprehensive analysis of data on bat communities from throughout the world, concluded that com- petitive interactions had little or no part in structuring the communities; rather, their structure had a great deal to do with sto- chastic processes. Predation also has been shown to be an important determinant of community structure (Sih et al., 1985). Removal of sea otters from nearshore communities along the coast of the western United States in- creased abundance of a major prey item (sea urchins). Abundant sea urchins decimated nearshore kelp communities, both in terms of abundance and diversity; simplification of the kelp community caused loss of many associated marine organisms. Thus, the sea otter can be classified as a keystone species in this system (Duggins, 1980; Estes and Palmisano, 1974; Estes et al., 1978; Simen- stad et al., 1978). Similarly, Brown and Heske (1990) classified a guild of three spe- cies of kangaroo rats in the Mohave Desert as keystone species because their removal decreased the abundance of bare areas (ger- mination sites for plants), changed the spe- cies composition of the plants, and favored invasion of the desert area by grassland spe- cies of mammals. Such effects were noted also in areas where species were introduced. Case and Bolger (1991) observed that in- troduction of mongoose, domestic dogs and cats, and Rattus on islands in various parts of the world constrains the distribution, col- onization, and abundance of reptiles. Pred- ators also affect microhabitat distribution of small mammals (Brown et al., 1988; Longland and Price, 1991). Kotler dem- onstrated that desert rodents forage in mi- crohabitats offering shelter from predators and that the effects of predation risk, in combination with resource availability, in- fluence structure of desert rodent assem- blages (Kotler, 1984, 1989; Kotler and Holt, 1989; Kotler et al., 1988). Community patterns. —Community pat- tern was defined by Elton (1966:22) as “‘the repetition of certain component shapes to form a connected or interspersed design.” Here we consider patterns in species rich- ness, abundance, and diversity. The num- ber of species (species richness) of mammals increases with area (the well-known species area curve; Brown, 1971; Brown and Ni- coletto, 1991; Connor and McCoy, 1979; Dritschilo et al., 1975), although Lomolino (1989) warned of statistical considerations when interpreting the slope of the species- area curve (see Coleman et al., 1982). The distributional extent and density of mam- mals are also related (Brown, 1984). Several taxa of mammals exhibit hyper- diversity (Dial and Marzluff, 1989), that is, their biodiversity is greater than what would be expected by chance alone. Latitudinal patterns in species diversity of mammals are well known (Fleming, 1973; Heaney, 1991; Harrison et al., 1992; McCoy and Connor, 1980; Owen, 1990a, 19906, Pagel COMMUNITIES AND ECOSYSTEMS 359 et al., 1991; Rosenzweig, 1993; Schum, 1984: Simpson, 1964; Willig and Sandlin, 1991; Willig and Selcer, 1989), but not all groups of mammals respond to latitude in the same way. Indeed, quadrupedal mam- mals (as opposed to bats) do not fit the clas- sic pattern of increasing the diversity of spe- cies aS one moves toward the equator (Lacher and Mares, 1986; Mares, 1992; Mares and Ojeda, 1982). Many reasons for this gradient in species diversity have been advanced, including the supposition of a longer, uninterrupted time for evolution in the tropics [although Dritschilo et al. (1975) showed that rodent species introduced to North America within the past 2,000 years do not have fewer mite species than species that arose in the Pleistocene as predicted by the time hypothesis], spatial heterogene- ity (Hafner, 1977; Kotler and Brown, 1988; M’Closkey, 1978), primary productiv- ity (Abramsky, 1989; Abramsky and Ro- senzweig, 1984: Brown, 1973; Brown and Davidson, 1977; Owen, 1988), potential evapotranspiration (Currie, 1991; Rosen- zweig, 1968), and disturbances (Fuentes and Jaksic, 1988). Bowers (1993) demonstrated that plant communities with high and low intensity of herbivory have lower diversity than when herbivory was at an intermediate intensity. Rosenzweig (1993) reviewed ev- idence from mammals and other taxa that reveals a productivity-diversity pattern with highest diversity at intermediate productiv- ities and suggests hypotheses to explain it, particularly the decline at high productivi- ties. Control of species diversity has been linked to the theory of limiting similarity, whereby the number of species in a com- munity may be limited by their niche over- lap (often measured as size ratios; Hutch- inson, 1959). Most data on size ratios, including that from mammals, do not sup- port limiting similarity (Brown and Lieber- man, 1973; Willig, 1986). In fact, the pres- ence of vacant niches in mammalian communities may facilitate invasions (Da- vis and Ward, 1988). Finally, the study of several other pat- terns provides insight into mammalian community dynamics. Differences in pat- terns of body mass of North American land mammals seen at different measurement scales have been attributed to diverse eco- logical and evolutionary processes oper- ating at those scales (i.e., competition, extinction, and allometric energetic con- straints; Brown and Nicoletto, 1991). Stage of succession affects mammalian diversity (Buckner and Shure, 1985; Foster and Gaines, 1991; Fox, 1982; Sly, 1976) and, in turn, mammals have a profound effect on patterns of plant succession by the processes of herbivory and disturbance; mammals usually facilitate the entrance of later suc- cessional (plant) species into a successional sere (Anderson et al., 1980; Huntly and In- ouye, 1987, 1988; Pearst, 1989; Platt, 1975; Tilman, 1983). Most recently, mammalian ecologists have begun to focus attention on patterns at the landscape scale. In particu- lar, current work is revealing the effect of sizes of habitat patches (particularly result- ing from habitat fragmentation) and corri- dors on dynamics of small mammal pop- ulations (Foster and Gaines, 1991; Henderson et al., 1985; Henein and Mer- riam, 1990; Laurance, 1991; Merriam and Lanoue, 1990). Community function. — Community function involves relationships among con- stituent species whereby energy and nutri- ents are exchanged among these species. However, other sorts of interactions among species affect the community. For example, the study of mammalian communities has contributed to our knowledge of ecological stability. McNaughton (1977, 1985) consid- ered how grazing mammals affected the re- lation among stability, diversity, and func- tional properties in grasslands of the Serengeti, concluding that the effect on grassland plant diversity may be different from the effect on grassland function (mea- sured as primary production). Trophic interactions among species are discussed in the section on Ecosystem Ecol- 360 MARES AND CAMERON ogy below. Here we consider the impact of such trophic interactions and address the question as to the effects mammalian con- sumers might have on ecological commu- nities. Hairston et al. (1960; hereafter HSS) concluded that herbivores were seldom food-limited and unlikely to compete for resources, whereas producers, carnivores, and decomposers competed in a density- dependent fashion for resources. This land- mark study stimulated much research into consumer effects in various taxa, including mammals. Mammals usually consume 2- 8% of available net production, but may eat as much as 30% under some conditions (P1- mentel, 1988), tending to support HSS. However, the addition of food results in in- creased population density, growth rate, and survival, and smaller home ranges, coun- tering predictions of HSS (Boutin, 1990; Desy et al., 1990; Dobson and Kjelgaard, 1985; Klenner and Krebs, 1991; Mares et al., 1976, 1982: Sullivan et al., 1983; Taitt and Krebs, 1983). The conclusion that not all plants are edible and that food is limiting has been strengthened by studies demon- strating that dietary intake by mammalian consumers is restricted by the nutrient and secondary plant compound content of their food (Batzli, 1986; Batzli et al., 1980; Ber- geron and Jodoin, 1987; Bryant et al., 1991; Bucyanayandi and Bergeron, 1990; Eshel- man and Jenkins, 1989; Hanley, 1982; Jon- asson et al., 1986; Jung and Batzli, 1981; Kerley and Erasmus, 1991; Kuropat and Bryant, 1983; Marquis and Batzh, 1989; Randolph et al., 1991; Schultz, 1964; Seagle and McNaughton, 1992; Sinclair et al., 1982, 1988; Snyder, 1992; Willig and Lacher, 1991). Mammalian consumers have a variety of other effects on community function (Hunt- ly, 1991; Huntly and Inouye, 1988; Paige, 1992; Whicker and Detling, 1988). In sum- mary, mammals affect plant production (Detling et al., 1980; Grant and French, 1980; Reichman and Smith, 1991), fitness (Belsky, 1986; Edwards, 1985; Maschinsk1 and Whitham, 1989; McNaughton, 1986; Paige and Whitham, 1987), pollination and seed dispersal (Borchert and Jain, 1978: Fleming, 1982; Golley et al., 1975; Howell and Roth, 1981), vegetative diversity (Archer et al., 1987; Batzli and Pitelka, 1970; Borchert and Jain, 1978; Bryant, 1987; Cof- fin and Lauenroth, 1988; Fox and Bryant, 1984; Fuentes et al., 1983; Grant et al., 1982; Lidicker, 1989; Reichman and Smith, 1985; Reichman et al., 1993; Spatz and Mueller- Dombois, 1973; Stapanian and Smith, 1986; Truszkowski, 1982), and nutrient content (Coppock et al., 1983a). The complexity of biotic and abiotic interactions can be pro- nounced. For example, Grant et al. (1977) demonstrated that addition of nitrogen and water affected composition and density of a short-grass prairie and, concomitantly, af- fected structure of the mammalian com- munity (see also Grant et al., 1980, for the effects of burrowing by fossorial mammals on plant production). Convergent evolution and the develop- ment of communities. —Community ecol- ogists have paid a good deal of attention to determining if communities develop over evolutionary time in a predictable manner. Because all species within a community re- spond to complex stimuli in an evolution- ary manner, it might appear that popula- tions evolving under broadly similar climatic regimes would develop suites of similar adaptations. Certainly it has long been known that several mammals are re- markably convergent, and this general mor- phological similarity is particularly preva- lent among desert rodents, perhaps because they inhabit areas that are especially chal- lenging to the physiology and ecology of small mammals (Eisenberg, 1975; Hatt, 1932: Schmidt-Nielsen, 1964). Pianka (1969, 1973, 1975, 1985, 1986) and Cody (1970, 1973, 1974, 1975) were among the first evolutionary ecologists to examine community convergence. Pianka conducted research on lizard communities in the United States, Australia, and Africa. Cody studied birds occurring on different continents in similar habitats (Mediterra- COMMUNITIES AND ECOSYSTEMS 361 nean chaparral-scrubland birds of Califor- nia and Chile). Both examined various as- pects of ecology and community structure, and devised quantitative methods for com- paring niche parameters of faunas. Broadly speaking, birds were more convergent than lizards, although in each area there were striking examples of ecologically and mor- phologically convergent pairs, as well as re- markably different species. Karr and James (1975) studied the bird faunas of forested habitats of North and Central America and of Africa. Utilizing multivariate techniques, they concluded that convergence was pro- nounced among some species that differed phylogenetically, whereas divergence was evident among some species with similar phylogenetic backgrounds. At about this same time, Mares (1975, 1976), for desert rodents, and Findley (1976), for bats, used multivariate analyses of morphoecological data to assess similar- ities and differences between faunas occur- ring on different continents. Both concluded that convergence was pronounced; mor- phology (and ecology) had evolved in many members of each fauna in a similar manner. Nevo (1979) demonstrated that fossorial rodents on many continents converged in ecological, morphological, behavioral, physiological, genetic, and many other char- acteristics in response to the subterranean environment. Mares (1980, 1993a, 19935) later extend- ed his original analysis, which had been lim- ited to an examination of desert and non- desert rodents in North and South America, to small mammals inhabiting all of the world’s deserts. His results showed that community-wide convergence of morphol- ogy and ecology generally was detectable when species with widely different phylog- enies were compared. Similar results were found by Berman (1985) in a rigorous mor- phological analysis of the evolution of bi- pedality among small mammals in deserts. Mares (1983:37-38) noted: “If one were to go into an unknown desert region, there are many predictions that could be made con- cerning the small mammal fauna... of the area... [AJ]t least some rodents ... would exhibit the following adaptations: special- ized kidneys .. . a counter-current heat ex- change system in the nasal region; modified brain cells responsible for ADH secretion; lowered metabolic rate; facultative torpor; ability to exist without free water; mini- mization of water loss through respiratory, excretory, and defecatory pathways; inflated tympanic bullae or elongate pinnae; bipe- dality ... [which]... could occur in all tro- phic categories except the completely fos- sorial niche ... [and] coexisting species might exhibit regular patterns of body size differences.” These comments about the pervasiveness of convergent evolution on the biology of organisms were in broad agreement with Nevo (1979). The International Biological Program dedicated a great deal of effort to assess the pervasiveness and predictability of conver- gent evolution between communities (Ma- bry et al., 1977; Orians and Solbrig, 1977; Simpson, 1977). The results of these exten- sive studies indicated that, differences in history, phylogeny, and climate notwith- standing, ecosystematic convergence can be quite pronounced, especially for some of the components of the ecosystem. Recent research on convergent evolution indicated that similar evolutionary adap- tations to similar physical environments may not only be striking, but may extend beyond morphological traits to complex be- havioral and ecological attributes. For ex- ample, Mares and Lacher (1987) showed that mammals that are specialized for life on isolated piles of boulders in different parts of the world can develop strongly conver- gent suites of characteristics that are asso- ciated with life in this rocky environment. These similarities will override phylogenet- ic similarities to such an extent that, for the traits examined, animals in different orders that inhabited very similar microenviron- ments (e.g., hyraxes, Cavia and Procavia of Africa, and the rock cavy, Kerodon, of the Brazilian Caatinga), were more similar to 362 MARES AND CAMERON one another than they were to their own confamilials. Curiously, when the entire mammal fau- na of the Brazilian Caatinga was examined, there was little or no faunal convergence evidence between the Caatinga’s fauna and those of other semiarid areas in the world (Mares et al., 1985). The Caatinga, although an extensive tropical dry area, has had a special history of isolation from grasslands where pre-adaptations for aridity might have developed over time, as they did for the other deserts and semideserts of the world. Rather, the Caatinga is a tropical dryland surrounded by moist forests, an unusual zone that undergoes periodic and cata- strophic droughts (perhaps every two de- cades). Mares et al. (1985) showed that the largely tropically adapted fauna of the Caa- tinga was unable to adapt to aridity because droughts likely functioned as a frequent bot- tleneck that regularly eliminated most small mammals from the region. This research made clear the role of history, climate, and surrounding habitats on the evolution of convergent assemblages of mammals. Research on convergent evolution is con- tinuing for many groups of organisms (e.g., Luke, 1986; Schluter, 1986, 1990). Many questions remain to be answered. What is the influence of history on the evolution of similar species in similar areas? How chal- lenging must an environment be to limit the evolutionary responses of organisms and thus make convergence likely? To what ex- tent can phylogeny be overridden by natural selection? At the higher levels of organiza- tion (e.g., alpha and beta diversity, coexis- tence, competitive interactions, predation effects), what are the factors that cause con- vergence to be manifested, and can con- vergence be measured in some meaningful manner when entire faunas are compared (see Mares, 1993a)? Ecosystem Ecology Energetics. —With the publication of Tansley’s (1935) classic paper on plant ecol- ogy, 1t was possible to begin formulating experiments that would describe the func- tional relationships of organisms in a de- fined area. Perhaps because it is difficult to define the boundaries of an ecosystem [Col- invaux (1973:296) noted: ““Ecosystems are in the eye of the beholder .. .”’], it follows that the breakthrough in ecosystem ecology was made by an investigator studying lakes, which by their nature have distinct bound- aries. The landmark paper on ecosystem ecology was Lindeman’s (1942) report on the energetics of organisms in Cedar Bog Lake in Minnesota. Lindeman determined the standing crop of the various trophic lev- els in the lake and then assigned caloric val- ues to the productivity at each level. Thus, the currency of systems ecology (energy) was defined, quantified, and applied. Addition- ally, it subsequently became possible to have at least a frame of comparison for param- eters of standing crop, turnover, productiv- ity, and so forth. After Lindeman, ecosystems were con- sidered a basic unit of ecology (e.g., Evans, 1956; Odum, 1953), and many ecologists, particularly those working in aquatic sys- tems, began conducting research on either natural systems or systems constructed in the laboratory (e.g., Slobodkin, 1962). If lakes have relatively well-defined bound- aries, and test tube communities even more so, terrestrial communities are notoriously difficult to control or even to obtain mea- surements of their component species. As Engelmann (1966) observed, it is a daunting task to apply a systems approach to a ter- restrial ecosystem. It was almost surely this difficulty in capturing, observing, and quan- tifying population sizes (standing crop), de- termining the energetics of respiration and of daily activities, estimating turnover rates, and obtaining the myriad of other data re- quired to understand how the system func- tioned, that delayed the application of Lindeman’s ideas (and those that had ex- panded systems theory in the intervening period) to a terrestrial system. It would be 18 years before a trophic dynamic study of a terrestrial community would be conduct- COMMUNITIES AND ECOSYSTEMS 363 ed. That classic paper would be provided by a mammalogist, Frank Golley (1960). Golley, who joined ASM in 1955 and would later publish an important text in mammalogy with David E. Davis (Davis and Golley, 1963) and field guides to the mammals of Georgia and South Carolina (Golley 1962, 1966), began a study of an old field terrestrial ecosystem whose vege- tation consisted largely of grasses and herbs. The main herbivore was a vole (Microtus pennsylvanicus) and the major predator was the least weasel (Mustela nivalis). As might be expected, Golley had to census plants, determine their energy content and the pro- portion of energy that the plants devoted to respiration, and estimate their productivity. Similar measurements (e.g., standing crop biomass and energy content, population dy- namics, growth, reproduction, assimilation efficiency, energy consumption) had to be made for Microtus and Mustela. Clearly, Golley’s study required a prodigious effort, yet it remains one of the few examples of energy flow through a simple terrestrial sys- tem (e.g., “Even the work of Golley ... is not very comprehensive,” Collier et al., 1973:420). This criticism notwithstanding, Golley’s work established the field of ter- restrial energetics in vertebrate populations (see also Golley, 1961, 1967, 1968, 1983; Golley and Golley, 1972; Golley et al., LOTS): Shortly after Golley published his paper, Odum et al. (1962) expanded the scope of research on energy flow in another old field ecosystem. They examined energy flow through more components of the food chain than Golley did, including grasshoppers, a cricket, a sparrow, and the old field mouse, Peromyscus polionotus. Their research al- lowed them to tease apart differences in en- ergy flow between vertebrates and inverte- brates, as well as between herbivores and granivores. Much research into the energetics of mammals was devoted to determining the energy costs associated with various daily activities for mammals. This was generally carried out in the laboratory on resting an- imals, or utilized physiological instrumen- tation to compare resting and active rates of metabolism. These investigations cen- tered on single species and the results often were compared to energetic assumptions and determinations made by Golley (e.g., Chew et al., 1965; Gessaman, 1973; Golley et al., 1965; Gorecki, 1965; Grodzinski and Go- recki, 1967; McNab, 1963, 1991; McNab and Morrison, 1963; Pearson, 1960). Terrestrial ecosystems were as difficult to study after Golley’s research had been pub- lished as they were before, but the publi- cation of his study on energy flow showed that, in principle, terrestrial systems, albeit extremely complex, were amenable to field research. Investigators thus began the dif- ficult task of examining energy flow through other systems. One of the first to publish on this topic was a mammalogist, Oliver Pear- son, who examined populations of several species of rodents and various carnivores (including feral house cats) in a large park in California (Pearson, 1964). Pearson cen- sused rodent populations to determine den- sity, then deduced the impact of carnivores on rodents by intensively collecting feces of predators. He also measured plant standing crop and estimated energetics of the organ- isms involved in energy flow through the system. This study was important because it dealt with a system which was more com- plex than that studied by Golley, although it was done over a much shorter time, ne- cessitating more assumptions than did Gol- ley’s work. Several studies dealing with one or an- other aspect of secondary productivity in ecosystems were published by Petrusewicz (1967), but it was another mammalogist who directed the research that would provide the next major energy flow study in a complex field situation. Robert Chew and his wife, Alice Eastlake Chew (Chew and Chew, 1965, 1970), conducted an extensive study on the energetics of a desert scrub community, in- cluding its mammals. Working in a creosote bush (Larrea tridentata) scrubland, the Chews determined bioenergetics of plants, including density, productivity, and stand- 364 MARES AND CAMERON ing crop, and gathered the same information on 13 species of small- and medium-sized mammals that occurred on the area. Their work remains one of the finest studies of energy flow in mammals ever conducted and provided important data to understand the pathways of energy flow through a desert system, ecological efficiencies of herbivores and granivores, and the net energy flow through various links in the food chain. Their research described the minor role played by small mammals (herbivores, granivores) in energy transfer in a com- munity, converting only 0.016% of the pri- mary above-ground production to mammal tissue that was then available as a food re- source to carnivores in higher trophic levels. This work provided dramatic quantitative data on the shape of the pyramids of energy and biomass. Following these early seminal studies, other investigators began to refine our un- derstanding of energy flow through mam- mal species and communities (e.g., Collier et al., 1975; Collins and Smith, 1976; Fle- harty and Choate, 1973; French et al., 1976; Gebczynska, 1970; Gebczynski et al., 1972; Grodzinski, 1971; Grodzinski and French, 1983; Kenagy, 1973; McNaughton, 1976; Merritt and Merritt, 1978; Montgomery and Sunquist, 1975; Myrcha, 1975; Soholt, 1973). These studies were conducted in temperate and tropical areas, and on both small and large mammals. The International Biological Program (IBP).—Undoubtedly, the major research stimulus to work on bioenergetics, and a continuing factor throughout the world on current interest in community dynamics, was the establishment of the IBP in the 1960s. Because of its importance to research on ecosystems, some background on IBP is provided. In 1962 Ledyard Stebbins, a plant genet- icist at the University of California, Davis, published a paper on the activities of the International Union of Biological Sciences, of which he was Secretary-General (Steb- bins, 1962; see Blair, 1977). In that report, he outlined the International Biological Program, a program of global ecological re- search. W. Frank Blair, who was then Pres- ident of the Ecological Society of America, and who had been one of the leading mam- malian ecologists in ASM before dedicating his research program to the evolutionary ecology of amphibians and reptiles (cf., Blair, 1939, 1941, 1953, 1955), became intimate- ly involved in the complex planning that ultimately resulted in the establishment of an internationally organized and funded program of comparative ecosystem research in 1967. The initial program had limited funding; broad-based financial support pro- vided by congressional action did not be- come available until Blair, in his role as Chairman of the US/IBP, led the fight to push funding bills through committees of both the House and Senate between 1967 and 1970. IBP was dedicated to elucidating the structure and function of the earth’s major ecosystems. The methodologies employed were those of population ecology, energet- ics, community structure, mathematical modeling, and elemental cycling, among others. At the heart of this multi-country research effort were the biome programs. These included programs focusing on the major terrestrial biomes (Tundra Biome, Grassland Biome, Desert Biome, Conifer- ous Forest Biome, Deciduous Forest Bi- ome, Tropical Forest Biome), as well as pro- grams dealing with the Conservation of Ecosystems, Man in the Andes, Circum- polar Peoples, Upwelling Areas, and Origin and Structure of Ecosystems, which exam- ined the role of convergent evolution in structuring communities of organisms in North and South America. IBP was big science in all of its glory, and with all of its problems (Blair, 1977). Be- cause it cut across disciplines and countries, IBP was an extremely difficult undertaking and was widely criticized by scientists who were not involved in the programs or who felt that this type of coordinated research was not the way to do science (Michell et COMMUNITIES AND ECOSYSTEMS 365 al., 1976). It was viewed negatively by some (e.g., Boffey, 1976), but time has provided a more balanced historical perspective. As McIntosh (1985:215) noted, “the status of ecology and ecologists at the inception of IBP was clearly ‘minor’, but IBP changed “the way ecology was done and the way ecologists thought about ecology” (McIn- tosh, 1985:219). IBP was a maturing force in the development of ecosystem ecology; it pushed this type of investigation into the forefront of organismal biology, giving it a high public profile and underscoring the im- portance of developing an understanding of how the natural environment functions. At- tempts to devise mathematical models of ecosystems were clearly less than successful (e.g., Berlinski, 1976), but ecosystem ecol- ogy has continued to develop, both concep- tually and methodologically (McIntosh, 1985). The effect of IBP on world ecology was pronounced (Kormondy and McCormick, 1981). In reviewing country after country, it is clear that field research flourished where IBP sites had been located. The program functioned as a training ground for students in the various fields of ecology, including mammalian community structure, energet- ics, population dynamics, and evolution. Literally thousands of papers on mammals have been published from work that was funded by, or related to, the IBP’s many foci. In Poland, for example, Kajak and Pieczynska (1981:287-—288) reported: ‘Four major periods can be distinguished in the development of Polish ecology after 1945: ... [f]rom 1969 to 1975 was a period of intense studies on ecological productivity and of ecosystem studies connected with. . . IBP ... [including especially s]tudies on smail mammals.” For Sweden, Sjors (1981: 305-306) noted, “The ... (IBP) meant in- creased contacts among ecologists all over the world. ... Thanks to the IBP [produc- tion and biomass studies] became highlight- ed in basic research.”’ In most countries where IBP research was conducted, mam- mal investigations were extensive. The results of the efforts of the IBP are still being witnessed today in mammalogi- cal research. There are ecosystem-oriented studies and research based in energetics that are currently providing important infor- mation on the ecology of populations and communities of mammals. Research stim- ulated by the projects or scientists who par- ticipated in IBP is still being conducted in a wide array of habitats throughout the world. Even as we approach two decades since the termination of IBP, there has probably been insufficient time to assess ob- jectively the impacts and contributions of the entire program on a global basis. How- ever, scientists involved with IBP not only conducted research on ecosystem function, community evolution, and ecosystem de- velopment, but were also instrumental in carrying on empirical research on the effects of abiotic factors on the structure of mam- malian communities. The Structure of Eco- systems Program was dedicated to this goal. IBP and ecosystem studies will be inti- mately associated in the future. Conclusions Mammalogists have contributed greatly to the development of community and eco- system ecology. Their influence has been pervasive and continuous, and extends from the very foundations of these fields of re- search. Present trends indicate that impor- tant empirical and theoretical contributions to elucidating patterns of community and ecosystem structure and function will con- tinue to be made by mammalogists. There is no doubt that members of the ASM have been, and will continue to be, at the fore- front of this research. Acknowledgments We thank O. J. Reichman and M. R. Willig for critical reviews of the manuscript. We also 366 MARES AND CAMERON thank J. K. Braun, R. B. Channell, and R. Hum- phrey for assistance in preparing the manuscript. Literature Cited ABRAMSKY, Z. 1989. Communities of gerbilline ro- dents in sand dunes of Israel. 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On the other hand, there has been a corresponding trend toward decreasing taxonomic spe- cialization as the practitioners of these dis- ciplines have chosen to study organisms on the basis of their suitability for testing eco- logical theory. This chapter attempts to describe how these trends have influenced the develop- ment of North American mammalogy, as well as how studies of mammals have con- tributed to the theory and data of modern ecology and evolutionary biology. When the ASM was founded in 1919, many of its charter members and earliest recruits in- cluded the leading natural historians of the early 20th Century (Merriam, Bailey, Jack- ag, son, Allen, Osgood, Nelson, Goldman). Over the 75-year history of the society, studies of mammals have continued to play key roles as classical natural history has evolved into modern evolutionary ecology. The history of changes in ecological and evolutionary studies of mammals reflect more fundamental changes in the devel- opment of modern science. As we shall see, many of the questions posed by early nat- ural historians have not yet been completely answered and are still the subject of major research programs today. This is not to say that there has been no progress. A great deal has been learned about how wild mammals survive, reproduce, and coexist in diverse habitats, and this knowledge frequently raises more questions than it answers. The questions have become more focused and the standards for acceptable answers have become more rigorous. New tools, such as mathematical models, field experiments, and statistical analyses, have been devel- oped to facilitate the interplay of theory and data. Broad syntheses have been attempted. In all of these developments, studies of mammals have played major roles. For convenience, this history can be di- 378 BROWN AND WILSON vided into several phases. The first, the dis- covery phase, began with the earliest studies of mammals in the Americas; the last, the evolutionary ecology phase, is a major theme of contemporary research. Discovery Phase Humans have always been curious about the plants and animals that share their world, and they have always had a special interest in their nearest relatives, other mammals. The earliest humans studied the ecology and behavior of mammals out of necessity, be- cause different mammal species were im- portant food sources, deadly predators, se- rious competitors, helpful mutualists, and objects of admiration and worship. As mod- ern human civilizations developed, they re- tained their fascination with the natural world and with the lives of their wild mam- malian relatives. Mammals figure promi- nently in the art and writing of ancient Ori- ental, Mediterranean, African, European, and American civilizations. As western civ- ilization emerged from the middle ages, Eu- ropean naturalists such as Linneaus, Cuvier, and Buffon began to describe, classify, and study the lives of their native mammals. These studies received added impetus when the voyages of discovery returned from around the world bearing specimens of amazing new kinds of mammals and other living things. North American mammalogy began in earnest when the newly arrived European colonists began to explore the continent and assess its natural resources. As with so many other human endeavors, the initial impetus for this exploration was economic. Beaver and other furbearers were among the ear- liest of North America’s vast natural re- sources to be exploited by Europeans. De- mand for beaver pelts drove fur trappers and mountain men into parts of the conti- nent that previously had been accessible only to indigenous tribes (Chittenden, 1954). The Hudson Bay Company and the Pacific Fur Company kept meticulous records of their annual trade in pelts that provided long- term records of population fluctuations and predator-prey dynamics. These data have been analyzed by several generations of ecologists, beginning with Elton (1942). Al- though the immediate influence of the fur trade on studies of natural history was lim- ited, one major contribution was a land- mark study of beaver by Lewis H. Morgan (1868), one of America’s first ethologists. The fur trappers did much to stimulate in- terest in wildlife and exploration when they returned to the outposts of civilization with tales of a vast continent inhabited by ani- mals unknown to Europeans. The early part of the 19th Century saw several exploring expeditions that contrib- uted importantly to our knowledge of mam- mals. When the newly independent United States had acquired the immense Louisiana Purchase from France in 1803, President Thomas Jefferson dispatched an expedition under command of Captains Merriweather Lewis and William Clark to survey and map the Missouri and Columbia rivers, to study the natural history and natural resources of the area, and to provide a detailed report of all Indian tribes and how to deal with them peacefully (Thwaites, 1904). Lewis and Clark’s journals provided the first descrip- tions of many North American mammals, and specimens were also brought back. Un- fortunately, the United States had no na- tional museum at the time, and all of the specimens ultimately were lost. Lewis and Clark’s collection was deposited in Peale’s Museum in Philadelphia; subsequently, most of it was purchased by P.T. Barnum and destroyed by fire in 1865 (Gunderson, 1976). Other notable early expeditions that obtained valuable information and speci- mens of mammals were those of J. J. Au- dubon and J. Bachman, and of T. Say. Mammalian natural history also benefit- ed from expeditions directed towards the discovery of a Northwest Passage that would provide access between the Atlantic and Pa- cific. Beginning in 1819, several expeditions EVOLUTIONARY ECOLOGY a7 to northern Canada were led by Sir John Franklin and Sir William Edward Parry. Sir John Richardson was surgeon-naturalist on the earlier Franklin expeditions and he also described birds and mammals collected on the Parry expeditions. Richardson’s (1829) Fauna Boreali-Americana contains a com- plete volume on mammals. All three of these early explorers have been honored with pat- ronyms proposed for ground squirrels: Spermophilus franklinii, S. parryi, and S. richardsonii. North American mammalogy, like other branches of natural history, is indebted to another set of explorations, begun in the 1850s to seek routes for a transcontinental railroad (Miller, 1929). After passage of the Railroad Surveys Bill in 1853, the Federal Government set out surveying parties that were accompanied by physician-naturalists from the U.S. Army Medical Corps. They made mammal collections of enormous breadth and value that were deposited in the newly founded (1846) Smithsonian In- stitution. These were first studied and de- scribed by Professor Spencer Fullerton Baird, whose Mammals of North America (1859, which appeared as Volume VIII of the Pacific Railway Survey Reports) pro- vided a state-of-the-art synopsis of the then 758 known species of North American mammals. Another physician-naturalist of the U.S. Army Medical Corps, Dr. Edgar Alexander Mearns, accompanied the survey of the U.S.-Mexican International Boundary. From his field work in 1892-1894, Mearns contributed over 30,000 specimens of plants and animals, including over 7,000 mam- mals, to the National Museum (Mearns, 1907). Earlier, Mearns had contributed to the specimens that established the verte- brate collections of the American Museum of Natural History in New York. Later, dur- ing two tours of duty in the Philippines, then accompanying President Theodore Roose- velt’s African expedition, and finally as a collaborator with Childs Frick on two ad- ditional African expeditions, Mearns con- tinued his field studies and collected many additional specimens. The discovery phase of American mam- malogy owes much to the physician-natu- ralists of the U.S. Army Medical Corps. In addition to Mearns and others associated with the Pacific Railroad and Mexican Boundary Surveys, a major contributor was Dr. Elliot Coues. Coues published his first scientific paper at 19 and received his M.D. 2 years later. In 1864 he joined the Army Medical Corps and spent the next 20 years doing field work, collecting specimens, and publishing extensively on mammals, birds, and other vertebrates. He served as the first curator of mammals after Baird had orga- nized the National Museum in 1879. He also served as secretary and naturalist to the Geological and Geographical Survey of the Territories under F. V. Hayden. Among other contributions, Coues wrote five monographs on rodents, which form Vol- ume 4 of the Hayden Survey Monographs (Coues, 1877a), and a classic revision of the family Mustelidae (Coues, 18775). Owing largely to the contributions of these explorer-physician-naturalists, most of the North American continent had been sur- veyed, and most, but by no means all, of the native mammals had been collected and classified, by the beginning of the 20th Cen- tury. Increasingly, naturalists were con- cerned, not with describing new species, but with understanding what determines the distribution and abundance of the species that they now knew about. They began to study the lives of wild mammals directly by observation and indirectly by trapping and tracking. The study of North American mammals had begun to pass from the dis- covery phase to a natural history phase. Natural History Phase When the ASM was founded in 1919, its charter members included some of the most prominent North American biologists. The majority of these, including Hartley H. T. 380 Jackson, C. Hart Merriam, Edward W. Nel- son, Wilfred H. Osgood, Marcus Ward Lyon, Jr., T. S. Palmer, Edward A. Preble, Glover M. Allen, Joseph Grinnell, Gerrit S. Miller, Jr., Angel Cabrera, A. H. Howell, Ned Hol- lister, Harold E. Anthony, Vernon Bailey, Edgar Alonzo Goldman, Laurance M. Huey, Remington Kellogg, Nagamichi Kuroda, Austin Roberts, Waldo L. Schmitt, Arthur deC. Sowerby, Witmer Stone, Oldfield Thomas, Alexander Wetmore, A. H. Winge, and Joel Asaph Allen (the first Honorary Member), were primarily taxonomists, still actively engaged in classifying species and documenting their distributions over the continent. Even though their systematic work represented the culmination ofthe dis- covery phase, their studies were becoming increasingly synthetic, analytical, and con- ceptual. It is no accident that these taxon- omists also made some of the most impor- tant contributions to natural history. Perhaps the most seminal of these early contributions that bridged the gap between taxonomy and natural history were those of C. Hart Merriam. Gerrit S. Miller, Jr., him- selfa talented taxonomist, argued that while the writings of Darwin had aroused initial interest in mammalian natural history, it was Merriam who developed the techniques for the systematic study of mammals (Mil- ler, 1929). Merriam, yet another medical doctor influenced by Baird, had an early interest in ornithology and an impressive combination of intellect, energy, and fore- sight that enabled him to establish in 1885 an organization that began as the Section of Ornithology in the Division of Entomology under the Commissioner of Agriculture. Within a year the Division of Ornithology had attained independence, and by 1888 it had expanded to the Division of Economic Ornithology and Mammalogy. Merriam’s later predilection for mammals was illus- trated by his staff's reference to the “Divi- sion of Economic Ornithology and Extray- agant Mammalogy” (Osgood, 1943). This unit, which became the Bureau of Biological BROWN AND WILSON Survey in 1905, and the cadre of distin- guished field and museum personnel assem- bled by Merriam between 1885 and 1910, were the major reasons for the rapid ad- vance in our knowledge of North American mammals early in this century. Merriam’s efforts were facilitated by the otherwise unremarkable decision by a man- ufacturing company to turn its attention from making clothes wringers to producing and marketing a truly better mousetrap, the “Cyclone” trap, which made its appearance in the 1880s. Merriam knew from his stud- ies of birds that a key to advancing the sys- tematics of mammals was to accumulate and study large series of uniformly prepared specimens from throughout the range. The new cyclone trap made this possible for small mammals (Miller, 1929). Merriam’s monumental contributions to mammalogy were made possible by a com- bination of personal science, inspired lead- ership, and ability to recruit outstanding sci- entists (Osgood, 1943). Merriam personally described 660 new species of mammals and published more than 600 papers (Grinnell, 1943). Perhaps his most important paper was the one that used the observed eleva- tional and latitudinal zonation of flora and fauna to develop the life zone concept (Mer- riam, 1890). In addition, Merriam empha- sized the use of cranial characters in clas- sification, and he perfected field and museum methods that are still in use today. He initiated a new publication series, North American Fauna, and wrote the first 11 vol- umes himself. From its first volume in 1889 to its 75th and most recent one (Timm et al., 1989), this series has been extremely influential; several volumes represent mile- stones in the transition from the discovery to the natural history phase of North Amer- ican mammalogy. Under Merriam’s lead- ership the Biological Survey became the pri- mary center of mammalogical research. Much of this was owing to his genius for picking exceptional colleagues. The group assembled at the Biological EVOLUTIONARY ECOLOGY 381 Survey comprised an extraordinary group of field and museum biologists. Beginning about 1883, Merriam had communicated with a Minnesota farm boy named Vernon Bailey, who had supplied him with difficult to obtain specimens, such as shrews. Soon after accepting the position in Washington, Merriam hired Bailey, thus beginning a close and productive friendship between two gi- ants of American mammalogy. Bailey and his wife, Florence, who was Merriam’s sis- ter, crisscrossed the continent collecting mammals and birds and described their studies in a series of volumes on the fauna of various states and geographic regions. Two other remarkable members of the Biological Survey were Edward W. Nelson and Edward Alphonso Goldman. Beginning in 1892, Nelson, who later became Chief of the Survey, undertook a 14-year biological survey of Mexico. He hired Goldman, then an 18-year-old California youth, to accom- pany him. The results of their collaborative study are undoubtedly the most important ever achieved by two individuals for a single country. They obtained 12,400 specimens of birds and 17,400 specimens (including 354 new species and subspecies) of mam- mals. In addition, they collected reptiles, amphibians, and plants, and their field re- ports contained a wealth of information on the vegetation and climate of Mexico (Gold- man, 1951). If Merriam’s life zone concept was the first important ecological principle that sig- naled the shift from the discovery phase to the natural history phase, Joseph Grinnell’s (1917a, 19175) niche concept was the sec- ond. Grinnell’s concept, which emphasized the role of environmental conditions in lim- iting the distribution of a species, was later redefined and formalized by Hutchinson (1957). Although Grinnell used a bird spe- cies, the California thrasher, to illustrate his idea of the niche, he made enormous con- tributions to both mammalogy and orni- thology. Grinnell not only published 554 papers between 1893 and 1939, he also started a mammalogical dynasty by training an exceptional cadre of students at the Uni- versity of California at Berkeley (Jones, 1991; Whitaker, 1994). Although the majority of the classic de- scriptive studies that marked the transition from the discovery phase to the natural his- tory phase were done on rodents, many were performed on other groups that have more unusual or conspicuous lifestyles, such as bats, ungulates, carnivores, and marine mammals. Pioneering studies on bats in- cluded Glover Merrill Allen’s (1939) classic treatise and two important papers by A. B. Howell (1920a, 19205) in the first volume of the Journal of Mammalogy. A subse- quent volume by Griffin (1958) emphasized behavioral and physiological studies of echolocation, but also summarized much of the information on natural history. These early studies were limited to insights that could be obtained from studies at roosts, direct observations of flying bats, and lab- oratory experiments, until the use of Japa- nese mist nets around the middle of the cen- tury. Carnivores and ungulates were the sub- jects of important early studies, especially those of E. T. Seton (e.g., 1909, 1923), which included a multivolume work on the lives of game animals (1929). More recent classic studies were Murie’s (1944) and Young and Goldman’s (1944) on wolves, Hall’s (1951; which included taxonomy as well as natural history) on weasels, Taylor’s (1956) on deer, and Altmann’s (1952) on elk. Important early studies of marine mammals included papers by Evermann (1921) and Kellogg (1921), both in the second volume of the Journal of Mammalogy. The more recent tradition of natural history studies is illus- trated by Bartholomew and Peterson’s (1967; the first Special Publication of the American Society of Mammalogists) mono- graph on the California sea lion and Le Boeuf and colleagues’ studies of the northern el- ephant seal (e.g., Le Boeuf and Reiter, 1988). Natural history studies gathered momen- 382 BROWN AND WILSON tum in the 1920s and 1930s, and they con- tinued to dominate ecological mammalogy until the 1960s. Some of these, such as those by Grinnell and his students on different areas in California (Grinnell and Storer, 1924: Grinnell et al., 1930, 1937), focused on particular geographic regions. Others were restricted to single species or a few related species. Natural history investiga- tions reached their epitome in monographic studies of various kinds of rodents. These included major works on woodrats (Finley, 1958; Linsdale and Tevis, 1951; Vorhies and Taylor, 1940), ground squirrels (Lins- dale, 1946), deer mice (McCabe and Blan- chard, 1950), microtines (Elton, 1942; Er- rington, 1963), and heteromyid rodents (Eisenberg, 1963; Reynolds, 1958, 1960). In contrast to these large, integrated studies of particular species or genera, the contribu- tions of two of the most influential mam- malian natural historians, W. J. Hamilton, Jr., and W. H. Burt, consisted primarily of a combination of books on all mammals and shorter papers on particular kinds (e.g., Burt, 1940, 1946; Hamilton, 1939; Layne and Whitaker, 1992; Muul, 1990). The natural history phase of research in mammalogy also saw the beginnings of the conservation movement. W. T. Hornaday (1899) detailed the life history and near ex- tinction of the North American bison, and Volume 2 of the Journal of Mammalogy contained a paper on the status of the Eu- ropean bison (Ahrens, 1921). The works of Seton (1909, 1923, 1929) are filled with ac- counts of the relentless killing, declining abundances, and contracting ranges of car- nivores and ungulates. The Biological Sur- vey monitored the status of furbearers and the fur trade (Ashbrook, 1922). Lang (1923) called attention to the plight of the white rhinoceros in Volume 4 of the Journal of Mammalogy. Aldo Leopold (e.g., 1933) emerged as an eloquent advocate for con- servation and developed wildlife manage- ment as an applied science based on the principles of natural history and ecology. E. P. Walker worked diligently to stimulate in- terest in mammalian conservation during his years at the National Zoological Park, and culminated his career with his opus on mammals of the world (Walker, 1964). Natural history is still a significant com- ponent of contemporary American mam- malogy. This is apparent from the success of the ASM’s Mammalian Species series of publications and from the large number of ““descriptive”’ papers appearing in the Jour- nal of Mammalogy and other journals. Mammalogy and the New Synthesis By the 1930s the study of ecology and evolution was already beginning to enter a new phase. The new synthesis was laying a theoretical and genetical foundation for the study of evolution. Fisher, Wright, and Hal- dane introduced mathematical models to characterize the genetic mechanisms of evo- lutionary change, as well as experimental and statistical techniques to test rigorously the predictions of these models. Simpson, Dobzhansky, and Mayr developed a broad view of evolution that incorporated not only genetic mechanisms, but also systematics, biogeography, paleontology, and ecology. In North American mammalogy, the in- fluence of the new synthesis is seen most clearly in two research programs. One 1s the work on the genetics of Peromyscus by F. B. Sumner and L. R. Dice. These studies rivaled those of Drosophila, if not for their elucidation of genetic mechanisms per se, then for their insights into the adaptive con- text of genetic variation. Sumner (e.g., 1932) showed that coat color and other traits of Peromyscus were heritable, and Dice and his students at Michigan, P. M. Blossom, W. F. Blair, and B. E. Horner, went on to explain geographic variation in coat color and morphology in terms of natural selec- tion by predators in environments that dif- fer in background coloration and vegetation structure (e.g., Dice, 1947; Dice and Blos- som, 1937; see also Benson, 1933). This research program is notable for its use of EVOLUTIONARY ECOLOGY 383 Peromyscus as an empirical “model sys- tem” for addressing general conceptual questions, for its combination of controlled experiments in the laboratory to test mech- anisms and comparative field observations to place the experimental results in a real- istic natural context, and for its use of rig- orous experimental designs and statistical analyses. The other major contribution of North American mammalogy to the new synthesis was G. G. Simpson’s interpretation of the historical record of evolution, based on his studies of fossil and Recent mammals. Simpson (1940, 1943, 1944, 1947a, 19475, 1950, 1953) focused on the evolution of the North and South American faunas, and on the effects of the interchange of species across the Interamerican and Bering land bridges. He also brought new quantitative approach- es to paleontology and comparative biology by developing mathematical techniques for assessing similarity among faunas, quanti- fying diversity, and measuring rates of evo- lutionary change. Simpson can be credited with primary responsibility for giving the new synthesis an historical and biogeo- graphic dimension. With a few conspicuous exceptions, such as Dice and Simpson, descriptive natural history studies predominated in North American mammalogy until after World War II. Evolutionary Ecology Phase In the late 1950s and 1960s, a major em- phasis on science in the U.S. and Canada was stimulated by military and scientific competition with the U.S.S.R. This period saw the emergence of modern evolutionary ecology. The seminal event was the Cold Spring Harbor Symposium in Quantitative Biology in 1957. This symposium is note- worthy for three things. First, it had several papers on the dynamics of small mammal populations (Chitty, 1957; Pitelka, 1957). These signaled a shift to North America of the research on the dramatic fluctuations in rodent populations that had been pioneered in Europe by Elton (1927, 1942). Second, the mix of genetics, ecology, and evolution indicated an effort to expand the new syn- thesis to include ecology. Here and in the symposium on the genetics of colonizing species held in Syracuse in the mid-1960s (Lewontin, 1968), the foundations of evo- lutionary ecology were laid. Finally, Hutch- inson (1957) in his “concluding remarks,” capped the symposium by presenting his theory of the multidimensional niche. This was by no means the first use of mathe- matical models in ecology, but it took the- oretical ecology beyond the problems of population growth and regulation that had preoccupied ecologists prior to that time. It provided a new conceptual framework to address questions about limiting factors, in- terspecific interactions, species diversity, and adaptation. Population dynamics. -Mammalian ecologists were well represented at the Cold Spring Harbor Symposium. Attendees in- cluded Frank Pitelka, Dennis Chitty, Paul Errington, John B. Calhoun, John J. Chris- tian, and David E. Davis. Charles Elton, perhaps the most eminent of all British ecol- ogists, had attracted much interest to the population fluctuations of microtines. Elton had begun field work in the Scandinavian arctic in the 1920s, and had summarized much of this work in his Voles, Mice and Lemmings (1942). Errington (1946, 1963) had been working in Iowa since the 1930s on the role of predation, disease, and other factors in limiting muskrat populations. In- fluential papers in the Cold Spring Harbor Symposium by Pitelka (1957) on lemming cycles at Point Barrow, Alaska, and by Chit- ty (1957) on the genetics and behavioral components of microtine population regu- lation signaled the seminal roles that these two newcomers would play in North Amer- ican mammalian ecology. The challenge that microtines pose to ecologists is to explain the dramatic mul- tiannual fluctuations in populations. 384 BROWN AND WILSON Whether microtine populations “‘cycle”’ and what causes the fluctuations are the two questions that have preoccupied microtine ecologists since Elton (1942) and Errington (1946, 1963). The chapter by Lidicker (1994) documents the history and accomplish- ments of the enormous research program that developed in both North America and Europe to address these questions (see also Gaines et al., in press; Henttonen et al., 1984; Krebs and Myers, 1974; Krohne, 1982; Lid- icker, 1988, in press; Taitt and Krebs, 1985; Tamarin, 1985). Although much attention has been de- voted to microtines, important investiga- tions of population dynamics have been performed on other mammals. Many stud- ies have focused on other rodents, because of their small size, ease of trapping, and occurrence in a wide variety of habitats (e.g., Adler and Tamarin, 1984; Brown and Heske, 1990; Brown and Zeng, 1989; Pet- ticrew and Sadler, 1974; Stickel and War- bach, 1960; Whitford, 1976). These have often implicated temporal variation in cli- mate and food supply as the primary cause of population fluctuations. Yet another per- spective is offered by large mammals, whose population dynamics often appear to be controlled by complex relationships be- tween food supply and susceptibility to pre- dation (e.g., Fowler and Smith, 1981; McCullough, 1979). Thus, mammals con- tinue to offer a wealth of different patterns of population fluctuations, of different mechanisms of population regulation, and of different kinds of populations for study. Species diversity and community struc- ture.—After formulating the multidimen- sional ecological niche in his ““Concluding remarks” at the Cold Spring Harbor Sym- posium, Hutchinson (1959) gave a presi- dental address to the American Society of Naturalists entitled ““Homage to Santa Ro- salia, or Why are there so many kinds of animals?” By explicitly focusing on patterns of species diversity, resource utilization, and coexistence, and on processes of population regulation, interspecific interaction, and ad- aptation, these two papers laid much of the foundation for modern community ecology. Although David Lack had addressed some of these problems in his Darwin’s Finches in 1947, they were not pursued vigorously until the late 1950s. Other important con- tributions at this time included Brown and Wilson’s (1956) treatise on character dis- placement and MacArthur’s (1958, 1960, 1965, 1970, 1972) empirical and theoretical studies. Data from mammals figured prominently in these studies in community ecology. Hutchinson (1959) used weasels as exam- ples of the regular ratios in the body sizes or trophic appendages that can be observed among coexisting species and that were hy- pothesized to reflect the influence of inter- specific competition on community struc- ture. Hutchinson and MacArthur (1959) used the frequency distribution of body sizes among all species of North American mam- mals to develop models of niche relation- ships and coexistence. Others were quick to exploit the advan- tages of mammals for studies in evolution- ary ecology. In 1959, Hall and Kelson pub- lished a major taxonomic treatise, The Mammals of North America, which con- tained, among other information, detailed range maps of every species. Simpson (1964) used this data base to quantify patterns of species diversity across the continent. Thus began a long tradition of using these range maps to address Hutchinson’s question about the ecological processes causing geo- graphic variation in species diversity (Brown, 1981; Hagmeir and Stults, 1964; MacArthur, 1972; Owen, 1990; Rapoport, 1982; Wilson, 1974; see also Fleming, 1973). Unfortunately, despite a great deal of re- search, the question remains largely unan- swered. The major geographic gradients in species richness, including the dramatic in- crease in diversity from poles to equator, have been increasingly well documented in mammals and other organisms, but inves- tigators have had only limited success in evaluating the contributions of several, and EVOLUTIONARY ECOLOGY 385 not necessarily exclusive, mechanisms that may have caused these patterns (e.g., Brown, 1988; MacArthur, 1972). One ecological legacy of Dice’s genetic research on Peromyscus was two elegant ex- perimental studies of habitat selection. Har- ris (1952) showed that forest and grassland races of P. maniculatus preferred artificial habitats of different structure in the labo- ratory. Wecker (1963, 1964) took this ap- proach to the field, where he showed not only that young mice exhibited a strong preference for appropriate habitat, but also that there were both inherited and learned components of this behavior. Rosenzweig, Dueser, M’Closkey, Price, and Morris (see references below) continued to investigate habitat selection, using it as a vehicle to understand population dynamics and com- munity structure. MacArthur’s student, Rosenzweig, hav- ing analyzed geographic variation in body size in North American mammals for his doctoral dissertation (Rosenzweig, 1966, 1968), began to study habitat selection, re- source utilization, and coexistence in desert rodents. Rosenzweig’s studies (e.g., Rosenz- weig, 1973; Rosenzweig and Sterner, 1970; Rosenzweig and Winakur, 1969; Rosenz- weig et al., 1975; Schroder and Rosenzweig, 1975) were the first of many (see Brown and Harney, 1993) that used the desert rodent system to address fundamental questions in community ecology. From these and other studies we have learned that species diver- sity and composition vary on geographic scales with precipitation and productivity (Brown, 1973, 1975), and on local to re- gional scales with soil and vegetation type (M’Closkey, 1976, 1978; Rosenzweig and Winakur, 1969; Rosenzweig et al., 1975). Coexisting species tend to be more different in body size, body shape, and other attri- butes than expected by random community assembly (Bowers and Brown, 1982; Brown, 1973; Dayan and Simberloff, in press; Fin- dley, 1989; Hopf and Brown, 1986), and they tend to use different microhabitats (Brown and Liebermen, 1973; Lemen and Rosenzweig, 1978; M’Closkey, 1981; Price, 1978; Rosenzweig, 1973; Rosenzweig and Winakur, 1969). These observations sug- gest that interspecific competition plays a major role in the organization of these com- munities. Field experiments in which some species increased in abundance or shifted their microhabitat use in response to re- moval of other species have provided ad- ditional direct evidence for interspecific competition (Bowers et al., 1987; Brown and Munger, 1985; Freeman and Lemen, 1983; Munger and Brown, 1981; Price, 1978; see also Larsen, 1986). Clever experiments that have altered the risk of predation have shown that it influences foraging behavior and microhabitat use and probably interacts with competition to affect community structure (Brown etal., 1987; Kotler, 1984a, 1984b, 1985: Thompson, 1982a, 1982b). Although studies of desert rodents rival those of Darwin’s finches and Anolis lizards for their contributions to community ecol- ogy, many questions remain unanswered and several research programs are pursuing them. Populations appear to be limited largely by food supplies and to fluctuate with climatic conditions that determine the availability of seeds, insects, and foliage (e.g., Beatley, 1976), but the coupling between the abiotic environment and population dy- namics varies among species and 1s poorly understood (Brown and Heske, 1990). There has been widespread agreement that differ- ences in microhabitat use promote coexis- tence, but the extent and significance of food resource partitioning has been much more controversial (Brown, 1975; Brown and Lieberman, 1973; Dayan and Simberloff, in press; Lemen, 1978; Mares and Williams, 1977; Rosenzweig and Sterner, 1970; Smi- gel and Rosenzweig, 1974). Although the importance of predation and interspecific competition no longer seems to be in doubt, the way that these processes separately and jointly affect population dynamics and community structure requires further study. Finally, the importance of character dis- placement and other kinds of coevolution- 386 ary responses to biotic interactions is re- ceiving considerable study, but remains largely unresolved. By no means were all of the important community-level studies were of desert ro- dents. Miller (1967), Dueser and Shugart (1978), Dueser and Hallett (1980), Morris (1984), Kirkland (1985), and others inves- tigated habitat selection and interspecific in- teractions of rodents and shrews in forest and grassland habitats. Competitive inter- actions among chipmunk species were stud- ied in coniferous forest habitats in several places in western North America (Brown, 1971; Chappell, 1978; Heller, 1971; Shep- pard, 1971). Findley (1973, 1976, 1993) used bats for pioneering studies of ecomorphol- ogy, the relationships between patterns of morphological variation among species and the composition of ecological communities. Moors (1984), Ralls and Harvey (1985), and Dayan et al. (1989) performed more de- tailed morphological and field studies to re- examine Hutchinson’s and Rosenzweig’s inferences about sexual dimorphism, re- source partitioning, and character displace- ment in mustelids. Fleming (1971, 1973, 1988; Fleming et al., 1972) and Wilson (1971, 1973; Wilson and Findley, 1970) pi- oneered studies of tropical communities of both terrestrial mammals and bats, and these were followed by others (August, 1983; Hei- thaus et al., 1975; Sanchez-Cordero and Fleming, 1993). Life history studies. —In terms of their use of direct observations in the field to learn about important events in the lives of in- dividual free-living mammals, the most di- rect descendants of the classical natural his- tory studies of the early 1900s were the life history studies of the latter half of the cen- tury. Because of their high densities and di- urnal habits, colonial sciurid rodents were frequently chosen for longitudinal studies of life histories. J. A. King’s (1955) work on black-tailed prairie dogs (Cynomys ludovi- cianus) was probably the most influential, if not the first, of the detailed field studies BROWN AND WILSON of a single population of marked individ- uals. This was followed by Armitage’s (1962) work on marmots, and then by many other studies using different species of ground squirrels (reviewed in Murie and Michener, 1984). These studies have been much more than descriptive natural history; they have been instrumental in gathering data to build and test theories of social behavior and life his- tory tactics. Together with studies of the wolf by Mech (1966, 1970), of Scottish red deer (Cervus elaphus) by Clutton-Brock et al. (1982), of African carnivores (e.g., Kruuk, 1972; Packer, 1986; Packer et al., 1988), and of primates (e.g., Altmann and Alt- mann, 1970; Cheney et al., 1988), the body of work on North American sciurids has been instrumental in the development of our ideas about the roles of environmental conditions and social interactions in deter- mination of individual reproductive success and in evolution of social systems. Perhaps the two most extreme and _ spectacular mammalian life histories—and ones that have far-reaching theoretical implica- tions—are the eusocial systems of naked mole rats and the semelparous life histories of some dasyurid marsupials. Mole-rats (Heterocephalus glaber) resemble social bees and ants, living in large colonies in which a single dominant female effectively cas- trates and enslaves her relatives (Jarvis, 1981). Marsupial mice (Genus Antechinus) resemble salmon and certain plants in that the males of several species are semelpa- rous; they put all of their resources into a single reproductive effort and then die after just one breeding season (Lee and Cock- burn, 1985). Another approach to studying the evo- lution of life histories and social systems that was pioneered by North American mammalogists involved allometric rela- tionships—patterns of variation with re- spect to body size. In 1963, McNab pub- lished an influential paper on the correlation between home range size and body size (see EVOLUTIONARY ECOLOGY 307 also Schoener, 1968). This was followed by several studies of the allometry of life his- tory traits, such as litter size, gestation length, and maternal investment in offspring (e.g., Calder, 1984; Clutton-Brock and Harvey, 1983; Eisenberg, 1981; Eisenberg and Wil- son, 1979; Peters, 1983). These studies have not only demonstrated correlates of body size that are expressed in allometric rela- tionships across large samples of mammal species, they have also pointed out devia- tions from these relationships that can be attributed to evolutionary constraints or to adaptations to special ecological condi- tions, or both. For other evolutionary and ecological approaches to the study of mam- malian life histories see Millar (1977) and Millar and Zammuto (1983). Coevolution. —Several early naturalists noted that mammals play potentially im- portant roles as dispersers, as well as con- sumers, of seeds. Smith (1970) put these kinds of interactions in a modern perspec- tive with a classic study of coevolution be- tween red squirrels (Tamiasciurus hudsoni- us and T. douglasii) and conifers. He showed that the two squirrel species have different morphological and behavioral traits that re- flect adaptations to the different kinds of conifers that predominate in their geograph- ic ranges, and the trees also exhibit adap- tations to promote dispersal and to limit consumption by the squirrels. Small forest- dwelling mammals, such as deer mice and voles, have been shown to play a major role in dispering the mutualistic mycorrhizal fungi that are obligately associated with the roots of many tree species (e.g., Maser et al., 1978). Howell (1979) found that a bat, Leptonycteris sanbornii, 1s the principal pol- linator of several century plant and cactus species in the Sonoran and Chihuahuan des- erts. Subsequently, much of the attention turned to the tropics, where both rodents and bats were shown to be important dis- persers of seeds of fleshy-fruited trees (e.g., Fleming, 1988; Janzen, 1983; Smythe, 1970). These studies have for the most part supported Janzen’s (1970) suggestion that animals, especially frugivorous and graniv- orous mammals and birds, play a major role in the structure and dynamics of tropical forests. Rodents and bats are particularly important in carrying seeds away from the parent tree, where they are subject to heavy predation from insect consumers and mi- crobial pathogens, to distant sites that may be more favorable for survival and germi- nation. Janzen’s (1981) discovery that in- troduced horses are important agents of seed dispersal for some tropical tree species led to the suggestion that the extinction of the Pleistocene megafauna and the extirpation of modern species of large mammals, such as tapirs and peccaries, may be causing sub- stantial changes in tropical forests (Janzen and Martin, 1982). Recently, evolutionary ecologists have speculated about coevolutionary relation- ships between parasitic or symbiotic organ- isms and their hosts (e.g., Holmes and Price, 1986; Price, 1980). Studies of mammals have supported suggestions that “parasites” may not always have significant negative effects on their hosts; in fact, some apparent parasites might even benefit their hosts (Munger and Holmes, 1988). Other fasci- nating symbiotic relationships have been discovered. Several tropical mammals have symbiotic insects that live in their fur, their nests, or both, and prey on lice, fleas, and other ectoparasites (e.g., Ashe and Timm, 1987: Timm and Ashe, 1988). In desert and arid grassland habitats bannertailed kan- garoo rats (Dipodomys spectabilis) and woodrats (Neotoma sp.) construct large dens that provide refuges for many kinds of in- vertebrates and small vertebrates (Monson and Kessler, 1940). In addition, the seed stores of the bannertailed kangaroo rats are inhabited by many kinds of fungi that have been suggested to have beneficial effects on their rodent hosts by enhancing the nutri- tional value of infested seeds (e.g., Hawkins, 1992; Reichman et al., 1985). 388 BROWN AND WILSON The Transition from Natural History to Evolutionary Ecology The transition. —The period of active re- search in mammalogy in North America, from about 1850 to the present, marked the transition from studies that emphasized de- scriptive taxonomy, morphology, distribu- tion, paleontology, and natural history to investigations that were motivated by the theoretical questions of modern disciplines such as biomechanics, physiology, behav- ior, genetics, evolution, systematics, ecol- ogy, and biogeography. The 19th-Century naturalists were generalists. The greatest of them, such as Cuvier, Darwin, Wallace, Bates, von Humboldt, and Prinz Maximil- ian zu Wied, were knowledgeable about plants, invertebrates, and vertebrates, stud- ied geology and paleontology as well as bi- ology, and developed concepts and theories to explain their empirical observations. Even the early 20th-Century mammalogists were amazingly diverse scientists. For example, Merriam published in geography and an- thropology as well as mammalogy (Grin- nell, 1943; Osgood, 1943), and Grinnell wrote influential papers on the behavior, ecology, biogeography, and systematics of both birds and mammals (Miller, 1943). The natural historians of the first half of the 20th Century represented a transition from the 19th-Century naturalists to mod- ern evolutionary ecologists. These natural historians, best represented by individuals such as Linsdale, Murie, Vorhies, and Ham- ilton, made detailed, descriptive studies of particular species that emphasized behav- ior, reproductive biology, and distribution with respect to habitat. Today their work may seem quaint, descriptive, and lacking theoretical motivation. It is important how- ever, to recognize the extent to which the natural historians laid the foundations for the more conceptual approach of contem- porary mammalogy. Taxonomic mammal- ogists were still describing new species and mapping their geographic ranges well into the present century. It was necessary to doc- ument the basic biology of these mammals before it was apparent which ones were well suited for addressing ecological and evolu- tionary questions of theoretical interest. The dependence of modern evolutionary ecologists on the work of their more de- scriptive antecedents is illustrated by two observations. First, many of the evolution- ary ecologists were trained either by natural historians or by taxonomists. Note, for ex- ample, the academic histories of Findley, Krebs, Lidicker, Eisenberg, Wilson, Brown, Fleming, and other mammalian evolution- ary ecologists (Jones, 1991; Whitaker, 1994). Second, the influence of the natural histo- rians is illustrated by the frequency with which the studies of Linsdale, Grinnell, Hall, Vorhies and Taylor, Findley, and others are cited in recent publications. The descriptive observations of the natural historians often provide the inspiration for the modern ex- perimental studies of evolutionary ecolo- gists. The role of theory.—The transition from natural history to evolutionary ecology can be attributed largely to the influence of mathematical theory and the seminal con- tributions of Hutchinson, MacArthur, and others. The foundations of the new synthe- sis were laid by the mathematical models of genetic evolutionary change of Fisher, Wright, and Haldane. Although this work was largely completed before World War II, the consolidation of the new synthesis did not come until the major works of Dobz- hansky (1937), Simpson (1944, 1953) and Mayr (1942, 1963). These major advances in understanding the evolutionary process demonstrated the power of mathematical models to motivate important experimental and synthetic empirical studies. The incorporation ofan evolutionary per- spective into studies of ecology and life his- tory can be attributed largely to the influ- ence of Hutchinson and his student, MacArthur. As mentioned above, Hutch- inson (1957, 1959) set much of the agenda EVOLUTIONARY ECOLOGY 389 for the next several decades with his papers on the niche and the diversity of species. MacArthur (e.g., 1960, 1970, 1972) fol- lowed with mathematical treatments of spe- cies abundance and diversity, competition and resource utilization, coexistence and coevolution, life history theory, optimal foraging, and island biogeography. There was hardly a topic in modern evolutionary ecology that MacArthur did not address. He was almost certainly the most influential ecologist who ever lived, an assessment that is borne out by the total number of times his papers have been cited (see Science Ci- tation Index). The specific mathematical models devel- oped by Hutchinson, MacArthur, and oth- ers have had mixed success. Some, such as the broken stick distribution of niches and the idea that complexity promotes stability, were misguided or just plain wrong, and have been abandoned. Others, such as r and K reproductive strategies and the limiting similarity of species were too simplistic; they represented important advances, but were eventually replaced by more complex and realistic theory. Still others, such as re- source-based competition equations and the theory of island biogeography are still wide- ly used to motivate both theoretical and em- pirical studies. Despite the mixed success of these models, their influence on the devel- opment of modern evolutionary ecology is enormous. Almost every influential empir- ical paper since 1960 cites theoretical lit- erature and attempts to evaluate predictions of mathematical theory. Even more important than its success in explaining evolutionary and ecological phe- nomena, however, was the way that math- ematical theory revolutionized the science. It led to more conceptual, question-asking, quantitative, analytical, experimental, and statistical approaches to both theoretical and empirical studies. To produce mathemati- cal theory requires conceptual innovation, quantitative skills, and analytical rigor. To test empirically the predictions of theory requires understanding the theory, choice of an appropriate system for study, design and execution of appropriate experiments or comparative observations, and rigorous sta- tistical analysis and inference. Mammalian systems for testing theory. — The appearance of compelling mathemati- cal models called for empirical tests of their assumptions and predictions in appropriate natural systems. Beginning with Hutchin- son and MacArthur’s (1959) paper on the distribution of body sizes among species, North American mammals have played a major role in the interaction between theory and data. Some of this was largely seren- dipitous. Thanks to the efforts of the natural historians, mammals had already been rel- atively well studied and young scientists trained in more descriptive mammalogy soon became interested in testing the excit- ing new theories. Furthermore, certain kinds of mammals possess combinations of characteristics that have made them excellent systems for quan- titative and experimental field studies. The influential roles of sciurid rodents, pri- mates, and ungulates in life history studies, of microtine rodents in studies of popula- tion dynamics, and of desert rodents in in- vestigations of coexistence and interactions of species are no accident. Each of these groups has specific traits that facilitate ob- servation, quantification, and experimental manipulation to obtain definitive tests of hypotheses and theoretical predictions. No organism is ideal for all kinds of studies, and some groups of birds, lizards, insects, plants, and intertidal organisms, have rivaled mammals as empirical systems for studies in evolutionary ecology. Neverthe- less, mammals have played and will con- tinue to play an influential role in the de- velopment of evolutionary ecology (see citations in the previous section). Increasing scientific rigor. —-As men- tioned above, the development of mathe- matical theory had a profound effect on the way that empirical studies of mammals were conducted. The emphasis shifted from qual- itative description motivated by economic 390 BROWN AND WILSON concerns or investigator fancy, to statisti- cally rigorous, experimental hypothesis- testing motivated by theoretical issues. Once empirical studies shifted from de- scribing the natural history of mammal spe- cies to evaluating the assumptions and pre- dictions of particular theories they then needed to provide more definitive answers. This required formulating and testing hy- potheses. Usually the goals of natural his- tory studies were essentially similar to Lins- dale’s (1946:vii): ““The need for an extensive study of the life of the California Ground Squirrel has grown with increasing rapidity as more and more questions have been raised about this animal, its habitat, distribution, and characteristics.”” There is no way to frame this objective in the form of a single hypothesis, or to satisfy this need except by doing the kind of broad, descriptive study that Linsdale did. This changed when the goal became to learn whether habitat het- erogeneity affects the dynamics of a micro- tine population or whether two desert ro- dent species are competing. Each of these questions can be cast as a specific hypoth- esis, and answered definitively with a single set of observations or experimental manip- ulations. Another impact of theory, then, was that it led to an increased emphasis on the design and execution of controlled experiments to give definitive tests of hypotheses. Connell (1961) brought to modern evolutionary ecology the approach, long practiced by British plant ecologists, of doing replicated manipulative experiments in the field. It did not take long for field experiments to be applied to mammalian ecology, first and most notable in manipulations of microtine populations by Krebs and colleagues (Krebs et al., 1969) and in Rosenzweig’s (1973) “habitat tailoring’ experiments on desert rodents. Now a large proportion of field studies in mammalian ecology are well-de- signed experiments, with appropriate con- trols, adequate replication, and standard- ized data collection. Of course, a number of conceptually or practically important ques- tions simply cannot be answered by manip- ulative experiments. It is either impractical to experiment on the spatial or temporal scale required to test the hypothesis (e.g., to address biogeographic questions), or it is illegal or unethical to perturb the natural system (e.g., in the case of endangered spe- cies). This does not diminish the need to adopt a rigorous, hypothesis-testing ap- proach, but it requires that carefully de- signed comparative observations be substi- tuted for artificial manipulations (e.g., Brooks and McLennan, 1991; Harvey and Pagel, 1991). Finally, the emphasis on evaluating the- ory, testing hypotheses, and doing experi- ments has led to the development of an in- creasingly powerful battery of statistical techniques. In fact, many of the analyses were developed by theoreticians, including Fisher and Wright, for testing empirically the predictions of their models. Statistical analyses are virtually absent from most of the natural history literature before World War II, although means and occasionally some measure of variance were sometimes reported. Now ecological papers contain such sophisticated experimental designs and statistical analyses that constant updating of biometric skills is required to interpret the results, let alone to do state-of-the-art research (e.g., see Dueser et al., 1989). It is hard to overestimate how much our science has changed since World War II. In just a few decades traditional descriptive natural history has fallen into disfavor in the classroom and the journals. It has been eclipsed by an evolutionary approach to ecology that asks theoretical questions, and uses sophisticated experimental and statis- tical techniques to answer them. Mammal- ogists have not simply responded to this revolution, they have often been in the fore- front, using the special advantages of mam- mals to make important conceptual and empirical advances. Summary The history of North American mam- malogy began with the exploration of the EVOLUTIONARY ECOLOGY 391 continent by Europeans. There was added incentive to study mammals, because one of the resources most valuable to the early colonists was fur, especially beaver pelts. After the fur trade slackened, official voy- ages to explore and survey the remote parts of the continent were usually accompanied by scientists, many of them physician-nat- uralists with particular interests in mam- mals. During this discovery phase, the early naturalists were concerned with describing and classifying the different kinds of mam- mals and beginning to accumulate infor- mation on their distributions and habits. By the beginning of the 20th Century, most of the species of North American mammals had been described and mam- malogists were beginning to specialize. One of the specialties was natural history, which encompassed all aspects of ecology and be- havior. In contrast to modern disciplines, natural history was a descriptive science. Its goal was to describe the environmental re- lationships and lives of particular species, groups of related species, or entire assem- blages of coexisting species. The new evolutionary synthesis began the transformation of the field sciences into modern theory-testing, experimental disci- plines. Early studies of mammalian genet- ics, adaptations, paleontology, and bioge- ography contributed importantly to the data and concepts of the new synthesis. 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WOLFF Introduction umankind is a product of organic evo- lution, as are all living organisms on the planet Earth. Although anthropologists may disagree as to the date of transition from Homo erectus to H. sapiens, the cul- tural transition of some 100 to 70 x 103 years B.P. by H. sapiens was profound. Modern humans developed the capacity for rapid cultural evolution and, in conjunction with a very large brain, began to set about taming the environment in ways we can scarcely comprehend except through the minds and evidence of archaeologists. Our early ancestors were gifted naturalists and keen observers of nature. The manner of life styles exhibited by organisms of concern to the early economic systems were well known and communicated by direct partic- ipation in hunting, gathering, and also pre- sumably by an oral tradition. Thus, a knowledge of the behavior and life history of animals and plants has been part and parcel to our cultural heritage as human be- ings (Count, 1973). By the middle of the 19th Century, Eu- ropean naturalists were beginning to move away from the naming and describing of floras and faunas and attempting to grapple with the more intangible aspects of biology. One aspect that preoccupied attention was 398 - \ \ Ss My, ", “appa 4 4, animal behavior. The behavior of organ- isms has always held a special fascination. Consider the admonition of King Solomon “Behold the ant, thy sluggard and consider her ways” (Proverbs 6:6, King James ver- sion of the Bible). By the middle of the 19th Century two major schools of thought had developed. On the one hand, the empiri- cists, following René Descartes, tried to an- alyze the behavior of non-human mammals in terms of a mechanistic model. Questions were posed concerning what an animal could perceive and thus respond to. Elaborate ex- periments were designed to determine the limits of human and non-human animal perceptions (Mach, 1959). On the other hand, a determined group of naturalists per- sisted in attempting to describe (in writing) what animals actually did in their natural habitat. Charles Darwin, arguably the finest 19th-Century English speaking, objective observer and recorder of nature, who wrote and communicated his thoughts in the 1800s, was also concerned with animal be- havior (Darwin, 1859, 1872). His influence was profound because he not only offered an explanation for morphological change through natural selection, but also suggested avenues for the study of behavioral change, ultimately controlled by natural selection. a AA — } ) rs GaAs = SA SS . J ' ee cA See = egygin A ~ BEHAVIOR 299) A Brief History of Ethology: its Origins, Reception, and Modification in America In 1973, Niko Tinbgergen, Konrad Lo- renz, and Karl von Frisch received the No- bel Prize in Physiology and Medicine. These three men exemplified the early 20th-Cen- tury fruit of the Darwinian revolution in terms of the analysis of animal behavior (see Lorenz, 1981 for a review). Lorenz empha- sized the close observation of behavior in- volving animals kept at semi-liberty, but habituated to human observers. The com- parative method was stressed. Tinbergen championed the observation of wild crea- tures and was ingenious in developing ex- perimental techniques applied to free-living populations. von Frisch was the consum- mate experimentalist and studied the per- ceptual capacities of fish and bees (von Frisch, 1950). The general theory that these three men developed was first consolidated in Tinbergen’s book, The Study of Instinct, published in English in 1951. The book out- lined a theoretical framework for the anal- ysis of behavior, but the analysis rested firmly on the correct description of an an- imal’s repertoire—the ethogram. It was not- ed that an animal’s behavior consisted at least of two major types of actions: 1) seek- ing an appropriate goal (appetitive behav- ior); and 2) satisfying a need (consumma- tory behavior). With this publication the framework was set for the next 20 years of research in North America and Europe. The theoretical framework built in Eu- rope on Darwinian foundations was resisted by many 20th-Century students of animal behavior in North America. This situation derived mainly from the fact that the North Americans were often associated with psy- chology departments that were strongly tied to the experimental method and Cartesian reductionism. Experimental design was par- amount and asa result two American schools developed: 1) those devoted to the physi- ological mechanisms underlying discrete behaviors—a reductionist position; and 2) those devoted to the analysis of how ani- mals learn. Both approaches (with a view toward public funding) were justified before the general public and elected officials on the grounds that animal “surrogates” could lead to a better understanding of human behavior. Thus, the study of non-human animals in and of themselves was subli- mated to utilitarian needs in terms of hu- man welfare. A possible third North Amer- ican tradition was grounded in an attempt to understand cognitive processes. While experimental designs were important, the concept of higher mental processes and how to study the phenomenon has remained elu- sive (Dewsbury, 1989a; Schusterman et al., 1986). Strangely enough, in Europe and North America, many of the earlier studies of mammalian behavior were undertaken by naturalists and wildlife managers who jus- tified their activities in terms of understand- ing the life history of organisms that were of economic importance in terms of “har- vesting” or “‘control’’ by humans (Leopold, 1933). In fact, the applied researchers in- vestigating vertebrate behavior were often considered outside the boundaries of “‘pure science” by many academics and such a dreary dichotomy was to persist for some time (Wilson and Eisenberg, 1990). Nev- ertheless, regardless of the motivation, an- imal behavior has held a great fascination for all observers across all cultures. The social behavior of animals has long preoccupied mankind. Aside from the won- ders of individualistic behaviors, the vari- ety of patterns displayed during mating, pa- rental care, and seemingly altruistic behaviors were of special concern after the Darwinian revolution. Darwin (1859), Kro- potkin (1902), and Deegener (1918) grap- pled with the problem. Tinbergen (1951) pointed out that a social system is basically a communication system and thus opened a new arena of research. A paper by W. D. Hamilton (1964) was revolutionary because it laid the groundwork for a rational analysis 400 EISENBERG AND WOLFF of how societies could evolve through nat- ural selection. Eisenberg (1966) outlined the evolutionary trends of social behavior with- in the class Mammalia. Trivers (1971, 1972, 1974) amplified and clarified some intricate problems raised by Hamilton (1964), and E. O. Wilson (1975) brought the most re- cent, comprehensive synthesis to the fore- front. Darwinian selection, Mendelian ge- netics, ecology, and behavior had been wedded into a system of testable hypothe- ses. This revolution in thought will be treat- ed in a later section. A Record of the Beginnings of Animal Behavior Studies in North America Given that the basis of ethology is an- chored in the systematic observation of an animal’s behavior, who can we identify as the first North American mammalian ethol- ogist? With all due respect, we must over- look the preliterate but viable cultures of hunter-gatherers that preceded European occupation of the continent. We suggest (among others) L. H. Morgan as a candi- date. Not only did he write a classic work on the beaver (Castor canadensis) (Morgan, 1868), but he also wrote a magnificent eth- nography of the Iroquois Indians in New York and Ontario (Morgan, 1851). While not an ethologist in the 20th-Century sense, he nevertheless was an objective observer and dutiful recorder of his observations. While such naturalists as Audubon and Bachman (1846-1854) recorded facts con- cerning the habits of their subjects, L. H. Morgan concentrated on a single species or a human culture and described their behav- ior and social structure in astonishing detail. Through the late 19th and early 20th cen- turies, mammalian behavior patterns con- tinued to be described often in a fragmented fashion or as a series of anecdotes. Ernest Thompson Seton (1953) made a fine con- tribution in the compilation of anecdotes by organizing descriptions of behavior with- in species accounts in the form of a func- tional classification, e.g., mating behavior, parental care, feeding and foraging, and the like (Note: Seton did not apply these exact subheadings, but the sense was there.) The beginning of a theoretical framework for behavior studies grounded in Darwinian theory started within North America during the late 19th and early 20th centuries with the work of C. O. Whitman, who observed that the courtship of pigeons was composed of numerous stereotypic components. The behavioral units and their sequencing were often characteristic of each domestic breed. Could some types of behavior be compared among breeds or species in the manner of a comparative anatomist? Were the units of behavior as expressions of nerve-muscle re- lationships subject to the laws of heredity (Whitman, 1899, 1919)? Whitman’s student, Wallace Craig, chose bird song for comparative study and soon discovered that while some songs were spe- cies specific and relatively fixed, other spe- cies show plasticity and a good deal of learn- ing in song development (Craig, 1918). Craig and Whitman were pioneers in their studies. Parallel efforts in Europe by Oskar Heinroth and Konrad Lorenz led to the founding of European ethology, but in North America, behavior studies developed on many dif- ferent fronts with little intellectual cross fer- tilization (Dewsbury, 19895). Application of these concepts to mammalian behavior was to occur much later (see the next sec- tion). Mammalian Behavior Studies Prior to 1965 Threads in the loom—behavior studies. — Ethology as a discipline did not become consolidated in the U.S. until the mid-1950s. Although a knowledge of “‘species-typical behavior’ was a working tool for all great naturalists, to presume that behavior stud- ies represent something new is to oversim- BEHAVIOR 401 plify a very complex situation. Our prede- cessors and seniors of the last 70 years were involved with behavior studies, whether or not their labors were organized into a formal system. For example, Vernon Bailey, who worked with the U.S. Biological Survey, was intrigued by the behavior of his subjects (Bailey, 1931). Ned Hollister, before he took command of the U.S. National Zoological Park, wrote a classic paper concerning the effects of captivity and captive diets on the skull morphology of African lions (Hollis- ter, 1917). Joseph Grinnell, the spirit of the Museum of Vertebrate Zoology at Berkeley during its most formative years, was one of the most astute observers of vertebrate be- havior ever to document his observations (Grinnell, 1914). A. Brazier-Howell was deeply concerned with the problems of form and function, a true behaviorist by anyone’s definition (Howell, 1944). Shadle (1946) with his delightful, yet incisive, observa- tions on the sexual life of porcupines is also a case in point. While on the subject of mammalian reproduction, the efforts of R. K. Enders (1935, 1952) and O. P. Pearson (1944) in mammalian behavior studies stand out, not to diminish their other considerable contributions. Many others could be cited (Bronson, 1989 for review). One area of the discipline of behavior that has not received much attention from the standpoint of the “behaviorist” is that vague area of energetics and behavior, or “‘eco- physiology,” which not only has had a long history, but also a profound influence on the types of questions that behaviorists ask. The beginnings may go back to Claude Ber- nard in the 19th Century but the fact of the matter remains that in the 1940s mam- malogists began asking hard questions con- cerning how mammals were able to with- stand the rigors of adverse environments. Morrison and B. K. McNab began to ask the questions and seek the answers (Mor- rison and McNab, 1962), as did Bartholo- mew (Bartholomew and Cade, 1957). Feed- back between the so-called behaviorists and the physiologists continued (McNab, 1983). Another area of research with a long his- tory of mammals as subjects includes be- havioral genetics. Sumner (1932) and sub- sequently Lee Dice literally pioneered the research on the genetics of non-domesti- cated mammals (Dice, 1933). Peromyscus was their genus of choice and it was a sound one. With the Michigan stocks, Howard (1948), Harris (1952), and King (1961) were to shape the thinking of younger biologists concerning the genetics of behavior in the 1950s (see also King, 1968). Population dynamics and the behavior of mammalian species at different densities has become a focus of interest since the synthe- sis published by Elton (Crowcroft, 1991 for review). The pioneers on this frontier of the 1950s included D. E. Davis, D. Chitty, J. B. Calhoun, and J. Christian (Anderson, 1989; Cockburn, 1988 for reviews). The role of density-dependent and density-indepen- dent factors on the regulation of population size was a “hot topic” at that time, and the discovery that endocrine changes could me- diate and be mediated by behavioral changes only added fuel to the fires of controversy (Calhoun, 1963a, 19636; Christian, 1963). That behavior could be linked to the genetic background of an individual led to a flurry of productive research and once again be- havioral studies were an integral part of the effort (Calhoun, 1963a; Harris, 1952). The unique sensory abilities of mammals had long been recognized, but D. R. Grif- fin’s publication on the echolocation of bats in 1958 was truly a watershed. Kellogg (1961) synthesized similar data for dol- phins. Bioacoustics became a field unto its own. At Cornell, W. J. Hamilton, Jr. and his colleagues initiated important studies on mammalian food habits. Although many other aspects of mammalian behavior were studied at Cornell, perhaps one of the most notable single-species monographs was James Layne’s contribution on the behavior and ecology of the red squirrel (Tamuasiurus hudsonicus) (Layne, 1954). The use of livetraps for the purpose of 402 EISENBERG AND WOLFF trap, mark, and release studies opened a new era in the studies of how mammals use space. H. B. Sherman invented a successful metal livetrap in the late 1930s that is marketed to this day. Sherman and his students at the University of Florida developed a series of studies aimed at clarifying microhabitat use and the spacing behavior of small mammals utilizing the trap, mark, and release scheme. William Burt, utilizing a livetrap modifi- cation of his own at Michigan, wrote an influential paper in 1940 proposing that some species of small mammals appeared to show territorial behavior (Burt, 1940). The study of nocturnal, cryptic mammals and their movements received an enormous assist with the introduction of radiotele- metric techniques in the 1960s. Perhaps the most pioneering group was associated with the University of Minnesota with their mag- nificent setup at the Cedar Creek Natural History Area (Tester et al., 1964). As an aside, immobilization of mammals with a reliable series of drugs and instru- ments for projection was revolutionary (Harthoorn, 1976). Younger students will not appreciate fully the revolution intro- duced by reliable telemetry and pharma- ceutical systems. Given the advanced techniques of trap, mark, and release, monographic treatises involving these methods began to supple- ment direct observation. The focus was of- ten ecological, but behavior became more and more a concern regardless of technique: Linsdale and Tevis (1951) on the dusky- footed woodrat, Neotoma fuscipes; Linsdale (1946) on the California ground squirrel; Linsdale and Tomich (1953) on Odocoileus hemionus; Moore (1957) on Sciurus niger; and Layne (1954) on Tamiasciurus hud- sconicus all appeared in the 1940s and 1950s. One of the benchmark field studies of mam- malian social behavior was John King’s monograph on the black-tailed prairie dog, Cynomys ludovicianus (King, 1955). This classic study demonstrated that careful ob- servations of marked individuals could yield insight into the use of space, mode of com- munication, and relations among kin. King’s effort paved the way for field experiments and ever more sophisticated studies of di- urnal sciurids (Murie and Michener, 1984, 1989 for review). Nocturnal small mammals still presented problems because direct observation was not possible. Eisenberg, following the tech- niques developed by Eibl-Eibesfeldt (1958) in Germany, developed the strategy of com- bining field studies with captive studies. With the aid of the electronic flash camera, behavior patterns of small, nocturnal mam- mals could be recorded on film for analysis (Eisenberg, 1962, 1963). Kaufmann in the late 1950s and early 1960s carried out a classic field study on a diurnal carnivore, the coati (Nasua narica) in Panama (Kaufmann, 1962). His creative analysis of the social use of space by female bands has stood the test of time. Shortly thereafter, Valerius Geist produced his clas- sic study of Ovis dalli and O. canadensis in British Columbia (Geist, 1971). Ungulate behavior studies had come of age. Kleiman (1967) stimulated interest in the compara- tive social behavior of the Canidae. McKay (1973), based upon his studies in the 1960s, brought the Asiatic elephant to the forefront of attention. DeVore, in his studies of the baboon (Pa- pio cynocephalus) in Kenya, ushered in the new era of primate studies; Schaller’s study of free-ranging mountain gorillas (Gorilla gorilla beringei) was a true milestone in the art of field work (DeVore, 1965; Schaller, 1963). They demonstrated that a field work- er could habituate the subjects to the pres- ence of an intruder. Eisenberg and Kuehn (1966) attempted a synthesis for neotropical primates. The pure ethological approach based on efforts as applied to mammals (Hediger, 1942) was summarized in R. F. Ewer’s (1969) classic, The Ethology of Mammals. New disciplines were already forming around the interface between ecology and behavior. Suitably inspired, Smythe and Wemmer working in the 1960s provided BEHAVIOR 403 important contributions (Smythe, 1970; Wemmer, 1977). With the inclusion of pop- ulation genetics the stage was set for the development of sociobiology as a synthetic discipline by Wilson in 1975 (see section From ethology to sociobiology). The watershed of the late 1960s.—In 1969, the Smithsonian Institution convened its public symposium under the broad title of Man and Beast, the results of which were published in 1971 (Eisenberg and Dillon, 1971). The symposium and its published results were an attempt to focus public at- tention on the relevance of animal behavior studies to understanding human behavior. To this end, the participants in the sym- posium included biologists, philosophers, psychologists, anthropologists and sociolo- gists. In part, the public symposium was in response to the recently published work of Konrad Lorenz titled in English translation, On Aggression. The notion that some as- pects of human behavior could have a ge- netic basis was anathema to some of the North American social scientists. As Wat- son (1914) had proclaimed some years be- fore, the human mind could be considered at birth as a tabula rasa, where environ- mental conditioning reigns supreme in forming the life of the infant, juvenile, and subadult. One member of the conference, E. O. Wil- son, who delivered a provocative paper on the evolution of territoriality, was deeply moved by the conference. By his own ad- mission, it inspired him to produce his clas- sic Sociobiology. The raging controversy that accompanied the publication of Wilson’s synthesis remains a remarkable quirk in the development of the behavioral sciences. Many of us regarded, with dismay, the vit- riolic attacks, often personal, to which Wil- son was subjected. However, wounds heal, and those aspects of philosophical confron- tation that seemed so desperately important in the early 1970s diminished, and by the time a sequel to the volume was prepared via the mechanism of a conference at the Smithsonian in 1986, barely a flicker oc- curred within the halls of academe. The re- sults of this conference were published in 1991 under the title: Man and Beast Revis- ited (Robinson and Tiger, 1991). A certain amount of emotional maturity must have occurred in the intervening 16 to 20 years, and one might hope that the healing process will continue. It should be noted that there were no philosophical vil- lains leading to the first major confronta- tion, following Man and Beast (1969). To the contrary, the philosophical confronta- tion of the mid-1970s was long overdue and, sadly, somewhat protracted in the manner in which the participants registered their viewpoints. One felt at the conclusion of the 1986 symposium in Washington, D.C., that the burning issues of the relevance of animal behavior studies to the interpretation of hu- man behavior had somewhat declined. This is not to say that the cross-fertilization dur- ing the intervening 20 years had not been useful. It simply says that rapid and facile generalizations forthcoming from popular- ists did not necessarily solve any of the cur- rent problems of the human race. Clearly the social scientists contributing to the 1986 symposium, such as Helen Fisher and Lio- nel Tiger, had gleaned a great deal from the earlier ruminations in 1969. The Influence of Some Seminal Institutions The American Museum of Natural His- tory and relations with the New York Zoo- logical Society. —The American Museum of Natural History (AMNH) was one of the earliest museums in the United States to create a separate Department of Animal Be- havior. The origin of the behavior group was established under G. Kingsley Noble (See Koestler, 1971, for an account of the midwife toad scandal and Noble’s role.). Al- though best known for his work with the Amphibia, Noble was a pioneer in the anal- ysis of the relationship between hormones and behavior (Noble, 1931). Thus, he 404 EISENBERG AND WOLFF founded an experimentally based discipline that was basically reductionist. After No- ble’s premature death, Frank A. Beach was appointed to head the group and created the Department of Animal Behavior while pur- suing the role of hormones and behavior (Beach, 1948). He recruited T. C. Schneirla in the late 1940s to join him. After World War II, the department began in earnest to assemble a graduate student group. Beach championed the hormone and behavior tra- dition, but also brought some of his own interests. Beach had been a student of Lash- ley, who had pioneered brain and behavior studies, and thus a second reductionist tra- dition was added. Beach left AMNH for Yale, and Schneirla succeeded him as chair. E. Tobach, L. Aronson, and D. Lehrman became the key players as former students. D. Lehrman, a contemporary, would later found the Institute of Animal Behavior at Rutgers. Aronson, pursuing brain-behavior relationships, would continue with fish, but also turned to cat behavior. Aronson be- came chair on the occasion of Schneirla’s retirement. Given the ties of the AMNH with the local New York universities and subse- quently with Rutgers, its influence was con- siderable. The research efforts were often grounded in attempting to understand phys- iological mechanisms underlying behavior and were often allied with colleagues in hu- man medicine. The application of the re- sults of animal-based research to human problems became for some a guiding ideal (Rosenblatt and Komisaruk, 1977). The New York Zoological Society (NYZS) maintained relations with the AMNH pri- marily through curators in various depart- ments of vertebrate zoology. Early in the Century, the NYZS sponsored field research with an aim to improve knowledge appli- cable to the proper captive maintenance of exotics. William Beebe was supported and his attempts to found field stations in the Neotropics are renowned. In the early 1900s Beebe had assembled groups of researchers in what is now Guayana. Beebe (1925) pub- lished the first behavioral ecology study of the three-toed sloth, an effort not to be equalled until research by Montgomery and Sunquist (1975). In the late 1960s, the NYZS established the unit that was to become ‘“Wildlife Conservation International,” thereby supporting a core group of mam- malogists concerned with the interface be- tween ecology and behavior including R. Payne, T. Struhsaker, and G. Schaller in the original assemblage. The University of Chicago.—The Uni- versity of Chicago established connections with the Field Museum of Natural History at an early stage. These close ties contrib- uted greatly to the study of zoogeography and ecology. Many students of the first au- thor’s generation studied the classic Prin- ciples of Ecology by Allee, Park, Park, Em- erson and Schmidt. The ecologists of the Chicago group also had a deep concern with the behavior of animals. Emerson concen- trated on social insects and the problem of the evolution of social behavior. Allee shared many of Emerson’s interests, but his con- cerns were more wide ranging. Although neither Emerson nor Allee may be consid- ered mammalogists, their contribution to the theoretical links between behavior and ecology is incalculable. Indeed the highest student award conferred at the annual meet- ings of the U. S. Animal Behavior Society is the W. C. Allee Award. Upon leaving Chicago, Allee joined the University of Florida where he had an influence on the direction of behavioral research at that in- stitution. Yale and the primatologists. —Robert Yerkes of Yale University pioneered the study of primate behavior. A psychologist by training, he founded what was to become the Yerkes Primate Institute at Orange Park, Florida (now at Atlanta, Georgia under Emory University). Although Yerkes’ ef- forts were directed at captive, nonhuman primates, he actively sponsored field re- search with a genuine concern for objective descriptions of naturalistic behavior (Yer- kes and Yerkes, 1929). Bingham and Nissen BEHAVIOR 405 were dispatched to Africa (Bingham, 1932; Nissen, 1931); while C. R. Carpenter was sent to Panama. Carpenter’s studies of Ateles and Alouatta stand today as classics (Car- penter, 1934, 1935). He went on to study Hylobates and Macaca in Asia (Carpenter, 1964, for a summary). Sherwood Wash- burn, a graduate student during the gibbon project, subsequently promoted primate studies after World War II. His students (including I. DeVore) created a nexus of ac- tive research, first at Chicago, and then at Berkeley, during the late 1950s and 1960s. The history of the Smithsonian in the pro- motion of animal behavior studies. —The beginnings of animal behavior studies at the Smithsonian were rooted in the traditions of natural history. The collections at the Na- tional Zoological Park (NZP) were studied and sketched by artists, most notably by Ernest Thompson Seton, to illustrate, in part, his Lives of Game Animals. Although Ned Hollister and William Mann made nu- merous contributions to mammalian nat- ural history, behavior studies and docu- mentation were not systematically approached until E. P. Walker became As- sistant Director of the NZP in 1930. Walker was interested in photography and pio- neered the techniques of the use of syn- chronized flash bulbs, allowing bats and fly- ing squirrels to be photographed in mid- flight. He recorded primate sounds with an early version of the sound spectrograph, and attempted to describe the vocal repertoire of the night monkey (4otus). His arduous pursuit of photography eventually led to the publication of Mammals of the World after his retirement (Walker, 1964). The creation of a unit at the NZP with the mandate of studying the ethology of higher vertebrates was not to occur until 1965. For the last 28 years, the NZP has provided leadership in the study of animal behavior and in the interface between be- havior and ecology. The full maturity of the Smithsonian’s role in behavioral studies came at two important points: 1969 when the symposium Man and Beast was con- vened; and in 1973 when a consortium among the University of Maryland, George Washington University, and the Smithsoni- an Institution hosted the XIth International Ethology Conference, marking the first time that this international body had convened in the USA. The University of California, Berkeley. — Zoologists at Berkeley had an early interest in animal behavior. Samuel J. Holmes pub- lished his Animal Intelligence in 1910, and W. E. Ritter published The California Woodpecker and I in 1938. Thereafter the animal behavior studies, particularly of higher vertebrates, mainly derived from the Museum of Vertebrate Zoology (MVZ). The emphasis at the museum was often behavior and ecology, or behavior and evolution, both approaches firmly anchored in the Darwin- ian tradition, and the guiding force in the museum was Joseph Grinnell. A student of David Starr Jordan, Grinnell was to found one of the great dynasties in American mammalogy (see Jones, 1991; Whitaker, 1994). Mammalian behavior studies were not the sole domain of the MVZ. The Department of Psychology also had some giants in the field of learning studies, including E. C. Tol- man (1932). Tolman’s influence was pro- found, because he did not pursue a reduc- tionist approach, but rather championed the more holistic approach of cognition and “higher mental processes.’”’ A. Kroeber, in the Department of Anthropology, stimulat- ed the study of human cultures on a com- parative basis (Kroeber, 1925) and Karl Sauer, in the Department of Geography, championed the analysis of the role of H. sapiens in altering the contemporary envi- ronments (1969). All the elements were in place for the synthesis at Berkeley that would commence in the mid-fifties. A case study of synergism: Berkeley, Cal- ifornia— 1955—1965.—To illustrate the in- terdependency of behavior studies with re- spect to related disciplines, allow us to pursue a case study—Berkeley, California (UC), from 1955 to 1965. At the beginning 406 EISENBERG AND WOLFF of the period, the great museum legacy of Grinnell was in place and viable. If we con- fine ourselves to senior staff who worked with mammals, F. A. Pitelka, A. Starker Leopold, O. P. Pearson, and S. B. Benson were powerful influences on the cadre of aspiring young mammalogists. The special- ties of ecology, wildlife management, phys- iological ecology, and systematics were well represented. In addition, the MVZ had close ties with the Department of Paleontology. Between 1957 and 1959, four new faculty were added to the biological sciences who had a significant impact on the ““mammal group”: W. Z. Lidicker, Jr., in the MVZ, P. V. Marler in Zoology, S. A. Washburn in Anthropology, and F. A. Beach in Psychol- ogy. Leopold, Beach, Washburn, and Marler were instrumental in developing the behav- ioral research station in the Berkeley hills, during the 1960s, but more importantly they actively encouraged interdisciplinary stud- ies at a significant crossroads in the matu- ration of behavioral research at the graduate level at UC. In addition, the long standing field station, ‘““The Hastings Reserve,” was emphasized as a place to do research. Lid- icker became a catalyst in promoting an in- terface between systematics and mamma- lian ecology. Those were indeed “‘heady” times. Washburn introduced primates as suitable subjects for field studies, Beach ex- tolled the virtues of the controlled experi- ment and a modified view of the reduction- ists’ vision of behavior, and Marler presented us with the philosophy of the ethologists. The original, senior faculty gave all of us an anchor associated with the MVZ and those virtues as set out by Grinnell. We may miss some names, but the younger mam- malogists who completed their Ph.D. de- grees in Anthropology, Psychology, Zoolo- gy, and Paleontology during that period included: W. J. Hamilton III, P. K. Ander- son, J. Mary Taylor, G. Heinsohn, M. Mu- rie, D. Isaac, J. Kaufmann, C. Thaler, T. Struhsaker, S. David Webb, B. LeBoeuf, T. Grand, S. R. Ripley, P. Jay, D. D. Thiessen, L. Clemens, and one of us (J. F. Eisen- berg)—J. O. Wolff was of the next genera- tion. In addition, we had many close asso- ciations with other vertebrate zoologists (pre- and postdoctoral) who went on to earn their “‘spurs’’ as behaviorists and systema- tists including: R. B. Root, D. Wilhoft, R. Behnke, Jerram Brown, D. Dewsbury, M. Konishi, J. Mulligan, K. Nelson, E. Neil, F. Notebaum, G. Orians, J. Nelson, and G. Hirsch (see also Marler, 1985). If we consider only the cadre of post-bac- calaureate ““mammalogists”’ within the pe- riod of that “‘magic’’ decade, 12 well-ac- claimed books have been produced as of 1993, one member became the President of the ASM, two members became President of the Animal Behavior Society (ABS), one member won the C. Hart Merriam Award at the ASM, one member was President of the American Society of Paleontologists (ASP), one member became the director of a major US metropolitan museum, and all taught and mentored graduate students and produced numerous publications. In their efforts, all had influence to the far corners of the Earth including (exclusive of the USA) Australia, Canada, Botswana, Namibia, Panama, Mexico, Uganda, Kenya, India, Sri Lanka, Madagascar, Venezuela, Honduras, Chilé, Argentina, and Brazil. The Years of Consolidation and Subsequent Fractionation The Second World War interrupted all aspects of pure biological research. Com- munication with European colleagues was almost non-existent. Some of the ideas from European ethologists had begun to be ac- cepted by American mammalogists, often paradoxically via the ornithological or ich- thyological literature. Visits by N. Tinber- gen and G. Baerends to North America dur- ing the 1950s helped disseminate some of these concepts, and the hiring of European ethologists at North American universities BEHAVIOR 407 facilitated the process (Dewsbury, 1989a, 1992). Notable among these early “immi- grants” were Peter Marler at Berkeley, Franz Sauer at Florida, Erik Klinghammer at Pur- due, and Fritz Walther at Missouri and sub- sequently at Texas A&M. Whether called ethology or animal behavior, the study of the behavior of mammals rapidly became a part of the curriculum at every major uni- versity in North America. There were par- allel developments in Australia, South Af- rica, New Zealand, Israel, Japan, Kenya, and India. Thus a European tradition had taken root in many new locations. Literally hundreds of students in the United States during the 1960s and 1970s became involved in animal behavior stud- ies. The short period of consolidation was followed by the creation of new subdisci- plines and new societies. The Animal Be- havior section of the Ecological Society of America became a full society in 1964. Through an arrangement with the British Society for the Study of Animal Behavior, a newly organized journal of Animal Be- haviour served as a publication outlet for the fledgling effort. Subsequently, new so- cieties were formed with their own journals based on taxonomic lines: Chiroptera, Pri- mates, Cetaceans, or a “wedding” between ecology and behavior. One of us (J. F. Eisenberg) remembers at our meeting of the ASM in 1964 in Mexico City when papers dealing with behavior were ararity. By 1983, at our meetings in Gaines- ville, Florida, the behavior section was well represented (231 presentations). In 1983, the ASM also published Special Publication No. 7, Advances in the Study of Mammalian Be- havior (Eisenberg and Kleiman, 1983). This volume marks a point of recognition, name- ly that behavioral studies had “come of age.” There were 27 participants contributing to the volume drawn not only from the United States, but also from Canada, Australia, En- gland, Germany, Israel, and France. In or- der to illustrate how behavioral studies span many disciplines, we will briefly outline the organization of this volume. Part one deals with the interwoven themes of structure, development, and function; obviously, the underpinnings of behavior. The second part of the volume deals with mechanisms of communication. Commu- nication is still the touchstone of behavioral studies. That is to say, whether an animal be solitary or social, it must have infor- mation concerning its conspecific neigh- bors, or for that matter, its competitors and potential predators. The third section deals with case studies of mammalian behavior. In this time when testable hypotheses seem to dominate as a reason for practicing sci- ence, we wish to remind everyone that good, solid descriptions are still the matrix and the foundation for all subsequent research. Part four was entitled, The adaptiveness of behavior: constraints, population mecha- nisms and evolution. Obviously, the recent developments and fragmentation of the ethological group are reflected in the eclectic nature of the subtitle. Clearly, behavioral studies have relevance to students of phys- iology, population ecology, genetics, and evolution. From Ethology to Sociobiology and Socioecology—the Last 25 Years The level of selection—the 1970s.—The last 25 years of research in mammalian be- havior still have been strongly influenced by Darwin’s theory of evolution by natural selection. Descriptions of ethograms and mechanistic aspects of specific behaviors that predominated throughout the 1960s were largely replaced by observational and empirical studies concerning the adaptive or evolutionary significance of behavioral patterns. Behavior was still looked upon as an adaptive strategy, but within a more re- fined context. Research became more ex- perimental and was conducted more often in natural environments. The “group selec- tion” arguments for behavior, such as alarm calls and other apparent altruistic behavior 408 (Wynne-Edwards, 1962), were largely, but not entirely, explained away by kin selection (Hamilton, 1964), individualistic selection (Williams, 1966), or selfish gene (Dawkins, 1976) theories. Hamilton’s kin selection, or inclusive fitness theory, presented concep- tual and mathematical reasoning to explain cooperative and nepotistic behavior among related individuals, and antagonistic or self- ish behavior exhibited toward nonrelatives. Also during this period an emphasis was placed on concepts, theory, and hypothesis testing, rather than studying a species per se. The state-of-the-art of animal behavior in the early 1970s was reviewed by Richard Alexander (1974) and further summarized by Alexander and Tinkle (1981), and of course E. O. Wilson’s (1975) treatise, So- clobiology—the New Synthesis. Parental investment and the influence of Robert L. Trivers. — Associated with kin se- lection and selfish gene theory, several piv- otal papers were published in the early 1970s that strongly influenced our understanding of mammalian behavior. Perhaps the most influential paper published during this time was Robert L. Trivers’ (1972) theory on pa- rental investment and sexual selection. Trivers proposed that when one gender pro- vided greater parental investment than the other, competition occurred among the lat- ter for the former. When applied to mam- mals, this theory explained the intense com- petition observed among males, the significance of social organs and secondary sex characteristics associated with sexual di- morphism, and the predominance of polyg- ynous mating systems (Geist, 1974; Ralls, 1977). Two other contributions by Trivers were his theories of reciprocal altruism (Trivers, 1971) and parent-offspring conflict (Trivers, 1974). Reciprocal altruism was used to explain communal nesting in bats (Trune and Slobodchikoff, 1978), helping among dolphins (Connor and Norris, 1982), and cooperative coalition behavior among male baboons (Papio anubis, Packer, 1977). Reciprocal altruism became an alternative explanation for apparent altruistic behavior EISENBERG AND WOLFF that did not have an inclusive fitness payoff. Supportive evidence for the parent-off- spring conflict theory was provided in wean- ing studies on bighorn sheep (Ovis cana- densis, Berger, 1979), red deer (Cervus elephas, Clutton-Brock et al., 1984), and Rhesus macaques (Macaca mulatta, Go- mendio, 1991). Facultative sex ratio adjustment. —In 1973, Trivers published a provocative the- ory on facultative sex ratio adjustment (Trivers and Willard, 1973). The theory states that females should provide more pa- rental investment in the sex offspring that exhibits the greater variance in reproductive success. In mammals, this is usually con- sidered to be males. Trivers argued that by providing more maternal investment in male offspring, sons would be healthier and better competitors as adults and thus pass on more genes than if their mothers pro- vided less investment, even though the male cohort could be reduced in numbers at adulthood. Likewise, dominant or high ranking females or those females in “‘good”’ condition should produce sons, or at least provide more investment in them, than they do in daughters. Conversely, lower ranking and less healthy females should produce daughters, or at least provide more invest- ment in them, than in sons. Support for this theory was found in such diverse mammals as Galapagoes fur seals (Arctocephalus gal- apagoensis, Trillmich, 1986), red deer (Clutton-Brock et al., 1968), opossums (Di- delphis virginiana, Austad and Sunquist, 1988; Sunquist and Eisenberg, 1993), toque macaques, (Macaca sinical, Dittus, 1977), and domestic swine (Sus scrofa, Meikle et al., 1993). In 1983, Joan Silk provided an alternative hypothesis, which stated that in social systems where females compete lo- cally for resources (referred to as the local- resource competition hypothesis), mothers should provide more investment in daugh- ters than in sons. Supportive evidence was provided for this theory in white-tailed deer (Odocoileus virginianus, Caley and Nudds, 1987) and several primate species (Clark, BEHAVIOR 409 1978; Silk, 1983). The relationship between social systems and male and female repro- ductive strategies with respect to facultative sex ratio adjustment remains an active area of research in mammal behavior in the 1990s. Evolutionarily stable strategies (ESSs).— Another significant development in animal behavior that came out of the 1970s was John Maynard Smith’s concept of an evo- lutionarily stable strategy or ESS (Maynard Smith, 1974, 1982). An ESS is a strategy which when adopted by most members of the population cannot be beaten by any other strategy in the game. The theory attempts to explain the “‘best”’ or optimal behavioral strategy for an individual to exhibit. This behavior is often dependent on what other members of the population are doing and therefore is subject to frequency-dependent selection (Dawkins, 1980). ESS theory was used to explain hawk-dove strategies in an- imal contests (Clutton-Brock et al., 1979), parental investment (Maynard Smith, 1977), balanced sex ratios (Maynard Smith, 1981), cooperative mating (Packer and Pusey, 1982), sex-biased natal dispersal (Krebs and Davies, 1987), and optimal foraging behav- ior (Belovsky, 1984). The theory was very helpful in demonstrating why altruism and group-benefit traits are not evolutionarily stable (Dawkins, 1976, 1980) unless they benefit the inclusive fitness of kin (Hamil- ton, 1964). ESS or optimality theory also contended that individuals would some- times be prevented from behaving opti- mally due to risk of predation or interfer- ence from better competitors and therefore would have to “make the best of a bad job” (Dawkins, 1980; Maynard Smith, 1982). These “‘conditional’’ ESSs (Dawkins, 1980) were used to explain “‘sneaky”’ mating tac- tics in subordinate red deer (Clutton-Brock et al., 1982) and reproductively-suppressed helpers in communal or cooperatively breeding mongooses (Helogale parvula), black-backed jackals (Canis mesomelas), and hunting dogs (Lycaon pictus), reviewed in Gittleman (1989). Since its inception in 1974, ESS theory has been a central theme in developing arguments for the adaptive significance of behavioral patterns. Optimization. —Optimization models began achieving prominence in animal be- havior in the 1970s when they were applied to “decision-making” rules associated with foraging efficiency, risk sensitivity, and life histories (R. M. Alexander, 1982; Maynard Smith, 1974). Optimality theory was first applied to foraging behavior in birds (Mac- Arthur and Pianka, 1966) and later to mam- mals, such as forage selection in moose (Alces alces, Belovsky, 1978) and hoarding behav- ior in chipmunks (Elliot, 1978). In general, herbivores exhibit a trade-off between max- imizing energy intake and some external constraint such as obtaining an adequate mix of nutrients (Owen-Smith and Novel- lie, 1982) or avoiding plant secondary com- pounds (Freeland and Janzen, 1974). Be- lovsky (1978) demonstrated that moose tended to optimize energy intake subject to a sodium constraint. Habitat choice for white-tailed deer during winter is a trade- off between maximizing energy intake with- in a thermal constraint (Schmitz, 1991). Caraco and Wolf (1975) calculated that the mean size of African lion prides was not optimal for foraging efficiency, but was probably evolutionarily stable with respect to defense of carcasses, feeding territories, or offspring (Packer et al., 1990). Optimality theory has also been applied to nursing be- havior and reproductive success in female house mice (Fuchs, 1982), territorial de- fense (Schoener, 1987), managing range- lands of the western United States (Painter and Belsky, 1993), foraging behavior of pri- mates (Robinson, 1986), and harvesting management for whales (Horwood, 1990) and white-tailed deer (Leberg et al., 1987). Optimality theory, evolutionarily stable strategies, and game theory have been used extensively by bird and insect behavioral ecologists, more so by British and European biologists than by North American mam- malogists. These three behavioral concepts have contributed considerably to behavior- 410 EISENBERG AND WOLFF al theory and should be used more by mam- mal behaviorists. Beware, however, that al- though these concepts provide a powerful set of tools, truly long-term studies may raise many more questions (Clutton-Brock, 1988). Sex-biased natal dispersal. — Historically, dispersal was examined from ecological or population-level perspectives (e.g., Lidick- er, 1975; Stenseth and Lidicker, 1992; see also Chepko-Sade and Halpin, 1987). Be- haviorists, on the other hand, were inter- ested in the proximate mechanisms and ul- timate consequences of dispersal to the individual. During the 1960s and 1970s, the general consensus regarding dispersal of ju- veniles away from their natal home range or social group was that adults forced the dispersal of their offspring to reduce re- source or reproductive competition or both in the natal home range (reviewed in An- derson, 1989; Shields, 1982). During the late 1970s and continuing to the present, an em- phasis has been placed on natal dispersal as being an adaptive mechanism for juveniles to separate from opposite-sex relatives to prevent inbreeding (Crockett, 1984; Harvey and Ralls, 1986; Pusey, 1987; Wolff, 1993). Packer (1979) was the first to propose that juvenile male baboons dispersed “‘volun- tarily” from their natal social group to avoid inbreeding with female relatives. This idea was criticized by Moore and Ali (1984), but later substantiated by Packer (1985). Since then, theoretical (Clutton-Brock, 1989a, 1989b) and empirical (Wolff, 1993) argu- ments have been made to demonstrate that juvenile dispersal is correlated with the presence of opposite-sex parents 1n the natal home range and does not result from pa- rental aggression. Several experimental studies conducted in the mid-1980s and early 1990s confirmed that juvenile dis- persal functions to avoid inbreeding (e.g., marmots, Marmota flaviventris, Brody and Armitage, 1985; white-tailed deer, Odocoi- leus virginianus, Holzenbein and Marchin- ton, 1992; and white-footed mice, Pero- myscus leucopus, Wolff, 1992). The current trend is to consider juvenile dispersal as an adaptive, evolved behavior that benefits the inclusive fitness interests of both the dis- persing juvenile and the relatives it left be- hind—in short, a possible long-term com- promise. Mating systems and certainty of paterni- ty.—An important component of mam- malian behavior has been male and female mating strategies, especially as they pertain to mate guarding, pair bonding, and pater- nal care. Early classifications of mammalian mating systems included the basic monog- amy, polygyny, polyandry, and promiscui- ty. This classification system proved to be too simplistic and was later divided to in- clude, for instance: serial and permanent monogamy, harem-defense and territorial polygyny, and broadcast and arena prom- iscuity (Wittenberger, 1981). In the late 1980s and 1990s, mating systems were fur- ther classified based on male and female mating bonds and defense systems that were ultimately based on ecological and social conditions (Clutton-Brock, 1989b; Eisen- berg, 1981). Although as many as 20 dif- ferent male and female bonding and defense systems have been described, mating sys- tems of over 95% of all mammal species reportedly are polygynous or promiscuous, with less than 5% being monogamous (Klei- man, 1977). Paternal care is extensive in monogamous species or even in some uni- male polygynous systems in which males are confident of paternity. As altruism is rarely described for mating systems in mammals, any type of paternal care must be associated with confidence of paternity. The use of molecular techniques such as electrophoresis and DNA fingerprinting that employ polymorphic blood proteins as ge- netic markers have revolutionized our thinking about male and female reproduc- tive strategies (Amos and Pemberton, 1992). Foltz (1981) was the first to use electropho- retic techniques to demonstrate that the old- field mouse, Peromyscus polionotus, was BEHAVIOR 411 truly monogamous with males and females forming long-term pair bonds and all the young of a given female were sired by her mate. Conversely, Birdsall and Nash (1973) had earlier demonstrated that Peromyscus maniculatus was promiscuous. Ribble (1992) used DNA fingerprinting to corrob- orate the monogamous mating system of Peromyscus californicus. Similarly, in uni- male polygynous black-tailed prairie dogs, Cynomys ludovicianus, and yellow-bellied marmots, Marmota flaviventris, paternity analyses confirmed that all offspring within a territory were sired by the resident male (Foltz and Hoogland, 1981; Schwartz and Armitage, 1980). Pope (1991) demonstrat- ed that the dominant male in multi-male troops of A/ouatta seniculus sired most off- spring. In species where males do not defend fe- males and competition for estrous females is intense, several males may mate with the same female, possibly resulting in sperm competition and multiple paternity (see EI- liot, 1978, for a review). Female Belding’s ground squirrels, Spermophilus beldingi, and thirteen-lined ground squirrels, Spermoph- ilus tridecemlineatus, mate promiscuously with three to five different males and litters are often sired by up to three different males. In both species, first males sire 60-75% of the offspring (Foltz and Schwagmeyer, 1988; Hanken and Sherman, 1981), and conse- quently, males do not guard females, but leave to search for more mates as soon as copulation is over. In some species, how- ever, first males do not have a reproductive advantage (Dewsbury, 1984), and in those species males are more apt to guard females after copulation (Sherman, 1989). An in- teresting correlation of species in which fe- males are promiscuous and sperm compe- tition occurs is that males have larger testes than in species in which females mate with only one male (Harcourt et al., 1981; Heske and Ostfeld, 1990). Electrophoretic paternity analyses have also revealed that many species that were once thought to be polygynous were in fact promiscuous, with a relatively large portion of the offspring sired by nonresident males (Peromyscus leucopus, Xia and Millar, 1991; Microtus pennsylvanicus, Boonstra et al., 1993). DNA fingerprinting has been used to relate reproductive success to harem mem- bership in red deer, Cervus elephas (Pem- berton et al., 1992); parentage, kinship, and cooperation in African lions, Panthera leo (Gilbert et al., 1991; Packer et al., 1991); demonstrate that high-ranking males sire most of the offspring in a troop of long- tailed macaques, Macaca fascicularis (DeRuiter et al., 1992): confirm that wolf (Canis lupus) packs consist of an unrelated pair and their related offspring (Lehman et al., 1992); and describe the unique mating systems in pilot whales (Globicephala me- las), in which pods consist of adult females and related males, but all mating occurs with nonpod members (Amos et al., 1991). Infanticide as a reproductive strategy. — John Calhoun was one of the first behav- lorists to document the killing of pups by adults while studying crowding behavior in Norway rats (Rattus norvegicus) in a semi- natural environment (Calhoun, 1963a). This early account considered infanticide an ab- errant pathological behavior associated with crowded or unnatural conditions. Infanti- cide was first observed in the wild in the early 1970s. Rudran, working with primates in both Sri Lanka and Venezuela, pioneered in the observations of infanticide and sug- gested a density dependent model as an ex- planation (Rudran, 1973). Hrdy (1977), while studying a naturally occurring popu- lation of langurs (Presbytis entellus) in Abu, expounded on the phenomenon. The initial reports of infanticide in wild populations of primates precipitated a series of often hasty observational and empirical studies on in- fanticide in a variety of mammal species (Hausfater and Hrdy, 1984). In 1979, Hrdy presented five hypotheses to explain the functional significance of infanticidal be- havior that had been observed in a variety 412 EISENBERG AND WOLFF of species in a variety of situations: 1) off- spring were killed to be eaten for food; 2) sexual selection—where males would kill pups to remove genetic competitors and ter- minate lactation to stimulate the onset of estrus in the victim female; 3) competition for resources— where females would kill off- spring of other females as a mechanism of competing for burrows or nest sites; 4) pa- rental manipulation of offspring numbers or sex ratio; and 5) social pathology. Eisenberg (1981) opposed a simplistic explanation and advocated that several mechanisms could possibly be operative under natural selec- tion. Observational and experimental field and laboratory studies tested these hypotheses and provided support primarily, but not ex- clusively, for the sexual selection and re- source competition hypotheses. Killing of offspring by strange males to terminate lac- tation and stimulate the onset of estrus was reported in several taxa of mammals in- cluding lions (Panthera leo, Packer and Pu- sey, 1983), horses (Equus caballus, Berger, 1983), several primate species (reviewed in Pusey and Packer, 1987), sciurids (e.g., Mc- Lean, 1983), and murids (Labov et al., 1985; Wolff and Cicirello, 1989). Resource-com- petition infanticide committed by females was reported in Belding’s ground squirrels (Spermophilus beldingi, Sherman, 1981), prairie dogs (Cynomys ludovicianus, Hoog- land, 1985), Peromyscus sp. (Wolff and Ci- cirello, 1991), and wild rabbits (Oryctolagus cuniculus, Kunkele, 1992). The current per- spective on infanticide in mammals 1s that killing of offspring by nonrelated adults 1s an adaptive and evolutionarily stable re- productive strategy. Killing of offspring as a social pathology, as originally proposed by Calhoun, seems to be not often recorded and certainly is not evolutionarily stable; however, long-term studies of long-lived mammals are sparse. Younger students must maintain an open mind (Clutton-Brock, 1988). Socioecology—the contemporary synthe- sis.—In the last 10 years, animal behavior has become behavioral ecology or socio- ecology. Behavior now includes an animal’s entire behavioral repertoire, which is shaped largely by the distributions and abundance of resources, risk of predation, and com- petition from conspecifics. Following E. O. Wilson’s introduction to this synthesis in 1975, several major contributions have been made to this field in the form of texts, and long-term case studies, and two new jour- nals have been produced: Behavioral Ecol- ogy, and Behavioral Ecology and Socio- biology. A major influence in this field in the 1980s has been the texts and edited volumes of John Krebs and Nicholas Davies (1984, with subsequent revisions). The editors and con- tributors to these books have used an evo- lutionary approach to synthesize published works derived from a variety of taxa into major concepts in animal behavioral ecol- ogy. In the most recent volume (Krebs and Davies, 1993), mammals have been used to address dispersal theory, sexual selection, parental investment, optimal foraging, ter- ritoriality, and many other evolutionary principles. All of these concepts should pro- mote future research. Other excellent and synthetic books include: Eisenberg and Kleiman’s Advances in the Study of Mam- malian Behavior (1983), Ecological Aspects of Social Evolution (Rubenstein and Wran- gham, 1987), Social Evolution (Trivers, 1983), Sociobiology and Behavior (Barash, 1982), and The Ecology of Social Behavior (Slobodchikoff, 1988). Comprehensive case studies that have made major contributions to the field of mammal behavioral ecology include Red Deer (Cervus elaphus): the Be- haviour and Ecology of Two Sexes (Clutton- Brock et al. 1982), Wild Horse (Equus cal- labus) of the Great Basin (Berger, 1986), as well as several summary texts such as Pri- mates in Nature (Richard, 1985), and Pri- mate Societies (Smuts et al., 1987), Primate Social Systems (Dunbar, 1988), Carnivore Behavior, Ecology, and Evolution (Gittle- man, 1989), Behavioral Ecology of Ground Squirrels (Michener and Murie, 1989), BEHAVIOR 413 Marmots: Social Behavior and Ecology (Barash, 1989), and Social Systems and Population Cycles of Voles (Tamarin et al., 1990). Applying behavioral theory to humans. — Comparisons of human behavior and so- cieties with those of nonhuman animals dates back to pre-Darwinian times and has always shadowed studies on mammals and behavior through time. We presented an historical aspect for the implications of ap- plying sociobiological theory to humans earlier in this chapter and illustrate here that human behavior is still a main concern of mammalogists as well as anthropologists and psychologists in the 1990s. Several promi- nent texts that have deservedly received at- tention in the last 20 years include Ortner (1983), Eibl-Eibesfeldt (1989), and Dissay- anake (1992), as well as the volumes edited by Napoleon Chagnon and William Irons, Evolutionary Biology and Human Social Behavior (1979), and George Barlow and James Silverberg’s Sociobiology: Beyond Nature/Nurture (1980). Martin Daly and Margo Wilson (1983) keep providing up- dated editions of their well-used undergrad- uate text Sex, Evolution, and Behavior. Donald Symons’ publication of The Evo- lution of Human Sexuality in 1979 sparked considerable controversy, primarily from the feminist movement, which countered with Hrdy’s The Woman that Never Evolved in 1981. The journal Ethology and Sociobiol- ogy was Started in 1979 and is strongly ori- ented toward humans. A new interdisci- plinary society was organized in the late 1980s, the Human Behavior and Evolution Society, which held its fifth annual meeting in 1993. The popular writing style of Rich- ard Dawkins’ The Selfish Gene and David Barash’s The Whisperings Within helped these books reach much of the general pub- lic—a laudable but perhaps futile effort. Al- though an integration of evolutionary the- ory into the social sciences has been a task with much resistance, mammal behavior- ists continue to promote the universal theme of evolution by natural selection applicable to the social systems of a// mammals. Yet, some caution is necessary, and a reading of Pepper (1958) could be of help. Some Advances in Sister Disciplines Form and function—paleontology.—The evolution of mammals and the behavior of early mammals has been an area of active research. Outstanding contributions have derived from the efforts of Crompton and his associates and students. Lillegraven and the Wyoming group have broadened our horizons with new perspectives on the eu- therian-marsupial dichotomy. Guthrie, in Alaska, has brought paleontology, behav- ior, and ecology to a grand synthetic treat- ment (1990; see Haynes, 1991). Paleocom- munities and their relevance for understanding community form and ex- tinction events in contemporary times has been pioneered also by Webb (1983), Val- kenburgh (1990), and Behrensmeyer et al. (1992). A little-appreciated area of research is the use by humans of animal resources as revealed by archaeologists (Sigler-Eisen- berg, 1988). Behavior and conservation.—The New York Zoological Society and the Smithsoni- an Institution deserve special note in this arena of research. In both institutions an emphasis on field studies with an aim to apply results to conservation issues has been overwhelming. From NYZS have come seminal studies on the behavior of the humpbacked whale (Megaptera), African lion (Panthera leo), African forest primates (Cercopithecidae), the giant panda (4//urop- oda), and the ungulates of the Tibetan pla- teau (Payne, 1983; Schaller, 1972, 1993; Struhsaker, 1975). From the Smithsonian- NZP came such studies as the behavior and ecology of the golden lion tamarin (Leon- topithecus), the ecology of the tiger (Panthe- ra tigris) in Nepal, the behavior and ecology of the Asiatic elephant (E/ephas maximus), 414 EISENBERG AND WOLFF and the behavior and conservation of Pere David’s deer (Elaphurus davidianus), as well as ecosystem issues (Beck and Wemmer, 1983: Kleiman et al., 1986; Seidensticker and Lumpkin, 1991; Sunquist, 1981). The US Fish and Wildlife Service and the US National Park Service, often in con- junction with the NZP and the US National Museum of Natural History, have taken a new turn in research emphasis by encour- aging important work on cetaceans, pinni- peds, manatees, and sea lions. Leadership in conservation biology is also noted (Scho- newald-Cox et al., 1983). This effort is often under-appreciated by those outside the ser- vice. Meanwhile, there have been wide- spread efforts to cope with human-animal conflicts as the march of human population growth proceeds (Redford and Padoch, 1992; Robinson and Redford, 1991; Smythe, 1991). Quo Vadis? Some readers may consider this docu- ment a rather personal account, and in many ways this is true, because John F. Eisenberg was deeply involved in the processes that led to the acceptance of mammalian behav- ior as a legitimate discipline of study in North America. 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This popularity is confirmed by the history of conservation, in which wild species of mammals, from American bison (Bison bi- son) in the 19th Century to the giant panda (Ailuropoda melanoleuca) in the late 20th Century have been prominently featured. Yet popularity alone is not enough to en- sure survival. Some characteristics of mam- mals, including thick, luxurious coats of hair, have prompted commercial exploitation, depletion and, in some cases extinction, within historical times. Higher energy de- mands imposed by homeothermy require larger areas of natural habitat to sustain populations of mammals, as compared with reptiles of similar body size and food habits. The large brains of mammals, together with lengthy periods of lactation and parental protection, generally correlate with rela- tively low reproductive rates. Animals with low reproductive rates are slow to recover from population reductions and fare poorly in unstable environments. Wild mammals are thus esthetically pop- ular, commercially valuable, and biologi- cally vulnerable. In a world increasingly 421 U.S. FISH AND WILDLIFE SERVICE DEPARTMENT OF THE INTERIOR NATIONAL WILDLIFE REFUGE dominated by human activities, political clashes over the fate of wild mammals will increase. The early successes of North American conservation stemmed more from shifts in public attitudes than from the sci- ence of mammalogy. Indeed, direct legal protection, popularly supported and mgor- ously enforced, remains a cornerstone of conservation. But the problems faced by mammalian species worldwide are now far more com- plex and subtle than direct overharvesting. These include habitat destruction, isolation through fragmentation, assorted effects of scale, genetic depletion, introduced organ- isms, and the prospects of global climatic changes. Since its inception, the ASM has actively promoted the conservation of wild mammals, but today’s more pervasive and complicated threats require greater involve- ment by mammalogists and other scientists. Thus, a major theme featured here is the increasing role of science in the formulation and evaluation of conservation. Before 1919 From the establishment of the first col- onies through the 19th Century, Americans 422 SHAW AND SCHMIDLY of European descent viewed wild animals as obstacles to progress that would, like the American Indian, vanish before the ad- vance of civilization. Wild mammals were, at best. perceived as temporary resources for uses ranging from subsistence by early settlers to a means of enriching speculators through the fur trade. Given such attitudes and conditions, game abundance around settlements declined. The Massachusetts Bay Colony, for example, first closed the season on deer in 1694 (Mat- thiessen, 1987). Subsistence hunting by settlers and mar- ket hunting by native Americans for trade with whites had begun to take its toll by the time of American independence. Principal- ly through analysis of early trade records, McCabe and McCabe (1984) estimated that white-tailed deer (Odocoileus virginianus) numbered between 24 and 34 million in pristine North America. By 1800, the pop- ulation had declined by an estimated 50- 65%. Deer rebounded slightly during the first half of the 19th Century, owing to the dis- placement of many native Americans from the East, but a resurgence of market hunt- ing, this time by Americans of European descent, forced the number of white-tailed deer to a low of between 300,000 and 500,000 by 1900 (McCabe and McCabe, 1984). Market hunting. —Market hunting flour- ished after the Civil War. Firearms 1m- proved, first with breech-loaders and then with repeating rifles and shotguns. During the same period, railroad transportation greatly expanded wild game markets to bur- geoning eastern populations. The white-tailed deer, of course, was not the only species to decline in the face of more efficient market hunting. American bison were slaughtered first for subsistence and later for the market value of their tongues and hides. Naturalist and anthro- pologist George Bird Grinnell, hunting bi- son along the Republican River in 1872, found the species even then in such serious decline that he thought extinction likely (Reiger, 1972). In 1874, Congress passed legislation to prohibit the killing of female bison by Americans of European descent, but President Grant gave the bill a pocket veto (McHugh, 1972). Further interest in protecting bison dissipated two years later with news that Custer and five companies of the 7th Cavalry had died at the Little Bighorn. Thereafter, European Americans accepted Phil Sheridan’s praise for bison hunters who were busily destroying the “‘In- dians’ commissary” (McHugh, 1972). The early conservation movement in North America. — The near extinction of the bison provided a rallying point for America’s first movement for wildlife preservation. This movement, beginning in the 1880s, resulted from pressure by sportsmen’s groups that flourished during that period, and from na- ture enthusiasts, who took much of their sentiment from 19th Century romanticism (Dunlap, 1988). Prompted by the American Ornithologists’ Union, Congress estab- lished the Office of Economic Ornithology and Mammalogy within the U.S. Depart- ment of Agriculture in 1885. Forerunner of the Bureau of Biological Survey and U.S. Fish and Wildlife Service, this new Office had Clinton Hart Merriam as its first chief. The early preservation movement gath- ered momentum in the 1890s with devel- opment of “realistic” nature stories, by Er- nest Thompson Seton and others. These stories attempted to use the science of that time (including the now discredited “‘sci- ence”’ of animal psychology) as a vehicle to deliver a moral message, and gained wide readership through popular magazines (Dunlap, 1988). Despite growing sentiment in favor of wildlife preservation, market hunting con- tinued. By 1900, most states had laws reg- ulating hunting, but inconsistencies be- tween neighboring states, together with ease of transporting wild animal products from one state to another, allowed de facto mar- ket hunting to continue. Growing sentiment in favor of wildlife protection led Congress to pass the Lacey Act in 1900. The Lacey CONSERVATION 423 Act, drawing on Congressional authority to regulate interstate commerce, made inter- state shipment of game taken in violation of state laws a federal offense. In addition, the Lacey Act imposed federal restrictions on importation of exotic wildlife. Sentiment toward predators was an en- tirely different matter. Neither hunters nor nature lovers of the early 20th Century ap- preciated the value of carnivores. The same sentimental view that advocated protection for “noble”’ species like the elk (Cervus ela- phus) depicted predators such as the gray wolf (Canis lupus) as cruel, cunning, de- structive, and even dangerous. Lacking a lobby, predators of the time did not lack opponents; stockmen looked to the federal government for support in their war on predators. Responding to the stockmen’s wishes, Congress authorized the expenditure of the first federal funds for predator control in 1914. The following year, the Bureau of Bi- ological Survey hired professional trappers and began implementing its Congressional mandate. Direct legal protection. —Through the ear- ly years of the 20th Century, efforts to aid wild mammals focused almost entirely upon direct legal protection. Motives stemmed from the desire of sportsmen to increase their hunting opportunities and from nature enthusiasts whose interest in wildlife was sentimental and aesthetic. Zoologists (the term ““mammalogist’”’ was not then in gen- eral use) had little direct involvement with efforts to improve the status of wildlife. Those who specialized in mammals studied taxonomy and made inferences concerning phylogeny. Moreover, many early mammal specialists lacked formal academic prepa- ration, having learned mammalogy through apprenticeships. In the absence of science, wildlife con- servationists developed measures based on cultural tradition, sentiment, and dogma, and used the law as the main vehicle for implementation. Given the rudimentary state of ecology at the time, such an ap- proach may have been unavoidable. The drawback of such a non-scientific basis was that its effectiveness and progress could not be objectively measured and evaluated. A program’s success, aside from a few obvious cases in which wild populations greatly ex- panded or declined, simply could not be determined. Ineffective or misguided pro- grams, such as the “buck laws” that pro- tected female cervids, were sustained for de- cades. After 1919 By the time that the ASM was founded in 1919, the term “‘conservation”’ had come into general use. Gifford Pinchot first used the word in its modern context, feeling the need for a term that included the taking of a sustainable yield from a managed resource (Trefethen, 1975). To sport hunters, of course, Pinchot’s goal of sustainable yield, developed initially for commercial timber, applied equally well to game. Application of Pinchot’s principles to wild mammals required information obtainable only through field studies. Given the limited development of ecological principles at the time, almost nonexistent funding for re- search, and the shortage of qualified field workers, field data would be long in coming. Wildlife conservation as applied to game would continue to be based on tradition and implemented through arbitrary seasons and bag limits that may have had little to do with biological reality. Controversy over policy on mammalian predators. — Popular sentiment in the years between the World Wars still favored the destruction of medium-to-large carnivores, both to protect livestock and to protect pop- ular game animals. Gradually, however, many of the naturalists and biologists with the Bureau of Biological Survey became concerned over the decline of large mam- malian predators and the accidental killings of other wild animals. Others accepted more traditional views of predators and em- 424 SHAW AND SCHMIDLY barked enthusiastically on their agency’s mission to eradicate them. Neither side could seek answers in science, as not even the most basic field studies of food habits, behavior, and population ecology of wild predatory mammals existed. Given that many of the ASM’s founders, including its first president, C. Hart Merriam, were past or present employees of the Bureau, that controversy was bound to divide the new society as well. Open opposition to government predator control flared at the society’s 1924 meeting, where two Survey biologists, Edward A. Goldman and W. B. Bell, were called upon to defend their agency’s policy (Dunlap, 1988). Thus began a protracted and often bitter controversy that would erupt from time to time for nearly half a century. The controversy was propelled not only by a lack of field data, but also by a fundamental question concerning the mission of the Sur- vey and of its successor, the U.S. Fish and Wildlife Service. Critics of predator control contended that the agency should work on behalf of publicly-owned wildlife, as it did in most other programs. Predator control was another matter. With cooperative fund- ing from states and livestock growers, it was becoming a service for the benefit of the livestock industry. As the predator control controversy con- tinued, gradual progress was made on the conservation and management of game spe- cies. Game recovery turned out to require more than mere legal protection. Changes in the land, brought about through agricul- ture, grazing, mining, and the clearing of forests took place at about the same time as excessive commercial hunting. Thus, with- out some type of habitat restoration, game protection often could not succeed. Science-based conservation programs in universities. —Early in the 20th Century, Frederick Clements (1916) gave the world his theory of plant succession and Victor Shelford (1913) described the concept of natural animal communities. These pio- neering treatises laid the theoretical foun- dations for the study of natural communi- ties by describing the process of plant succession and by presenting criteria for de- fining the original biomes or major habitat associations of North America. Wildlife conservation could now take advantage of these discoveries and did so, albeit slowly at first. What was needed was a formal text- book and academic programs in wildlife conservation and management. The unifying textbook (Leopold, 1933) appeared and, shortly thereafter, its author accepted a professorship in game manage- ment at the University of Wisconsin, the first of its kind in the United States. Leopold and his students provided some of the first ecological studies on wild animals that could be applied directly to conservation and management. Academic programs in wildlife manage- ment received another important boost through one of the many ideas of J. N. “Ding” Darling. Darling helped set up a special research unit at Iowa State Univer- sity, paying some of the initial costs himself. The U.S. Fish and Wildlife Service expand- ed Darling’s prototype into a series of Wild- life Cooperative Research Units at major universities to bolster graduate programs in wildlife conservation and management. Public funding for conservation. —Through the mid-1930s, state wildlife conservation agencies received virtually all of their funds from the sale of hunting and fishing licenses. These funds were generally insufficient for wildlife research and, more importantly, the money from license sales was controlled by state legislatures, who often transferred funds to state projects unrelated to wildlife. The solution to the problems of inade- quate funding, and the allocation of fish and game monies to other state projects, came in the form of the Federal Aid to Wildlife Restoration Act in 1937. Often called sim- ply the Pittman-Robertson (P-R) Act, it was arguably the most important federal legis- lation affecting American wildlife. The Act placed a federal excise tax on the manufac- ture of sporting arms and ammunition, and CONSERVATION 425 redistributed the revenue, via federal au- thorities, to state wildlife conservation agencies on a matching basis. To qualify for this federal aid, each state had to pass enabling legislation ensuring that all funds collected through license sales would be used only for fish and wildlife pur- poses. State wildlife agencies now had a broader, more sustainable source of fund- ing, and one that was virtually immune to policial manipulation. Within a year, 43 of the then 48 states complied, and the other five followed soon thereafter (Williamson, 1987). In 1939, P-R apportioned $890,000 to the states. By 1986, that figure had grown to over $107 million (Kallman, 1987). Federal aid funds were earmarked for wildlife restoration, not for law enforce- ment. These monies made possible much of the desperately needed research on wild- life habitat problems and on the implemen- tation of solutions. Finally, legal regulations of harvests were being supplemented by habitat improvement. Progress after World War IT.—The pros- perity after World War IJ prompted many changes in wildlife conservation. Returning servicemen exchanged uniforms for hunting garb and state license sales boomed. Cor- respondingly, P-R reapportionment soared from $817,500 in 1945 to nearly $11 mil- lion in 1949 (Kallman, 1987). Increased revenue led to more wildlife research and management. The postwar years brought about increas- es in international cooperation and trade. As international concerns in general grew, so did interest in wildlife management and conservation on a global scale. The Inter- national Union for Conservation of Nature and Natural Resources (IUCN) was formed in 1948 as an independent international or- ganization to promote wise and sustainable use of the world’s natural resources. Mem- bership in the IUCN consisted of national government, governmental agencies con- cerned with conservation, and private or non-governmental organizations (NGOs). Leadership from the IUCN has helped de- velop international treaties on behalf of wildlife. In 1961, another important NGO, the World Wildlife Fund, came into being. The World Wildlife Fund’s primary mission was to raise money on behalf of vanishing spe- cies throughout the Earth. Both the IUCN and the World Wildlife Fund were based in Switzerland. The first postwar international conven- tion affecting wild mammals was the Inter- national Convention for the Regulation of Whaling, which met in Washington, D.C., late in 1946. Superceding the earlier 1931 Convention, this one established the Inter- national Whaling Commission (IWC), charged with reviewing harvests and estab- lishing quotas. The Commission issued few restrictions until the early 1960s when, faced with clear evidence of depleted stocks and an international lobby opposed to whaling, it gradually shifted toward more protection. In 1982, the IWC agreed to set commercial whaling quotas at zero by 1986 and to re- view the effects of this protection on whale stocks by 1990 (Lyster, 1985). Sustainable harvests.—Detailed under- standing of the effects of harvest on wild mammals has been slow in coming because the species most likely to be affected by har- vest are large, have low rates of increase, and long generation times. These traits make conclusive field investigations lengthy and expensive. Furthermore, large mammals fall under the jurisdiction of established wildlife agencies, subject to their own priorities and pressures exerted by various interest groups. Such agencies are often reluctant to approve the sort of long-term, high-visibility field investigations that would be required to im- prove the predictability of the effects of game harvests. Game harvests have remained imprecise and unrefined since the turn of the century. About the best that can be said about tra- ditional seasons and bag limits is that, with rare exception, they avoid overharvests. Even into the 1980s, a leading specialist in the harvest of large mammals concluded that 426 SHAW AND SCHMIDLY the principle change in hunting regulations in the United States over the past several decades was a relaxation of the ban against hunting on Sundays (Caughley, 1985). Broader public interest.— Although regu- lation of hunting changed little in postwar years, public interest in non-game species has increased substantially. Concern over rare and endangered species led to passage of the first Endangered Species Act in 1966. More symbolic than substantive, the Act did little more than authorize the Secretary of the Interior to develop and maintain a list of vanishing wildlife threatened with ex- tinction. The environmental movement in the late 1960s led to passage of the Endangered Spe- cies Act of 1969, curbing imports on wild animals (and parts thereof) threatened in their native lands. Four years later another Endangered Species Act retained refined el- ements from its two predecessors and ex- tended federal protection to native wildlife threatened with extinction. Section 6 of this Act provided for federal funds for use by state wildlife agencies on behalf of endan- gered species. Since the Act’s Section 7 pro- tected critical habitat of endangered species from any development using federal funds, it provided for interagency consultation to resolve conflicts and suggest alternatives (Yaffee, 1988). In 1972, Congress passed the Marine Mammal Protection Act (MMPA). This Act applied to all marine mammals and placed a moratorium on their harvest or harass- ment. It also established regulatory author- ity over commercial use of marine mam- mals and products made from them. Finally, recognizing that marine mammals play 1m- portant roles in marine ecosystems, the Act prohibited reduction of marine mammal populations to the point that they cease to perform their ecological functions (Dunlap, 1988; Trefethen, 1975). Exploitation vs. protection.—One of the most persistent controversies in wild mam- mal conservation is the conflict over con- trolled exploitation versus preservation. With its long and generally successful tra- dition in game management, wildlife con- servation in the United States and Canada generally leans toward controlled exploita- tion, principally through sport hunting. Not only can sport hunting help populations re- cover, it can provide landowners with in- centives to maintain natural habitat and can generate important revenue. Nonetheless, the preservationist view—that the best way to ensure survival of wild animals is through complete protection from exploitation—has gained favor during the past 2 decades. Management of endangered species in most cases precludes exploitation. Populations of many furbearing and, especially, marine mammals have recovered well when afford- ed complete protection. Each approach can work under some conditions, but decisions often are clouded by ideological divisions between the two camps. This division pre- vents some private conservation organiza- tions from working together more effective- ly and presenting a united front on broader conservation issues. Given proper habitat, most North Amer- ican game mammals fare quite well, wheth- er subjected to regulated hunting or afforded complete protection. Wild species found in increasingly crowded developing nations, however, may not be so fortunate. While tourism attracted by the large mammals of East Africa offers justification for protec- tion of wildlife in national parks, un- checked human population growth in nations like Kenya may soon overcome that advantage (Myers, 1979, 1985). Rather than have parks steadily converted to subsistence farms, a better strategy may be to employ would-be farmers in a sustainable harvest of wild mammals and in processing them for sale. Unfortunately, there is no clear an- swer. Just as either controlled harvest or complete protection can ensure the survival of most species of wild mammals in North America, either strategy could result in ex- tinction in the poorer, more crowded de- veloping nations. Even in North America, the debate over CONSERVATION 427 exploitation continues among professional mammalogists and wildlife managers. One important example is game ranching, used in various forms in Europe, New Zealand, South Africa, the United States, and Can- ada. Game ranching 1s practiced on private land and involves to some degree the “‘pri- vatization” of what is usually regarded as public property. Proponents argue that game ranching offers important economic incen- tives to private landowners who would oth- erwise convert wildlife habitat to more prof- itable uses. While the practice may require intensive management and acceptance of some rather artificial conditions, it may of- fer the only real hope for retaining large wild mammals on private lands. Legislation aimed at encouraging private game ranching in Alberta, Canada, recently generated sharp controversy. Geist (1988) argued that privatization would undermine what has generally been successful wildlife conservation. Further, any shift from public to private ownership would leave popula- tions of large wild mammals at the whims of market forces. When market demand was high, incentives to overharvest would be powerful. Conversely, when market de- mand slacked off, neglect would ensue. If Geist’s (1988) arguments are valid, and if they apply to wild mammals outside of Alberta, then they challenge a basic premise of the IUCN’s World Conservation Strat- egy. Can wild mammals be exploited on a sustainable basis by market forces? Put an- other way, can markets themselves become sufficiently stabilized to ensure the long-term survival of wild mammals? And, if privately owned wild mammals are successfully es- tablished, will their wild counterparts be re- garded as competitors to be destroyed? The international wildlife trade. —Just as unregulated market hunters in the United States depleted wild mammals in the 19th Century, unregulated international com- merce in wild mammals and parts thereof began to threaten numerous species by the mid-20th Century. After a decade of prompting by the IUCN, a Convention on International Trade in Endangered Species (CITES) convened in Washington, D.C., in March, 1973. The Convention decided to list the more imperiled species in its Ap- pendix I and to require both an export per- mit from the country of origin and an im- port permit from the country of destination. Species less critically threatened, but none- theless rare, are listed in its Appendix IJ and require an export permit from the country of origin. In both cases, permits are issued by a “scientific authority,” typically a wild- life or natural resource management agency. Practically speaking, legal trade of Ap- pendix I is negligible between signatories. Appendix II listings, however, allow trade at the discretion of the originating country but require record keeping and regular re- porting. These public records prove useful in monitoring trade and population trends for periodic status review. At the 1976 review meeting of the Con- vention in Berne, Switzerland, members voted to adopt strict criteria for listing and delisting species. Under these ‘“‘Berne cri- teria,” the information required for listing a species need not be as detailed or conclu- sive as that for delisting. This arrangement reversed the traditional burden of proof, placing it on those who advocate exploita- tion rather than on those who urge protec- tion. Predictably, controversy ensued, but the rationale of erring on the side of pro- tection prevailed. Projections of global declines in wild mammals. — Despite the considerable prog- ress in conservation during the 1960s and 70s, the 1980s opened with extraordinarily pessimistic projections for the Earth’s wild species. Deforestation, particularly of the little-known but species-rich tropical moist forests, was accelerating. Field studies showed that the recovery potential or resil- iency of tropical moist forests was far lower than that of temperate forests. International trade in wildlife and products from wildlife increased, spurred by rising demand in con- sumer nations and by increasing effort to use natural resources, such as wildlife and 428 forest products, to balance trade and to off- set growing indebtedness incurred by pro- ducer nations. Besides local habitat losses and heavier commercial exploitation, wild species be- gan facing threats from large-scale impacts to their environments. Ocean dumping and its resulting pollution increased in both scope and intensity. Atmospheric threats, first from acid precipitation and later from de- pletion of atmospheric ozone and increases in “greenhouse” gases, caused unprece- dented effects upon entire biomes. Thus, 7he Global 2000 Report to the President of the United States in 1980 projected that from 15 to 20% of the world’s wild species, if current trends continued, would be extinct by the year 2000 (Barney, 1980). While the task force labored over The Global 2000 Report ... the IUCN devel- oped a comprehensive plan to offset some of the report’s more dire projections. The UCN’s World Conservation Strategy rec- ognized that humanity would continue to exploit the Earth’s seas and soils, but sought to thwart exploitation’s impact by shifting it toward sustainable development. This ba- sic change is analogous to the difference be- tween mining a nonrenewable resource and cropping a renewable one. Insofar as wild mammals were con- cerned, the World Conservation Strategy of- fered several recommendations, aimed principally at large mammals. First, a series of large nature reserves (of sufficient size to sustain wild populations of large mammals) should be established. Second, controlled exploitation, ranging from traditional sport hunting to less conventional game cropping, should be permitted in or around such ar- eas. Properly done, such harvest would al- low sustainable exploitation of meat and trophies, as well as providing employment and revenue. This is especially important in developing nations. Finally, the World Con- servation Strategy recommended preserving wild species of mammals because of the ge- netic diversity their populations contain, potentially useful for the improvement of SHAW AND SCHMIDLY existing livestock and for the creation of “new” domesticated animals in the future (IUCN, 1980). In short, the IUCN’s plan presented conservation as an integral part of economic development, rather than as the antithesis to it. Many conventional types of development clearly are not sustainable. One of these is the large-scale clearing and conversion of tropical moist forests, either for commercial logging or for conversion of lowland forest to farms and pastures. Once the primary forests are cleared, recovery of the ecosys- tems to anything resembling their original state becomes unlikely. Tropical forests hold their nutrients not in soils, but in decaying plant and animal matter near the soil sur- face. Clearing and burning deprives the al- tered ecosystem of nutrients needed for re- covery, and land surfaces become exposed for the first time to the direct effects of sun and wind. Insect and pest outbreaks follow, and remaining patches of tropical moist for- est succumb to isolation and the combined physical and biological changes along their edges (Lovejoy et al., 1986). New Approaches to the Conservation of Mammals Threats to the long-term survival of free- living wild mammals are larger and more complex than ever before. Participants in a recent conference in Washington, D.C., ex- amined the effects of atmospheric changes, largely the “greenhouse effect,’ on biodi- versity (Peters, 1988). The climatic changes brought about by increasing levels of at- mospheric carbon dioxide could trigger sig- nificant geographic shifts in plant and ani- mal communities. Thus national parks and other reserves, already suspected as being of insufficient size, may prove even less ef- fective at sustaining wild mammals as cli- mates shift. One possible solution would be to leave or develop north-south corridors of natural habitat between protected areas CONSERVATION 429 in an effort to accommodate climatically- induced shifts in geographic ranges. As threats increase in scale, so must ef- forts in ecological research. Ecological stud- ies of wild mammals, particularly large spe- cies, increasingly are being carried out with the replication and controls needed in good experimental designs. In addition, the larger the scope of ecological investigations, the greater the cost. Thus, large-scale studies can become prohibitively expensive. One elegant and straightforward solution to these problems is the systematic use of wildlife management as scientific research (Mac- Nab, 1983). Rather than apply one general management practice to a region the size of a state, wildlife agencies could deliberately vary practices, be they harvest levels, hab- itat improvements, or other options, in ways that would allow direct comparisons and evaluations. Some areas could be left alone to serve as “‘controls.’’ This systematic ap- proach to management would require more careful planning and more detailed moni- toring, but their potential benefits would certainly be worth the extra effort. A similar framework with which to in- tegrate wildlife management with research is called comprehensive planning (Crowe, 1983). Adopted to varying degrees by some state wildlife agencies, comprehensive plan- ning provides for periodic review of man- agement practices using pre-established cri- teria. A particular program in wildlife management is planned, implemented, re- viewed, and then reassessed routinely, thus allowing for improvement or, if necessary, replacement. Done properly, comprehen- sive planning not only provides important new research, but also reduces the political machinations that occur within agencies. Rather than deciding on a program’s fate purely through competing political forces, agencies can evaluate it through analysis of field data. Even when a management pro- gram completely fails to meet its objective, useful information can be obtained and the effort justified. A potentially far-reaching technique for large-scale field studies is a collection of computer software packages known as Geo- graphical Information Systems (GIS). GIS links attribute data (e.g., biogeographical province, biome type, species occurrence, topographic features) with positions on the earth (McLaren and Briggs, 1993). Two principal approaches are inventory, consist- ing of descriptive data, mapping, and da- tabase management, and analysis, com- prised of modeling and statistical treatments (Berry, 1993). Commonly used in natural resource management since the 1980s, GIS applications also are indispensible in de- tailed spatial studies of mammalian ecology (August, 1993). Gap analysis is a particular application of GIS designed to target spatial ““gaps”’ in state- wide habitat protection systems. Once identified, such “‘gaps’’ often can be filled to ensure adequate protection of threatened species and rare natural communities. Gap analysis offers the advantages of identifying needs of several species at once as well as presenting a more proactive approach in which conservation measures may be taken before situations become desperate (Scott et al., 1991). Wild mammals and the maintenance of biodiversity. — Wildlife conservation began as game management, with the aim of pro- ducing a “surplus” for sport hunting. Game management could be improved by field studies of the ecology of a game species in general and its responses to harvest and changes in land use in particular. Thus, game management succeeded by meeting the needs of game species one at a time. It seemed only reasonable in the early days of endangered species conservation to contin- ue this tradition from game management, except that the objective was restoration rather than harvest. Effective as it was for mostly temperate game mammals, this single-species man- agement proved inadequate in the face of such serious and widespread threats as de- forestation and increased international traf- ficking of wildlife. Of the roughly 4,100 spe- 430 SHAW AND SCHMIDLY cies of mammals on Earth, only a small fraction has been studied sufficiently to per- mit development of detailed conservation plans. Conservationists began to realize that there was neither enough time nor resources to rely exclusively on single-species man- agement. New challenges required new ap- proaches. Professional wildlife conserva- tion began to shift from efforts to save “species A”’ (typically a large mammal with popular appeal) to preserving biodiversity on an ecosystem level. This biodiversity approach offers two dis- tinct advantages over single-species man- agement. First, it allows more efficient al- location of time and resources. Instead of 4,100 management plans for wild mam- mals, it can rely on protecting reserves lo- cated in the roughly 193 biogeographical provinces or principal habitat types on which those 4,100 mammals depend for survival in the wild. Second, it recognizes the im- perative of saving self-sustaining ecosys- tems, a goal consistent with the IUCN’s view of sustainable uses of natural resources. Concern for preserving biodiversity be- gan attracting biologists from outside the traditional ranks of wildlife management. Population geneticists and evolutionary ecologists started to supplement their basic research with investigations into sustaining biodiversity. A new field, conservation bi- ology, appeared along with an edited book of the same name in 1980 (Soulé and Wil- cox, 1980). In 1987, the Society for Con- servation Biology was established with its journal, Conservation Biology. This new discipline is more broadly based than conventional wildlife management. Although conservation biology is interdis- ciplinary and includes many specialties, two of the more longstanding ones featured here are conservation genetics and insular ecol- ogy. Conservation genetics. —The importance of conservation genetics escaped the notice of most wildlife managers, who knew that genetic depletion posed a problem for do- mesticated mammals but saw little evidence of its practical significance to wild ones. Thriving populations of white-tailed deer, for example, founded from only a few in- dividuals, suggested that wild species had a greater resistence to genetic problems im- posed by small, isolated populations. The first clues that wild species might suf- fer from inbreeding appeared in studies of captive-bred zoo mammals in which more inbred populations consistently produced fewer surviving offspring than did less in- bred ones (Ralls et al., 1979). Why was there such a marked difference between the zoo populations and their free-living, trans- planted counterparts? Part of the answer stems from the fact that small populations of wild animals lose genetic variation in two stages (Franklin, 1980). The first is the so- called “founder effect” (Mayr, 1963), which occurs when a population undergoes sudden and severe numerical reduction, leaving only a small number of surviving “founders.” Fewer founders mean that rarer genes are likely to be lost for future generations, re- ducing genetic variation. The founder effect may be followed by additional genetic loss through inbreeding, genetic drift, or both. At low numbers, close relatives are likely to breed with one anoth- er. Also, small populations suffer from ge- netic drift, the loss of rarer genes by chance. These processes deplete genetic variability for each generation that a population is kept at low numbers. Zoo populations have been subjected to both stages of genetic losses. Reintroduced game populations typically experience only the founder effect, quickly increasing their numbers and reducing the effects of in- breeding and genetic drift. Insular ecology.—Insular ecology is an applied version of the classic theories of is- land biogeography (MacArthur and Wilson, 1967). These theories predict that islands will be colonized by wild species at a rate inversely proportional to distance from the mainland. Moreover, species on islands be- CONSERVATION 431 come extinct at rates inversely proportional to island size, the rationale being that the smaller the island, the smaller the popula- tions, and the smaller the populations, the greater the threat of extinction. These basic theories seem simple and plausible enough, and they are supported by studies of land-bridge islands separated from mainlands since sea levels rose at the end of the Pleistocene (Wilcox, 1980). When the islands were peninsulas, they presumably contained the same levels of species diver- sity that occurred on the mainland to which they were connected. Since the time of 1so- lation by rising sea water can be reliably estimated, comparisons of historical levels of species on those islands can be compared with diversity on mainlands. The resulting differences compare closely with those pre- dicted by island biogeography (Wilson and Willis, 1975). Protected areas of natural habitat are in- creasingly fragmented and isolated from one another in human-dominated landscapes. The species preserved on such habitat is- lands may be subject to the same general patterns of extinction incurred by species on land-bridge islands. To the extent that the analogy holds (a matter of some debate at the time of this writing), isolated habitat preserves may lose many species. Mammals seem to be the class of vertebrates most vulnerable to this effect of insular ecology (Wilcox, 1980). Except for bats, mammals are more limited than birds in their dis- persal, so their prospects for recolonizing isolated habitat preserves are limited. Mammals have higher metabolic demands than do reptiles and amphibians, and thus require larger areas over which to forage. Large mammalian carnivores, empirically recognized as ‘“‘extinction prone”’ (Ter- borgh, 1974), require the largest areas of all and it may be that this area requirement is at least as important in their demise as con- flict with human activity. Indeed, one recent model predicted that no national park or other habitat reserve anywhere in the world was large enough to sustain a population of large carnivores indefinitely (Belovsky, 1987). An increasing role for mammalogists. — Perhaps the broadest question of all con- cerns the role that the discipline of mam- malogy will and should play in conserva- tion. Mammalogists concerned with conservation like to think that their research will lead to more effective conservation. Al- though distinguished authorities (Caughley, 1985; Geist, 1988) have argued that early wildlife conservation in North America suc- ceeded despite the science of the day and not because of it, the situations in which we find ourselves today differ markedly from those that confronted Hornaday and Grin- nell. The forces contributing to the loss of wild mammals are not just local market hunters, but large-scale habitat disruption, unprecedented atmospheric and oceanic pollution, and international trafficking. Many of these new threats are highly tech- nical and require the technological assis- tance and conceptual innovation that can best be provided by science. Mammalogists will play an increasingly important role in ensuring the survival of wild mammals into the 21st Century and beyond. Summary and Conclusions The conservation of wild mammals be- gan largely with direct legal protection aimed at curbing excessive hunting and trapping. Such measures were based little on science, but the fact that many depleted populations recovered, especially those of North Amer- ican ungulates, attested to the utility of legal protection in dealing with overhunting. In recent decades, habitat alterations, habitat fragmentation, and genetic deple- tion have joined overharvesting as threats to the survival of wild species of mammals. These new threats have stimulated devel- opment of new scientific subdisciplines, such as conservation biology, and emerging tech- 432 SHAW AND SCHMIDLY nologies, including geographical informa- tion systems. In the future, the conservation and management of wild mammals will de- pend even more on mammalogy and related sciences. Literature Cited Aucust, P. V. 1993. GIS and mammalogy: building a database. Pp. 11-26, in GIS applications in mam- malogy (S. 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Pp. 522-534, in Ecology and evolution or iP Harvard MCZ Librar wy TN 1 4 066 239 _+tfoo DATE DUE DEMCO, INC. 38-2931 msaeeenealee = So eee ES peaeistatearee = eessateesistomennstostuttcd ae es 2 = 3 eee : Sas Sees SMES aS 5.25 Sree cee ee ee 3 = nosgt SEE