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READINGS IN 
MAMMALOGY 



J. Knox Jones, Jr. 
Sydney Anderson 



Museum of Natural History 

The University of Kansas 

19 70 



HARVARD UNIVERSITY 

Library of the 

Museum of 

Comparative Zoology 

Gift of E. E. Williams 



Readings In Mammalogy 



Selected from the original literature 
and introduced with comments by 



J. Knox Jones, Jr. 

The University of Kansas, Lawrence 



AND 



Sydney Anderson 

The American Museum of Natural History, New York City 



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Monograph No. 2 

Museum of Natural History 

The University of Kansas 

1970 






Monograph No. 2 

Museum of Natural History, The University of Kansas 

ix-{-586 pp., 1970 



Lawrence • Kansas 



MUS. COMP. ZOOL" 
LIBRARY 

MAR 12 1980 

HARVARD , 
UNIVERSITY ' 



PRINTED BY 
THE XJNIVERSITY OF KANSAS PRINTING SERVICE 



PREFACE 

This anthology is intended as an introduction to the study of mammals, 
principally for those who already have some biological background and who 
want to know the general scope of the field of mammalogy. The subdisciplines 
or specialties of mammalog>% its relationship to other biological fields, and 
specific examples of the type of work done by mammalogists are here intro- 
duced by means of a selection of complete papers in their original form. We 
hope that these will help college students looking forward to graduate work in 
biology obtain a realistic general view of mammalogy as a possible specialty. 
Also, beginning graduate students in related disciplines such as ornithology, 
mammahan physiology, or ecology, or undergraduate majors in wildlife man- 
agement, may find their perspectives broadened by perusal of the present 
selection of papers and the introductory commentaries. 

The published literature on the scientific study of mammals, which, broadly 
speaking, comprises the field of mammalogy, includes about 90,000 separate 
papers, and new papers are now being published at the rate of 5000 to 6000 
each year, the actual number depending on where one draws the borders of 
the discipline. Precise borders do not exist. Mammalogy, like other scientific 
fields, draws from and contributes to various areas of human knowledge. Our 
selection of the 64 papers here reproduced was influenced by : ( 1 ) our con- 
cept of the scope of mammalogy and of a reasonable and representative bal- 
ance of its parts at this time; (2) our desire to illustrate various ways in which 
a wide variety of information can be presented in published form; and (3) 
our awareness that most of our readers will be English-speaking Americans, 
which led us to use articles published in English and selected predominantly 
from American sources. Nevertheless, we judge that the broad sweep of 
concepts and methods portrayed is relevant to students of mammalogy in all 
parts of the world. We have selected short papers, in general less than 20 pages 
in length, in preference to either longer papers or excerpts therefrom — chiefly 
because of space, but also because we want the serious student, who may later 
contribute to the literature himself, to see each published work in its entirety 
as one tangible contribution to knowledge. He can then grasp its concept, its 
methodology, its organization, its presentation, its conclusions, and perhaps 
even its limitations. On the latter score we would note that, although we think 
the papers selected are worthy contributions and make the points we wish to 
emphasize, we do not pretend to have selected the finest papers ever published. 
We could have used a somewhat different selection to serve much the same 
purpose, and we are sure someone else would use a different selection to 
represent his views of mammalogy. 

Although many college and university libraries have some or most of the 
journals and other sources from which papers were selected, we decided an 
anthology was warranted for those who want an overview of the field, who 
may not know where to find the relevant literature, or who want the conve- 
nience of a collection of separate papers. Many undergraduate students are 
largely unaware of the existence of, or the nature of, the technical literature 
of science, although their textbooks are replete with terminal citations. Hope- 



Monograph No. 2 

Museum of Natural History, The University of Kansas 

ix-\-586 pp., 1970 



Lawrence • Kansas 



MUS. COMP. ZOOU 
LIBRARY 

MAR 12 1980 

HARVARD 
UNIVERSITY ' 



PRINTED BY 
THE tJNIVERSITY OF KANSAS PRINTING SERVICE 



PREFACE 

This anthology is intended as an introduction to the study of mammals, 
principally for those who already have some biological background and who 
want to know the general scope of the field of mammalogy. The subdisciplines 
or specialties of mammalogy^ its relationship to other biological fields, and 
specific examples of the type of work done by mammalogists are here intro- 
duced by means of a selection of complete papers in their original form. We 
hope that these will help college students looking forward to graduate work in 
biology obtain a realistic general view of mammalogy as a possible specialty. 
Also, beginning graduate students in related disciplines such as ornithology, 
mammalian physiology, or ecology, or undergraduate majors in wildlife man- 
agement, may find their perspectives broadened by perusal of the present 
selection of papers and the introductory commentaries. 

The published literature on the scientific study of mammals, which, broadly 
speaking, comprises the field of mammalogy, includes about 90,000 separate 
papers, and new papers are now being published at the rate of 5000 to 6000 
each year, the actual number depending on where one draws the borders of 
the discipline. Precise borders do not exist. Mammalogy, like other scientific 
fields, draws from and contributes to various areas of human knowledge. Our 
selection of the 64 papers here reproduced was influenced by: (1) our con- 
cept of the scope of mammalogy and of a reasonable and representative bal- 
ance of its parts at this time; (2) our desire to illustrate various ways in which 
a wide variety of information can be presented in published form; and (3) 
our awareness that most of our readers will be English-speaking Americans, 
which led us to use articles published in English and selected predominantly 
from American sources. Nevertheless, we judge that the broad sweep of 
concepts and methods portrayed is relevant to students of mammalogy in all 
parts of the world. We have selected short papers, in general less than 20 pages 
in length, in preference to either longer papers or excerpts therefrom — chiefly 
because of space, but also because we want the serious student, who may later 
contribute to the literature himself, to see each published work in its entirety 
as one tangible contribution to knowledge. He can then grasp its concept, its 
methodology, its organization, its presentation, its conclusions, and perhaps 
even its limitations. On the latter score we would note that, although we think 
the papers selected are worthy contributions and make the points we wish to 
emphasize, we do not pretend to have selected the finest papers ever published. 
We could have used a somewhat different selection to serve much the same 
pmpose, and we are sure someone else would use a different selection to 
represent his views of mammalogy. 

Although many college and university libraries have some or most of the 
journals and other sources from which papers were selected, we decided an 
anthology was warranted for those who want an overview of the field, who 
may not know where to find the relevant literature, or who want the conve- 
nience of a collection of separate papers. Many undergraduate students are 
largely unaware of the existence of, or the nature of, the technical literature 
of science, although their textbooks are replete with terminal citations. Hope- 



fully, many of our readers will be provoked to go to the library to seek out 
additional information on mammals, once they learn the interest and value of 
subjects treated in the pages of the Journal of Mammalogy and other scien- 
tific sources. 

We have formulated our ideas for this anthology over the past three years 
and we are grateful for suggestions received from many persons in that time. 
We are grateful also to editors, publishers, and living authors for permission 
to include their works in Readings in Mammalogy. 

J. Knox Jones, Jr. 
Sydney Anderson 



IV 



CONTENTS 

Introduction __ — -. 3 

Section 1 — Systematics 

Grinnell, J. 

The museum conscience. Museum Work, 4:62-63, 1922 9 

Thomas, O. 

Suggestions for the nomenclature of the cranial length 

measurements and of the cheek-teeth of mammals. Proc. 

Biol. Soc. Washington, 18:191-196, 1905 11 

Hall, E. R. 

Criteria for vertebrate subspecies, species and genera: the 

mammals. Ann. New York Acad. Sci., 44:141-144, 1943 17 

LiDiCKER, W. Z., Jr. 

The nature of subspecies boundaries in a desert rodent and its 
implications for subspecies taxonomy. Syst. Zool., 11:160-171, 1962 _. . 21 

Hershkovitz, p. 

Generic names of the four-eyed pouch opossum and the woolly 

opossum (Didelphidae). Proc. Biol. Soc. Washington, 

62: 11-12, 1949 33 

Allen, J, A. 

Two important papers on North-American mammals. Amer. 

Nat., 35:221-224, 1901 35 

Merriam, C. H. 

Descriptions of two new species and one new subspecies of 

grasshopper mouse, with a diagnosis of the genus Onychomys, 

and a synopsis of the species and subspecies. N. Amer. 

Fauna, 2:1-5, pi. 1, 1889 __.__.. 39 

Handley, C. O., Jr. 

Descriptions of new bats {Choeroniscus and Rhinophylla) from 
Colombia. Proc. Biol. Soc. Washington, 79:83-88, 1966 46 

Benson, S. B. 

The status of Reithrodontomys montanus (Baird). Jour. 

Mamm., 16:139-142, 1935 52 

Hoffmeister, D. F., and L. de la Torre 

A revision of the woodrat Neotoma stephensi. Jour. Mamm., 

41 :476-491, 1960 56 

Lawrence, B., and W. H. Bossert 

Multiple character analysis of Canis lupus, latrans, and 

familiaris, with a discussion of the relationships of 

Canis niger. Amer. Zool., 7:223-232, 1967 72 

Patton, J. L., and R. E. Dingman 

Chromosome studies of pocket gophers, genus Thomomys. 

I. The specific status of Thomomys umbrinus (Richardson) 

in Arizona. Jour. Mamm., 49:1-13, 1968 82 



Nadler, C. F., and C. E, Hughes 

Serum protein electrophoresis in the taxonomy of some 
species of the ground squirrel subgenus Spermophilus. 
Comp. Biochem. Physiol, 18:639-651, 1966 95 

Machado- Allison, C. E. 

The systematic position of the bats Desmodus and 

Chilonycteris, based on host-parasite relationships 

(Mammalia; Chiroptera). Proc. Biol. Soc. Washington, 

80 : 223-226, 1967 108 



Section 2 — Anatomy and Physiology 

Hill, J. E. 

The homology of the presemimembranosus muscle in some 

rodents. Anat. Rec, 59:311-314, 1934 115 

Hooper, E. T. 

The glans penis in Sigmodon, Sigmomys, and Reithrodon 

(Rodentia, Cricetinae). Occas. Papers Mus. Zool., 

Univ. Michigan, 625:1-11, 1962 119 

Hughes, R. L. 

Comparative morphology of spermatozoa from five marsupial 

families. Australian Jour. Zool., 13:533-543, pi. 1, 1965 130 

MOSSMAN, H. W. 

The genital system and the fetal membranes as criteria for mammalian 
phylogeny and taxonomy. Jour. Mamm., 34:289-298, 1953 142 

NOBACK, C. R. 

Morphology and phylogeny of hair. Ann. New York Acad. Sci., 
53:476-492, 1951 152 

Vaughan, T. a. 

Morphology and flight characteristics of molossid bats. 

Jour. Mamm., 47:249-260, 1966 169 

Rabb, G. B. 

Toxic salivary glands in the primitive insectivore Solenodon. 

Nat. Hist. Misc., Chicago Acad. Sci., 170:1-3, 1959 181 

Forbes, R. B. 

Some aspects of the water economics of two species of 

chipmunks. Jour. Mamm., 48:466-468, 1967 184 

Pearson, O. P. 

The oxygen consumption and bioenergetics of harvest 

mice. Physiol. Zool., 33:152-160, 1960 187 

Bartholomew, G. A., and R. E. MacMillen 

Oxygen consumption, estivation, and hibernation in the kangaroo 

mouse, Microdipodops pallidus. Physiol. Zool., 34:177-183, 1961 196 

Scholander, p. F., and W. E. Schevill 

Counter-current vascular heat exchange in the fins of 

whales. Jour. Applied Physiol., 8:279-282, 1955 203 



Section 3 — Reproduction and Development 

Hamilton, W. J., Jr. 

The reproductive rates of some small mammals. Jour. 

Mamm., 30:257-260, 1949 209 

Spencer, A. W., and H. W. Steinhoff 

An explanation of geographic variation in litter size. 

Jour. Mamm., 49:281-286, 1968 --- 213 

Sharmax, G. B. 

The effects of suckling on normal and delayed cycles of reproduc- 
tion in the red kangaroo. Z. Siiugetierk., 30:10-20, 1965 219 

Wright, P. L., and M. W. Coulter 

Reproduction and growth in Maine fishers. Jour. Wildlife 

Mgt., 31:70-87, 1967 230 

Jones, C. 

Growth, development, and wing loading in the evening bat, 

Nycticeiiis liwneralis (Rafinesque). Jour. Mamm., 

48: 1-19, 1967 248 

Butter worth, B. B. 

A comparative study of growth and development of the 

kangaroo rats, Dipodomys deserti Stephens and Dipodomys 

merriami Mearns. Growth, 25:127-138, 1961 267 

Allen, J. A. 

Cranial variations in Neotoma micropus due to growth and 

individual differentiation. Bull. Amer. Mus. Nat. Hist., 

6:233-246, pi. 4, 1894 279 

LiNZEY, D. W., and A. V. Linzey 

Maturational and seasonal molts in the golden mouse, 

Ochrotomys nuttalli. Jour. Mamm., 48:236-241, 1967 294 



Section 4 — Ecology and Behavior 

Caughley, G. 

Mortality patterns in mammals. Ecology, 47:906-918, 1966 303 

Frank, F. 

The causality of microtine cycles in Germany. Jour. 

Wildlife Mgt., 21:113-121, 1957 316 

Burt, W. H. 

Territoriality and home range concepts as applied to 

mammals. Jour. Mamm., 24:346-352, 1943 325 

Miller, G. S., Jr. 

Migration of bats on Cape Cod, Massachusetts. Science, 

5:541-543, 1897 -..- 332 

Brown, L. N. 

Ecological distribution of six species of shrews and 

comparison of sampling methods in the central Rocky 

Mountains. Jour. Mamm., 48:617-623, 1967 335 

Davis, D. E., and J. J. Christian 

Changes in Norway rat populations induced by introduction 

of rats. Jour. Wildlife Mgt., 20:378-383, 1956 342 



Pearson, O. P. 

A traffic survey of Microtus-Reithrodontomys runways. 

Jour. Mamm., 40:169-180, 1959 ..-' 348 

EsTES, R. D., and J. Goddard 

Prey selection and hunting behavior of the African wild 

dog. Jour. Wildlife Mgt., 31:52-70, 1967 360 

Layne, J. N. 

Homing behavior of chipmunks in central New York. Jour. 

Mamm., 38:519-520, 1957 379 

SUTHERS, R. A. 

Comparative echolocation by fishing bats. Jour. Mamm., 

48:79-87, 1967 381 

ElSENBERG, J. F. 

The intraspecific social behavior of some cricetine rodents of the 

genus Peromyscus. Amer. Midland Nat., 69:240-246, 1963 390 

McCarley, H. 

Ethological isolation in the cenospecies Peromyscus 

leucopus. Evolution, 18:331-332, 1964 397 

Lyman, C. P. 

Activity, food consumption and hoarding in hibernators. 

Jour. Mamm., 35:545-552, 1954 399 

Real, R. O. 

Radio transmitter-collars for squirrels. Jour. Wildlife 

Mgt., 31:373-374, 1967 407 



Section 5 — Paleontology and Evolution 

Reed, C. A. 

The generic allocation of the hominid species hahilis as a problem in 
systematics. South African Jour. Sci., 63:3-5, 1967 411 

HiBBARD, C. W. 

Microtus pennsylvanicus (Ord) from the Hav Springs local fauna 

of Nebraska. Jour. Paleont., 30:1263-1266, 1956 414 

Wilson, R. W. 

Tvpe localities of Cope's Cretaceous mammals. Proc. South 

Dakota Acad. Sci., 44:88-90, 1965 418 

Radinsky, L. B. 

The adaptive radiation of the phenacodontid condylarths and the 

origin of the Perissodactyla. Evolution, 20:408-417, 1966 421 

Miller, G. S., Jr., and J. W. Gidley 

Synopsis of the supergeneric groups of rodents. Jour. 

Washington Acad. Sci., 8:431-448, 1918 431 

Wood, A. E. 

Grades and clades among rodents. Evolution, 19:115-130, 1965 449 

Durrant, S. D., and R. M. Hansen 

Distribution patterns and phvlogeny of some western ground 

squirrels. Syst. Zool., 3:82-85, 1954 465 



Guthrie, R. D. 

Variability in characters undergoing rapid evolution, an analysis 

of Microtus molars. Evolution, 19:214-233, 1965 469 

Jansky, L. 

Evolutionarv adaptations of temperature regulation in 

mammals. Z. Saugetierk., 32:167-172, 1967 - -- 489 



Section 6 — Zoogeography and Faunal Studies 

Dice, L. R. 

The Canadian Biotic Province with special reference to 

the mammals. Ecology, 19:503-514, 1938 497 

GUILDAY, J. E. 

Pleistocene zoogeography of the lemming, Dicrostonyx. 

Evolution, 17:194-197, 1963 509 

KooPMAN, K. F., and P. S. Martin 

Subfossil mammals from the Gomez Farias region and the tropical 
gradient of eastern Mexico. Jour. Mamm., 40:1-12, 1959 513 

FiNDLEY, J. S., and S. Anderson 

Zoogeography of the montane mammals of Colorado. Jour. 

Mamm., 37:80-82, 1956 525 

Jones, J. K., Jr., and T. E. Lawlor 

Mammals from Isla Cozumel, Mexico, with description of 

a new species of harvest mouse. Univ. Kansas Publ., 

Mus. Nat. Hist., 16:411-419, 1965 528 

Davis, W. B. 

Relation of size of pocket gophers to soil and altitude. 

Jour. Mamm., 19:338-342, 1938 537 

Davies, J. L. 

The Pinnipedia: an essav in zoogeography. Geographical 

Rev., 48:474-493, 1958 .' 542 

Hagmeier, E. M. 

A numerical analysis of the distributional patterns of 

North American mammals. II. Re-evaluation of the provinces. 

Syst. Zool., 15:279-299, 1966 562 



Literature Cited 583 



READINGS IN 
MAMMALOGY 



INTRODUCTION 

The overall unity of the different fields of science and of other aspects of 
human experience, or at least their interdependence, is evident in both theory 
and practice. Nevertheless, this is an age of specialization. The sheer volume 
of information, the current rate of increase in knowledge, the changing and 
often elaborate techniques that must be learned, and human limitations all 
have contributed to the production of specialties. 

A definition of the specialty of mammalogy as "all scientific study of mam- 
mals" is too broad, for that definition encompasses, for example, all parts of 
animal physiology in which any mammal, such as a white rat in the laboratory, 
may happen to be used. It also would include much of medical practice, 
because humans are mammals. Generally speaking, those scientists who call 
themselves mammalogists are interested in the mammal as an animal — as an 
organism — not just as a specific case of some more general phenomenon, be it 
the nature of life or the nature of the nerve impulse. For example, a physiolo- 
gist who is interested in comparative studies between different mammals or in 
the function of a physiological process as an adaptive mechanism may regard 
himself as a mammalologist. A physiologist who studies one kind of laboratory 
animal and is interested in explaining a process in terms of progressively sim- 
pler mechanisms rarely will regard himself as a mammalogist. Both types of 
study, of course, contribute to biological knowledge. 

Life is best comprehended in terms of four basic concepts: first, that 
biology, as all of science, is monistic, assuming one universe in which the same 
natural laws apply to living and non-living things; second, that life is a dynamic 
and self-perpetuating process; third, that the patterns of life change with time; 
finally, that these factors together have resulted in a diversity of living forms. 

Different branches of biology tend to focus or concentrate on different 
concepts. Thus, the above four concepts are focal points, respectively, of ( 1 ) 
physiology and biochemistry, (2) ecology, (3) evolutionary biology, and (4) 
systematic biology. Mammalogy is the study of one systematic group or taxon, 
the Class Mammalia. Studies emphasizing different aspects of mammalian 
biology are evident in our section headings and in the specific papers repro- 
duced. Biology as a whole and mammalogy specifically may be best likened 
to a woven fabric rather than to a series of compartments. 

We feel that a unifying conceptual scheme for "mammalogy" lies in the 
realm of "systematic mammalogy." This scheme is unifying because it includes 
the basis for subsequent study and the only meaningful framework for the 
synthesis of existing knowledge of mammals. On this point, George Gaylord 
Simpson, in introducing his classic The Principles of Classification and a Classi- 
fication of Mammals (1945) wrote (Simpson at that time used the term 
"taxonomy" as we use "systematics" ) : 

"Taxonomy is at the same time the most elementary and the most 
inclusive part of zoology, most elementary because animals cannot be 
discussed or treated in a scientific way until some taxonomy has been 
achieved, and most inclusive because taxonomy in its various guises and 



branches eventually gathers together, utilizes, summarizes, and imple- 
ments everything that is known about animals, whether morphological, 
physiological, psychological, or ecological." 

Knowledge of the identity of any animal studied is essential so that the 
results may be compared with other knowledge about the same kind of animal 
and with the same kind of knowledge about different animals. 

We originally had hoped to develop the history of mammalogy along with 
our other objectives, but when the hard fact of page limitation was faced, 
some selections whose chief justification was historical were sacrificed. In the 
comments beginning each section, some historical information helps place the 
selections in an understandable framework. To attain variety we have 
included papers both of restricted and of general scope; for example, papers 
pertaining to local faunas and continental faunas, to higher classification and 
infraspecific variation, and to contemporary serum proteins and millions of 
years of evolution. 

Every serious student of mammalogy, whether amateur or professional, 
researcher or compiler, writer or reviewer, artist or teacher, must learn to use 
the literature. One does not learn all about mammals because that is impossi- 
ble. One learns what one can, where to look for further information, and, 
more important, how to evaluate what one finds. 

Most of the literature on mammals is in technical journals, a few of which 
are devoted exclusively to mammalogy: Journal of Mammalogy (USA), 
Mammallv (France), Zeitschrift fur Saugetierkunde (Germany), Sauge- 
TiERKLrxDLiCHE MiTTEiLUNGEN (Germany), LuTRA (Benelux countries). Lynx 
(Czechoslovakia), Acta Theriologica (Poland), The Journal of the Mam- 

MALOGICAL SOCIETY OF JaPAN, AuSTR.\LLVN MaMMAL SOCIETY BULLETIN, and 

Bulletin of the British Mammal Society. Also there are the specialized 
Folia Primatologica, an international journal of primatology, founded in 
1963, and a number of serial publications such as Journal of Wildlife Man- 
agement, Bulletin of the Wildlife Disease Association, and journals issued 
by various game departments and conservation agencies that may deal in large 
part, but not exclusively, with mammals. However, much of the published 
information on mammals, as on most aspects of biology, is widely scattered. 
About 40 journals include 50 per cent of the current Hterature, but to cover 70 
per cent, at least 150 journals must be consulted. Articles in the Journal of 
Mammalogy (now more than 800 pages each year) comprise only about 
three per cent of all current titles on mammals, for example. 

Some categories of literature other than journals are books, symposia, 
transactions of various meetings or groups such as the Transactions of the 
North American WildHfe and Natural Resources Conference (the 34th was 
issued in 1969), yearbooks such as the International Zoo Yearbook (the tenth 
was published in 1970), newsletters such as the Laboratory Primate Newslet- 
ter, Carnivore Genetics Newsletter, or Bat Research News, major revisions or 
compilations of special subjects, bibHographies, and abstracts. The chief 
bibliographic sources for mammalogists are the Journal of Mammalogy, 
through its lists of Recent Literature, Saugetierkut>jdliche Mitteilungen, 
through its "Schriftenschau" section, the Zoological Record, published by the 



Zoological Society of London, Biological Abstracts (quite incomplete for 
some branches of mammalogy), and the quarterly Wildlife Review that is 
issued by the U.S. Fish and WildUfe Service (along with the three collections 
of Wildlife Abstracts — a misnomer because only citations are included — 
compiled therefrom and published in 1954, 1957, and 1964); one especially 
useful bibliography to older papers on North American mammals is that com- 
piled by Gill and Coues (in Coues and Allen, 1877). Some individuals and 
institutions maintain records in the form of card files, or collections of sepa- 
rates, or both, over many years for special subjects, special geographic areas, 
or other more general purposes. It is important for the student to remember 
that large-scale faunal reports, catalogues, revisionary works, and the like 
often are valuable as bibliographic sources as well as sources of other informa- 
tion. Some of these reports are mentioned in the introductory remarks to 
several sections. 

An individual who delves into the literature on a particular subject usually 
begins with one or more pertinent recent works and proceeds backward in 
time by looking up publications cited in the later works or found in other 
bibliographic sources. 

An amazing amount of published information on a given subject frequently 
is available to the person willing to look for it. However, paradoxically, there 
is often no pubhshed record for what one might suppose to be nearly common 
knowledge. The questioning mind must return to nature when the Hterature 
holds no answer, exactly what the authors of papers reproduced in this anthol- 
ogy have done. 

A few decades ago only a small number of American colleges and universi- 
ties offered a formal course in mammalogy, and only since about 1950 have 
such courses been widely offered. It is not surprising, therefore, that only 
two textbooks, Cockrum's Introduction to Mammalogy (1962) and Principles 
in Mammalogy by Davis and Golley (1963) have been published in EngHsh. 
The formCT has a systematic orientation and the latter is predominantly eco- 
logical. Some instructors use general works like Recent Mammals of the 
World, A Synopsis of Families (edited by Anderson and Jones, 1967), Mam- 
mals of the World, a three- volume work by Walker et al. ( 1964), or Hamilton's 
( 1939) American Mammals as texts or as references along with other suggested 
readings. Accounts of the mammals of certain states or regions also may be 
used as texts by persons in those places. Other general works of reference 
value are Bourhere's Natural History of Mammals ( 1954), Young's The Life of 
Mammals (1957), Crandall's Management of Wild Mammals in Captivity 
(1964), and the fascicles on mammals in the Traite de Zoologie (edited by 
Grasse, 1955 and later). Two classic general works less readily available are 
An Introduction to the Study of Mammals, Living and Extinct by Flower and 
Lydekker (1891) and Mammalia by Beddard (1902) in the Cambridge Natu- 
ral History series. 

Compact field guides to the mammals of a few parts of the world are avail- 
able, such as those of Burt and Grossenheider ( 1964 ) , Palmer ( 1954 ) , and 
Anthony (1928) for parts of North America, and Van den Brink (1967) for 
Europe. 



The dates in the tvvo preceding paragraphs suggest the recent expansion in 
the volume of work in mammalog)'. Another such measure is membership in 
The American Society- of Mammalogists, which grew from 252 in 1919 to more 
than 3200 in 1969, and half of the growth occurred after 1957. Persons inter- 
ested in mammalog)' are in\ited to appl>- for membership in this society', mem- 
bers of which receive the Journal of Mammalogy. 

Human medicine, veterinary- medicine, animal husbandry, and animal 
physiology (including much work with a comparatiNcly few species of mam- 
mals in the laboratory), all preceded mammalogy as separate disciplines deal- 
ing with mammals. Many of the first mammalogists (as defined here) trained 
themselves in one of these disciplines and some also practiced in fields other 
than mammalogy. C. Hart Merriam, who founded the U.S. Biological Survey, 
studied medicine, as did E. A. Mearns, who N\Tote on mammals of the Mexican 
boundary (1907). Harrison Allen %\Tote much of his first review of North 
American bats ( 1864 ) while on furloughs from duty as a surgeon in the Union 
army in the Ci\il War. Mammalogy continues to interact %\ith the above- 
mentioned fields to their mutual benefit. 

Another largely separate but partly overlapping field that flowered slightly 
later than mammalogy is genetics. We have included no papers on mammalian 
genetics as such, although the rele\ance of genetics is evident in some of our 
selections. A recent book on Comparative Genetics of Coat Color in Mammals 
by Searle (1968) contains about 800 references, including some fascinating 
works on species other than the oft-studied mouse (Mus musculus). 

Our six groupings of papers are somewhat arbitrary. Ecology is as closely 
allied to physiology or zoogeography as to behaxior, and anatomy could as well 
have been placed with development as with physiology. The present arrange- 
ment as to the sequence of sections and the contents of sections seems to be 
about as convenient and useful as any other, and that is the extent of our expec- 
tations. We imply no hierarchy of subdisciplines. 

In selecting works to be included here, we have, in addition to the consider- 
ations already noted, sought papers in which different kinds of mammals were 
compared, and in which different approaches, styles, and methods of presenta- 
tion were used. Individual papers often pertain to more than one area of study. 
In fact, we favored papers that illustrated the rele\ance of different disciplines 
and methods of study to each other. Perhaps the reader will be able to ap- 
preciate our moments of anguish as the final selections w-ere made for this 
anthology. 

Our introduction for each section is brief. We hope that our comments aid 
the reader in considering ( 1 ) some historical aspects that make the papers 
more meaningful, (2) the major areas of study and some major concepts that 
the papers illustrate, (3) the existence of related Hterature, to which we can 
only call attention by citing a few examples, and (4) the continuous transfer 
of ideas, methods, and results from one worker to another, from one field of 
science to another, and between science and other fields of human endeavor. 



SECTION 1— SYSTEMATICS 

A sound classification provides the necessary framework upon which other 
knowledge about mammals can be built. In order to classify organisms, it 
first is necessary to know their similarities and differences; in other words, 
structures and their functions need to be observed, described, and compared, 
and taxa need to be recognized and named before a useful and meaningful 
classification can be constructed. The field of study relating to classification 
frequently is called "taxonomy," although the broader term "systematics" is 
also widely used and is preferred by us. 

Prior to the first decade or so of the 20th century, the practice of mamma- 
Han taxonomy generally was based on a "hit-or-miss" typological approach, 
which, although it fostered considerable advancement in cataloguing the 
faunas of the world, was limited in perspective and potential. The develop- 
ment of evolutionary thought and the spectacular growth of genetics have led 
to the "new systematics," the biological species concept of today, as discussed 
in detail in such syntheses as Huxley (1943), Mayr et al. (1953), Simpson 
(1961), and Mayr (1963 and 1969), among others. Blackwelder's (1967) 
recent text in taxonomy also is deserving of mention here. 

Technological advances in the means of collecting, preparing, and storing 
specimens resulted in the accumulation of series of individuals of the same 
species (the invention of the break-back mouse trap might be mentioned here 
along with the relatively recent widespread use of mist nets for capturing bats ) 
and thus in turn allowed for assessment of variations within and between 
populations. Sophisticated studies of intergradation, hybridization, and the 
cenospecies concept in the past few decades are examples of results from tech- 
nological and conceptual advances in this area. 

To imply that all early taxonomic treatments of mammals were either 
inconsequential or poorly conceived would be a gross error. Pallas' (1778) 
revision of rodents, for example, was a monumental work far advanced for its 
day, as were many other outstanding contributions by 18th and 19th century 
mammalogists that could be mentioned. Nevertheless, one has only to compare 
the descriptions and accounts of Pallas with those found in papers reprinted 
here by Merriam, Handley, and Hoffmeister and de la Torre to appreciate the 
tremendous revolution in systematic practice. It is of interest to note that the 
80-year-old paper by Merriam still is valid with reference to the specific status 
of grasshopper mice. The short contribution by J. A. Allen not only provides 
an example of a review, but deals in some detail with two substantial revision- 
ary works published at the turn of the century. Among the larger modern 
revisionary studies that might be recommended to the student are those of 
Osgood (1909), Jackson (1928), Hooper (1952), Pearson (1958), Lidicker 
(1960), and Packard (1960). Ellerman's (1940, 1941, 1948) well organized 
review of living rodents and Hill's ( 1953 and subsequent volumes ) somewhat 
more rambling and less critical coverage of the primates are also noteworthy 
as attempts to summarize selected bodies of knowledge of important groups of 
mammals. 



The goal of scientific nomenclature is to assure that each kind of organism 
has a unique name, and only one name. The International Code of Zoological 
Nomenclature ( latest edition, 1961 ) forms the legalistic framework for dealing 
with nomenclature, both past and present. The presently reprinted paper by 
Hershkovitz points up some of the kinds of nomenclatorial problems faced by 
the systematist. The Code is administered by the International Commission 
on Zoological Nomenclature but, as Blair (1968) pointed out, the Commission 
"has no way of enforcing its decisions, and the burden of holding names to 
conformity with the [Code] falls on the individual worker and on editors of 
scientific pubHcations." 

The emphasis in this section is mostly at the level of species and subspecies 
( for example, the papers by Benson and by Lidicker ) . Higher categories are 
dealt with primarily in Section 5. Attempts over the years by taxonomists to 
standardize techniques and definitions are illustrated by the papers of Thomas 
and Hall. The short essay by Grinnell also bears on this point. 

The final four selections illustrate the application of new techniques and 
concepts to specific taxonomic problems, all of which were clarified in ways 
that might have been impossible otherwise. The treatment by Lawrence and 
Bossert of the problem of the relationships of the red wolf uses standard 
cranial measurements but analyzes them by discriminant analysis, a concep- 
tually simple but computationally difficult statistical technique that has become 
generally applicable only with the development of digital computers. The 
karyological studies reported by Patton and Dingman treat some taxonomically 
interesting and previously confusing gophers in Arizona and enabled the 
authors to extend and refine the tentative conclusions based on other evidence; 
this paper also provides a good example of the careful integration of a new 
systematic approach with ecological and distributional considerations. Sero- 
logical methods have been employed in taxonomic studies for many years, but 
new methods such as the serum protein electrophoresis used by Nadler and 
Hughes are increasing the useful means of approaching systematic problems 
at the biochemical or molecular level. Machado-AlHson's contribution on host- 
parasite relationships illustrates the relevance of taxonomic data from one 
group, in this case ectoparasites, to the taxonomy of a different (host) group, 

bats. 

Many papers in other sections of this anthology touch on systematics in 
one way or another, and the usefulness to the taxonomist of information from 
a variety of sources will be immediately evident to the reader. Two journals 
devoted to the concepts and practices of systematics and in which contributions 
in mammalogy regularly appear are Systematic Zoology and Zeitschrift fur 

ZOOLOGISCHE SySTEMATIK. 



The Museum Conscience 



THE scientific museum, the kind 
of museum with which my re- 
marks here have chiefly to do, 
is a storehouse of facts, arranged acces- 
sibly and supported by the written 
records and labeled specimens to which 
they pertain. The purpose of a scien- 
tific museum is realized whenever some 
group of its contained facts is drawn 
upon for studies leading to publication. 
The investment of human energy in the 
formation and maintenance of a re- 
search museum is justified only in 
proportion to the amount of real 
knowledge which is derived from its 
materials and given to the world. 

All this may seem to be innocuous 
platitude — but it is genuine gospel, 
never-the-!ess, worth pondering from 
time to time by each and every museum 
administrator. It serves now as a 
background for my further comments. 

For worthy investigation based upon 
museum materials it is absolutely es- 
sential that such materials have been 
handled with careful regard for ac- 
curacy and order. To secure accuracy 
and order must, then, once the mere 
safe preservation of the collections 
of which he is in charge have been 
attended to, be the immediate aim of 
the curator. 

Order is the key both to the accessi- 
bility of materials and to the apprecia- 
tion of such facts and inferences as 
these materials afford. An arrange- 



ment according to some definite plan 
of grouping has to do with whole col- 
lections, with categories of specimens 
within each collection, with specimens 
within each general category, with the 
card indexes, and even with the place- 
ment of the data on the label attached 
to each specimen. Simplicity and 
clearness are fundamental to any 
scheme of arrangement adopted. Noth- 
ing can be more disheartening to a 
research student, except absolute chaos, 
than a complicated "system," in the 
invidious sense of the word, carried 
out to the absurd limits reo nmended 
by some so-called "efiiciency expert." 
However, error in this direction is rare 
compared with the opposite extreme, 
namely, little or no order at all. 

To secure a really practicable scheme 
of arrangement takes the best thought 
and much experimentation on the part 
of the keenest museum curator. Once 
he has selected or devised his scheme, 
his work is not done, moreover, until 
this scheme is in operation throughout 
all the materials in his charge. Any 
fact, specimen, or record left out of 
order is lost. It had, perhaps, better 
not exist, for it is taking space some- 
where; and space is the chief cost 
initially and currently in any museum. 

The second essential in the care of 
scientific materials is accuracy. Every 
item on the label of each specimen, 
every item of the general record in 



The Ml'seum Conscience 



the accession catalog, must be precise 
as to fact. Many errors in published 
literature, now practically impossible 
to "head off," are traceable to mistakes 
on labels. Label-writing having to do 
with scientific materials is not a chore 
to be handed over casually to a "25- 
cent-an-hour" girl, or even to the 
ordinary clerk. To do this essential 
work correctly requires an exceptional 
genius plus training. The important 
habit of reading every item back to 
copy is a thing that has to be acquired 
through diligent attention to this 
very point. By no means any person 
that happens to be around is capable 
of doing such work with reliable 
results. 

Now it happens that there is scarcely 
an institution in the country bearing 
the name museum, even though its 
main purpose be the quite distinct func- 
tion of exhibition and popular educa- 
tion, that does not lay more or less 
claim to housing "scientific collections." 
Yet such a claim is false, unless an 
adequate effort has been expended both 
to label accurately and to arrange 
systematically all of the collections 
housed. Only when this has been done 
can the collections be called in truth 
scientific. 

My appeal is, then, to every museum 
director and to every curator responsi- 
ble for the proper use as well as the 
safe preservation of natural history 
specimens. Many species of vertebrate 
animals are disappearing; some are 
gone already. All that the investigator 
of the future will have, to indicate the 



nature of such then extinct species, 
will be the remains of these species 
preserved more or less faithfully, along 
with the data accompanying them, in 
the museums of the country. 

I have definite grounds for present- 
ing this appeal at this time and in this 
place. My visits to the various larger 
museums have left me with the un- 
pleasant and very distinct conviction 
that a large portion of the vertebrate 
collections in this country, perhaps 90 
per cent of them, are in far from satis- 
factory condition with respect to the 
matters here emphasized. It is ad- 
mittedly somewhat difficult for the 
older museums to modify systems of 
installation adopted at an early period. 
But this is no valid argument against 
necessary modification, which should 
begin at once with all the means avail- 
able — the need for which should, in- 
deed, be emphasized above the making 
of new collections or the undertaking 
of new expeditions. The older materials 
are immensely valuable historically, 
often irreplaceable. Scientific interests 
at large demand special attention to 
these materials. 

The urgent need, right now, in every 
museum, is for that special type of cura- 
tor who has ingrained within him the 
instinct to devise and put into opera- 
tion the best arrangement of his 
materials — who will be alert to see and 
to hunt out errors and instantly make 
corrections — who has the museum con- 
science. 

March 29, 1921. 



10 



Vol. XVIII, pp. 191-196 September 2, 1905 

PROCEEDINGS 



OF THE 



BIOLOGICAL SOCIETY OF WASHINGTON 



SUGGESTIONS FOR THE NOMENCLATURE OF THE 

CRANIAL LENGTH INIEASUREMENTS AND OF 

THE CHEEK-TEETH OF MAMMALS. 

BY OLDFIELD THOMAS. 



Although various reasons prevent the general success of such 
a wholesale revolution in scientific terms as is described in 
Wilder and Gage's Anatomical Technology (1882), where the 
many arguments in favor of accurate nomenclature are admira- 
bly put forth, yet in various corners of science improvements 
can be suggested which, if the workers are willing and in touch 
with each other, may be a real help in reducing the inconvenience 
of the loose or clumsy terminology commonly in vogue. 

Two such suggestions, due largely to the instigation of Mr. 
Gerrit S. Miller, Jr., form the subject of the present paper. 

I. Length Measurements of the Skull and Palate. 

In giving the length measurement of the skull, not only do 
different authors at present use different measurements in de- 
scribing the skulls of similar or related animals, but in doing so 
they designate these measurements by terms of which it is often 
difficult or impossible to make out the exact meaning. Such a 
name as ' ' basal length ' ' has I believe been used by one person 
or another for almost every one of the measurements to be here- 

34— Proc. Biol. Soc. Wash., Vol. XVIII, 1905. (191) 



11 



192 



Thomas — Nomenclature of Measurements. 



after defined, and readers are expi'cted to know by heart every- 
thing that the user has ever written on the sul)ject, footnotes 
and all, in order to understand what is meant by the particular 
term employed. Such a state of things has many inconveniences, 
and it is hoped the present communication, if it meets with the 
approval of other workers on the subject, may do a little toward 
putting an end to the existing confusion. 

As long ago as 1894,* Ijy agreeing with Dr. Nehring for the 
definition of the terms ])asal and basilar in our own future writ- 




ings, I made a first step in this direction, and the present is 
an amplification of the principle then adopted. 

All the difficulty has arisen from the fact that both at the 
anterior and the posterior ends of the skull there are two meas- 
urement points, so that there are four different ways in which 
the l)asal length of the skull may l)e taken, and under that 
name some authors have adopted nearly every one of them. 

It is clear that if a definite name be given to each one of the 
four measurements, authors, by using these names, will be en- 
abled to give the measurements they fancy without causing con- 
fusion in the minds of their readers as to their exact meaning. 

*Ann. & Mag. Nat. Hist., Ser. 6, XIII, p. 203. 



12 



Thomas — Nomenclature of Measurements. 193 

The different points are: 

Anteriorly : 1 . Tiik Gnatiiion, the most anterior point of the 

premaxilke, on or near the middle line. 
2. The Henselion, the back of the alveolus of 

either of the median incisors, the point used 

and defined by Prof. ITensel in his cranio- 

logical work. 
Posteriorly: 3. The Basiox, a point in the middle line of the 

hinder edge of the basioccipital margin of 

the foramen magnum. 
4. The Condylion, the most posterior point of 

the articular surface of either condyle. 

A fifth measuring point to })e referred to below is the Pala- 
TioN, the most anti'rior point of the hinder edge of the bony 
palate, whether in the middle line or on either side of a median 
spine. 

Now using these words for. the purposes of definition, I would 
propose>, as shown in the diagram, the following names for the 
four measurements that may be taken between the points above 
defined : — 

1. Basal length, tlie distance from Basion to Gnathion. 

2. Basilar len(;th, the distance from Basion to Henselion. 

3. Condylo-basal lenoth, the distance from Condylion to 

Gnathion. 

4. Condylo-basilar length, the distance from Condylion to 

Henselion. 
In addition there may be: 

5. Gre.\test len(;th, to be taken not further divergent from 

the middle line than either condylion. A long diagonal 
to a projecting bulla or paroccipital process would thus 
be barred . If however the words ' ' between uprights ' ' 
be added the measurement would be between two ver- 
tical planes pressed respectively against the anterior 
and posterior ends of the skull at right angles to its 
middle line. 

6. Upper length, from tip of nasals to hinder edge of occipi- 

tal ridge in middle line. 

The difference between the words basal and basilar, which at 
first seemed trivial and indistinctive, is founded on the use of 



13 



194 Thomas — Nomenrlnture of Measurements. 

the Englisli word ])asal by the older writers, such as Flower and 
others, who used tlie lueasurenient from tlie gnatliion; wliile 
basilai' is an adaptation of tlie German of Hensel and liis school, 
who used the ^' ha.^ilar-lcinge'" from the henselion. These 
names again, coml)ined with condylo-, readily express the points 
which are used hy those who like to adopt tlie condylion as a 
posterior measuring point. 

But further, the association of the ending " al " with a meas- 
urement from the gnathion, and " ilar " with one from the 
henselion, if once defined and fixed, may l)e utilized in a second 
case of similar character. 

The length of tlie l)ony palate is a measurement given hy all 
careful descrihers, hut tlu.' anterior measuring point used is again 
either the gnathion or henselion, doubt as to which is l)eing 
used often nullifying the valu(^ of the measurement altogether.* 
To avoid this doubt T would suggest, exactly as in the other 
case, that the name of the measurement from the gnathion 
should end in " al " and tliat from the henselion in "ilar." 
We should then liave: 

Palatal LE\(/rn, the distance from gnathion to palation. 

Palatilar LEX(iTii, the distance from henselion to palation. 

The indeterminate " palate length " would then be dropped 
altogether. 

II. The Names of the Cheek-teeth of Mammals. 

Although the cheek-teeth of mammals, the molars and pre- 
molars, have l)een studied and written about ever since the birth 
of zoology, no uniform system of naming them has been evolved 
and there is the greatest divergence between the usage of differ- 
ent workers on the subject. In old days all were called molars 
or grinders; tluMi the premolars were distinguished from the 
true molars (although French zoologists, Winge in Denmark, 
and Ameghino in Argentina, continued to use a continuous 
notation for the two sets of teeth combined) and the usual habit 
among zoologists in general was to speak of them individually 
as " second premolar," " third molar," and soon. Even here, 
however, an important difference cropped up owing to Hensel 

* I may explain that in my own descriptions the palate of any given animal has al- 
ways been measnred from tlie same anterior point, gnathion or henselion, as the skull 
itself, this latter being indicated by the use of the words basal or basilar. 



14 



Thomas — Nomenclature of Measurements. 195 

and his school in lu'rnuiny numbering the premolars from be- 
hind forwards, while naturalists of other nations counted from 
before backwards, as with the incisors and molars, a difference 
often productive of fatal confusion. 

Of late years, however, partly owing to an increasing concensus 
of opinion that the seven cheek-teeth of Placentals, four pre- 
molars and three molars, are serially and individually homolo- 
gous with the seven of Marsupials, formerly reckoned as three 
premolars and four molars, many naturalists have again begun 
to think that a continuous numeration might be the best one. 

But the difficulties in the way of its adoption are very great, 
largely owing to the a])sence of any convenient and suitable word 
in English less clumsy than " cheek-tooth," to express a tooth 
of the combined premolar and molar series. To speak of the 
" first cheek-tooth " or of the " predecessor to the fourth cheek- 
tooth " would l)e so retrogressive a step that I am sure no 
one would adopt it. But if instead of trying to find a word 
for the series combined with a numeral to show the position, 
we were to have a name for each tooth, we should get some- 
thing of the immense convenience we have all realized in having 
definite names for the canine and the carnassial teeth, the latter 
name being found of value in spite of the fact that the upper 
and lower carnassials are not homologous with each other. Such 
names might be made from the positions of the teeth if their 
meanings were not so obtrusive as to confuse the minds of per- 
sons who do not readily understand how a tooth should be called 
' ' the second " or " secundus ' ' when it is actually the most an- 
terior of the series. 

Now it fortunately happens that while the Latin terms ' ' pri- 
mus, " " secundus, ' ' etc, , express the serial positions too clearly 
for the convenience of weak minds. Latinized Greek terms have 
just about the right amount of unfamiliarity which would enable 
them to be used as names without their serial origin being too 
much insisted on, IVIoreover, their construction is similar to 
the process we all use in making generic names, and so far as I 
know they have never been previously utilized in zoology. 

Then, after Latinizing the Greek ordinal terms -ptoru^^ etc. 
for the cheek-teeth of the upper jaw, the same modification as 
is already used in cusp nomenclature might be adopted for those 
of the mandible. 



15 



196 



Thomas — Nomenclature of Measurements. 



We should thus have, counting from before backwards: 







UPPER JAW. 


LOWER JAW 


Cheek-tooth 1 


Protus 


Protid 




2 


Deuterus 


Deuterid 




3 


Tritus 


Tritid 




4 


Tetartus 


Tetartid 




5 


Pemptus 


Pemptid 




6 


Hectus 


Hectid 




7 


Hebdonius 


Heljdoniid 



To avoid any doubt, I would expressly allocate these names 
to the permanent teeth of placentals, leaving the names of the 
marsupial teeth to be settled in accordance with their placental 
homologies. 

For the milk teeth a further modification would l;)e available 
by prefixing the syllable Pro- to the names of the respective 
permanent teeth. We could thus for example in the case of a 
third lower milk premolar call it tlie protritid, and so use one 
word instead of foui'. 

Of course I have no supposition that this system would ever be 
frequently or generally used, l)ut I am convinced that in many 
special cases, and particularly in such descriptions and cata- 
logues of isolated teeth as paleontologists often liave to give, it 
might result in considerable convenience and saving of space. 



16 



CRITERIA FOR VERTEBRATE SUBSPECIES, 
SPECIES AND GENERA: THE MAMMALS 

By 

E. Raymond Hall 

University of California, Berkeley, California 

Mr. Chairman, members of the American Society of Ichthyologists and 
Herpetologists, members of the American Society of Mammalogists, and 
guests: We had expected as a speaker at this time one of the senior 
mammalogists who now is unable to attend. I am glad to appear as a 
substitute because the subject under discussion is one in which I am 
especially interested. In these extemporaneous remarks I propose: (1) 
to indicate some steps which I think useful to take in classifying mam- 
malian .specimens as to subspecies; (2) to express my personal views 
as to criteria for subspecies, species, and genera of mammals; (3) to 
illustrate how some of these criteria for subspecies and species may be 
applied to closely related insular kinds of mammals; and (4) to suggest 
a way in which subspecies may disappear without becoming extinct. 

When I undertake to classify mammalian specimens as to subspecies 
or species, or when I present a series to a beginning student for classifica- 
tion, I like to observe the following steps: (a) select for initial, intensive 
study a large series, 30 or more individuals, from one restricted locality; 
(b) segregate these by sex; (c) arrange specimens of each sex from oldest 
to youngest; (d) divide these into age-groups and within a given group, 
of one sex, from one locality, of what is judged to be one species, measure 
the amount of so-called individual variation; (e) with this measurement 
as a "yardstick," compare individuals, and if possible series, comparable 
as to sex and age (and seasons where characteristics of the pelage are 
involved) from this and other localities. The differences found are 
usually properly designated as geographic variations and form the basis 
for recognition of subspecies, which in turn comprise one of the tools used 
by some students of geographic variation. 

As to criteria for the recognition of genera, species and subspecies of 
mammals, it seems to me that if crossbreeding occurs freely in nature 
where the geographic ranges of two kinds of mammals meet, the two 
kinds should be treated as subspecies of one species. If at this and all 
other places where the ranges of the two kinds meet or overlap, no cross- 
breeding occurs, then the two kinds are to be regarded as two distinct, 
full species. The concept of a species, therefore, is relatively clear-cut 

(141) 



17 



142 ANNALS NEW YORK ACADEMY OF SCIENCES 

and precise; the species is a definite entity. Furthermore, if a zoologist 
knows the morphological characteristics diagnostic of the species, he has 
no difficulty in identifying a particular individual as of one species or 
another. In identification of subspecies, difficulty is frequently en- 
countered, especially with individuals which originate in an area of 
intergradation. 

The category next higher than the species, namely, the genus, is less 
definite and more subjective as regards its limits than is the species. As 
the species is the definite, clear-cut starting point for defining subspecies, 
the species is likewise the starting point for consideration of genera. 
Degree of difference is the criterion for a genus. The genus lies about 
midway between the species and the family. Because the limits of the 
family, like those of the genus, are subjective, it follows that the criterion 
for recognition of genera, although precise enough at the lower point of 
beginning, the species, is elastic at the upper end — namely, at the level 
of the family. 

In summary, the criterion for subspecies is intergradation, that for 
species is lack of intergradation, and that for genera is degree of difference. 
These ideas agree in general with the ideas expressed by the previous 
speakers. 

One of the situations in which it is difficult, or impossible, to apply 
these criteria to conditions actually existing in nature is comprised in 
some insular populations. Frequently the populations on two islands 
near each other differ enough to warrant subspecific or possibly specific 
distinction. A means of deciding on specific versus subspecific status for 
these populations is to find on the adjacent mainland a continuously dis- 
tributed, related kind of mammal which there breaks up into subspecies. 
Ascertain the degree of difference between each pair of mainland sub- 
species which intergrade directly. If the maximum degree of difference 
between the insular kinds is greater than the difference between the two 
subspecies on the mainland, which intergrade directly, and greater than 
that between either insular kind and the related population on the nearby 
mainland, the two insular kinds may properly be treated as full species. 
If the maximum degree of difference between the insular kinds is no 
greater than, or less than, the difference found on the mainland between 
pairs of subspecies which intergrade directly, the insular kinds may 
properly be treated as subspecies of one species. In fine, the criterion is 
degree of difference with the limitation of geographic adjacency, rather 
than intergradation or lack of it. 

Now to my fourth point, namely the suggestion that many subspecies 
disappear without becoming extinct. Permit me first to observe that 



18 



HALL: CRITERIA FOR MAMMALS 143 

although species and subspecies seem to have the same kinds of dis- 
tinguishing characters, which appear to be inherited by means of essen- 
tially the same kinds of mechanisms in the germ plasm, there are two 
noteworthy differences between species and subspecies. One already 
implied is that, in a species which is continually distributee! over a given 
area, its characters at the boundaries of its range are sharp, definite, and 
precise. Some of its characters comprised in size, shape and color, at 
any one place are either those of one species or instead unequivocally 
those of some other, whereas the characters of a subspecies, particularly 
at or near the place where two subspecies meet, more often than not are 
various combinations of those of the two subspecies and in many indi- 
vidual characters there is blending. 

Second, through a given epoch of geological time while a species is in 
existence, one or more of its subspecies may disappear and one or several 
new subspecies may be formed. Subspecies, therefore, on the average 
are shorter-lived than species. 

Now the disappearance of subspecies is to be expected on a priori 
grounds if we suppose that new subspecies are formed in every geological 
epoch. There is reason to believe that in the Pleistocene, the epoch of 
time immediately preceding the Recent, there were even more species of 
mammals than there are now. In each of several successively corre- 
sponding periods of Tertiary time before the Pleistocene, probably there 
were as many species as now. Probably too, these species then were 
about as productive of subspecies as species are now. Had even half of 
these subspecies persisted, either as subspecies unchanged or in con- 
siderable part by becoming full species, there would now be an array of 
species and subspecies many times as numerous as actually does exist. 
It is obvious therefore that many disappeared. 

In accounting for this adjustment of numbers of kinds of mammals, I 
have spoken of the disappearance of subspecies rather than of their ex- 
tinction because I can imagine how a species, say, the pocket gopher 
Thomomys townsendii, in the middle Pleistocene with three subspecies 
(geographic races) could have come down to the present by means of 
each of the three subspecies having gradually changed its characters into 
those of one of the three subspecies existing today in the area of northern 
Nevada that I have in mind. In this way, disappearance of subspecies 
living in the Pleistocene has been accomplished, without their having 
become extinct in the sense that the subspecies left no living descendants. 
Of course this has to be true for some of the subspecies of each successively 
preceding epoch if any animals at all persist, but what I wish to empha- 
size is the strong probability that many, perhaps more than 50 per cent, 



19 



144 ANNALS NEW YORK ACADEMY OF SCIENCES 

disappeared thus without actually becoming extinct, when, for example, 
two successive stages of the Pleistocene, south of the ice sheet, are con- 
sidered. In this regard it is pertinent to recall that each of three 
Pleistocene kinds of pocket gophers, Thomomys (probably species tal- 
poides) gidleyi, Thomomys (probably species townsendii) vetus, and 
Thomomys (probably species hottae) scudderi, from a short distance over 
the northern boundary of Nevada, differs from living representatives cor- 
responding to it (several subspecies of one species) in greater width la- 
bially of the individual cheek teeth of the lower jaw. Significant for the 
thesis being defended is the point that each and all of these Thomomys in 
the Pleistocene differed, at least as regards the shape of the teeth, in the 
same way from the three living species which I feel confident are their 
descendants. 

Let us suppose that three hypothetical subspecies of Thomomys 
townsendii in middle Pleistocene time each gradually changed into three 
different subspecies inhabiting about the same areas in upper Pleistocene 
time, and that these in turn were the ancestors of the three subspecies 
living in those same general areas today. A total of nine kinds is thus 
accounted for. At any one time there was geographical intergradation, 
which has reference to horizontal direction. Also there was intergrada- 
tion up through time, which has reference for present purposes to a 
vertical direction. If I had before me all the material necessary to sub- 
stantiate this or a similar case, I would be inclined to recognize nine sub- 
species of one species. This hypothetical case emphasizes the import- 
ance of intergradation, the criterion for subspecies. 

In review : I have mentioned some preliminary steps useful for a person 
to take when he aims to analyze variation in mammals and to establish 
species and subspecies thereon; intergradation is the criterion for sub- 
species and degree of difference is the criterion for genera; degree of 
difference with the limitation of geographic adjacency may be used as 
the criterion for insular populations (the classification of which is doubt- 
ful as between subspecies and species); and, finally, I have sought to 
stress the importance of intergradation as a criterion for subspecies by 
showing how subspecies may disappear without becommg extinct. 



20 



The Nature of Subspecies Boundaries 
in a Desert Rodent and its Implications 
for Subspecies Taxonomy 



WILLIAM Z. LIDIGKER, JR. 



IT SEEMS to me that the wide diversity 
of opinion which exists concerning the 
usefulness of trinomial nomenclature re- 
volves in large measure on the more basic 
issue of whether or not it is possible to 
recognize infraspecific categories which 
reflect genetic relationships. As recently 
pointed out by Sneath (1961), taxonomic 
categories which are not based on rela- 
tionships are thereby rankless and cannot 
logically be included in a taxonomic 
hierarchy. Thus if the subspecies cate- 
gory is used merely as an instrument for 
describing geographic variation in a few 
characters or as a device for cataloging 
geographic variants (as is done by many 
taxonomists), artificial classifications of 
convenience are characteristically pro- 
duced. Such convenience classifications 
usually contain rankless groups (the 
"false taxa" of Sneath) which cannot be 
allocated in the taxonomic hierarchy. This 
is simply because categories based on a 
few arbitrary characters are themselves 
arbitrary, and lead to the objection of 
Brown and Wilson (1954) and others that 
trinomials based on one group of char- 
acters need not bear any relation to those 
based on different traits. Many of the 
same philosophical difficulties apply to 
systems such as that recently proposed 
by Edwards (1954) and Pimentel (1959) 
in which the subspecies would become a 
measure of isolation, by restricting its use 
to completely isolated and "obviously dif- 
ferent" populations. 

If on the other hand studies of infra- 
specific populations are focused on dis- 
covering evolutionary diversity or degrees 
of relationship between the various popu- 



lations, I see no philosophical objection 
to the use of the trinomen. The question 
then reduces to one of the feasibility and/ 
or desirability of searching for such rela- 
tionships, and of deciding what level of 
dissimilarity if any justifies use of the 
formal trinomen. It is primarily these 
two subsidiary questions which are ex- 
amined in this paper, with the frank hope 
that the subspecies can be rescued from 
the rankless limbo of the morph, ecotype, 
and form. If this rescue operation should 
prove successful, attention can then be 
directed to other problems of greater bio- 
logical interest, such as whether or not 
determinations of genetic relationships 
within a species, which are based on 
phenotj^es, can serve as a basis for specu- 
lations on phylogeny. Obviously geogra- 
phic relations would have to be con- 
sidered at this level, but, assuming that 
such information is taken into account, it 
would be highly informative to contrast 
phenetic and phylogenetic subspecies 
classifications. In any case, analyses of 
infraspecific relationships would very 
likely provide valuable clues concerning 
the environmental forces which have in- 
fluenced the development of the existing 
evolutionary diversity. 

In a previous paper (1960) I attempted 
to determine the genetic relationships 
among populations within a species of 
kangaroo rat (Dipodomys merriami 
Mearns, 1890) by a careful analysis of 20 
morphological features. I concluded at 
that time that at least in well-known ter- 
restrial species an attempt to recognize 
relative relationships within a species was 
at least possible. And, at the same time it 



21 



SUBSPECIES BOUNDARIES 



161 



was apparent that (besides the philosophi- 
cal objections already pointed out) the 
subspecies category by itself was com- 
pletely inadequate for describing the 
complex geographic variation occurring 
in that species. It is the raw data from 
this former investigation that I have used 
here to test further the reliability of those 
tentative conclusions. 

The search for relationships among 
populations of the same species implies a 
search for total genetic differentiation (or 
at least its phenotypic manifestations), 
and hence of lineages with partially in- 
dependent evolutionary origins such that 
they have some internal homogeneity and 
their own adaptive tendencies. To detect 
this kind of differentiation it seems impor- 
tant to analyze, among other things, the 
populations occurring at the boundaries 
between differentiating groups, just as in 
the analysis of species relationships it is 
the boundaries between them, or areas of 
sympatry, where the most significant in- 
formation on relationships is to be found. 
This is not to say that information con- 
cerning the regions of greatest divergence 
or adaptive peaks (in this case peaklets) 
of infraspecific populations is not impor- 
tant, but only that such data should not 
be the only source material for taxonomic 
judgments. Thus it is the intent of this 
paper to focus attention on the previously 
all but ignored subspecies boundaries, 
and to examine the nature of these areas 
in Dipodomys merriami as I had pre- 
viously and without the benefit of this 
analysis defined them (Lidicker, 1960). 
Because the determination of these intra- 
specific units was guided in this case by 
a desire to find populations of comparable 
evolutionary relationship, careful scrutiny 
of the intergrading zones between them 
and surrounding areas should be of par- 
ticular interest. Comparisons will also 
be made with levels of differentiation in 
areas in which no subspecies boundary 
was recognized, as well as with one re- 
gion in which species level differentiation 
was postulated to have been reached by 
an island isolate. 



The second and related purpose of the 
paper is to describe a method which helps 
to accomplish the first objective by meas- 
uring total differentiation, or lack of 
similarity, in many diverse characters, 
and hence is proposed as a criterion of 
relationship. But at the same time the 
technique does not require the hard 
working taxonomist to have either access 
to a digital computer or facility with 
matrix algebra. 

The Method 

Most quantitative techniques available 
to the systematist, which concern them- 
selves with determining relationships, 
and hence with similarities as well as dif- 
ferences, either involve the analysis of 
qualitative or discontinuous characters 
and thus are most useful at the species or 
genus level (e.g., Michener and Sokal, 
1957; Lysenko and Sneath, 1959), or in- 
volve calculations sufficiently complex 
(e.g., Williams and Lance, 1958) that they 
are avoided by most practicing systema- 
tists. What seems to be needed is an ad- 
ditional technique which is sufficiently 
adaptable to handle continuously variable, 
as well as discontinuous, characters of 
diverse types (and so is useful in infra- 
specific studies), and which at the same 
time is sufficiently practical that it will be 
widely useful. To this end the following 
proposed method is dedicated. It is not 
intended as a substitute for discriminant 
function analysis (Fisher, 1936; Jolicoeur, 
1959) and related methods which attempt 
to discriminate between previously con- 
ceptualized populations by using combina- 
tions of variables. 

An analysis of relationship should 
ideally compare relative similarities and 
not differences. However, since the num- 
ber of similarities between populations 
within a species is very large, it is much 
easier to measure their differences and 
consider that the reciprocal of the amount 
of difference represents a measure of 
similarity. Thus as the amount of differ- 
ence approaches zero, the reciprocal ap- 



22 



162 



SYSTEMATIC ZOOLOGY 



preaches infinity. The problem then be- 
comes one of summing the amount of 
difference in many diverse characters. To 
do this we must be able to express the 
differentiation for each trait by a pure 
number (no units). Cain and Harrison 
(1958), for example, accomplished this 
by dividing the differences which they 
observed between means by the maxi- 
mum value recorded for each character. 
The resulting ratios, which they called 
"reduced values," express the observed 
differences in terms of a fraction of the 
maximum size of each character. Al- 
though this permits the comparison of 
diversity among traits of different abso- 
lute size, it does not take into account 
either the possibility that various char- 
acters may have different variabilities, 
or the statistical significance of the ob- 
served mean differences. Furthermore, 
maximum size would seem to be a statistic 
of dubious biological importance in con- 
tinuously varying characters. On the 
other hand, all of these important vari- 
ables, the variance of each trait, character 
magnitude, as well as a consideration of 
whether or not mean differences have a 
high probability of representing real dif- 
ferences, are taken into account by ex- 
pressing differentiation as a proportion 
between the observed differences between 
samples and the maximum amount of dif- 
ference expected on the basis of chance 
sampling variation. Only mean differ- 
ences greater than that amount which 
may be due to chance would then be con- 
sidered as real differences. For our pur- 
poses the maximum chance variation ex- 
pected in any comparison can be equated 
to the minimum difference required for 
statistical significance (at any given con- 
fidence level). This minimum significant 
difference (msd) can be calculated in a 
number of ways. One possibility is to 
determine the standard error of the mean 
for each character for each sample. Then 
in comparing two samples for this char- 
acter, 2 SEj +2SF,^_^ = msd. This provides 
a conservative estimate of msd with con- 
fidence limits usuallv well in excess of 



95%. For large studies, however, these 
calculations would be extremely laborious, 
as well as perhaps overly conservative, 
and a short-cut is suggested. 

If we can assume that each quantitative 
character in a given species exhibits a 
characteristic variability throughout its 
range, then calculations would be tre- 
mendously reduced if we were able to de- 
termine the expected or pooled standard 
deviation (5,,) and standard error (Sp_) 
of samples for which say r2>20. Very 
small samples would have to be grouped 
with adjacent samples whenever possible, 
or if necessary either ignored or have 
separate msd-values calculated for them. 
Under these conditions 4sp_represents our 
best estimate of Tusd. Unfortunately con- 
fidence limits cannot be calculated for its 
reliability, although again it is generally 
a conservative estimate. The statistic Sp 
can be conveniently determined by averag- 
ing the weighted variances for several 
samples of adequate size (Hald, 1952: 
395). Note that as the estimate of s^ im- 
proves it approaches the population stand- 
ard deviation (a), and hence is applicable 
to a wider range of sample sizes. Better 
estimates of Sp require knowledge of the 
total number of individuals in each of the 
populations sampled (see Cochran, 1959: 
72), an obvious impossibility in this type 
of problem. In the examples given in this 
paper 45 p. was estimated by using the 
standard deviation of one large sample 
collected near the center of the species' 
range, and by assuming n = 20. This ex- 
pediency seemed justified because of the 
close similarity in values of s calculated 
for a given trait among several samples, 
and because of the likelihood that s ap- 
proaches a under these circumstances. 

Still another method of deriving the 
statistic msd, but one not used in this re- 
port, involves a more laborious, but sta- 
tistically more precise, procedure. The 
confidence limits for the difference be- 
tween any pair of means can be calcu- 
lated (see Dixon and Massey, 1957:128) 
whether or not we assume that we know 



23 



SUBSPECIES BOUNDARIES 



163 



the variance characteristic of each trait 
(s^) or use only the pertinent sample 
variances (sj and s|). For a large study, 
the calculations are very much reduced if 
one can estimate Sp (see above), and per- 
haps even use only samples in which 
n>20. If these simplifications are pos- 
sible, a pair of confidence limits can be 
computed which will be characteristic for 
each trait studied. In either case, one con- 
fidence limit gives us our msd, since mean 
differences greater than this can with a 
known probability be considered real. We 
need not be concerned with the possibility 
that the mean differences are even larger 
than those observed. 

Consider then only those characters in 
which the differences in the mean values 
(Xi— X2) for a given pair of locations 
(samples) are greater than the minimum 
significant differences. Now, divide these 
significant differences in mean values by 
the minimum significant difference char- 
acteristic for that trait (or for that pair 
of samples). This procedure gives us our 
pure number which can be designated as 

di, d.,, dn for successive characters, 

each representing a measure of differen- 
tiation in one character between one pair 
of samples. Having defined the amount 
of differentiation in each character 
in terms of a pure number, we can 
now add these to arrive at an esti- 
mate of total differentiation in the char- 
acters studied (2c?i). In interpreting this 
statistic in any real situation, however, it 
seems apparent that the distance between 
the two samples compared should be 
taken into account. Obviously an amount 
of total differentiation exhibited between 
two samples which are close together geo- 
graphically would be more significant 
than the same amount of differentiation 
between samples geographically distant. 
To compensate for this effect of distance, 
I have divided the total differentiation 
by the distance (in miles) between the 
two samples. The resulting figure, which 
I have called D or the Index of Differen- 



tiation,^ represents the proportion of sig- 
nificant change that occurs between the 
two locations per mile. Then the re- 
ciprocal of D easily gives us our measure 
of similarity between populations. D need 
now only be further divided by the total 
number of characters studied, including 
those of course in which no differentia- 
tion occurred, to arrive at the mean char- 
acter differentiation per mile {MCD/mi.). 

The importance of considering distance 
between samples will depend in large 
measure on the specific problem under in- 
vestigation. Obviously air-line distance 
between samples does not always accu- 
rately reflect the real magnitude of the 
distance or barriers between them. I feel 
that this is not a serious difficulty, how- 
ever, since we are concerned with the 
abruptness of differentiation between ad- 
jacent populations and not with barriers 
per se. Moreover, in some ways D acts as 
a measure of restriction on gene flow, be- 
cause, if distance is kept constant, D will 
tend to increase as gene flow is reduced. 
Another potential difficulty with the dis- 
tance calculation is that it carries the 
assumption that if the two localities be- 
ing compared were actually closer to- 
gether, the amount of total differentiation 
shown would be less. This is not always 
true because not only are there sometimes 
large areas which exhibit very little geo- 
graphic variation, but also there exist un- 
avoidable gaps in specimen collections. 
For these reasons I felt that in the pres- 
ent analysis of D. merriami it was neces- 
sary to consider both 2c?i and B in assess- 
ing differentiation. 

One further complication seems worth 
considering. This concerns variation in 
the direction of change between different 
characters. It seemed to me more signifi- 
cant if one or two characters were found 
to change significantly in a direction op- 
posite to that of the other characters, 
than if they all changed in the same di- 



1 Note that this is in no way similar to the 
"differentiation index" of Kurten (1958) 
which compares growth gradients. 



24 



1G4 



SYSTEMATIC ZOOLOGY 



rection. Thus for each such direction 
change, I arbitrarily added one half the 
(Z-value for that specific character to 2d. 
This also serves to oppose any tendency 
to give too much weight to characters 
which may not be entirely independent in 
their variation, or to those varying allo- 
metrically. Otherwise no allowance has 
been made for differentially weighting 
characters which might be considered to 
have greater phylogenetic importance. 
Presumably this could be readily done, if 
there were some sound basis for making 
such judgments. Sneath ( 1961 ) , however, 
points out some of the dangers inherent 
in attempts to do this, and argues for 
considering each character equally. 

Table 1 summarizes the calculations 
for 2<i, D, and MCD/mi. for one pair of 
localities in southeastern Arizona. Note 
that a value of 3.476 has been included in 
2d for color changes. Ordinarily color 
characters should be quantified so that 
they can easily be added into this scheme. 
Unfortunately in my study, I did not 
quantify in numerical terms the six color 
features analyzed. This necessitated my 
determining when significant changes 
had occurred by reference to the color 
descriptions of each sample. Whenever 
important color changes were found be- 



tween samples, I included in 2d for each 
such change a figure which represented 
the average d-value for all pairs of locali- 
ties in the boundary region under study 
which exhibited the same number of color 
changes as the sample pair being calcu- 
lated. For example, if two samples dif- 
fered in three color features and if the 
average d for all pairs of samples in that 
region which also differed by three color 
features was 1.50, then 4.5 (3 x 1.50) 
would represent the combined value of d 
for the three color traits. Although this 
represents an unfortunate complication, 
it should not detract from the validity of 
the overall method being proposed. 

Figures 1, 2, and 3 show the differentia- 
tion observed in 20 characters in D. mer- 
riami in selected portions of its large 
range. It is important to emphasize that 
these 20 characters were chosen in the 
original investigation (Lidicker, 1960) 
independently of the conclusions of other 
authors concerning what they considered 
important characters in distinguishing 
subspecies. The list thus includes not 
only most of the "taxonomically impor- 
tant" characters of other authors but 
numerous additional features as well. I 
chose for illustration regions which dem- 
onstrate various levels of differentiation 



Table 1 — Calculations for Total Differentlation, the Index of Differentiation, and the 
Mean Character Differentiation per Mile in Dipodomys merriami for a Pair or 
Localities in Southeastern Arizona (Vicinities of the Huachuca and Santa Rita 
Mountains 54 Miles Apart). 



character * 




Xi- 


-Xa(mm.) 


msd 




d. 


hind foot length 

ear length 

basal length of the skull 

cranial length 

rostral width 

1 direction change (ear) 

2 color changes 


1.40 

0.62 

0.54 

0.78 

0.19 

(ids) 
(2Xd for those pairs of 
localities with two color 
changes) 


0.68 
0.52 
0.52 
0.48 
0.06 


2di 
D 

MCD/mi. 


2.059 
1.192 
1.039 
1.625 
3.167 
0.596 

3.476 




= 13.154 
= 0.244 
= 0.012** 



* See Lidicker (1960) for a description of these characters. 
*♦ Total of 20 characters studied. 



25 



SUBSPECIES BOUNDARIES 



165 




>.40(>20) 

>.35(>l5)or>40«20) 
>.25{>IO)or>.35«l5) 
>.20(>IO)or>.25(<IC) 
>.l5{>IO)or>.20{<IO) 
>.IO(>IO)or).l5 (<I0) 
>.05(>5)or>.IO(<IO) 
<.05 or >.05«5) 
.00 (0) 



Fig. 1. Observed diflferentiation of Dipodomys merriami in southeastern Arizona and 
adjacent Mexico and New Mexico. Numbers on the lines connecting the various sample 
localities represent the calculated values for D and in parenthesis Sd,. The key to the 
intensity of stippling is based on these same statistics. The scale associated with each map rep- 
resents a distance of 25 miles. See also the text for a more complete explanation of the figures. 



26 



!6G 



SYSTEMATIC ZOOLOGY 





"^S %_oo'.oQ^' 




Las Vegas 





\ Aguongo 




Fallon X 

Fig. 2. Observed differentiation of D. merriann in a) northern Nevada, b) southern 
Nevada and adjacent Mojave desert of California, and c) small area in extreme southern 
California. For a more complete explanation of the figures and a key to stippling intensity, 
see the text and Figure 1. 



ranging from essentially none to that 
judged to be at the species level. Figure 
1 shows the boundary region between D. 
merriami merriami and D. m. olivaceus 
(nomenclature based on Lidicker, 1960) 
in southeastern Arizona and adjacent 
Mexico and New Mexico. Figure 2 illus- 
trates areas in northern Nevada (a), 
southern Nevada and the adjacent eastern 
Mojave desert of California (b), and fi- 
nally a small area in southern California 
at the boundary of D. m. collinus and D. 
m. arenivagus (c). Figure 3 represents 
the southern tip of the Baja California 
peninsula (a), and southern Sonora 
where the boundary between D. vi. mer- 
riami and D. m. mayensis is found (b). 



The first of these (3a) is of particular in- 
terest as it shows the entire range of D. 
m. melanurus and the adjacent island 
populations of D. m. margaritae and the 
presumed allopatric species D. insularis. 
Notice that the key takes into account 
both D and 2<i (but gives greatest weight 
to D) and is arranged so that increased 
intensity of stippling represents increased 
differentiation. Heavy dashed lines repre- 
sent the locations of previously estab- 
lished subspecies boundaries, and double 
dashed lines previously established spe- 
cies boundaries (see Lidicker, 1960). 
Each drawing also indicates the location 
of one prominent town so that each chart 
can be placed geographically; all are ori- 
ented with north upward. 



27 



SUBSPECIES BOUNDARIES 



167 




Fig. 3. Observed differentiation of D. merriami in a) southern Baja California, and 
b) southern Sonora. For a more complete explanation of the figures and a key to stippling 
intensity, see the text and Figure 1. 



Discussion of the Method 

The method described and its pictorial 
representation as shown in the figures 
gives us a geographically oriented sum- 
mary of statistically significant differen- 
tiation in the characters studied. Its most 
important feature is that it takes into ac- 
count the variability of each character as 
well as its magnitude, and concerns itself 
only with diversity which has a high 
probability of being real. Clearly, the 
more characters examined by the investi- 
gator, the greater will be his chance of 



discovering all of the existing differences 
between populations, and the better will 
be his estimate of genetic diversity. In 
the present case there is a remarkable 
correlation between the subspecies and 
species boundaries as previously de- 
scribed by the author and the bands of 
rapid character changes as defined by the 
Index of Differentiation.- It is clear that 
in this case subspecies boundaries uni- 



2 No particular correlation is evident, how- 
ever, with many of the taxonomic conclusions 
of previous authors. 



28 



168 



SYSTEMATIC ZOOLOGY 



formly appear as relatively narrow zones 
of high levels of differentiation or low 
levels of similarity, and, although it can- 
not be determined from the figures, these 
are usually, but not always, in areas of 
partial or complete isolation between pop- 
ulations. If the Index method truly de- 
scribes genetic diversity, then our con- 
fidence is bolstered in the possibility of 
using the subspecies category for char- 
acterizing infraspecific lineages. 

Besides the degree of differentiation, 
other suggested criteria for the recogni- 
tion of such lineages include the following 
considerations: 1) the continuity of the 
zone of differentiation; 2) diversity of the 
two postulated adaptive peaks; 3) differ- 
ences in the environments to which the 
adjacent populations are adapted, or con- 
sideration of the possibility that the two 
populations are adapted to the same en- 
vironment in a different way; 4) geologic 
or paleontologic evidence of separate evo- 
lution. Moreover, it would seem to be a 
simple matter to devise modifications of 
the Index of Differentiation so as to in- 
corporate discontinuous and qualitative 
characters. This would extend the useful- 
ness of the method, not only to infraspe- 
cific populations which differ by such 
characters, but also to the species level. 
However, above the infraspecific level the 
problems of convergence, giving different 
weight to different characters (that is 
identifying primitive or generalized char- 
acters), and correlated characters (see 
especially discussions by Cain and Harri- 
son, 1960) are aggravated. It might be 
added in passing, however, that these 
sources of error are not so great a prob- 
lem as might be expected, because the 
proposed method emphasizes large num- 
bers of characters and overall similarities. 
Under these circumstances a few con- 
vergent or pleiotropic traits would alter 
the results very little. Moreover, the 
problem of differentially weighting char- 
acters often leads into circular arguments 
as pointed out by Sneath (1961). 

Although the proposed method incor- 
porates a number of compromises with 



mathematical sophistication, I think that 
it is sufficiently accurate to be of consid- 
erable utility to the practicing taxono- 
mist. Furthermore, several modifications 
are suggested for improving precision if 
this seems appropriate. The method will 
not of course make any decisions for the 
investigator, as it should not, but it will 
give him additional objective criteria on 
which to base his decisions. The fact that 
the conclusions suggested by the calcula- 
tions and analysis of D's are similar if not 
identical to those proposed without the 
benefit of the method suggests that the 
method does not produce unreasonable 
results, and therefore must not suffer un- 
duly from its lack of statistical elegance. 

Discussion of Results 

An obvious, but important, conclusion 
derived from a study of the figures is that 
statistically significant differences can be 
found between the vast majority of the 
population pairs. This serves to empha- 
size what is really intuitively obvious, 
namely that the ability to prove that two 
populations are statistically different in 
one or several characters is only a meas- 
ure of the persistence and patience of the 
systematist. To base formal subspecific 
descriptions on this kind of evidence 
seems to me to be almost meaningless as 
well as a contribution to the degradation 
of the subspecies category to the extent 
of losing it as a legitimate member of the 
taxonomic hierarchy. Furthermore, this 
is precisely the philosophy which usually 
seems to nurture the widespread empha- 
sis on naming with its often accompany- 
ing neglect of relationships, which has 
stimulated so much critical comment (see 
for example Wilson and Brown, 1953, and 
Gosline, 1954). 

The description of differentiation pro- 
vided in the figures carries the further im- 
plication that all levels of differentiation 
are found in D. merriami, and no obvious 
dividing line between subspecies and non- 
subspecies, and species for that matter, is 
thereby indicated. The method thus gives 



29 



SUBSPECIES BOUNDARIES 



169 



US information regarding how different 
(or similar) populations are, but does not 
tell us which ones we should call subspe- 
cies. This finding is consistent with cur- 
rent concepts of intraspecific variation, 
and permits the systematist to decide 
what degree of relationship has phylo- 
genetic significance for the particular or- 
ganism involved, and finally what level, 
if any, he wants to recognize with formal 
subspecies descriptions. In the present 
example subspecific boundaries are found 
to be usually associated with continuous 
bands of differentiation characterized by 
D-values greater than 0.15. 

The fact that this study has failed to 
reveal some biologically meaningful divi- 
sion marking the subspecies level does 
not mean of course that some such divi- 
sion will not be possible in the future. 
However, such a line of demarcation is 
obviously not a prerequisite to the success 
of the proposed method, which only con- 
cerns recognition of degrees of evolution. 
Nevertheless, one possible criterion for 
such a division which occurs to me is the 
relationship between the observed gene 
flow between two adjacent populations 
and that amount expected on the basis of 
the extent of physical contact existing 
between them. If the observed gene flow 
turned out to be less than that expected, 
or discriminating in terms of what genes 
were allowed to flow, this would serve as 
an indication that partially independent 
lineages were involved. This idea would 
not diminish in any way the obvious im- 
portance of geographical barriers in in- 
hibiting gene flow, but merely suggests 
that some day it may be possible to ask 
the question — would a high level of differ- 
entiation persist between two geograph- 
ically partially isolated populations if the 
barrier were reduced or eliminated? Or 
to put it in another way, how much re- 
duction in the physical barrier between 
them can these two populations resist be- 
fore gene flow becomes free flowing? This 
genetic concept of a subspecies argues 
that there are numerous infraspecific pop- 
ulations which by virtue of their past iso- 



lation (not necessarily complete) show 
some inhibition of gene flow between 
them and their neighbors, which would 
tend to slow down the dedifferentiation 
process. If the geographic isolation is 
current, the argument must be stated that 
such a reduction in gene flow would occur 
if they were not so isolated. This reason- 
ing is merely a corollary of the fact that 
not all attempts by a species for isolation 
and differentiation result in species for- 
mation. There are a number of reasons 
why gene flow might be inhibited in such 
cases, and one of these is interdeme ge- 
netic homeostasis (Lerner, 1954). Other 
factors might be partial ecological or be- 
havioral barriers to free interbreeding. 
Although this suggestion for a biologi- 
cally meaningful subspecies criterion is 
mainly speculative, it seems to me to be 
one possible direction that future develop- 
ments in intraspecific analysis might 
take. The following definition of a sub- 
species is thus perhaps premature, but 
is offered because it is only a slight 
modification of widely used current 
definitions, but yet incorporates the con- 
cept outlined above; at the same time it 
does not commit one to any specific cri- 
teria for the recognition of subspecies. A 
subspecies is a relatively homogeneous 
and genetically distinct portion of a spe- 
cies which represents a separately evolv- 
ing, or recently evolved, lineage with its 
own evolutionary tendencies, inhabits a 
definite geographical area, is usually at 
least partially isolated, and may intergrade 
gradually, although over a fairly narrow 
zone, with adjacent subspecies. This does 
not say that subspecies are "incipient spe- 
cies." It does say that subspecies are 
populations which have made initial steps 
in the direction of species formation, such 
that they might form species if suitable 
isolating conditions should develop, or 
they may be populations which have not 
reached the species level and are dedif- 
ferentiating. Obviously most subspecies 
will not become species, and likewise the 
process of dedifferentiation may become 
relatively stabilized through diverse selec- 



30 



170 



SYSTEMATIC ZOOLOGY 



live pressures on either side of the inter- 
grade zone. 

It seems to me then that the Index of 
Differentiation or some similar device can 
give us an often needed additional cri- 
terion for judging relationship between 
populations. And it is these relative 
relationships that are of primary interest; 
and if used as guide lines to the recogni- 
tion of subspecies will permit the legiti- 
mate retention of this category in the 
taxonomic hierarchy. Such an evolution- 
ary philosophy applied to infraspecific 
analysis has a number of important ad- 
vantages, not least of which is that it 
focuses attention on the speciation proc- 
ess and not on geographic variation per 
se, and thus emphasizes that the steps 
which can lead to species divergence must 
be initiated long before the process is 
actually completed. Other advantages not 
already alluded to include a consistency 
in applying the concept of relationship to 
all taxa and hence justifying to some ex- 
tent the nomenclatorial equivalence of 
species and subspecies, provision of a 
more uniform goal for infraspecific sys- 
tematists, and greater usefulness of sub- 
species to non-taxonomists because of the 
greater nomenclatorial stability and more 
reliable predictability of genetic differ- 
ences in unstudied trails that would 
result. 

There is little doubt that this approach 
will be considered impractical in some 
groups of organisms, but this seems of 
relatively little importance to the present 
discussion. Whereas a technique must be 
usable, no limits should be placed on the 
conceptualization of direction and signifi- 
cance of inquiry. I have confidence that 
systematists are not so unimaginative 
that appropriate procedures will not rap- 
idly follow perception of important and 
necessary goals, as they have already 
done to some extent. Present day taxon- 
omy is fraught with practicality, but is 
nevertheless shaken by criticism as to 
where it is all leading. 



Summary 

A growing dissatisfaction with much 
of what is now subspecies taxonomy and 
the associated indiscriminant use of the 
trinomen has caused many taxonomists to 
re-examine the basic tenets of intraspe- 
cific analysis. This "soul searching" has 
raised the important questions of whether 
or not it is possible or even desirable to 
use the subspecies category as a rankable 
taxon below the species level in the taxo- 
nomic hierarchy and at what level of dis- 
similarity, if any, formal trinomial no- 
menclature becomes appropriate. It is 
argued here that if the subspecies is to be 
preserved from degradation to the level of 
the rankless morphs, ecotypes, and forms, 
it must be based on degrees of relation- 
ship or evolutionary divergence. More- 
over, the determinations of relative ge- 
netic relationships implies an emphasis 
on similarities between the various sub- 
populations comprising a species, as well 
as careful scrutiny of events occurring in 
the boundary regions between them. 
This paper is therefore concerned with 
characterizing some of these postulated 
boundary areas, as well as some areas of 
lesser and greater amounts of differentia- 
tion, in the kangaroo rat Dipodomys mer- 
riami. 

To accomplish this, a method is out- 
lined which serves to sum the observed 
statistically significant differentiation in 
many diverse characters between adja- 
cent populations. In doing this, the 
method takes into account the variability 
and magnitude of each character. The 
estimate of total differentiation thus ob- 
tained can then be divided by the distance 
between the samples being compared to 
give the Index of Differentiation (D). The 
reciprocal of this statistic can also be 
taken as a measure of similarity. The 
Index of Differentiation can be further 
divided by the number of characters 
studied to give the mean character dif- 
ferentiation per mile (MCD/mi.). The 
system involves no complicated mathe- 
matical procedures, and yet contains only 



31 



SUBSPECIES BOUNDARIES 



171 



minor compromises with statistical so- 
phistication. Furthermore it is readily 
adapted to visual portrayal and analysis. 

The results of this analysis demonstrate 
a very close agreement between levels of 
differentiation as determined by the In- 
dex of Differentiation and the taxonomic 
conclusions previously arrived at, when 
an attempt was made to base subspecies 
on the relative relationships among infra- 
specific populations. Under these condi- 
tions subspecies boundaries are uniformly 
characterized by a high level of differen- 
tiation which occurs over a relatively nar- 
row zone, and is usually but not always 
associated with partial or complete isola- 
tion between populations. Moreover the 
analysis has emphasized the nearly ubi- 
quitous occurrence of statistically signifi- 
cant differences between populations, and 
hence of the futility of basing formal sub- 
species on this kind of evidence. And 
finally a continuum of levels of differen- 
tiation was found, ranging from none at 
all to the species level. 

It is concluded from this evidence that 
it is indeed possible to gather evidence 
on the relative relationships of the vari- 
ous portions of a species, and it is sug- 
gested that data of this sort should form 
the foundation for subspecific diagnosis. 
This approach tends to focus attention on 
the speciation process itself instead of on 
geographic variation 'per se. Various other 
advantages of this system are pointed out, 
and speculation is presented concerning 
the possible determination of a biologi- 
cally meaningful division between sub- 
species and lesser categories. 

Acknoivledyments 

1 am greatly indebted to the following 
individuals who have critically read this 
manuscript, but who do not necessarily 
share the views which I have expressed: 
S. B. Benson, N. K. Johnson, 0. P. Pear- 
son, F. J. Sonleitner, and C. S. Thaeler. 
The figures were prepared by G. M. 
Christman nf the Museum of Vertebrate 
Zoolog}'. 



REFERENCES 

Brown, W. L., Jr., and E. 0. Wilson. 1954. 
The case against the trinomen. System. 
Zool., 3:174-176. 

Cain, A. J., and G. A. Harrison. 1958. An anal- 
ysis of the taxonomist's judgment of affin- 
ity. Proc. Zool. Soc. London, 131:85-98. 
1960. Phyletic weighting. Proc. Zool. Soc. 
London, 135:1-31. 

Cochran, W. G. 1959. Sampling techniques. 
John Wiley, New York. 

Dixon, W. J., and F. J. Massey, Jr. 1957. In- 
troduction to statistical analysis. McGraw- 
Hill, New York. 

Edwards, J. G. 1954. A new approach to infra- 
specific categories. System. Zool., 3:1-20. 

Fisher, R. A. 1936. The use of multiple meas- 
urements in taxonomic problems. Ann. Eu- 
genics, 7:179-188. 

GosLiNE, W. A. 1954. Further thoughts on 
subspecies and trinomials. System. Zool., 
3:92-94. 

Hald, a. 1952. Statistical theory with engi- 
neering applications. John Wiley, New 
York. 

Jolicoeur, p. 1959. Multivariate geographical 
variation in the wolf, Canis lupus L. Evolu- 
tion, 13:283-299. 

Kurten, B. 1958. A differentiation index, and 
a new measure of evolutionary rates. Evo- 
lution, 12:146-157. 

Lerner, L M. 1954. Genetic homeostasis. 
Oliver and Boyd, London. 

Lidicker, W. Z., Jr. 1960. An analysis of in- 
traspecific variation in the kangaroo rat 
Dipodomys merriami. Univ. California 
Pubis. Zool., 67:125-218. 

Lysenko, O., and P. H. A. Sneath. 1959. The 
use of models in bacterial classification. 
Jour. Gen. Microbiol., 20:284-290. 

Mearns, E. a. 1890. Description of supposed 
new species and subspecies of mammals, 
from Arizona. Bull. Amer. Mus. Natur. 
Hist., 2:277-307. 

Michener, C. D., and R. R. Sokal. 1957. A 
quantitative approach to a problem in classi- 
fication. Evolution, 11:130-162. 

Pimentel, R. a. 1959. Mendelian infraspecific 
divergence levels and their analysis. Sys- 
tem. Zool., 8:139-159. 
Sneath, P. H. A. 1961. Recent developments 
in theoretical and quantitative taxonomy. 
System. Zool., 10:118-139. 
Williams, W. T., and G. N. Lance. 1958. 
Automatic subdivision of associated popu- 
lations. Nature, 182:1755. 
Wilson, E. O., and W. L. Brown, Jr. 1953. 
The subspecies concept and its taxonomic 
application. System. Zool., 2:97-111. 

WILLIAM Z. LIDICKER, JR. is Assistant 
Curator of Mammals at the Museum of Verte- 
brate Zoology and Assistant Professor in the 
Department of Zoology at the University of 
California, Berkeley. 



32 



Vol 62, pp. 11-12 March 17, 1949 

PROCEEDiNCS 

OF THE 

BIOLOGICAL SOCIETY OF WASHINGTON 

GENERIC NAMES OP THE FOUR-EYED POUCH 
OPOSSUM AND THE WOOLLY OPOSSUM (Didelphidae) 

By Philip Hershkovitz 



Published opinions on the status of Philander Tiedemann 
(Zoologie, vol. 1, p. 426, 1808) are not convincing for lack of 
evidence that the work cited had been carefully studied or 
even consulted. Tiedemann 's system of classification is Lin- 
naean with names for all hierarchies recognized (orders, 
families, genera, species) properly proposed and, for his time, 
adequately diagnosed. The following abstract from the "Zoo- 
logie" exposes the nature of the name Philander. 

p. 426] Geschlecht 1. 

Opossum. Philander (Didelphys L.) 

(Sarigue) 

[Generic description follows] 

p. 427] [Description continued] 

Es gibt gegen 10 bekannten Arten: 

1) Das Virginische Opossum. P. virginianus (Did. opossum L.) 
(le sarique Buff. T. X. p. 279.) 

Korper rothlich braun. Ueber jedem Auge ein gelblieh 

weiser Flecken. Sehwanz so lang als der Leib. 

1 Fuss und 3 Zoll lang ohne den Sehwanz. 

In Virginien, Mexico, Peru u. s. w. 

Schreb. tab. 146, A. B. 

Edw. Tyson Carigueya seu marsupiale Americanum or tho 

anatomy of an opossum. Philos. Transact. V. 1698. p. 105, 

V. 1704, p. 1576. 

William Cowper an account of the anatomy of those parti 

of a male opossum that differ from the female. Ibid. V. 

1704. p. 1576. 

2) Das mausartige Opossum P. murinus (Did. murina L.) (la 
marmose Buff. T. X. p. 335.) 

p. 428] [Specific description follows] 

3) Das kurzgeschwanzte Opossum. P. brachyurus (Did. 
brachyuros Penn.) (le touan Cuvier Tabl. Element, d'hiat. 
nat. p. 125.) 

[Specific description follows] 

The above three species are all that were included in the genua 
PMlander. It is perfectly clear from the description and the references 
to Buffon, Linnaeus and Schreber, that the first species P. virginianus 
is merely a new name for the four-eyed pouch opossum, Didelphis 
opossum Linnaeus. The second species is a Marmosa, the third a Mono- 
delphis. As P. virginianvs is virtually tautonymic, it is here designated 

5— Proo. Biol. Soc. Wash., Vou 62, 1949 (U) 



33 



12 Proceedings of the Biological Society of Washington 

genotype of Philander Tiedemann, Designation of the woolly opossum, 
Didelphis philander Linnaeus, as genotype by Thomas (Catalogue of the 
Marsupialia and Monotremata in the collection of the British Museum, 
p. 336, 1888) is untenable. In reality, the Philander of Thomas and sub- 
sequent authors is the homonym Philander Burmeister 1856, with type 
Didelphis philander Linnaeus. 

Arguments presented by Allen (Bull. Amer. Mus. Nat. Hist., vol .13, 
pp. 188-189, 1900) against usage of Philander Tiedemann stem from a 
misunderstanding of the original composition of the genus and are not 
relevant. Nevertheless, Allen's substitution of his own Cahiromys {D. 
philander Linnaeus type) for Philander authors (not Tiedemann), is 
accidentally valid. Tate's (Ibid., vol. 76, p. 164, 1939) rejection of 
Philander Tiedemann is based primarily on the misidentification of P. 
virginianus as a Didelphis, and secondarily on the "homonymity" with 
Philander Brisson, 1762. This last in spite of the fact that Tate (op. cit. 
p. 161) listed Philander Brisson as an unavailable synonym of Meta- 
chirops Matschie! With all due respect for Tate's doubtful endorsement, 
Brisson 's system of classification is non-Linnaean and merits no con- 
sideration. Furthermore, it already has been shown by Hopwood (Proc. 
Zool. Soc. London, vol. 117, p. 533, 1947), that Brisson 's generic names 
are pre-Linnaean and unavailable in any case. Hopwood (op. cit. p. 
635) erred, however, in naming " Didelphys philander Linnaeus" the 
genotype of Philander Tiedemann. In addition, he disinterred Philander 
Gronovius, 1763, with the same genotype designated. Names by Grono- 
vius are no better than those of Brisson and need not be revived at 
this late date (c/. Opinion 89, International Commission on Zoological 
Nomenclature). 

To avoid the possibility of future confusion, disposition must be made 
of two other and unused generic names each with several species includ- 
ing those under discussion. Genotype of Gamba Liais (Climats, geol. 
faune et geogr. bot. Bresil, p. 329, 1872) is hero designated Gamba 
palmata Liais (= Chironectes minimus Zimmermann) ; genotype of 
Cuica Liais (loc. cit.) is here designated Cuica murina Liais (= Mar- 
mosa murina Linnaeus). 

Pertinent data presented are summarized in the following synonymies. 
Genus Philander Tiedemann (Four-eyed pouch opossums). 

Philander Tiedemann, Zoologie, vol. 1, p. 426, 1808 (genotype, 
P[hilander] virginianus Tiedemann = Didelphis opossum Linnaeus). 

Metachirops Matschie, Sitz-ber. Gessellseh. naturforsch. Fr. Berlin, 
p. 268, 1916 (genotype, Didelphis opossum Linnaeus). 

Eolothylax Cabrera, Genera Mammalium, (Monotremata, Marsu- 
pialia), Mus. Nac. Cien. Nat., Madrid, p. 47, 1919 (genotype, Didelphis 
opossum Linnaeus). 

Genus Caluromys Allen (Woolly opossums). 

Philander Burmeister, Erliiuterungen Fauna Brasiliens, p. 74, Berlin 
1856 (genotype, Philander cayopollin Burmeister — Didelphis philander 
Linnaeus; homonym of Philander Tiedemann, 1808). 

Caluromys Allen, Bull. Amer. Mus. Nat. Hist., vol. 13, p. 189, 1900 
(genotype, Didelphis philander Linnaeus). 

Micoureus Matschie, Sitz-ber. Gesellsch. naturforsch. Fr. Berlin, pp. 
259, 269 (genotype, Didelphis laniger Desmarest = D. lanata Olfers; 
homonym of Micoureus Lesson, 1842). 

Mallodelphys Thomas, Ann, Mag. Nat. Hist., ser. 9, vol. 5, p. 195, 1920 
(substitutp name for Micoureu.t Matschie). 



34 



REVIEWS OF RECENT LITERATURE. 

ZOOLOGY. 

Two Important Papers on North-American Mammals. — The 

literature relating to recent work on North-American mammals is so 
scattered, and the results have been the outcome of investigations 
by such a number of different workers, and based on such varying 
amounts of material, that it is a great gain when a competent author- 
ity on any given group can go over it and coordinate the efforts of 
his predecessors in the light of, practically, all of their material, 
combined with a vast amount in addition. In other words, the 
monographic revision of any of the larger genera of North-American 
mammals by an expert is a distinct advance, for which all mammalo- 
gists may well feel grateful. It is with pleasure, therefore, that we 
call attention to two recent contributions of this character — Mr. 
Vernon Bailey's " Revision of American Voles of the Genus JNIicro- 
tus," and Mr. W. H. Osgood's " Revision of the Pocket Mice of the 
Genus Perognathus." 

Mr. Bailey's revision ^ of the American voles, or meadow mice, is 
" based on a study of between five thousand and six thousand speci- 
mens from more than eight hundred localities, including types or 
topotypes of every recognized species with a known type locality, 
and also types or topotypes of most of the species placed in syn- 
onymy." With such material at command, and with a wide experi- 
ence with the animals in life, and personal knowledge of the actual 
conditions of environment over a large part of the range of the group, 
Mr. Bailey has had peculiar advantages for his work, and his results 
are subject to revision only at points where material is still deficient, 
or from some other point of view. This revision, while obviously 
not final, presents a new starting point for future workers, and is 
likely to be a standard for many long years to come. 

The little animals here treated are the short-tailed field mice, 

1 Revision of American Voles of the Genus Microtus. By Vernon Bailey, 
Chief Field Naturalist, Division of Biological Survey, U. S. Department of Agri- 
culture. Prepared under the direction of Dr. C. Hart Merriam, Chief of the 
Division. North Americafz Fauna, No. 17, pp. I-8S, with 5 plates and 17 text- 
figures. Issued June 6, 1900. 

221 



35 



2 22 THE AMERICAN NATURALIST. [Vol. XXXV. 

familiarly typified by our common " meadow mice " of the Eastern 
States. The group is divisible into several well-marked subgenera, 
formerly generally known under the generic term " Arvicola," which 
has had to give way to the less known but older term "Microtus." 
The group is especially distinctive of the northern hemisphere north 
of the tropics, and is found throughout North America from the 
mountains of Guatemala and southern Mexico northward, increasing 
numerically, both in species and individuals, from the south north- 
ward till it reaches its greatest abundance in the middle and colder 
temperate zones, again declining thence northward to the Arctic 
coast. They are vegetable feeders, and often do considerable dam- 
age to trees and crops ; they are active in the winter, forming long 
burrows or tunnels under the snow ; they are also very prolific, breed- 
ing several times a year, young being found throughout the warmer 
months. 

The seventy species and subspecies recognized by Mr. Bailey are 
arranged in nine subgenera ; between the extreme forms the differ- 
ences are strongly marked, but the intermediate forms present grad- 
ual stages of intergradation. The subgenus Neofiber, of Florida, 
embracing the round-tailed muskrat, and the subgenus Lagurus, of 
the semi-arid districts of the northwestern United States, present the 
most striking contrast, not only in size but in many other features. 
The former is perhaps the largest known vole, while the latter group 
includes the smallest. 

Mr. Bailey's paper, being a synopsis rather than a monograph, 
leaves much to be desired in point of detail, but is admirable in its 
way, and covers the ground with as much fullness as his prescribed 
limits would permit. Of the twenty-six synonyms cited, it is notice- 
able that thirteen relate to our common eastern meadow mouse, and 
date from the early authors, while two other eastern species furnish 
three others, also of early date. Only six of the remaining ten are 
of recent date, showing that of some fifty-five forms described within 
the last ten years, by nine different authors, forty-eight meet with 
Mr. Bailey's approval. Four of the remaining seven are identified 
with earlier names which for many years have been considered 
indeterminable, but which Mr. Bailey claims to have established on 
the basis of topotypes. 

While he may be correct in these determinations, it would have 
been of interest to his fellow-specialists if he had stated the basis of 
his determination of certain type localities, notably those of Richard- 
son's species, described as from the " Rocky Mountains," or similarly 



36 



No. 41 1 -J REVIEWS OF RECENT LITERATURE. 223 

vague localities. If he has some " inside history " to fall back upon, 
it is only fair that the secret should be made public. 

It may be said further, in the way of gentle criticism, that it is 
hardly fair wholly to ignore such knotty points as the allocation of a 
few names which he omits, since they form part of the literature 
of the subject, as, for example, Hypudiziis ochrogaster Wagner, Arvi- 
cola noveboracensis Richardson, and some of Rafinesque's names. 
Mr. Bailey describes as new two species and one subspecies. 

Mr. Osgood's " Revision of the Pocket Mice " ^ is an equally wel- 
come contribution, and has been prepared upon much the same lines, 
with equal advantages in the way of material and field experience. 
The pocket mice of the genus Perognathus are confined to a limited 
portion of North America, being found only west of the Mississippi, 
and ranging from the southern border of British Columbia south to 
the valley of Mexico. They are strictly nocturnal and live in bur- 
rows, are partial to arid regions and seem to thrive even in the most 
barren deserts. Their habits are hence not well known, as they are 
very shy and even difficult to trap. They are mouse-like in form, but 
only distantly related to the true rats and mice. Their most obvious 
character is the possession of cheek pouches which open externally. 

The pocket mice vary greatly in size, form, and in the nature of 
their pelage, which may be either soft or hispid ; but between the 
wide extremes there are so many closely connecting links that it is 
difficult to find any sharp lines of division, although two subgenera 
are fairly recognizable. The whole number of forms here recognized 
is 52 — 31 species and 21 additional subspecies, about equally divided 
between the subgenera Perognathus and Chaetodipus. Of these, 
thirteen are here for the first time described. Out of a total of 61 
specific and subspecific names applied to forms of this group, 9 
are relegated to synonymy. Of these 6r names, it is interesting to 
note that 52 date from 1889 or later, and that of these, eight prove 
to be synonyms, three of them having become so through the identi- 
fication of older names thought ten years ago to be indeterminable, 
but since reestablished on the basis of topotypes. 

A previous revision of this group was made in 1889 by Dr. C. 
Hart Merriam, on the basis of less than two hundred specimens — 

1 Revision of the Pocket Mice of the Genus Perognathus. By Wilfred H. 
Osgood, Assistant Biologist, Biological Survey, U. S. Department of Agriculture. 
Prepared under the direction of Dr. C. Hart Merriam, Chief of Division of Bio- 
logical Survey. North American Fauna, No. 18, pp. 1-72, Pis. I-IV, and 15 text- 
cuts. Issued Sept. 20, 1900. 



37 



2 24 ^-^^ ^ M ERICA N NA TURA LIS T. [ V ol. X X X \' . 

all of the material then available — when the number of currently 
recognized forms was raised from six to twenty-one. Dr. Merriam's 
work, however, cleared the way for a better conception of the group, 
rectifying important errors of nomenclature and making known many 
new forms. Mr. Osgood, with fifteen times this amount of material, 
seems to have settled all of the remaining doubts regarding the appli- 
cation of certain early names, and, besides coordinating the work 
of his predecessors, has immensely extended our knowledge of the 
group. The paper is admirable from every point of view and does 
great credit to its author. t_ p^ ^ 



38 



No. 2. NORTH AMERICAN FAUNA. October, 1889. 



DESCRIPTIONS OF TWO NEW SPECIES AND ONE NEW SUBSPECIES OF 

GRASSHOPPER MOUSE, 

WITH A DIAGNOSIS OF THE GENUS ONYCHOMYS, AND A SYNOPSIS OF THE SPECIES 

AND SUBSPECIES. 



By C. Haet Merriam, M. D. 



A. DESCRIPTIONS OF NEW SPECIES AND SUBSPECIES. 

ONYCHOMYS LONGIPES sp. uov. 

(Texas Grasshopper Mouse.) 

Type f|5| 9 ad. Merriam Collection. Concho County, Texas, March 11, 1887. 
Collected by William Lloyd. 

Measurements (taken in the flesh by collector).— Total length, 190°"°; 
tail, 48 [this measurement seems to be too short] ; hind foot, 25; ear 
from crown, 13 (measured from dry skin). 

General characters. — Size larger than that of the other known repre- 
sentatives of the genus, with larger and broader ears, and much longer 
hind feet. Ears less hairy than in 0. leucogaster, with the lanuginous 
tuft at base less apparent ; tail longer and more slender. 

Color. — Above, mouse graj-, sparingly mixed with black-tipped hairs, 
and with a narrow fulvous stripe along each side between the gray of 
the back and white of the belly, extending from the fore-legs to the root 
of the tail; under parts white. 

Cranial characters. — Skull longer and narrower than that of 0. leuco- 
gaster (particularly the rostral portion), with much longer nasals, aud a 
distinct supraorbital " bead" running the full length of the frontals and 
there terminating abruptly. The nasals overreach the nasal branch of 
the premaxillaries about as far as in leucogaster. The iucisive foram. 
ina, as in 0. leucogaster, barely reach the anterior cusp of the first 
molar. The roof of the palate extends further behind the last molar 
than in leucogaster, and gives off a median blunt spine projecting into 
the pterygoid fossa. The palatal bones end anteriorly exactly on a line 
2541— No. 2 1 1 



39 



2 NORTH AMERICAN FAUNA. [No. 2. 

with the interspace between the first and second molars. The presphe- 
noid is excavated laterally to such a degree that the middle portion is 
reduced to a narrow bar less than one-third the width of its base. The 
condylar ramus is lower and more nearly horizontal than in leucogaster, 
and the angular notch is deeper. The coronoid process resembles that 
of leucogaster. 

ONYCHOMYS L0:NGICAUDUS sp. nov. 

(Long-tailed Gkasshoppeu Mouse.) 

Type^sISi ^ a<l- St. George, Utah, January 4, 1889. Collected by Vernon Bailey. 

Measurements (taken in the flesh by the collector). — Total length, 145 j 
tail, 5/) ; hind foot, 20 ; ear from crown, 10 (measured from dry skin). 

General characters. — Similar to 0. leucogaster, but smaller, with longer 
and slenderer tail. Pelage longer, but not so dense. General color 
above, cinnamon-fawn, well mixed with black-tipped hairs. 

Cranial characters. — Skull smaller and narrower than that of 0. leuco- 
gaster; zygomatic arches less spreading ; nasais less projecting behind 
nasal branch of premaxillaries. The coronoid and condylar processes 
of the mandible are shorter, and the coronoid notch is not so deep as 
in leucogaster. The presphenoid shows little or no lateral excavation. 
The incisive foramina do not quite reach the plane of the anterior cusp 
of the first molar. The shelf of the palate projects posteriorly consid- 
erably beyond the molars, and terminates in a nearly straight line with- 
out trace of a median spine. 

ONYCHOMYS LEUCOGASTER MELANOPHRYS subsp. nov. 

(Black-eyed Grasshopper Mouse.) 

Type, lilf (? ad. Kanab, Utah, December 22, 1888. Collected by Vernon Bailey. 

3Ieasure7nents {tnken in the flesh by collector). — Total length, 154; 
tail, 41 ; hind foot, 21. Ear from crown 10 (measured from the dry skin). 

Size of 0. leucogaster. Ear a little smaller. Hind foot densely furred 
to base of toes. Color above, rich tawny cinnamon, well mixed with 
black-tipped hairs on the back, and brightest on the sides; a distinct 
black ring round the eye, broadest above. This ring is considerably 
broader and more conspicuous than the very narrow ring of leucogaster. 

Cranial characters. — Skull large and broad ; very similar to 0. leuco- 
gaster in size and proportions, but with zygomatic arches less spread- 
ing posteriorly, interparietal narrower, nasals not reaching quite so far 
beyond the nasal branch of premaxillaries, and antorbital slit narrower. 
Presphenoid moderately excavated, as in leucogaster. The incisive fo- 
ramina reach past the plane of the first cusp of the anterior molar. The 
condylar ramus is longer and directed more obliquely upward than in 
leucogaster, with the coronoid and infra-condylar notches deeper. 

Note. — In order to render the preceding diagnoses of new forms 
more useful, the following brief descriptions of the skulls of the two 



40 



Oct., 1889.1 REVISION OF THE GENUS ONYCHOMYS. 3 

rdvioas ly knowu species are appended for coinparisou, together with 
figures of the skull of the type of the genus {0. leucogaster): 

Onychomys leucogaster Max. — Skull large and broad, with zygomatic arches spread- 
inf posteriorly. Antorbital slit larger than in the other known species. Palate 
hort, ending posteriorly in a short median spine (see figure). 

Onychomys torridus Coues. — SkuU small , narrow, with zygomatic arches not spread- 
ing, and vault of cranium more rounded than in any other member of the genus. In- 
terparietal relatively large. Nasals projecting far beyond nasal branch of premaxil- 
lary. Incisive foramina very long, extending back to second cusp of first molar. 
Shelf of palate produced posteriorly nearly as far as in longicaudus, and truncated. 
Presphenoid slightly excavated laterally. Mandible much as in longicaudus, but 
with coroaoid process more depressed and condylar ramus more slender. 

B. DIAGNOSIS OF THE GENUS ONYCHOMYS. 

The striking external differences which distinguish the Missouri 
Grasshopper Mouse from the other White-footed Mice of America 
(Hesperomys auct.) led its discoverer, Maximilian, to place it in the 
genus Hypiidceus [=Evotomys^ Coues), and led Baird to erect for its re- 
ception a separate section or subgenus, which he named Onychomys. 
Coues, the only recent monographer of the American Mice, treats Ony- 
chomys as a subgenus, and gives a lengthy description of its characters. 
Since, however, some of the statements contained in this description 
are erroneous, and the conclusions absurd,* and since the most impor- 
tant taxonomic characters are overlooked, it becomes necessary to re- 
define the type. A somewhat critical study of the cranial and dental 
characters of Onychomys in comparison with the other North American 
White-footed Mice has compelled me to raise it to full generic rank. 
It may be known by the following diagnosis : 

Genus ONYCHOMYS Baird, 1857. 

Baird, Mammals of North America, 1857, p. 457 (subgenus). 

Type, HypudoBus leucogaster, Max. Wied, Reise in das innere Nord Amerika, ii, 

1841, 99-101 (from Fort Clark, Dakota). 
Hesperomys auct. 

First and second upper molars large and broad ; third less than half 
the size of the second. First upper molar with two internal and three 
external cusps, the anterior cusp a trefoil when young, narrow, and on a 
line with the outside of the tooth, leaving a distinct step on the inside. 
Second upper molar with two internal and two external cusps, and a 
narrow antero external fold. Last upper molar subcircular in outline, 
smaller than in Hesperomys^ and less indented by the lateral notches. 

* Coues says : " Although unmistakably a true Murine, as shown by the cranial and 
other fundamental characters, it nevertheless deviates much from Mus and Hesper- 
omys, and approaches the Arvicolines. Its affinities with Evotomys are really close." 
(Monographs of North American Rodentia, 1877, p. 106.) As a matter of fact, Ony- 
chomys has no alhnities whatever with Evotomys, or any other member of the Arvico- 
line series, its departure from Hesperomys being in a widely different direction. 



41 



4 NORTH AMERICAN FAUNA. [No. 2. 

Lower molar series much broader than iu Hesperomys, First lower 
molar with an anterior, two internal, and two external cusps, and a 
postero-internal loop. In Hesperomys the anterior cusp is divided, so 
that there are three distinct cusps on each side. Second lower molar 
with two internal and two external cusps, an antero-external and a pos- 
terointernal fold. Third lower molar scarcely longer than broad, sub- 
circular in outline, with the large posterior lobe of Hesperomys reduced 
to a slight fold of enamel, which disappears with wear. 

Coronoid process of mandible well developed, rising high above the 
condylar ramus and directed backward in the form of a large hook 
(see accompanying cut). Nasals wedge-shaped, terminating posteri- 
orly considerably behind the end of the nasal branch of the premaxil- 
laries. 





Fig. 1. Fig. 2. 

1. Lower jaw of Onj/cAomy* Zewco^asJer. 2. Lower jaw of fl'esperojni/a Zewcopw8. 

Body much stouter and heavier than in Hesperomys. Tail short, 
thick, and tapering to an obtuse point. 

Fore feet larger than in Hesperomys ; five tuberculate, as usual in the 
Murine series. Hind feet four-tuberculate, and densely furred from 
heel to tubercles. Tubercles phalangeal, corresponding to the four an- 
terior tubercles of Hesperomys^ that is to say, the first is situated at 
the base of the first digit, the second at the base of the second digit? 
the third over the bases of the third and fourth digits together, the 
fourth at the base of the fifth digit. The fifth and sixth (or metatarsal) 
tubercles of Hesperomys are altogether wanting. 

C. SYNOPSIS OP SPECIES AND SUBSPECIES. 

(1) By External Characters. 

Length, about ISC'"™ ; tail, about 40 ; hind foot, about 21 ; ear from crown, 10. Color 
above, mouse-gray ; black ring around eye inconspicuous 0. leucogaster. 

Size of 0. leucogaster. Color above, rich tawny cinnamon, brightest on the sides; 
black ring round eye conspicuous 0. leucogaster melanophrya. 

Length, about 145™™ ; tail, about 55; hind foot, 20; ear from crown, 10. Color above, 
cinnamon fawn 0. longicaudus. 

Length, about 190™"'; tail, about 50; hind foot, 25; ear from crown, 13. Color 
above, mouse-gray, with a narrow fulvous stripe along the sides 0. longipes. 

Length, about 135™™; tail, about 45; hind foot, 20; ear from crown, 10. Color 
above, uniform dull tawny cinnamon; no black ring around the eye. Tail thick 
with a dark stripe above reaching three-fourths its length ; rest of tail white. 

0. torridiiJi. 



42 



Oct., 1889.] 



Palate ending 
posteriorly 



REVISION OF THE GENUS ONYCHOMYS. 5 

(2) By Cranial Characteks. 

th a blunt me- S ^ 'i'stinct supraorbital bead longipea. 

no distinct supraorbital bead leucogaster. 



th a blunt nie-S 
dian spine y 



<> ( skull large and broad melanophrys. 

with straiirht or .. . . ~ • i i i i 

Ifrl tl ' n } I J nosive foramina barely reach plane 

8 ig y CO - "^ skull smaller I of first molar longicaudus. 

and nar- <; 
L rower I incisive foramina reach second cusp 
I of til 



vex edge 

L rower | inci 

' tirst molar torridus. 

Cranial measurements of the known forma of the genua Onychomys 



Basilar length of Hensel (from foramen magnum to incisor) 

Zygomatic breadth 

Greatest parietal breadth 

Interorbital constriction 

Length of nasals 

Incisor to post-palatal notch 

Foramen magnum to incisive foramina 

Foramen magnum to palate 

Length of upper molar series (on alveolte) 

Length of incisive foramina 

Length of mandible 

Height of coronoid process from angle 

Katios to basilar length: 

Zygomatio breadth 

Parietal breadth 

Nasals 

Molar series (on alveolae) 

Incisive foramina 

Foramen magnum to incisive foramen 

Foramen magnum to palate 



O. leucogaster, ; vfplanonhrvo 
Fort Buford, -S^^rte"' 



Dakota. 



Kanab, Utah. 



4418$ 


4419d" 


5393 cT 


5894 cT 


22 


22 


22.3 


21.6 


15 


15.2 


15.4 


1.^5 


12.9 


12.7 


12.8 


12.5 


4.5 


4.5 


5.2 


4.8 


10.8 


11.6 


10.7 


10.7 


12 


12 


11.7 


11.5 


14.7 


14.6 


15 


14.5 


9.7 


10 


10.2 


9.9 


4.5 


4.2 


4.6 


4.8 


5 


5.7 


5 


5 


15.5 


15.8 


15.7 


15.3 


6.5 


7.3 


6.8 


6.8 


68,1 


69 


69 


71.7 


58.9 


57.7 


57.3 


57 


49 


52.7 


47.9 


49.5 


20.4 


ISJ 


20.6 


22 


22.7 


25.9 


22.4 


23.1 


66 


66.3 


67.3 


67 


44 


45.4 


45.7 


45.8 



Longipes, 
Concho 
County, 
Texas, 



23.3 
15.5 
12.2 

4.4 
12.5 
12.4 
15.7 
10.6 

4.4 

5.3 
16 

7.2 

66.6 

52 

52.3 

20 

22.7 

67.3 

45.4 



Basilar length of Hensel (from foramen magnnm to incisor) 

Zygomatic breadth 

Greatest parietal breadth 

Interorbital constriction 

Length of nasals 

Incisor to post-palatal notch 

Foramen magnum to incisive foramina 

Foramen magnum to palate 

Length of upper molar series (on alveolae) 

Length of incisive foramina 

Length of mandible 

Height of coronoid process from angle 

Batios to basilar length : 

Zygomatic breadth 

Parietal breadth 

Nasals 

Molar series (on alveolae) 

Incisive foramina 

Foramen magnum to incisive foramen ., 

Foramen magnum to palate. 



Longicaudus. 
St. George, Utah. 



Torridus, 

Grant 

County, 

N. Mex. 



5895? 



19.3 

13 

11.2 
4.7 

10 

10.5 

13.5 
8.8 
3.8 
4.3 

13.4 
6.2 

67.3 

58 

51.8 

19.6 

22.2 

68.3 

45.5 



5896,/ 5897 cf 



2839 cT 



19.3 


19.4 


13 


18.1 


11.5 


11.2 


4.7 


4.8 


9.5 


9.7 


10.5 


10.4 


13.4 


13.3 


8.7 


8.7 


3.8 


3.8 


4,3 


4 4 


13.5 


13.2 


6.3 


6.2 


67.3 


68 


59.5 


57.7 


49.2 


50 


19.6 


19.5 


22.2 


22.6 


69.4 


68.5 


45 


44.8 



18.5 
12.5 
11.4 
4.2 
9.6 
10 

12.5 
8.5 
3.5 
5 

13.2 
5.8 

67.5 

61.6 

51.8 

18.9 

27 

67.5 

45.8 



43 



PLATE I. 

Figs. 1, 2, 3, 4, and 5, Onychomys leucogaater, $ young. (Skull No. 4422. ) Fort Baford, 
Dakota. 

1. Skull from above, and left under jaw from outside (X 2). 

2. Crowns of left upper molars from below (x 10). 

3. Crowns of left lower molars from above ( X 10). 

4. Crowns of right upper molfirs from the side ( X 10). 

5. Crowns of right lower molars from the side (X 10). 

Figs. 6 and 7, Onychomys leucogaster, $ ad. (No. 5012). Valentine, Nebraska. 

6. Crowns of left upper molars from below ( X 10). 

7. Crowns of left lower molars from above (X 10). 

Figs. 8 and 9, Onychomys longicaudus, $ ad. (No. 5896). St. George, Utah. 

8. Crowns of left upper molars from below (X 10). 

9. Crowns of left lower molars from above ( X 10). 

38 



44 



North American Fauna, No. 2. 



Plate I. 




1-5. Onychomys leucogaster, d j'oung. 
6,7. Onychomys leucogaster, $ adult. 
8, 9. Onychomys longicaudus, d axlult. 



45 



Vol. 79, pp. 83-88 23 May 1966 

PROCEEDINGS 
OF THE 

BIOLOGICAL SOCIETY OF WASHINGTON 



DESCRIPTIONS OF NEW BATS {CHOERONISCUS 
AND RHINOPHYLLA) FROM COLOMBIA 

By Charles O. Handley, Jr. 
U. S. National Museum, Washington, D. C. 

An imperfectly known endemic mammalian fauna is found 
on the Pacific coast and Andean foothills of northwestern 
Ecuador and Colombia and northward into Panama, where it 
crosses to the Caribbean slope and continues into Costa Rica 
and Nicaragua and in some instances even into Mexico. The 
relatives of its endemic species are mostly South American, 
but some are Mexican. Species characteristic of this fauna, 
snch as Carollia castanea, Vampyressa nymphaea, Heteromys 
australis, Oryzomys bombycinus, and Hoplomys gymnurus, 
were among the mammals collected in the course of virological 
studies of the Rockefeller Foundation on the Pacific coast of 
Colombia in 1962 and 1963. In addition there were striking 
new species of Choeroniscus and Rhinophylla. 

1 am grateful to Wilmot A. Thornton, Center for Zoonoses Research, 
University of Illinois, Urbana (formerly at Universidad del Valle, Cali, 
Colombia) for the opportunity to study the Colombian material here 
reported. Richard G. Van Gelder, American Museum of Natural History 
(AMNH); Philip Hershkovitz and J. C. Moore, Chicago Natural History 
Museum ( CNHM ) ; Bernardo Villa-R, Instituto de Biologia, Mexico ( IB ) ; 
Barbara Lawrence, Museum of Comparative Zoology, Harvard University 
(MCZ); J. Knox Jones, Jr., Museum of Natural History, University of 
Kansas (KU); William H. Burt, Museum of Zoology, University of 
Michigan (UMMZ); A. Musso, Sociedad de Ciencias Naturales La Salle 
(LS); and Juhani Ojasti, Universidad Central de Venezuela (UCV) 
kindly permitted me to study comparative material. Specimens in the 
U. S. National Museum are designated by the abbreviation (USNM). 
Studies which led to the following descriptions were supported in part 
by National Science Foundation Grant G-19415. 

All measurements are in millimeters. For definition of cranial mea- 
surements see Handley (1959: 98-99). Capitalized color terms are 
From Ridgway (1912). 

11— Proc. Biol. Soc. Wash., Vol. 79, 1966 (83) 



46 



84 Proceedings of the Biological Society of Washington 

Choeroniscus 

There are few specimens of the poorly known glossophagine genus 
Choeroniscus in collections. The limits of variation in the genus are 
incompletely known (Sanborn, 1954), and until now its separation from 
Choeronycteris has been questionable. A specimen of a new species of 
Choeroniscus from the west coast of Colombia greatly extends knowledge 
of the genus and strengthens its stature as a genus distinct from Choero- 
nycteris. 

Choeroniscus periosus, new species 

Holotype: USNM no. 344918, adult female, alcoholic and skull, 
collected 1 February 1963, by Wilmot A. Thornton, at the Rio Raposo, 
near sea level, 27 km south of Buenaventura, Departamento de Valle, 
Colombia, original niunber 592. 

Etymology: Greek periosus, immense. 

Distribution: Known only from the type-locality. 

Description: Body size large (forearm 41.2; greatest length of skull 
30.3). Dorsal mass effect coloration (after three month's submersion in 
formalin) rich blackish-brown; basal three-fourths orange-brown in dorsal 
hairs; underparts but slightly paler than dorsum. Vibrissae abundant 
and conspicuous on snout and chin. Ears, chin, noseleaf, hps, membranes, 
legs, feet, and fingers blackish. Lancet of noseleaf relatively narrow, with 
three notches on each side near tip, and with prominent vertical median 
ridge on anterior face. Membranous "tongue-channel" on chin im- 
usually well developed, protruding 1.5 mm forward and 2.0 mm up 
from lower lip; dorsal and anterior edges scalloped. Ear short, tip 
rounded, antitragus well defined; tragus spatulate, 3.8 mm long, with 
margins entire ( except for prominent posterior notch opposite anterior 
base), and with anterior edge and posterior basal lobe thickened. Inter- 
femoral membrane broad, naked. Hind legs naked. Calcar shorter than 
foot, not lobed. 

Rostrum longer than braincase; cranium little elevated from basi- 
cranial plane; profiles of rostrum and cranium evenly tapered, without 
sharp angle in between; no orbital ridges or processes; zygoma absent; 
lambdoidal crest low; sagittal crest absent; maxillary toothrows sub- 
parallel; palate relatively broad anteriorly and narrow posteriorly; 
posterolateral margin of palate not notched; postpalatal extension 
parallel-sided, tubular, reaching posterior to level of mandibular fossae; 
mesopterygoid fossa reduced to a straight-sided, V-shaped notch; hamular 
processes greatly inflated and approaching, but not quite touching, 
auditory bullae; basial pits prominent, separated by broad median ridge. 

2 12 3 
Dentition weak. Dental formula -,-,—, — — 30. Upper incisors 

small, vmicuspid; inner upper incisors (P) separated by a space three to 
four times the width of the teeth; larger, outer upper incisor (P) sep- 
arated by somewhat less than its own width from P and from canine. 



47 



New Bats from Colombia 85 

Upper canine with small posterobasal cusp. Upper premolars very nar- 
row; median cusp, particularly of anterior premolar, very little higher 
than weU-defined anterior and posterior cusps. Upper molars with cusps 
greatly reduced; M^ and M- similar in size and shape, M^ slightly 
shorter and broader. Upper premolars widely spaced; molars closer 
together, but not touching. Lower premolars narrow, with well-defined, 
subequal anterior, posterior, and median cusps. Metaconid cusps of 
lower molars enlarged and protoconid cusps reduced; paraconid cusps in 
line with protoconids, not inflected. Anterior lo\\"er premolar close 
behind, but not touching, canine; spaces between premolars great, but 
spaces between P^ and Mi and between other molars, much less. 

Measurements (All external dimensions taken from specimen in alco- 
hol): Total length 62, tail vertebrae 10, hind foot 12, ear from notch 
15, forearm 41.2, tibia 13.3, calcar 7.9. 

Greatest length of skull 30.3. zygomatic breadth 11.0, postorbital 
breadth 4.7, braincase breadth 9.9, braincase depth 7.4, maxillary tooth 
row length 10.8, postpalatal length 7.0, palatal breadth at \P 5.2, pal- 
atal breadth at canines 4.6. 

Comparisons: C. periosus can be distinguished from all other species 
of Choeroniscus by its longer (longer than braincase), more robust 
rostrum; more inflated hamular process; and larger size {e.g., forearm 
41.2 vs. 32.4-36.9; greatest length of skull 30.3 vs. 19.3-24.4; maxillary 
tooth row 10.8 vs. 6.5-9.2). It is allied with the Amazonian species C. 
minor, C. intermedius, and C. inca, and distinguished from the Central 
American and northern South American C. godmani, in having the 
posterolateral margin of the palate unnotched and the craniiun not so 
markedly elevated from the basicranial plane. 

Remarks: With the addition of C. periosus, the genus Choeroniscus 
includes five nominal species. C. periosus is much the largest species; 
C. inca Thomas, C. intermedius Allen and Chapman, and C. minor 
Peters are intermediate in size; and C. godmani Thomas is smallest. 

Choeroniscus is the most specialized of a group of nominal glossopha- 
gine genera which may be characterized briefly as follows: 

Teeth nearly normal pterygoids normal Lichonycteris 

Teeth shghtly reduced pterygoids? Scleronycteris 

Teeth reduced; PM high pterygoids shghtly Hylonycteris 

specialized 

Teeth reduced; PM high pterygoids specialized Choeronycteris 

Teeth greatly reduced; pterygoids greatly speciahzed Choeroniscus 

PM low 

Lichonycteris has 26 teeth and the other genera have 30. 

As here understood, the genus Choeronycteris includes Musonycteris 
harrisoni Schaldach and McLaughlin, which is distinguished from 
Choeronycteris mexicana Tschudi principally by its strikingly elongated 
rostrum and associated modifications in proportions. The disparity in 



48 



86 Proceedings of tJie Biological Society of Washington 

rostral proportions is much greater, however, between Choeroniscus 
godmani and Choeroniscus periosus than between Choeronycteris mexi- 
cana and Choeronycteris harrisoni. Thus, to distinguish C. harrisoni as 
representative of a separate genus tends to obscure relationships in this 
segment of the Glossophaginae. Muson-ycteris should be regarded as a 
synonym of Choeronycteris. 

Specimens examined: Choeroniscus godmani. COLOMBIA: Meta: 
Restrepo, 1 (MCZ). COSTA RICA: Vicinity of San Jose, 3000 ft, 5 
(AMNH). HONDURAS: Cantoral, 1 (AMNH); La Flor Archaga, 2 
(AMNH). MEXICO: Chiapas: Pijijiapan, 50 m, 1 (UMMZ); Guer- 
rero: 1 mi. SE San Andres de la Cruz, 700 m, 1 (UMMZ); Oaxaca: 
16 km ENE Piedra Blanca, 1 (IB); Sinaloa: San Ignacio, 700 ft, 1 
(KU). NICARAGUA: El Realejo, 1 (KU), 2 (USNM). VENEZUELA: 
Boli\'.\r: 38 km S El Dorado, 1 (UCV); Distrtto Federal: Caracas 
(Santa Monica), 900 m, 1 (LS); Chichiriviche, 1 (UCV). Choeroniscus inca. 
BRITISH GUIANA: Kamakusa, 1 (AMNH); Kartabo, 1 (AMNH). 
ECUADOR: Los Pozos, 2 (AMNH). VENEZUELA: Bolivar: Chi- 
manta-tepui, 1300 ft, 9 (CNHM). Choeroniscus intermedins: TRINI- 
DAD: Irois Forest, 1 (AMNH); Maracas, 1 (AMNH), Princesto\\Ti, 1 
(holotype of C. intermedius, AMNH); Sangre Grande, 1 (AMNH). 
Choeroniscus minor. BR.\ZIL: P.ara: Belem, 3 (USNM). PERU: 
Pasco, San Juan, 900 ft, 1 (USNM); Puerto Melendez, above Maranon, 
1 (AMNH). Choeroniscus periosus. COLOMBIA: Valle: Rio Raposo, 
1 (holotype of C. periosus, USNM). Also, numerous specimens of 
Lichonycteris, Hylonycteris, and Choeronycteris (including C. harrisoni). 

Rhisophylla 

The carolliinine genus Rhinophylla has until now been kno\Mi only 
from the basin of the Rio Amazonas and the lowlands of northeastern 
South America (Husson, 1962: 152-153). The sole representative of 
the genus, R. pumilio Peters, has been regarded as closely related to, 
but more speciahzed than, the species of the abundant and widespread 
genus Carollia (Miller, 1907: 147). It is thus rather surprising to find 
in the collection of W. A. Thornton from the west coast of Colombia a 
number of specimens of a striking new species of Rhinophylla that is 
even more strongly differentiated from Carollia than is R. pumilio. 

Rhinophylla alethina, new species 

Holotype: USNM no. 324988, adult male, skin and skull, collected 13 
July 1962, by Wilmot A. Thornton, at the Rio Raposo, near sea level, 27 
km south of Buenaventura, Departamento de \'alle, Colombia, original 
number 172. 

Etymology: Greek, alethinos, genuine. 

Distribution: Known only from the t>3)e-locality. 

Description: Size large for genus (forearm 34.9-37.2 mm). Col- 
oration blackish, darkest anteriorly, paler posteriorly. In holotype, head 
and nape black, shading to Fuscous-Black on rump; underparts varying 



49 



New Bats from Colombia 87 

from black on chin to Fuscous-Black on chest and to Natal Brown on 
abdomen. Another specimen (Univ. del Valle 220) slightly paler: Fus- 
cous-Black anteriorly and Natal Brown posteriorly on dorsum, and 
correspondingly paler on underparts. Hairs of dorsum and abdomen 
sharply tricolor: at mid-dorsum Slate-Black basally, with broad Benzo 
Brown median band; on sides, neck, and shoulders median band pales 
almost to Ecru-Drab and shows through to surface rather prominently. 
Noseleaf, lips, ears, tragis, fingers, forearms, legs, feet, and all mem- 
branes blackish. Fur soft, woolly; legs, feet, interfemoral membranes, and 
basal two-thirds of forearm hairy; interfemoral membrane fringed. Inter- 
femoral membrane narrow ( about 5 mm at base ) ; calcar short ( less than 
length of metatarsals); tibia and forearm stout; pinna with anterior 
margin convex, posterior margin concave, tip blunt, antitragus triangular; 
tragus usually blunt, with upper posterior margin entire or notched; 
lancet of noseleaf longer than broad, upper margins slightly concave; 
horseshoe of noseleaf with median half of base bound to lip; chin orna- 
ment composed of four parts — a central triangular element ( apex down ) , 
a pair of narrow, elongated lateral elements converging ventrally but 
not meeting (their outer margin more or less scalloped), and a small, 
circular median ventral element. 

Skull like that of Rhinophylla pumilio but rostrum shghtly heavier 
( broader and deeper anteriorly ) , and a distinct low sagittal crest present. 

Dentition, with the exception of inner incisors, extremely weak and 

2 12 3 
reduced; formula -=32. Inner upper incisor (P) large, 

adz-shaped, with cutting edge entire; outer upper incisor (P) small, 
featureless. Canine simple, without cingulum or subsidiary cusps. Ante- 
rior upper premolar (P^) small and featureless; posterior upper premolar 
( P* ) almost rectangular, longer than broad, with large median cusp and 
tiny posterior cusp. NP short and M" shorter, almost triangular in occlusal 
shape, each with a single prominent internal cusp (the metacone); 
protocone obliterated; paracone barely indicated in M\ obliterated in M^; 
parastyle and metastyle, particularly the latter, low and weakly devel- 
oped; M^ reduced to a tiny featureless spicule. 

Inner lower incisors (Ii) large, trilobed (occasionally bilobed); I2 
small, unicuspid. Canine simple, without accessory cusps. Premolars 
simple, unicuspid; anterior premolar wider than any succeeding tooth. 
Molars very narrow, tricuspid; anterior and posterior cusps low on Mi 
and M2 and more or less obliterated on Ms. 

Measurements (Extremes in parentheses, preceded by means and 
followed by number of individuals ( only adults included ) . Measurements 
of the total length, ear, and weight were made by the collector in the 
field. All other measurements were made by me in the laboratory. ) : Total 
length $ 55, 58; hind foot $11 (11-11) 4, $ 11 (10-11) 6; ear from 
notch S 15, 16; forearm $ 36.4 (35.5-37.2) 4, $ 35.7 (34.9-36.6) 4; 
tibia 9 12.3 (11.2-12.9) 4, $ 12.0 (11.5-12.5) 4; calcar 2 3.1 (3.0- 
3.5) 4, $ 3.4 (3.3-3.5) 5. Weight $ 12 gm, 16 gm. 



50 



88 Proceedings of the Biological Society of Washington 

Cranial measurements of male holotype: Greatest length of skull 19.5, 
zygomatic breadth 10.7+ ; postorbital breadth 5.3, braincase breadth 8.9, 
braincase depth 7.5, maxillary tooth row length 4.9, postpalatal length 7.2, 
palatal breadth at M" 6.4, palatal breadth at canines 5.1. 

Comparisons: Specimens of R. alethina are slightly larger than speci- 
mens of R. pumilio from the valley of the Rio Amazonas; have the inter- 
femoral membrane narrower; calcar shorter; hind legs stouter; legs, feet, 
and interfemoral membrane ( including posterior margin ) more hairy; 
fur more woolly in texture; and coloration, including that of lips, ears, 
and membranes, darker, more blackish. As noted in the description, the 
skulls of the two species are very similar. However, except for the inner 
incisors, the teeth of R. alethina are smaller and weaker, and the tooth 
rows are shorter than in R. pumilio. R. alethina has cutting edges of V 
and I2 entire rather than notched; P* shorter; cusps of upper molars more 
reduced; and I2, P\ M^, and lower molars notably smaller. 

Aside from its relative R. pumilio, R. alethina is likely to be confused 
only with the Glossophaginae and with Carollia castanea. Its non-exten- 
sible tongue and lack of rostral elongation are sufficient to distinguish 
it from the Glossophaginae. From Carollia castanea it can be distin- 
guished easily by its blacker coloration, narrow, fringed interfemoral 
membrane, hairy legs, simple chin ornament, and smaller, simplified teeth. 
In most of these characteristics R. alethina differs more from the species 
of Carollia than R. pumilio does. 

Specimens examined: Rhinophxjlla alethina. COLOMBIA: Valle 
Rio Raposo, 11 (including the holotype, USNM), 1 (Univ. del Valle). 
Rhinophylla pumilio. BRAZIL: ParA: Belem, 52 (USNM). ECUADOR: 
Boca de Rio Curaray, 2 (USNM). PERU: Pasco: San Juan, 900 ft, 
4 (USNM). 

Literature Cited 

Handley, C. O., Jr. 1959. A revision of American bats of the genera 
Euderma and Plecotus. Proc. U.S. Nat. Mus., 110: 95-246, 
27 figs. 

HussoN, A. M. 1962. The bats of Suriname. Zoologische Vemhande- 
lingen, Rijksmus. Nat. Hist., Leiden, 58: 1-282, 30 pis., 39 
figs. 

Miller, G. S., Jr. 1907. The families and genera of bats. U.S. Nat. 
Mus. Bull. 57, xvii + 282 pp., 14 pis., 49 figs. 

RiDGWAY, R. 1912. Color standards and color nomenclature, iv + 44 pp., 
53 pis. 

Sanborn, C. C. 1954. Bats from Chimanta-tepui, Venezuela, with re- 
marks on Choeroniscus. Fieldiana- Zoology, 34: 289-293. 



51 



BENSON — STATUS OF REITHKODONTOMYS MONTANUS 139 

THE STATUS OF REITHKODONTOMYS MONTANUS (BAIRD) 

By Seth B. Benson 

The status and relationships of Reithrodontomys montanus have been uncer- 
tain ever since this harvest mouse was named and described by Baird in 1855. 
Study of the type specimen, and of specimens collected in the type locality 
of R. montanus, has revealed that all the specimens, except the type itself, are 
examples of the species Reithrodontomys megalotis (Baird). Confusion has 
arisen because these specimens have been mistakenly referred to R. montanus. 

The nomenclatural history is as follows. Baird (1855, p. 355) described 
Reithrodon montanus on the basis of a single specimen collected by a Mr. 
Kreutzfeldt [ = J. Creutzfeldt, botanist of Gunnison's expedition] at "Rocky 
Mountains, Lat. 38°." Later, Baird (1857, p. 450) gave the locality as 
"Rocky Mountains, 39°." Coues (1874, p. 186) listed Ochetodon montanus 
as a questionable species. This he also did later (1877, p. 130), stating 
"The single specimen is too imperfect to permit of final characterization, or 
to enable us to come to any positive conclusion; but if the size and coloration 
it presents are really permanent, we should judge it entitled to recognition 
as a vahd species. At present, however, we regard it with suspicion and are 
unwilhng to endorse its validity." 

This remained the status of the name until Allen (1893, p. 80), after exam- 
ining the type specimen, stated "I have therefore no hesitation in recognizing 
Reithrodontomys montanus (Baird) as a well-marked, valid species, which will 
probably be found to range from the eastern base of the Rocky Mountains 
eastward to middle Kansas." 

WTien Allen (1895) revised the harvest mice the type of montanus was still 
unique. In his treatment of the species (pp. 123-125) he determined the type 
locality to be the upper part of the San Luis Valley in Colorado. He stated 
that "Until this region has been thoroughly explored for 'topotypes' of R. 
montanus, it would be obviously improper to reject this species as unidentifi- 
able or to give the name precedence over R. megalotis for the form here recog- 
nized under that name." 

At this time the species currently recognized as albescens was not known, 
although Allen actually had specimens which he confused with the form now 
known as R. megalotis dychei (see Howell, 1914, p. 31). Subsequently Cary 
(1903, p. 53) described Reithrodontomys albescens from Nebraska, stating 
that the species required "no close comparison with any described Reithro- 
dontomys." Bailey (1905, p. 106) described Reithrodontomys griseus from 
Texas, and remarked that it probably graded into albescens. 

In 1907 Cary visited Medano Springs Ranch in search of topotypes of R. 
montanus. He collected twenty specimens, most of them immature, which 
he identified as montanus. Cary (1911, pp. 108-110), following a manuscript 
of A. H. Howell, regarded R. montanus as a species related to R. albescens and 
R. griseus. He placed albescens as a subspecies of montanus. 



&2 



140 



JOURNAL OF MAMMALOGY 



When Howell (1914) revised the harvest mice, the specimens from the type 
locality of montanus consisted of the type specimen and the specimens col- 
lected by Gary at Medano Springs Ranch. In this revision Howell altered 
his earlier opinions concerning the relationships of montanus. He wrote 
(p. 26) "The species, although combining in a remarkable degree the char- 
acters of the megalotis and albescens groups, seems not to be directly connected 
with either of them. It is perhaps best placed in the megalotis group, but 
seems not to intergrade with any member of it." He pointed out that the 
relationships of the species were yet not clear, since the type specimen did not 
agree with any of the "topotypes" collected by Gary, but instead resembled 
specimens of R. a. griseus from Texas. Because the color of the "topotypes" 
agreed with the original description of montanus, he decided to "consider the 
tj-pe skull aberrant, and to continue to use the name for the form represented 




Fig. 1. Drawings Made from Photographs of Skulls of Harvest Mice. Natural 

Size 

a. Reithrodontomys megalotis subsp., no. 61120, Mus. Vert. Zool., from Medano Ranch, 
15 miles northeast of Mosca, Alamosa County, Colorado. 

b. Reithrodontomys montanus montanus, type specimen, no. 1036/441, U. S. Nat. Mus., 
from upper end of San Luis Valley, Colorado. 

c. Reithrodontomys montanus griseus, no. 58737, Mus. Vert. Zool., from 3 miles north 
of Socorro, Socorro County, New Mexico. 

by the modern series." It might be mentioned here that no specimens of the 
albescens group have as yet been taken near the type locality of montanus. 

In 1933, Miss Annie M. Alexander and Miss Louise Kellogg collected 
harvest mice from several localities in Golorado and New Mexico including 
the type localities of R. megalotis aztecus and R. montanus. Two of the three 
specimens from the Medano Ranch, 15 miles northeast of jMosca, Alamosa 
Gounty, Golorado, were adults similar to adult topotypes of aztecus. The 
third, a young individual, was so much smaller that at first I judged it was of a 
different species. I suspected then that Howell's treatment of montanus was 
the result of confusing two distinct species, one a small form like albescens, the 
other a larger one hke megalotis. The occurrence of two species at this 
locality seemed possible, since albescens occurs with dychei in Nebraska, 
griseus is known to occur with dychei in Kansas, and in 1933 I collected mega- 
lotis and griseus together in the bottom-land of the Rio Grande, three miles 



53 



BENSON — STATUS OF REITHRODONTOMYS MONTANUS 141 

north of Socorro, New Mexico, which is in the same drainage system as San 
Luis Valley. 

At my request the Bureau of Biological Survey loaned me 16 of the speci- 
mens collected by Gary at Medano Ranch. Only one of these was fully 
adult (the one whose skull is figured as montanus in Howell's revision) . Among 
the younger specimens were some which matched the smallest of the three 
specimens collected by Miss Alexander and Miss Kellogg, and the rest formed 
a series approaching the largest specimens. The adult specimen collected by 
Gary is smaller than the other two adults, yet is similar to them in most 
characters. It was obvious that all belonged to a single species. I concluded 
that all the Medano Ranch specimens I had examined were of the species 
currently known as megalotis. It was also obvious that if the type of montanus 
were conspecific with the other San Luis Valley specimens, megalotis would 
become a synonym of montanus, since montanus has priority. 

Through the courtesy of Dr. Remington Kellogg and others in charge of the 
collection of mammals in the United States National Museum, I was granted 
the loan of the type specimens of R. megalotis and R. montanus. After study- 
ing these specimens I reached the following conclusions: (1) The Medano 
Ranch specimens are conspecific with the type of megalotis; (2) the type 
specimen of montanus is specifically distinct from megalotis, and is conspecific 
with albescens and griseus. Some characters in which the type of montanus 
and specimens of griseus (MVZ no. 41192, from Hemphill Go., Texas; no. 
56220, from 44 miles northwest of Roswell, N. M.; and no. 58737, from 3 miles 
north of Socorro, N. M.) differ from megalotis are: smaller size; shorter, more 
depressed rostrum; narrower interorbital space; relatively shorter brain case. 

As a result, megalotis is not a synonym of montanus, and montanus becomes 
the specific name for the species currently known as albescens. Until addi- 
tional specimens of montanus from San Luis Valley are available to allow a 
more thorough appraisal of its characters, it seems best to regard albescens and 
griseus as valid races of montanus, although it is quite likely that griseus may 
become a synonym of montanus. The three races here recognized are : 
Reithrodontomys montanus montanus (Baird) 
Reithrodontomys montanus albescens Gary 
Reithrodontomys montanus griseus Bailey. 

It may be well to remark here that all the available information indicates 
that the species R. montanus is rarely abundant and that it prefers more arid, 
sandier ground than does its relative R. megalotis, although both species may 
be found together. 

The racial identity of the San Luis Valley megalotis has also presented some 
problems. At first I referred them to the race aztecus because some of them 
fell within the range of variation present in specimens from within the 
distributional area assigned to aztecus in Howell's revision. In addition, 
there was so much variation in size in the few adults available to me that I 



54 



142 JOURNAL OF MAMMALOGY 

felt it was possible they did not truly represent the population, and so could 
not serve as a satisfactory basis for the description of a new race. However, 
Mr. Howell, who has restudied the problem with the aid of a greater amount 
of material than was available to me, has concluded that the San Luis Valley 
megalotis represent an unnamed race. He will describe this race in another 
article. 

LITERATURE CITED 

Allen, J. A. 1893. List of mammals collected by Mr. Charles P. Rowley in the San 
Juan Region of Colorado, New Mexico and Utah, with descriptions of new spe- 
cies. Bull. Amer. Mus. Nat. Hist., vol. 5, pp. 69-84. April 28, 1893. 

1895. On the species of the genus Reilhrodontomys. Bull. Amer. Mus. Nat. 

Hist., vol. 7, pp. 107-143. May 21, 1895. 

Bailey, V. 1905. Biological Survey of Texas. U. S. Dept. Agric, North Amer. 
Faima no. 25, 222 pp., 16 pis., 24 figs. October 24, 1905. 

Baird, S. F. 1855. Characteristics of some new species of North American Mammalia, 
collected chiefly in connection with U. S. Surveys of a Railroad route to the 
Pacific. Proc. Acad. Nat. Sci. Philadelphia, vol. 7, April, 1855, pp. 333-336. 

1857. General report upon the mammals of the several Pacific Railroad 

routes. U. S. Pac. R. R. Expl. and Surv., vol. 8, pt. 1, xxxiv + 764 pp., 60 pis. 

Gary, M. 1903. A new Reithrodontomys from western Nebraska. Proc. Biol. Soc. 
Washington, vol. 16, pp. 53-54. May 6, 1903. 

1911. A biological survey of Colorado. U. S. Dept. Agric, North Amer. 

Fauna no. 33, 256 pp., 12 pis., 39 figs. August 17, 1911. 

CouES, E. 1874. Synopsis of the Muridae of North America. Proc. Acad. Nat. Sci. 
Philadelphia, 1874, pp. 173-196. 

1877. No. I. — Muridae, in Coues and Allen, Monog. North Amer. Rodentia 

(= U. S. Geol. Surv. Terr. [Hayden], vol. 9), pp. 481-542. 

Howell, A. H. 1914. Revision of the American harvest mice. U. S. Dept. Agric, 
North Amer. Fauna no. 36, 97 pp., 7 pis., 6 figs. June 5, 1914. 

Museum of Vertebrate Zoology, University of California, Berkeley, California. 



55 



A REVISION OF THE WOOD RAT NEOTOMA STEPHENSl 
By Donald F. Hoffmeister and Luis de la Torre 

Within the last few years, some field guides to mammals of the United 
States have appeared which do not include the wood rat Neotoma stephensi. 
The imphcation is that Neotoma stephensi is not a valid species. Some spe- 
cific characters of Neotoma stephensi were enumerated in the original descrip- 
tion by Goldman in 1905, and its specific distinctness (from Neotoma lepida) 
was reaffirmed by Goldman in 1932. Because of the previous confusion of 
Neotoma stephensi with Neotoma lepida, and even the subsequent confusion 
of the two species following Goldman's review (Jour. Mamm., 13: 59-67, 
1932), it is somewhat understandable that some authors might question the 
validity of stephensi. Even the recently pubhshed work by Hall and Kelson 
(The Mammals of North America, 2: 690, 1959) fails to show the coexistence 
of N. lepida and N. stephensi in parts of their range, a fact which lends addi- 
tional evidence for the distinctness of the two species. With more adequate 
material, and using Goldman's work as a starting point, we have attempted 
to define more clearly the species N. stephensi. 

Many persons have made available, for study, specimens of Neotoma 
stephensi in their collections. We should especially like to thank Richard G. 
Van Gelder, Stanley P. Young, Viola Schantz, Laurence Huey, Seth B. Benson, 
William Z. Lidicker, and William H. Burt. Specimens from the following 
collections have been examined (the abbreviations in parentheses are used 
under Specimens examined): American Museum of Natiural History (AM); 
United States Biological Survey (BS); Grand Canyon National Park Museum 
(GC); San Diego Society of Natural History (SD); University of California, 
Museum of Vertebrate Zoology (UC); University of Illinois, Museum of 
Natural History (UI); University of Michigan, Museum of Zoology (UM). 
Capitalized color terms are from Ridgway ( Color Standards and Color Nomen- 
clature, 1912). All measurements are in millimeters. Under Additional records 
we have included localities from which the species is known but from which 
we have not examined specimens. The Graduate College of the University 
of Illinois has financially aided us in this study. Illustrations were prepared 
by Alice A. Boatright and Harry C. Henriksen of the University of Illinois. 

GENERAL CHARACTERS OF THE SPECIES 

Obvious characters of Neotoma stephensi, which in part are diagnostic, are 
the presence of a semi-bushy tail ( bushier than in all species except N. cinerea ) 
in a medium- to small-sized Neotoma; dusky coloration extending down the 
top of the foot one-fourth to one-third the distance below the ankle; skull 
resembling IV. lepida. A closer study indicates the following characters are 
diagnostic: 

Baculum. — Exclamation-mark-shaped or wedge-shaped (Fig. 1); small, being 
one-fifth or less than the length of the baculum in N. lepida; smaller than in 



56 



Nov., 1960 HOFFMEISTER AND DE LA TORRE— NEOTOMA 477 

any species of Neotoma found in the United States; similar in size and shape 
to that of Neotoma phenax, except not indented along sides and thus not 
"violin-shaped." When everted from the prepuce, the distinctively small size 
of the baculum in N. stephensi is clearly noticeable, and in contrast to the 
condition in Neotoma lepida, N. albigula, and N. mexicana. In one specimen 
of N. s. relicta, the baculum is identical to that in N. s. stephensi. 

Skull. — Teeth: The pattern of M^ together with features of M^ serves to 
distinguish N. stephensi in most cases. In M^, the antero-medial fold is usually 
absent or, if present, is shallow, approaching albigula, never deeply re-entrant 
as in mexicana. In M', the postero-labial fold (Fig. 1) is directed postero- 
mediaUy and "terminates" posterior to the lingual fold. In N. lepida, the 
postero-labial fold (Fig. 1) is directed medially and less posteriorly, nearly 
meeting the lingual fold. In M^ of stephensi, the second loph is usually long 
and narrow, extending diagonally across the tooth (Fig. 1). In this regard, 
it is similar to N. mexicana and N. albigula, but differs from N. lepida in 
which the second loph is usually broad labially and nearly at right angles to 
the long axis of the toothrow (Fig. 2). 

In N. stephensi, the lingual fold of M3 is as deep as or deeper than the 
labial fold (Fig. 2), whereas in N. lepida and N. albigula, the lingual fold is 
shorter than the labial fold. In N. mexicana, both conditions seem to occur. 

Rostrum: The rostrum is narrower than in any other species within the 
range of N. stephensi ( Fig. 3 ) . Generally, the nasals in stephensi are truncate 
posteriorly, rarely sharply pointed as is common in lepida and albigula 
(Fig. 3). The posterior extensions of the premaxillaries seldom expand pos- 
teriorly as in albigula, but are more as in mexicana except that they are longer. 

Interorbital, region: The region between the orbits is broader and less 
depressed than in either lepida, albigula, or mexicana. In some instances, it 
is difficult to distinguish between stephensi and lepida on the basis of this 
character. The supraorbital ridges in stephensi tend to remain lateral as they 
continue forward toward the rostrum, whereas in the other species these 
ridges approach the midUne, ending almost in line with the posterior exten- 
sions of the premaxillaries (Fig. 3). 




second loph ^ » . ^ . 

stephensi 




postero-labial fold 



stephensi iepida lepida 

Fig. 1. — Third upper molar (x6.5) and baculum (x2.4) of Neotoma stephensi and 
Neotoma lepida. 



57 



478 



JOURNAL OF MAMMALOGY 



Vol. 41, No. 4 



Of perhaps lesser diagnostic significance when compared with N. lepida 
are the following skull characters: upper incisors strongly recurved; tubercle on 
outer face of mandible at base of lower incisor hardly noticeable, whereas 
more nearly knoblike in lepida. 

External features. — The bushiness of the tail, particularly the terminal third, 
approaches that of Neotoma cinerea. The tail is far more bushy than in any 
other species within the range of stephensi, and probably exceeds that of 
any wood rat except cinerea. In young stephensi, only a few weeks old, the 
tail already is bushy, and specific recognition is possible on this character. 

On the hind foot, a wedge of dusky-colored hair may extend onto the dorsal 
surface as much as one-third the distance to the base of the toes. In most 
specimens of N. lepida, particularly in those races which are not melanistic, 
the dorsal surface of the foot is whitish, with the dusky color stopping at the 
tarsal region. 

The underparts are suffused with an ochraceous or buffy wash in nearly 
all specimens. In N. stephensi stephensi the throat region also shows this same 
wash, but the region between the forelegs is whitish. In JV. stephensi relicta, 
the wash does not extend onto the throat and thus it is usually white. The 
coloration of the underparts in N. s. stephensi is similar to that in most speci- 
mens of the dark races of IV. lepida, such as monstrabilis and harteri, and is 
thus noticeably different than in the light-colored races of the latter species. 
Where N. lepida occurs within the range of N. stephensi, nearly all specimens 
of lepida have light-colored underparts and thus this character aids in dis- 
tinguishing the two. 



upper molars 



lower molars 






£mi 




stephensi 



lepida 



albigula 



stephensi 



lepida 



Fig. 2. — Occlusal view of right upper molars of Neotoma stephensi, N. lepida, N. albigula, 
and left lower molars of N. stephensi and N. lepida ( x6.5). 



58 



Not;., 1960 



HOFFMEISTER AND DE LA TORRE— NEOTOMA 



479 







Stephens' 



tepida 



albigufa 



mexicona 



Fig. 3. — Dorsal view of anterior part of skull of Neotoma stephensi, N. lepida, N. 
albigula, and N. mexicana ( X 1 ) . 

VABIATION 

Age. — In N. stephensi, we can recognize four groups which include young 
animals, old animals, and two categories between these extremes. These 
groups are based on the degree of eruption and wear of the upper molar teeth. 
We attempted to corroborate this grouping by the use of other characters, 
such as closure of sutures, size and proportion of various parts of the skull, 
and molt, but these proved to be of httle help. Further discussion of the 
younger groups is given under Growth and Reproduction. 

Group 1. Immatures; M^ not erupted or in the process of erupting and 
occlusal surface of posterior loph isolated from that of more anterior lophs. 

Group 2. Young adults; females, at least, sexually mature. Folds of M^, 
as seen laterally, continuing down below alveolus; M^ fully erupted and oc- 
clusal pattern usually complete with posterior loph rarely isolated. 

Group 3. Adults; folds of M^ not extending to alveolus, but to or below 
an arbitrary midpoint between alveolus and occlusal surface. 

Group 4. Old adults; folds of M^ very short and not reaching midpoint 
between occlusal surface and alveolus. Folds may be entirely absent. 

Sexual. — Although there is a size difference between males and females, 
it is less marked in certain age groups. From our sample, we find that in 
Groups 1 and 2, the sexual difference is slight. In Group 3, males usually 
average larger than females in most measurements. For example, in specimens 
from the Hualpai Mountains (65 5, 109 9 ), the Grand Canyon (45 5, 49 2 ), 
and Wupatki (455, 499), the males are larger than the females by per- 
centages ranging from 1 to 13 in most measurements. In all three localities, 
however, the females average larger than the males in length of maxiUary 
toothrow as follows: Hualpai Mountains, 2.3; Grand Canyon, 1.2; Wupatki, 
1.2 per cent. The larger average size of the toothrow in females is also indi- 
cated in specimens from other localities. Group 4 is represented by too few 
individuals to determine sexual differences. Aside from the quantitative dif- 
ferences pointed out, the skull of adult females is characteristically short and 
broad, in contrast to the long and narrower skull of the males. 



59 



480 JOURNAL OF MAMMALOGY Vol. 41, No. 4 

No sexual difference in color was apparent. 

Color. — The color of an "average" specimen consists of a light buff wash 
extending from the chest to the inguinal region. The chest is white, with 
the throat a buffy color with the hair plumbeous basally and buffy-tipped. 
The white of the chest may extend anteriorly to the chin as a median narrow 
stripe. The inguinal area is whitish. 

The coloration of the underparts, including the buffy wash, throat, and 
chest color, in any one population, may be highly variable. For example, 
near Montezuma Well, Yavapai County, Arizona, one specimen has 98 per 
cent of the underparts heavily washed with a dark buff, one has little or no 
buff, and one has no white on the chest and throat. Still other specimens 
from here show varying stages of intermediacy. In other populations, indi- 
viduals can be found that have the throat entirely white, with the basal 
portions of the hairs not plumbeous or gray-colored. The whitish throat is 
"typical" of another, unrelated species — albigula. Such occurrences of "white- 
throatedness" are widely scattered throughout the range of the species, being 
found in populations from the Hualpai Mountains in the northwest to the 
Burro Mountains in the southeast. 

The extreme of this white-throatedness is found in N. stephensi relicta. In 
this race, nearly all individuals, and probably every adult, have white throats. 
Within the race stephensi, certain populations have most of the adults with 
white throats. This is true for the populations at Hilltop, west end of Grand 
Canyon National Park, but is not true for other populations within the Park 
or for most specimens from the Hualpais. The population from the Burro 
Mountains, New Mexico, has all of the specimens white-throated. In general, 
specimens with the entire throat region white have the buffy wash over the 
abdominal region greatly reduced or entirely lacking. Thus most specimens 
of relicta and specimens of stephensi from Hilltop and the Burro Mountains 
lack the buffy wash. 

Variation of the dorsal coloration within a population is less easily observed. 
The geographical variation of this color, within subspecies, is discussed beyond 
and illustrated in Plate I. 

GROWTH AND REPRODUCTIGN 

In the absence of growth data for IV. stephensi, we have been guided by 
previous work in other species of Neotoma, especially in N. albigula from 
Arizona (Richardson, Jour. Mamm., 24: 134, 1943). Although two species 
may well differ markedly in their rate of growth and reproductive patterns 
due to different heredity and different environmental conditions, we have 
used the N. albigula information to put forth tentative conclusions, leaving it 
to future work to prove or disprove the validity of our interpretations. We 
have, thus, assumed that the progress of growth is essentially the same in 
N. albigula from Arizona as it is in IV. stephensi from that area, and that the 
gestation period in N. stephensi is, as in other species, approximately 30 days 



60 



Nov., 1960 



HOFFMEISTER AND DE LA TORRE— NEOTOMA 



481 



in length. From the growth curve of head and body size in N. albigula ( Rich- 
ardson, op. cit.), approximate ages and thus dates of birth were calculated for 
our sample of immature specimens ( Group 1 ) of N. stephensi. Table 1 indi- 
cates the chronological distribution of Group 1 and Group 2 specimens studied, 
and the dates of capture of pregnant and lactating females. 

The near disappearance of Group 1 individuals following the middle of 
August, and the clear increase of Group 2 animals from this time on, strongly 
suggest that Group 2 is a composite group. Group 2 specimens taken in June, 
July and August most likely are young born late in the preceding year, that is, 
in August, September and October. Specimens taken in September and 
October, however, probably represent young of the year, born in the early 
months following the earliest breeding period. 




ian«tK-iXfiiiHi''Wu*'M3SiaMM:A~'-^ %^M* 



PLATE I 

Variation in the intensity of the over-all color in 'Scotoma stephensi. The darkest- 
colored populations are represented by the darkest area; the lightest, by the lightest area. 



61 



482 



JOURNAL OF MAMMALOGY 



Vol. 41, No. 4 



Table L — Bimonthly distribution of Group 1 and Group 2 individuals, ivith dates of 
capture and age of pregnant and lactaiing females 



Date of 
Capture 



Group 1 



Group 2 



Pregnant ? ? 



Lactating ? 9 



April 


16-30 






May 


1-15 


1 


1 




16-31 


1 




June 


1-15 


3 






16-30 


5 


1 


July 


1-15 


6 


8 




16-31 


6 


1 


Aug. 


1-15 


6 


5 




16-30 




3 


Sept. 


1-15 


1 


4 




16-30 


1 


11 


Oct. 


1-15 




11 



Apr. 30 (Group 4) 



June 18 (Group 3) 
July 13 (Group 2) 



Late Sept. 



June 26 ( Group 3 ) 
July 15 (Group 2) 



Aug. 22 (Group 4) 



Using the growth rate of IV. albigula as a guide, the dates of birth of Group 
1 individuals begin in early March, and thus mating must begin early in Feb- 
ruary. The dates of birth appear to form two groups — one including March 
and April, and the other from the middle of May to the middle of July. This 
suggests two litters but, if a litter can follow another in a period of 15 days, as 
has been reported for N. albigula, it is quite possible that IV. stephensi may 
have more than two litters. The usual litter seems to consist of two young, as 
indicated by four cases of pregnant females containing two embryos each. It 
is of interest that one of the pregnant animals taken on 13 July, and a lactating 
female taken 15 July, were clearly of Group 2. The date of capture, in addition 
to the age group of these animals, certainly seems to indicate that females 
reach sexual maturity the second season after birth. These females must have 
been born in the spring or summer of the preceding year. 

HABITAT 

Neotoma stephensi occupies an ecological niche quite distinctive from that 
of Neotoma lepida. In our collecting experience, IV. stephensi is found in 
rocky situations, usually where the rocks are in piles, and usually where there 
are piiions and junipers. Neotoma stephensi is not a cliff dweller, although 
it may be found in the general vicinity of cliffs, but is found where the rocks 
have rolled down and become stacked. However, even though suitable rocks 
may be present, N. stephensi most likely will not be found if piiions and 
junipers are absent. This wood rat is frequently found associated with the 
piiion mouse, Peromyscus truei, the brush mouse, Peromyscus boylii, or the 
cactus mouse, Peromyscus eremicus. 

Within Grand Canyon National Park, Neotoma stephensi is to be found in 
several ecological situations. In the majority of places, N. stephensi was found 
in rocky situations where there were piiion, juniper, scrub oak and cliffrose. 
In these situations, it was usually associated with Neotoma mexicana, but in 



62 



Nov., 1960 HOFFMEISTER AND DE LA TORRE— NEOTOMA 483 

a few cases, with IV. alhigula. In Long Jim Canyon, N. stephensi was in a 
rocky place within the yellow pine forest. At Cedar Mountain, the species 
was at the lowest edge of the pinon-juniper belt. Here, on the rocky, desert 
slopes, there were many cacti and agave plants and only a few straggling 
piiions or junipers. N. stephensi widely overlapped the range of N. albigula 
here. At Hilltop, near the western boundary of the Park, N. stephensi was 
in rocky places decidedly below the piiion-juniper zone and in an area 
where there were sagebrush, Indian paintbrush and grasses. Here, Perog- 
nathus intermedins, Neotoma albigula, Eutamias dorsalis, and even Pero- 
myscus truei and P. hoylii were present. 

In the vicinity of Rimrock and Montezuma Well in eastern Yavapai County, 
Arizona, N. stephensi was found along the fractured limestone outcrop 
extending horizontally near the top of the low mesas. This outcrop was 5 to 
8 feet in height and was fractured along its length into large blocks. N. 
stephensi occurred in the crevices among these blocks, along with many 
Peromyscus eremicus. Rat houses and piles of droppings were evident all 
through the outcrop. About 40 feet below the limestone stratum there oc- 
curred a short dark lava outcrop which was much more finely fractmred. 
Neotoma albigula was found here as well as on the valley floor where it 
lived among the cacti. No N. albigula was taken among the blocks of lime- 
stone where N. stephensi occurred. These field observations made by John S. 
Hall suggest an important difference in the habitat preference of N. stephensi 
and N. albigula, even in areas where these two species are very near to 
each other. 

At the western edge of the range of Neotoma stephensi, in the Hualpai 
Moimtains, it may also occur above the pinon-juniper zone in the scrub oak 
and yellow pine. However, it was taken in rocky situations and in association 
with Peromyscus boylii. 

Occasionally, N. stephensi will desert its preferred rocky habitat and move 
into or under man-made structures. At Pasture Wash, a female with half- 
grown young was living among bales of hay in the loft of an unused bam. 
Near McMillen Mine, individuals had homes under large sheets of building 
material which had been on the ground for a long period of time. 

In New Mexico, according to Bailey (N. Amer. Faima 53: 188, 1931), 
N. stephensi in the Burro Mountains live in "stick nests placed about logs or 
brush, and in places their burrows entered the ground about the bases of 
rocks with many sticks piled about the entrances." Bailey stated that they 
occupy the juniper-piiion plateau region, frequenting rocky places and even 
cliffs. 

Neotoma stephensi Goldman 

Range. — Central Arizona, from Hualpai Mountains on the west to western 
New Mexico on the east, and from McMillenville on the south to extreme 
south-central Utah (Navajo Mountain) on the north (Fig. 4). 



63 



484 



JOURNAL OF MAMMALOGY 



Vol. 41, No. 4 



Diagnosis. — A medium-sized species of Neotoma with a bushy tail (bushier 
than in any other species except IV. cinerea); dusky coloration on dorsal sur- 
face of foot extending from ankle nearly one-third distance to base of toes; 
small baculum, exclamation-mark-shaped (Fig. 1); upper molariform teeth 
with following combination of characters: M^ with antero-medial fold absent 
or poorly developed, and M^ with postero-labial fold and second loph directed 
obliquely (Figs. 1, 2); last lower molar with deep lingual fold as deep or 
deeper than labial fold (Fig. 2); skull broad and flat interorbitally; rostrum 
narrow; nasals truncate posteriorly (Fig. 3). 

Neotoma stephensi stephensi Goldman 

Neotoma stephensi Goldman, 1905, Proc. Biol. Soc. Wash., 18: 32, 2 Feb. 
Neotoma lepida stephensi, Goldman, 1910, N. Amer. Fauna 31: 80, 19 Oct. 
Neotoma stephensi stephensi, Goldman, 1932, Jour. Mamm., 13: 66, 9 Feb. 




Fig. 4. — Distribution of the subspecies of Neotoma stephensi. 



64 



Nov., 1960 HOFFMEISTER AND DE LA TORRE— NEOTOMA 485 

Type.— Adult female, U.S. National Museum (Biol. Surv.), No. 117466, 
from Hualpai Mountains, 6,300 ft., actually at Horse Tank (see Remarks), 
Mohave County, Arizona, collected on 1 July 1902 by Frank Stephens; original 
no. 4192. 

Range. — From the Hualpai, Chemehuevis, and Harquahala mountains in 
western Arizona east along the MogoUon Plateau to the Burro and Gallinas 
mountains in southwestern New Mexico (see map, Fig. 4). 

Diagnosis. — A race showing considerable variation throughout its range 
but possessing the following characteristics: color of dorsum dark, being 
darkest in central Arizona and southwestern New Mexico (Plate I); sides 
above lateral line with narrow fulvous band near Pinkish Buff; nose, fore- 
head and cheeks grayish or plumbeous; hair of throat usually plumbeous 
basally; top of tail appears dark, almost black, because more black hairs and 
few or no white hairs interspersed or show through; size large, as indicated 
by weight in adult males of usually more than 180 grams; skull large, usually 
averaging more in greatest length than 41.2 mm. in adult males; upper tooth- 
row long, usually 8.4 mm. or more; skull with supraorbital ridges frequently 
beaded and heavy. 

Comparisons. — Since there is considerable variation within the subspecies 
stephensi, groups of populations of this race have been compared with the 
relatively homogeneous "population" of relicta. 

From relicta, the race stephensi from the Hualpai Mountains, Hackberry, 
Harquahala Mountains, and Grand Canyon National Park differs as follows: 
darker coloration (but less different than in other populations of stephensi); 
more grayish nose, forehead and cheeks; not "white-throated" except for 
specimens from HiUtop; markedly heavier in weight; broader skull, both 
actually and relatively to its length (especially marked in specimens from 
the Hualpai Mountains); longer toothrow and broader interorbitally (es- 
pecially in specimens from the Hualpais). 

Central Arizona populations (for discussion, see under Remarks) differ 
from N. s. relicta as follows: color markedly darker, both on the dorsum and 
sides; dorsal tail stripe more blackish, less gray; body-weight, length of tooth- 
row, and interorbital width greater, but not so pronounced as in topotypes of 
stephensi from the Hualpai Mountains; differ from relicta in other features 
the same way as do topotypes of stephensi. 

Populations from eastern Arizona and southwestern New Mexico differ 
from N. s. relicta as follows (for discussion, see under Remarks) : color darker, 
including facial region, sides and tail; throat tending to be partially or entirely 
white (in the latter case showing similarity to relicta); externally larger and 
heavier; skull with nasals broad, tending to be bell-shaped anteriorly, but 
constricted posteriorly; ascending arms of premaxillaries broader; differ from 
relicta in other features as do topotypes of stephensi. 

Measurements. — See Tables 2 and 3. 

Remarks. — As mentioned under Comparisons, there is considerable varia- 



65 



486 



JOURNAL OF MAMMALOGY 



Vol 41, No. 4 



Table 2. — External and cranial measurements of "Group 3" male specimens of Neotoma 
stephensi stephensi. Grouped localities are as follows: Western Arizona (Hackberry, 
Hualpai Mts., Lucky Star Mine); Northern Arizona (Grand Canyon); Central Arizona 
(Red Lake, Wupatki area); Southeastern Arizona (McMillenville area, Nantanes Plateau, 
Black River); Western New Mexico (Burley, Burro Mts., Glenwood) 





Western 


Northern 


Central 


Southeastern 


Western 




Arizona 


Arizona 


Arizona 


Arizona 


New Mexico 


Number 


8 


4 


6 


3 


4 


Total length 


301.2 


311.2 


314.0* 


308.3 


298.3* 




283.0-334.0 


305.0-320.0 


303.0-320.0 


302.0-313.0 


290.0-310.0 


Head and body 


173.6 


175.8 


183.2* 


174.0 


169.5" 




161.0-201.0 


172.0-178.0 


171.0-203.0 


165.0-182.0 


165.0-177.0 


TaU 


127.6 


135.0 


132.7* 


134.3 


127.3" 




120.0-135.0 


127.0-144.0 


125.0-138.0 


131.0-137.0 


120.0-133.0 


Hind foot .— 


32.3 


31.5 


32.7 


31.7 


31.6 




31.0-34.0 


29.0-34.0 


32.0-34.0 


31.0-32.0 


30.0-33.0 


Condylobasal length. 


39.5' 


39.7 


40.0 


38.6 


37.3 




37.6-41.5 


39.3-40.1 


37.7-42.5 


37.7-39.3 


36.5-39.2 


Zygomatic breadth ... 


22.r 


21.2 


21.3" 




20.4" 




21.0-23.0 


20.6-21.8 


20.6-21.9 


21.0^ 


20.^-20.8 


Interorbital 


5.7 


5.4 


5.5 


5.5 


5.3 




5.6-6.0 


5.1-5.7 


5.3-6.0 


5.4-5.6 


5.0-5.6 


Breadth of rostnmi . 


6.5 


6.4 


6.1 


6.5 


6.1 




5.9-6.9 


6.3-6.5 


5.9-6.4 


6.2-7.0 


5.6-6.5 


Depth of rostrum ... 


6.8 


6.9 


6.8 


6.7 


6.3 




6.5-7.0 


6.8-7.1 


6.5-7.1 


6.4-7.1 


6.1-6.5 


Nasal 


15.5 


16.0 


16.3 


16.0 


15.1 




15.0-16.2 


15.4-16.8 


15.7-17.5 


15.8-16.3 


14.1-16.8 


Incisive foramen 


9.1 


9.0 


9.5 


8.7 


8.4 




8.8-9.5 


8.8-9.4 


9.0-10.2 


8.2-9.2 


8.0-9.0 


Palatal bridge 


7.6 


7.5 


7.5 


8.1 


7,7 




7.4-7.9 


7.3-7.6 


7.0-7.7 


7.9-8.4 


7.5-7.9 


Maxillary toothrow . 


8.7 


8.3 


8.5 


8.9 


8.6 




8.3-9.3 


8.1-8.6 


7.9-9.0 


8.7-9.2 


8.4-8.8 



tion within the subspecies N. s. stephensi as here delimited. This variation 
can be discussed by grouping the populations into three segments, from (1) 
the Hualpai Mountains, including others from western Arizona and the Grand 
Canyon region, (2) central Arizona, and (3) eastern Arizona and western 
New Mexico. We prefer to describe these three "variants" but not to give 
them names. 

The first group of populations in western Arizona possesses the following 
characteristics: hght color (see Plate I); long toothrow, broad across zygo- 
matic arches, broad interorbitally, yet skull is only of average length; large 
foot, average length of body, and short tail. Within this group of populations, 
those specimens from the type locahty (Hualpai Mountains) have certain 
unique features such as relatively short but broad skulls, long toothrows, broad 
interorbital regions, greater weight, and slightly paler than "average" colora- 
tion for the subspecies. If only topotypes are used for comparison with other 



66 



Nov., 1960 



HOFFMEISTER AND DE LA TORRE— NEOTOMA 



487 



populations of N. stephensi, the impression may be gained that the population 
is quite distinct. However, when the range of variation in all characters from 
throughout the geographic range of stephensi is taken into consideration, 
the differences are less impressive and not as significant. In many features, 
topotypes of stephensi are not "typical" or "average" for the race. 

In central Arizona, there is a series of populations of N. stephensi which 
possesses characteristics of an average difference distinguishing it from neigh- 
boring populations. This series, depicted by the dark area in Plate I, com- 
prises populations from Black Tank to the north, south through Deadman's 
Flat, Wupatki Monument, Winona, Walnut, Verde Valley, and west to Red 
Lake and Fort Whipple. Specimens from as far south as McMillenville and 
the Natanes Plateau in Gila County are not included. This complex of popula- 
tions possesses the following features, many of which are of an average sort: 
color dark; dorsal tail stripe often black; sides with the ochraceous color along 
the lateral line greatly restricted; body long, as long or longer, on the average, 
than in any population; body weight intermediate between that of relicta and 



Table 3. — External aand cranial measurements of "Group 3" female specimens of Neotoma 
stephensi stephensi. Grouped localities are as in Table 2 





Western 


Northern 


Central 


Southeastern 




Arizona 


Arizona 


Arizona 


Arizona 


Number 


12 


5 


5 


3 


Total length 


274.2 


298.3'^ 


309.8^ 






264.0-329.0 


279.0-323.0 


293.0-322.0 


304.0^ 


Head and body 


170.1 


168.3" 


175.0* 






148.0-195.0 


160.0-180.0 


173.0-179.0 


164.0^ 


Tail 


129.0 


130.0" 


134.8^ 






106.0-141.0 


119.0-143.0 


118.0-148.0 


140.0^ 


Hind foot 


32.0 


31.3« 


33.3* 






30.0-34.0 


30.0-32.0 


33.0-34.0 


32.5^ 


Condylobasal length -. 


38.8" 


36.6 


38.6 


38.8^ 




36.8-40.7 


35.9-37.5 


38.0-39.7 


38.2,39.3 


Zygomatic breadth .... 


21.8' 


20.7 


20.7 


21.6 




21.1-23.2 


20.4-20.9 


20.5-20.9 


21.2-22.0 


Interorbital 


5.4 


5.4 


5.4 


5.7 




4.7-5.8 


5.2-5.7 


5.0-5.7 


5.3-6.0 


Rostrum breadth _ 


6.3 


5.9 


6.3 


6.4^ 




6.0-6.6 


5.6-6.0 


6.1-6.5 


6.3,6.5 


Rostrum depth 


6.6 


6.1 


6.5 


6.7^ 




6.2-7.0 


5.5-6.2 


6.4-6.7 


6.5,6.8 


Nasal 


15.3 


14.3 


15.7 


15.5= 




13.9-16.6 


13.7-14.6 


15.3-16.3 


14.9,16.1 


Incisive foramen 


8.5 
7.9-8.8 


8.4 
8.1-8.8 


9.1 
8.5-9.5 


8.7= 




8.5,8.9 


Palatal bridge 


7.6 


7.2 


7.2 


7.8 




6.9-8.5 


6.9-7.9 


6.5-7.5 


7.5-8.5 


Maxillary toothrow ... 


8.9 


8.4 


8.6 


9.0 




8.4-9.5 


8.1-8.8 


8.5-8.8 


8.6-9.3 



67 



488 JOURNAL OF MAMMALOGY Vol. 41, No. 4 

Specimens from the Hualpai Mountains; skull long and narrow, with the per- 
centage of zygomatic breadth to greatest length in adult males being between 
48.4 and 50.4; for the Hualpais, 51.7 to 53.6; for the Grand Canyon, 49.7 to 
51.4; similar percentages for adult females from the respective localities are 
between 49.2 and 53.8; 50.8 to 54.8; 51.6 to 53.5. The length of the upper 
toothrow and width of the interorbital region are intermediate between 
relicta and specimens from the Hualpai Mountains. 

Although this complex of populations may possess some average differences 
of color and size, we feel that it has not reached the subspecific stage of 
differentiation. 

In western New Mexico and eastern Arizona, there is a group of populations 
that has certain characters in common, and differs in an average way from 
N. s. stephensi in western Arizona. This group includes localities from 25 mi. 
N Springerville and from Springerville in Arizona southeast to the Burro 
Mountains, New Mexico, and northeast to Grants. Some features of this 
group, many of which are not diagnostic, include: nasals broad, almost bell- 
shaped anteriorly; posterior arms (ascending branches) of premaxillae on 
dorsum of skull broad; nasals, posteriorly, constricted more by premaxillae 
than in most other populations; color dark, as dark as that in central Arizona 
populations except for specimens from Burley. For remarks about the white- 
throatedness of specimens from the Burro Mountains, see page 480. One 
specimen from Grants, Catron County, New Mexico, in many ways exemplifies 
the extreme of these characters listed: nasals bell-shaped anteriorly, con- 
stricted posteriorly; posterior, ascending arms of premaxillae broad; inter- 
orbital region broad; color dark, with the addition of a heavy, rich fulvous 
wash over the entire underparts. This specimen lacks 90 per cent of the tail, 
and our first reaction was that this specimen was not a bushy-tailed Neotoma 
stephensi. The heavy wash of fulvous on the underparts is duplicated in one 
of three specimens of Neotoma mexicana from 5 mi. SE Grants. However, 
careful analysis, particularly of cranial features, indicates that the specimen 
is N. stephensi, not N. mexicana. This individual is either aberrant or reflects 
the extreme characters of this group of populations we have described above. 
We prefer the latter interpretation. The fulvous wash on the underparts may 
reflect the "influence" of the black lava near Grants. We do not think this 
fulvous wash represents a "dichromatic condition" that Goldman (N. Amer. 
Fauna 31: 81, 1910) alluded to, although more specimens may indicate that 
such is the case. A specimen from 4 mi. W McCartys, which is near Grants, is 
a very young animal and shows none of the features of the Grants' specimen. 

According to Laurence Huey, the type locality should be regarded as Horse 
Tank at the southern end of the Hualpai Mountains. Mr. Huey informs us 
that Frank Stephens provided him with this information. 

Specimens examined. — Total number, 163, from the following localities: Arizona — 
Mohave County: Hackberry, 7 (BS); Democrat Mine, 13 mi. ESE Kingman, Hualpai Mts., 
1 (UI); Hualpai Mtn. Park, Hualpai Mts., 1 (UI); 1 mi. N Hualpai Peak, Hualpai Mtn. 



68 



Not;., 1960 HOFFMEISTER AND DE LA TORRE— NEOTOMA 489 

Park, 7,000 ft., 1 (UI); Pine Lake, Hualpai Mtn. Park, 6,000 ft, 1 (UI); Hualpai Mts., 
5,600 ft., 7,000 ft., 6 (BS), 1 (UI); Horse Tank, 5 (SD); Lucky Star Mine, Chemehuevis 
Mts., 3 (SD); Yuma County: Harquahala Mts., 5,000 ft., 3 (BS); Coconino County: Hilltop, 
S side GCNP [= Grand Canyon Nat. Park], 4 (UI); Lower end Prospect Valley, 5,200 ft., 
2 (BS); Pasture Wash Ranger Station, 6,300 ft., GCNP, 3 (UI); Pasture Wash, Jet. rds. 
W9A & W9, GCNP, 1 (UI); 8 mi. N Pine Spg., Hualpai Indian Reservation, 3 (BS); 
E side Cedar Mt.. 6,400 ft., GCNP, 2 (UI); Yaki Bum, S rim Grand Canyon, 2 (GC); 
Yavapai Point Station, S rim Grand Canyon, 3 ( GC ) ; Grand Canyon Village, S rim Grand 
Canyon, 1 (GC); S rim Grand Canyon, 1 (GC); S boundary GCNP, nr. Rowes Well, 
GCNP, 1 (UI); School athletic grounds. Village, GCNP, 7 (UI); Shoshone Point, GCNP, 

2 (UI); Wayside Museum, S rim Grand Canyon, 1 (GC); 1 mi. E, V2 mi. S Desert View 
Pt, GCNP, 1 (UI); Grandview Pt., GCNP, 1 (UI); Long Jim Canyon, 3 (UI); W side 
Zuni Pt., 7,200 ft., GCNP, 6 (UI); Rt. 64, SE Boundary GCNP, 1 (UI); Cataract Canyon, 
12 mi. WSW Anita, 2 (BS); Red Butte, 2 (BS); Black Tank Lava Beds, 6,100 ft, 3 (UC); 
Lava Field, 12 mi. N Deadman's Flat, NE San Francisco Mt., 1 (UC); 2.6 mi. W Wupatki 
Ruins, 8 (UC); Wupatki Indian Ruins, 35 mi. NE Flagstaff, 5,100 ft, 1 (BS), 6 (UC); 
Deadman's Flat, NE San Francisco Mt., 6,400 ft., 2 (UC); 4 mi. NE Deadman Ranger 
Station, San Francisco Mt, 6,600 ft., 1 (BS); Red Lake, 5 (BS); 3 mi. NW Winona, 
6,200 ft., 6,400 ft, 2 (BS); Aztec Tank, 5,800 ft., 2 (BS); Winona, 6,400 ft, 2 (UC); 
Wahiut, 1 (BS); Wabut Canyon, 5 mi. S Mt. Elden, 6,500 ft., 1 (BS); Anderson Mesa, 
Anderson Canyon, 30 mi. SE Flagstaff, 6,500 ft., 1 (BS); Yavapai County: Pine Flat, 
Jumper Mts., 20 mi. NW Simmons, 3 (BS); 5 mi. S, 1 mi. W Sedona, 1 (UI); 2 mi. N 
Montezimia WeU, 3 (UI); 2 mi. N Rimrock, 1 (UI); Montezuma WeU, 3,500 ft., 2 (BS); 

3 mi. N Ft Whipple, 1 (BS); 6 mi. NW Camp Verde, 1 (UI); Mayer, 1 (BS); Gila 
County: 7 mi. N Payson, 4,500 ft., 1 (BS); Black River, 5 mi. above mouth White River, 
4,600 ft., 1 (BS); nr. sawmill, 25 mi. NE Rice [nov/ San Carlos], Natanes Plateau, 5,800 ft., 
3 (BS); McMillen Mine, 5 mi. E, 12y2 mi. N Globe, 4 (UI); Cazador Spring, S base 
Natanes Plateau, San Carlos Indian Reservation, 4,000 ft., 1 (BS); McMillenville, 4,300 ft., 
3 (BS); Apache County: Zuni River, 3 (BS); 8 mi. S St Johns, 5,800 ft, 4 (BS); 25 mi. 
N Springerville, 2 (BS); Springerville, 7,000 ft., 1 (BS); Greenlee County: 3 mi. W Gosper 
Ranch, 6,000 ft, 1 (BS); Gosper Ranch, Blue River, 5,000 ft, 2 (BS); New Mexico— 
Valencia County: Grants, 1 (BS); 4 mi. W McCartys, 1 (UM); Socorro County: Burley 
[22 mi. N Augustine], 3 (BS); Catron County: Largo Canyon, 1 (UC); Whitewater 
Canyon, 5 mi. NE Glenwood, 5,450 ft., 1 (AM); Glenwood, San Francisco Valley, 5,000 
ft, 1 (BS); Grant County: Burro Mts., 8 (BS). 

Additional records. — Arizona — Coconino County: S side Bass Camp, 8 mi. NW Grand 
Canyon (BS); 1 mi. N Bass Camp, 5,200 ft, (BS); 3 mi. S Bass Camp, 5,400 ft, (BS); 
Bass Camp (BS); nr. Bright Angel Trail, Grand Canyon, (BS); S Yaki Point, in yellow 
pine, Grand Canyon (BS); top of rim nr. Village, Grand Canyon, 6,800 ft., (BS); Grand 
View Point, Grand Canyon, (BS); Trash Tank, S rim Grand Canyon, (GC); Trash Wash, 
S rim Grand Canyon, ( GC ) ; N Red Butte, Main Road, Grand Canyon, ( BS ) ; Red Butte, 
Museum of Northern Arizona; Wupatki Nat'l Monument, 5,100 ft., Museum of Northern 
Arizona; Wupatki Indian Ruins, 35 mi. NE Flagstaff, 5,100 ft, (BS); Yavapai County: 
Fools Gulch, Weaver Mts., (BS). 

Neotoma stephensi relicta Goldman 
Neotoma stephensi relicta Goldman, 1932, Jour. Mamm., 13: 66, 9 Feb. 

Type.— Adult female, U.S. National Museum (Biol. Surv.), No. 67780, from 
Keams Canyon, Navajo County, Arizona, collected on 22 July 1894 by A. K. 
Fisher; original no. 1649. 



69 



490 



JOURNAL OF MAMMALOGY 



Vol. 41, No. 4 



Table 4. — External and cranial measurements of "Group 3" specimens of Neotoma 
stephensi relicta. Localities represented are as follows: Utah — Navajo Mt., Rainbow 
Bridge; Arizona — Rainbow Lodge, Cedar Ridge, Keams Canyon; New Mexico — Wingate 

area, Long Canyon, Blanco 



Females 



Males 



Number 

Total length 

Head and body 

Tail 

Hind foot 

Condylobasal length 

Zygomatic breadth ... 

Interorbital 

Breadth of rostrum . 

Depth of rostrum . 

Nasal 



Incisive foramen 

Palatal bridge 

Maxillary toothrow 



10 

296.7' 
273.O-320.0 

163.0" 
153.0-175.0 

133.7" 
120.0-145.0 

30.4" 
28.0-33.5 

36.3« 
33.7-38.0 
20.0« 
18.4-20.2 

5.2 
4.8-5.7 
5.9 
5.5-6.3 
6.2 
5.8-6.5 
14.7' 
13.5-15.8 

8.4 

7.8-9.0 

7.2 

6.7-7.8 

8.1 

7.7-8.3 



10 
304.7" 
283.0-333.0 

172.0" 
159.0-187.0 

130.9 
123.0-144.0 
31.2 
29.0-33.0 
37.8« 
36.8-38.6 
20.5" 
20.0-21.1 
5.3" 
5.2-5.4 
6.0" 
5.5-eA 
6.6 
6.4-7.0 
15.4 
14.9-16.0 
8.8 
8.5-9.4 
7.4 
7.1-7.9 
8.2 
7.9-8.4 



Range. — East of the Colorado River, from Navajo Mountain in extreme 
south-central Utah, south to the Little Colorado River, and eastward in New 
Mexico to the San Juan Basin at the north and the Zimi Mountains at the 
south (see map, Fig. 4). 

Diagnosis. — A race of Neotoma stephensi characterized by markedly pale 
buffy color, with much less blackish and brownish than in other populations 
of species; sides, above lateral line, with large extent of buffy color, which 
varies between Pinkish Buff and Light Ochraceous-Salmon; nose, forehead 
and cheeks buffy, less plumbeous tiian other subspecies; hairs on throat 
usually white throughout (base not plumbeous); top of tail appears grayish 
because few dark hairs present; underparts usually without fulvous wash; 
size small, being best indicated by Hght weight (adult males less than 117 
gms.); skull small, greatest length averaging less than 41.2 mm. in adult males; 
upper toothrow short, usually less than 8.4 mm.; skull narrow, with interorbital 
width usually 5.3 mm. or less and narrow across zygomata, with males usually 



70 



Nov., 1960 HOFFMEISTER AND DE LA TORRE— NEOTOMA 491 

averaging less than 21.0 mm.; skull delicate for the species, with supraorbital 
ridges not heavily beaded. 

Comparisons. — For a comparison with N. stephensi stephensi, and the geo- 
graphic variants within that subspecies, see the account of N. s. stephensi. 

Measurements. — See Table 4. 

Remarks. — N. s. relicta is a pale race inhabiting the mountainous areas of 
the elevated, short grass region of northeastern Arizona. The race does extend 
into New Mexico and Utah, but its principal center of distribution is in 
Arizona. 

N. s. relicta is quite distinctive from many populations of N. s. stephensi 
adjacent to its range. It is less distinctive from some other populations farther 
removed. However, with a combination of characters (principally on the 
basis of color), relicta and stephensi can be distinguished. As here delimited, 
relicta shows less morphological variation geographically than does stephensi. 
Specimens from the eastern part of Grand Canyon National Park, referred to 
stephensi, show considerable approach toward specimens from Cedar Ridge, 
referred to relicta. These two localities are less than 45 miles apart. The 
intermediacy is in color and, to some extent, size of the skull. Specimens 
from Wingate and Gallup are of a color intermediate between that of relicta 
and stephensi, but the skulls of the adult specimens seem more as in relicta, 
to which subspecies they are referred. 

Specimens examined. — Total number, 62, from the following localities: Utah — San 
Juan County: Rainbow Bridge, 4,000 ft., 1 (UC); nr. War God Spring, 8,500 ft., Navajo 
Mt, 1 (AM); Navajo Mt. Trading Post, SE side Navajo Mt., 1 (UC); Arizona — Coconino 
County: Rainbow Lodge, Navajo Mts., 6,400 ft., 2 (BS); 5 mi. S simmiit, Navajo Mt., 1 
(UC); Cedar Ridge, 30 mi. N Tuba, 3 (BS); Cedar Ridge, 6,000 ft., 10 (UC); Tuba, 
1 (BS); Navajo County: Long Canyon, 6,450 ft., 1 (AM); Keams Canyon, 80 mi. N 
Holbrook, 20 (BS); Keams Canyon, 6,200 ft., 6 (UC); Apache County: Ganado, 6,500 ft., 
5 (BS); St. Michaels, 7,000 ft., 2 (BS); New Mexico— Sen Juan County: Blanco, 1 (BS); 
McKinley County: Gallup, 1 (BS); Wingate, 2 (BS); Fort Wingate, 3 (BS); 12 mi. S 
Gallup, 1 (BS). 

Museum of Natural History, Univ. of Illinois, Urbana. Received 18 August 1959. 



71 



Am. Zoologist, 7:223-232(1967). 

Multiple Character Analysis of Canis lupus, latrans, and familiaris, 
With a Discussion of the Relationships of Canis niger 

Barbara Lawrence, Museum of Comparative Zoology, Harvard University, 

and 
William H. Bossert, Department of Biology, Harvard University, 

Cambridge, Mass. 

Synopsis. A multiple character analysis was undertaken of a broadly representative sample 
of three species: Canis lupus (wolf), C. latrans (coyote), and C. familiaris (dog). These species 
are clearly and significantly distinguished by the technique of linear discrimination. The analy- 
sis provides a basis for the identification of skulls not obviously distinguishable by size or other 
diagnostic charactei^s. 

Early populations of Canis n. niger and C. n. gregoryi (red wolf) are compared with the three 
species above and are found to form a cluster with lupus and to be sharply distinct from the 
other two species. Additional comparisons show that while lupus lycaon and niger both overlap 
with lupus, they are distinct from each other. This entire cluster is quite distinct from latrans, 
with niger being the farthest removed. A sample population of C. ?!. gregoryi, from the edge of 
the extending range of C. latrans, was examined and found to show too great a range of vari- 
ation to be attributed to a single species. 

With the advent of white man in North a unit. When a particular subspecies is re- 
America and his consequent modification ferred to, a trinomial is used, as Canis lu- 
of the environment by lumbering and pus lycaon. Canis niger, the red wolf, is 
clearing for farming, coyotes have been ex- usually considered to include three sub- 
tending their range (Young and Jackson, species. Their status is uncertain, and Ca- 
1951). As they have extended their range, 7us niger as used in the present work refers 
on the fringes of their newly acquired ter- to the typical form, C. n. niger, and to those 
ritories, animals which are difficult to iden- southeastern populations, presently called 
tify have frequently been captured. In the C. n. gregoryi, which show no evidence of 
South, as often as not, these are called red hybridization and which were collected 
wolves, in the Northeast, coydogs. In both from well outside the range of latrans. Ca- 
parts of the country these animals occur nis familiaris, the dog, presents no prob- 
where coyotes have moved into areas that lem because, in spite of its variability, it is 
formerly were inhabited by small races of monotypic. 

wolf. Coincident also with these shifts in The present study was undertaken be- 

distribution has been an upward revision cause attempts to identify skulls of the 

in the reported weights for coyotes. Young northeastern population of rather large- 

and Jackson (1951), eliminating a few out- sized members of the genus Canis bogged 

sized individuals, give a range of 18-30 down in a mass of overlapping characters, 

pounds for typical western coyotes, while It was then decided that before such fringe 

Burt (1946) gives a range of 23-50 pounds populations could be identified we needed 

for Michigan coyotes. The latter overlaps to know what, if any, combinations of 

with weights of a long series of wolves from characters reliably separated known Canis 

Algonquin Provincial Park (unpublished lupus, latrans, and familiaris, particularly 

data from the Ontario Department of if size were eliminated as a character. This 

Lands and Forests) and, as a result, size part of the work will be described in detail 

alone becomes a less useful criterion in dis- in section I. 
tinguishing between wolves and coyotes. While these three species are unquestion- 

In the following discussion, since Canis ably distinct, the red wolf, currently called 

lupus, the wolf, and Canis latrans, the coy- Canis niger, is a more problematical entity 

ote, are both composite species, these names and will be discussed in section II in the 

as used in the text refer to each species as light of our findings in section I. 

(223) 



72 



224 



Barbara Lawrence and William H. Bossert 



SECTION I 

The purpose of this part of the study 
was to determine what, if any, combina- 
tions of characters separate the three spe- 
cies, C. lupus, C. latrans, and C. familiaris, 
and how widely they are separated. To do 
this, we have used a biased random selec- 
tion of 20 adult members, including males 
and females, of each species. In latrans, 
wide geographic distribution within the 
original range of the species was an impor- 
tant factor in choice of specimens. In lu- 
pus, only North American races were used 
and large individuals were avoided. In fa- 
miliaris, the selection was deliberately bi- 
ased to include the most wolf-like and coy- 
<ote-like animals. 

Characters to be used were not randomly 
selected but chosen because of their known 
value in distinguishing the species in- 
volved. Forty-two different measurements 
(see appendix) were taken on as many as 
225 skulls. The measurements of 125 of 
these were then variously plotted to esti- 
mate regression lines. Based on these, 24 
possibly significant characters were selected, 
13 dealing with skull shape and 11 with 
tooth form, to test for diagnostic value. 
Since we wished to ascertain whether or 
not, regardless of size, skulls of each of the 
species had certain unique characters or 
combinations of characters, size was elimi- 
nated as a factor by relating all measure- 
ments to total length of skull. The mean 
and standard deviation of these 24 charac- 
ters, as a fraction of total length, were com- 
puted for each of the selected series. 
The value of each character in distin- 
guishing a pair of species was tested by 
computing single character distances for 
the pair, dividing the difference in means 
for the two populations by the average 
standard deviation. 

From this analysis, nine cranial and six 
tooth measurements were found to be most 
diagnostic, although no single character 
was found without overlap between a pair 
of species. These were the measurements 
used in our linear discrimination. 

In the following non-numerical descrip- 
tion of differences between the species con- 
sidered, the numbers of the measurements, 



which are expressions of these differences, 
and which were used in our linear discrimi- 
nation, are given in parentheses. For de- 
scriptions of the measurements see Appen- 
dix A. 

When lupus and latrans are compared, 
it is found that the most significant differ- 
ences are in the relative development of 
the rostrum and of the brain case. W^olves 
have a relatively small brain case and mas- 
sive rostrum. The latter is presumably a 
reflection of the large size of the animals 
on which they prey. Breadth of palate (7, 
19), large teeth (11, 12, 13, 15, 20), and 
heavy maxilla (8), all contribute to the 
formation of powerful jaws. The position 
of the anterior root to the zygomatic arch 
and its massiveness help to buttress the 
teeth and strengthen the crushing action 
of the jaws. In the intermediate region of 
the skull, the strength of the masticatory 
apparatus shows in the depth of the jugal 
bone (18) and in the size of the temporal 
fossa. The one provides attachment for the 
masseter muscle, the other space for the 
temporal muscle. This space is difficult to 
measure, but the relation between the 
broadly spreading zygomatic arches (4) and 
the narrow brain case (6) expresses it well. 
Size of the temporal muscle is also shown 
by the development of a large sagittal crest. 

Coyotes, preying as they do on small spe- 
cies, have opposite skull proportions and 
small, narrow teeth. Compared with the 
brain case, the rostrum is slender, the max- 
illa and the anterior root of the zygomatic 
arch less massive, the temporal fossa small- 
er, and the jugal narrower. All of this gives 
the skull a rather long slender appearance 
as compared with that of a wolf. This over- 
all distinction is a good one and has often 
been used as diagnostic in separating wolf 
and coyote skulls, but it can be confusing. 
Ratios of total length to zygomatic 
breadth in long, narrow, wolf skulls may 
overlap with these ratios for short, broad, 
coyote skulls. If width of the brain case, 
width across molars, and width between 
premolars anteriorly are also taken into ac- 
count, the characteristic, relatively-small 
brain case of a typical wolf skull is imme- 
diately apparent. 



73 



Multiple Character Analysis of Cayiis 



225 



Dogs present a different problem. Essen- 
tially they are small wolves, distinguishable 
from coyotes by many of the wolf-like pro- 
portions of rostrum and brain case. How- 
ever, their great variability means that no 
single set of characters is equally diagnos- 
tic for all kinds. Key characters for sepa- 
rating lupus and latrans are based on a cer- 
tain intraspecific homogeneity which is not 
too difficult to describe or to see. C. famili- 
aris lacks this homogeneity and often super- 
ficially resembles either of the other two 
more than it does other familiaris. This 
means that the best combinations of char- 
acters to be used for purposes of identifica- 
tion vary depending on whether the animal 
in question is large and wolf-like or small- 
er and coyote-like. Certain of the highly 
modified breeds are, of course, easily iden- 
tified by the disproportionate development 
of brain case or rostrum. Other less modi- 
fied forms may be distinguished by the in- 
flation of the frontal sinuses and resultant 
steep angle of the forehead. They may also 
be recognized by a bend in the mid-region 
of the skull so that rostrum and brain case 
meet at more of an angle than is usual in 
wild canids. 

Turning to the less modified kinds, and 
these include many mongrels, the large 
dogs differ from wolves in having relatively 
small teeth, and having the skull elongated 
in the interorbital region so that the dis- 
tance between the tooth row and the bulla 
(2) is long compared with the length of the 
tooth row (10) . The palate also is elon- 
gated so that its posterior margin lies well 

posterior to m-. The brain case often looks 
atypically heavily ossified. The sagittal 
crest is usually drawn out less far beyond 
the occiput; when it is strongly developed 
and projecting, the dorsal margin usually 
curves strongly down at the tip. Briefly, 
big dogs look rather as if they had out- 
grown themselves and were never meant to 
be that size. 

For the most part, wolf-like proportions 
of brain case and rostrum distinguish most 
dogs from coyotes. Long, narrow-skulled 
dogs may approach coyotes in some of their 
length-breadth proportions, but not in all 



of them, and a coyote-like elongation of the 
tooth row is not usually accompanied by 
coyote-like proportions of the teeth. 

Disparate proportions of the teeth which 
show as differences in certain of them also 
help to distinguish dogs and coyotes. The 
relatively greater size of the canine (13) in 
dogs may be a reflection of their relation- 
ship with wolves. The greater width across 
the incisors (15) is partly an expression of 
larger tooth size; however, it also expresses 
the greater premaxillary width of dogs. In 
contrast, the last upper molar is small (14). 
This tooth, as frequently happens with the 
anteriormost or posteriormost of the cheek 
teeth, is the most variable tooth in the up- 
per jaw. Nevertheless, its average smaller 
size in dogs than in wolves and coyotes is a 
good diagnostic feature and may be one of 
the results of domestication. The last char- 
acter to be considered is characteristic of 
most coyotes and is one of the best expres- 
sions of the general narrowing of the pre- 
molars and carnassials in this form. The 
posterior part of pj (22) is relatively long 
compared both to the length of the tooth 
(20) and to its maximum width. Because of 
this lengthening, a second accessory cusp 
behind the main cusp is usually present in 
coyotes and has often been used as diagnos- 
tic (Gidley, 1913). 

We have applied the technique of linear 
discrimination as described by Kendall 
(1946). Jolicoeur (1959), who has used line- 
ar discrimination to somewhat different 
ends, gives an excellent graphical explana- 
tion of the technique. The computations 
were done on an IBM 7094 computer using 
the BIMD 05 program developed by the 
University of California at Los Angeles 
Medical School. In short, the technique 
finds the weighted sum of a number of 
characters which is most different for two 
populations, that is, the weighted sum of 
characters which best separates the popula- 
tions. The sum itself is called the discrimi- 
nant function, and the weights, determined 
by the computations, are called the dis- 
criminant coefficients. The mean value of 
the discriminant function for each of the 
populations can be obtained by multiply- 



74 



226 



Barbara Lawrence and William H. Bossert 



ing the mean value of each character over 
the population by the discriminant coeffi- 
cient for the character and then summing. 
If an individual is known to belong to one 
of a pair of populations, he can be identi- 
fied by evaluating the discriminant func- 
tion separating the pair for his values of 
the characters (that is, summing the 
weighted measurements for the specimen) 
and assigning him to the population hav- 
ing the closest mean value of the function. 
The accuracy of the identification will de- 
pend, of course, on the degree to which the 
populations are separated by the discrimi- 
nant function. A useful measure of the 
multiple character difference between two 
populations is the D- statistic of Mahalo- 
nobis (see Rao, 1952) . This is a general 
extension of the distance comparisons for 
single characters mentioned earlier. 

For this study the discriminant coeffi- 
cients and the D- statistic for each pair of 
the selected populations of C. latrans, lu- 
pus, and familiaris were computed using 
the fifteen characters discussed above. The 
discriminant coefficients are given in Table 
1 along with the mean values of the dis- 

TABLE 1. Results of pairwisc discriminant analysis 
for C. latrans, lupus, and familiaris. 





Discriminant coefficient 




lupus vs. 


latrans vs. 


lupus vs. 


Measurements* 


latrans 


familiaris 


familiaris 


2 


3.389 


— 16.876 


— 6.900 


4 


— 7.107 


14.670 


8.494 


6 


14.971 


— 11.182 


— 6.760 


7 


— 0.495 


— 11.246 


— 5.124 


8 


— 7.313 


—33.699 


— 7.849 


10 


9.889 


—24.989 


— 10.108 


11 


14.984 


66.749 


26.784 


12 


— 12.510 


—25.968 


— 1.089 


13 


—24.891 


—77.655 


— 4.088 


20 


-32.167 


5.155 


22.738 


22 


87.360 


35.272 


—33.076 


14 


3.652 


63.729 


0.606 


15 


— 8.932 


—28.702 


— 3.531 


18 


3.299 


31.510 


0.784 


19 


1.230 


— 15.404 


— 10.638 


Average discrimi 


- 






nant function 








value for latrans 4.79 


— 14.6 




for lupus 


3.10 




— 4.73 


for familiaris 




— 17.8 


— 5.44 


D^(D) 


64.1 (8.0) 


119.9(10.9) 


27.2(5.2) 



criminant functions for the populations, D^ 
and D. The last value is roughly the dif- 
ference in standard deviations between the 
mean values of the function for the two 
populations. We see that latrans differs by 
eight and nearly II standard deviations 
from lupus and familiaris, respectively, 
while lupus and familiaris differ by only a 
little more than five. 

A clear view of the degree of separation 
of the populations achieved by the dis- 
criminant functions results from the a pos- 
teriori identification of the original indi- 
vidual specimens using the functions. For 
each of the pairwise discriminations the 
specimens were assigned to one species ten- 
tatively. A final identification was then 
made by assigning the specimen to that 
species for which two tentative assignments 
had been made. For example, if between 
latrans and lupus the specimen was as- 
signed to lupus, between latrans and fa- 
miliaris to latrans, and between lupus and 
familiaris to lupus, then the specimen was 
identified as lupus. In this way all sixty of 
the specimens were unambiguously and 
correctly identified; there was no overlap 
in the values of the various discriminant 
functions for the populations on which 
they were based. Figure 1 gives a plot of 
the populations using the latrans-lupus and 
latrans-familiaris discriminant functions as 



5 - 





J. 



J. 



* Measurements are numbered as in Appendix. 
Each must be divided by total length of skull, 
measurement 1. 



--14 -15 ^16 -17 -18 ' 

FIG. 1. Linear discrimination of C. latrans (C), 
C. lupus (W), and C. familiaris (D). The contours 
indicate the extreme range of individuals in the 
populations used. The latrans-familiaris discrimi- 
nant function is used as the abscissa and the lat- 
rans-lupus discriminant function is used as ordi- 
nate. 



75 



Multiple Character Analysis of Canis 



227 



coordinate axes. This figure shows the rela- 
tive separations of the populations as well 
as the lack of overlap. 

SECTION II 

As stated earlier, in North America, in 
addition to C. lupus and C. latrans, a third 
species of wild Canis, C. niger, the red 
wolf, is currently recognized. Young and 
Goldman (1944) describe it as a wolf which 
is somewhat intermediate between lupus 
and latrayis, with a distribution limited to 
the south-eastern part of the United States. 
This is a unique situation since all other 
wolves in both Eurasia (Pocock, 1935) and 
North America are races of C. lupus. 
Ranges as plotted for lupus and niger by 
Young and Goldman (1944) show an over- 
lapping of lupus with niger in the south- 
eastern part of the former's range. Even 
more surprising is the overlapping of all 
three species of Canis at the western edge 
of the range of niger and the eastern edge 
of that of latrans (Young and Jackson, 
1951; Young and Goldman. 1944). Such an 
occurrence together of three closely related 
members of the genus Canis is without 
parallel elsewhere in the world. The situ- 
ation is obviously peculiar, and various au- 
thors have attempted to explain it. It is 
not pertinent here to review these discus- 
sions; suffice it to say that for the most part 
they have concentrated on the relationship 
between niger and latrans. The most re- 
cent effort to unravel the problem is a 
paper by McCarley which includes an in- 
teresting discussion of the possibility of hy- 
bridization and population replacement 
(1962) where latrans is encroaching on the 
range of niger. 

Implicit in McCarley's interpretation of 
his data, though not explicitly stated, is the 
fact that, while closely related species usu- 
ally differ most from each other where their 
ranges meet or overlap, the opposite is true 
of these forms in the south-central states. 
Here, at the western edge of the range of 
niger, the small C. n. rufus Audubon and 
Bachman 1851 is often difficult to tell from 
C. latrans frustror Woodhouse 1851, while 
at the eastern end of its range, the larger C. 
n. niger Bartram 1791 is said to resemble C. 



lupus lycaon Schreber 1775 (Young and 
Goldman, 1944). Essentially, as presently 
defined, niger appears as a population in- 
termediate in characters between a large 
western latrans and a small eastern lupus. 
Efforts to determine the true status of 
niger will be helped if we first understand 
some of its taxonomic history. Because of 
the complications of priority, Canis rufus 
from Texas with three subspecies of in- 
creasing size from west to east now figures 
in the literature as Canis niger of Florida 
with three subspecies of decreasing size 
from east to west. The three related forms 
are the same in each case, but depending 
on which end of the range one starts from, 
the reasons for the primary distinction of 
the species are different. Canis rufus as a 
Texas phenomenon had a quite different 
reason for being set apart than did Canis 
niger as a Florida phenomenon. The ear- 
liest descriptions of a small wolf in the 
south-central states are based on the occur- 
rence of a medium-sized non-coyote in east- 
ern Texas. Animals were found which re- 
sembled coyotes in size but not in cranial 
characters, and the difference in size be- 
tween these animals and the big plains 
wolves was so gieat that the two were 
scarcely compared. Typical coyotes were 
also found to occur in the same area. The 
fact that two distinct kinds of Canis were 
recognized is more important than the rea- 
sons why the name rufus was selected for 
the one and frustror for the other (Young 
and Goldman, 1944; Young and Jackson, 
1951). Once rufus was set apart as a dis- 
tinct species of wolf, efforts were made to 
determine the eastern limits of its range. A 
reasonable number of specimens was avail- 
able from Louisiana, but progressing to- 
wards Florida the number of available 
specimens diminishes rapidly. There are 
very few from that part of the range where 
nigei- and lupus lycaon supposedly meet. 
Since, in addition to this, there are almost 
no extant specimens of C. lupus lycaon 
from the southeastern states, it is easy to 
see why the relationship between the east- 
ern red wolf, C. n. niger, and C. lupus ly- 
caon has not been more thoroughly ana- 
lyzed. 



76 



228 



Barbara Lawrence and William H. Bossert 



If the study of the small wolves in the 
southern states had begun with niger in 
Florida and been based on adequate series, 
it is highly unlikely that niger ever would 
have been separated as a species from lupus. 
The biologically difficult problem of re- 
concilino; the existence of two similarly- 
sized forms of wolf in one continuous habi- 
tat would never have arisen and the area 
of systematic uncertainty would have been 
more properly limited to the eastern edge 
of the coyote's extending range. 

The purpose of this part of the present 
work has been to establish whether or not 
two distinct species of wolf occur in the 
southeastern United States. The following 
discussion presents our evidence for con- 
sidering that the wolves of this area all be- 
long to the species lupus and that niger is 
not a distinct species. Unequivocal estab- 
lishment of the status of niger has seemed 
a necessary preliminary to understanding 
and identifying the widely varying popula- 
tions from west of the Mississippi presently 
identified as n. gregoryi Goldman 1937 and 
n. rufus. 

In order to be as certain as possible that 
we were excluding latrans from our sample 
population, the series selected for a linear 
discrimination was limited to all available 
specimens of C. n. niger and C. n. gregoryi 
collected before 1920 from Louisiana, Ala- 
bama, and Florida; in addition, a Florida 
skull previously identified as C. lupus lyca- 
on was included. In the following discus- 
sion this series is referred to as C. niger. 
The type of floridanus Miller 1912 (^= ni- 
ger), though it could not be included be- 
cause the skull is too broken, falls within 
the range of variation of the rest of the 
series. 

In our linear discrimination, comparison 
was made with the broadly representative 
series of the three species, lupus, latrans, 
and familiaris, used in the first section. It 
was also made with a series of ten males 
and ten females, all adult, of Canis lupus 
lycaon, the race whose range has been pre- 
sumed to overlap with that of niger in the 
Southeast. The individuals were randomly 
selected from 71 specimens from Algonquin 
Provincial Park in Canada and weighed 



from 48-81 pounds (average 58). It was nec- 
essary to use a northern population be- 
cause adequate series from farther south 
were not preserved before wolves were ex- 
terminated. 

To the eye, the specimens of niger stud- 
ied appear /upu5-like and this is borne out 
by the numerical analysis. As a first step 
in the analysis, all of the individual speci- 
mens in the niger and lycaon populations 
were identified using the discriminant func- 
tions presented in the previous section. All 
were assigned to the lupus category; they 
were on the whole both less coyote-like and 
less dog-like than the original lupus popu- 
lation. In itself this provides little infor- 
mation about the relationships of lupus to 
these populations, of course, since the iden- 
tification tacitly assumes the individuals to 
be from the latrans, lupus, or familiaris 
groups. The study was continued, there- 
fore, by computing the discriminant func- 
tion coefficients and D^ values for all pairs 
of the five populations. The values of D^ 
are given in Table 2. Using these with the 

TABLE 2. The generalized distance, D*, between pop- 
ulatiojis described in the text. 

C. latrans 
C.lupus 64.1 C. lupus 

C. familiaris 119.9 27.2 C. familiaris r i^jjus 

C. lupus lycaon 69.5 10.0 



C. niger 



116.0 20.3 



66.6 
87.6 



lycaon 
56.0 



cluster grouping technique discussed by 
Rao (1952), the lycaon and niger popula- 
tions form a cluster with the selected lupus 
population. The average D^ within this 
cluster is 28.8, while the average D^ of its 
members to populations outside the cluster 
is 71.8. Although the lycaon and niger 
populations are fairly distinct, they are 
even more distant from the latrans and ja- 
miliaris species groups, and have a common 
similarity to the lupus population. These 
relationships are shown fairly well in Fig- 
ure 2, the plot of the populations using the 
latrans-lycaon and lycaon-niger discrimi- 
nant functions as coordinate axes. The lat- 
ter axis provides maximum separation of 
the wolf populations. Notice that the lu- 



ll 



Multiple Character Analysis of Canis 



229 



3r 





N 



_L 



_L 



I 



N 



II 12 13 14 15 

FIG. 2. Linear discrimination of C. latrans (C), C. 
lupus (\V), C. lupiis lycaon (A), and C. n/ger (N). 
The lycaon-niger discriminant function is used as 
the abscissa and the latrans-lycaon discriminant 
function is used as ordinate. 

pus population falls intermediate to, and 
completely bridges, the gap between lycaon 
and niser. 

Although we did not include recently 
collected specimens of red wolf from Lou- 
isiana in our linear discrimination, the 
relative position of each individual speci- 
men was computed and, while found to be 
clearly wolf, the specimens were spread 
somewhat o\er the range from niger to ly- 
caon. 

It now appears that the early populations 
described as Canis niger and n. gregoryi 
from the southeastern wooded regions, east 
of the range of Canis latrans, are a local 
form of Canis lupus, not a distinct species 
of wolf. The situation in the areas where 
these small wohes and the large coyote, 
C. /. frustror, meet is much more confused. 
The present study has not attempted to go 
beyond McCarley's conclusions (1962). We 
have, however, tested our methods on a 
small series from Fallsville, Newton Coun- 
ty, Arkansas. The specimens, collected in 
1921 and identified as Canis niger gregoryi 
(Young and Goldman, 1944), span the 
whole range of variation from coyote to 
wolf. Figure 3 shows this variation of the 
individuals using the latrans-lycaon and 
lycaon-niger discriminant function as co- 
ordinate axes, as in Figure 2. 

DISCUSSION 

To date most efforts to measure differ- 
ences between wolf, coyote, and dog skulls 



11 12 13 14 15 

FIG. 3. Evaluation of discriminant functions for 
the series of C. niger gregoryi from Fallsville, Ar- 
kansas. The coordinate axes are identical to those 
of Figure 2. 

have used a few specific measurements such 
as width between the premolar teeth ante- 
riorly, or have relied on standard length- 
breadth comparisons of the whole skull as, 
for instance, relation of zygomatic width to 
total length. Such data are useful but show 
too much overlap to separate reliably the 
species involved. They are also inadequate 
as an expression of the basic differences be- 
tween the skulls. These basic differences 
center around the differential development 
of different segments of the skull which, in 
their extreme form, are easily seen. Brain 
case, rostral, and interorbital shape of a 
t^pical coyote are quite different from 
those of a typical wolf. The significance of 
cranial measurements in expressing these 
differences in proportion depends on the 
multiple relationships of each measure- 
ment with a number of others, when size 
has been eliminated as a factor. The tech- 
nique of linear discrimination has allowed 
us to make use of these multiple relation- 
ships in comparing skulls. The results of 
these comparisons showed that all three 
species are sharply distinct, with lupus and 
familiaris resembling each other more than 
either does latrans. 

Since size has been eliminated as a char- 
acter, the numerical values of the discrimi- 
nant function may show two skulls to be 
most closely related which on the basis of 
size alone would be easy to tell apart. The 
same may be true of other unmeasurable 
but diagnostic characters. 

Often, of course, there is little difficulty 
in distinguishing between the three species 



78 



230 



Barbara Lawrence and William H. Bossert 



without resort to the kind of analysis de- 
scribed above. In addition to differences 
already discussed in the text, certain spot 
differences are often highly diagnostic: flat- 
tened, rugose bullae characterize dogs. Coy- 
otes have the dorso-posterior part of the 
brain case well inflated, with the maximum 
width of brain case in the region of the 
parietotemporal suture, the frontal shield 
not tilted up, and the postorbital constric- 
tion close to the postorbital processes. In 
wolves and dogs, the maximum width of 
the brain case is usually at the roots of the 
zygoma; the frontal shield tilts up, and the 
postorbital region is elongated, so that the 
constriction at the anterior part of the 
brain case and that behind the postorbital 
processes are well separated and the area 
between inflated. Further accentuating the 
different appearance of this region is the 
fact that the dorsal surface of the brain case 
in wolves and dogs is lower relative to the 
postorbital processes than in coyotes. The 
orbit in coyotes tends to be large; this 
shows both in vertical dimensions and in 
its length as compared to that of the zygo- 
matic arch. In coyotes also, as distinct from 
dogs and wolves, there is a round protuber- 
ance of the occiput, often thin-walled, over 
the vermis of the cerebellum; certain dif- 
ferences in the teeth, though not precisely 
measurable, are also rather diagnostic. 
These are well reviewed in Young and 
Jackson (1951) and will not be repeated 
here. In addition, the present authors have 

found useful the fact that in coyotes M- 
measured lateromedially has the distance 
from the outer border of the tooth to the 
base of the paracone less than the distance 
from this point to the inner margin of the 
tooth, while the reverse is true in wolves 
and dogs. Wear makes this a difficult meas- 
urement to take precisely, but the differ- 
ence, expressing as it does the plumper 
para- and metacones of wolves and dogs, is 
a significant one. None of these characters 
is completely reliable, just as is none of 
those described earlier. Used in combina- 
tion, and with total size included, they are 
adequate to identify most canids. 

The significance of the present study lies 
in the fact that linear discrimination, based 



on characters tested for their diagnostic 
value, can separate similarly-sized individ- 
uals of each of the three species considered. 
A corollary of this is the fact that a small 
wolf does not assume the characters of a 
large coyote, nor is the reverse true. Cri- 
teria have been observed and tested which 
distinguish the two species and these may 
be used to separate individuals which ap- 
proach each other in size. This has made 
possible a re-examination of the specific 
status of the red wolf, long a biologically- 
puzzling phenomenon. From the evidence 
at hand, it appears that from central Lou- 
isiana east to Florida the large canids hith- 
erto called C. niger and niger gregoryi are 
no more than subspecifically distinct from 
Canis lupus. Preliminary study of a small 
sample from the western part of the red 
wolf's range shows typical lupus and typical 
latrans both present, with the possibility of 
hybridization as McCarley has suggested. 
In investigating this possibility, we can now 
assume that w^e are considering only two 
species of wild canid, not three as has been 
previously supposed, and that we have over- 
lapping and possible hybridization of these 
two distinct species, not an intergrading 
from coyote to wolf across the southern 
states as has sometimes been postulated. 
Our test analysis of the Fallsville specimens 
has also confirmed what has been apparent 
for a long time, that cranial variation in 
localized series currently called C. niger 
gregoryi or C. niger rufus is atypically wide 
for a race of North American Canis. Not 
only is it greater than the range for a local 
population of a given subspecies of either 
lupus or latrans, but it is also wider than 
the range for either species taken as a 
whole. Either this means sympatry of lo- 
cally similar forms which have the same 
chromosome number and essentially similar 
karyograms (Benirschke and Low, 1965; 
Hungerford and Snyder, 1966) , or it means 
hybridization. Before this can be decided, 
both the morphological and the behavioral 
characteristics of these populations need to 
be studied in more detail. 

appendix a 
Following are listed the 42 measurements 



79 



Multiple Character Analysis of Canis 



231 



taken on the entire series. In the first para- 
graph are given the 24 tested for diagnos- 
tic value. The 16 of these used in our line- 
ar discrimination are italicized. In the sec- 
ond paragraph is a briefer listing of the re- 
maining 18 characters, which were found to 
be not taxonomically reliable. 

Skull. 1. Total length from sagittal crest 
to alveoli of I—; 2. Minimum distance from 
alveolus of M- to depression in front oj 
bulla at base of styloid process; 3. Mini- 
mum length of rostrum from orbital mar- 
gin to alveolus of I-; 4. Zygomatic width; 
5. Breadth across postorbital processes; 6. 
Maximum breadth of brain case at parieto- 
temporal suture; 7. Maximum crown width 
across upper cheek teeth; 8. Minimum dis- 
tance taken at right angles from alveolar 
margin of molars to orbit; 9. Maximum di- 
ameter of orbit, parallel to medial edge and 
starting at most ventral point; 10. Crown 

length of upper cheek teeth from C - M-; 
1 1. Crown length of P- externally; 12. Mini- 
mum crown width of P- taken between 
roots; 13. Maximum antero-posterior width 
of upper canine taken at base of enamel; 

14. Crown width of M-; 15. Crown width 
across upper incisors; 16. Height of brain 
case vertical to basi-sphenoid and not in- 
cluding sagittal crest; 17. Maximum width 
across occipital condyles; 18. Minimum 
height of jugal at right angles to axis of 
bone; 19. Minimum width between alveoli 

of P-. Lower jaw. 20. Crown length of P-; 
21. Maximum crown width of P--; 22. 

4 

Length of posterior cusps of P-, along line 
parallel to base from back of tooth to point 
below notch posterior to main cusp; 23. 
Crown length of M- parallel to main axis; 
24. Maximum crown width of M- at right 
angles to main axis. 

Skull. Condylo-basal length; palatal 
length; length of brain case; interorbital 
width; width of rostrum; width of nasals; 
height of nasal aperture; alveolar length of 
upper cheek teeth; alveolar length of P-; 
maximum width of P- anteriorly; antero- 



posterior diameter of I-; height of bullae; 
height of posterior bony nares. Lower jaw. 
Total length; distance from back of tooth 
row to condyle; alveolar length P- - M-; 

alveolar length C - M-; crown length C - 



M-. 

3 



ACKNOWLEDGMENTS 



The authors are indebted to Mr. John L. Para- 
diso of the United States National Museum, Dr. 
George B. Kolenosky of the Ontario Department 
of Lands and Forests, Dr. Douglas H. Pimlott of 
the University of Toronto, and Dr. Claude Minguy 
of the Department of Fish and Game of the Prov- 
ince of Quebec for making available much impor- 
tant material. 

This work has been supported by National Sci- 
ence Foundation Grant GB-1265. Computer time 
was supported by National Science Foundation 
Grant GP-2723. 



REFERENCES 

Benirschke, K., and R. J. Low. 1965. Chromosome 
complement of the coyote (Canis latrans). Mam- 
malian Chromosomes Newsletter No. 15, arranged 
by the Section of Cytology, The Univ. of Texas, 
M. D. Anderson Hospital and Tumor Institute, 
Houston, Texas, p. 102, 1 fig. 

Burt, W. H. 1946. The mammals of Michigan. 
Univ. of Michigan Press, Ann Arbor, xv -|- 288 
p., illustr. 

Gidley, J. W. 1913. Preliminary report on a recent- 
ly discovered Pleistocene cave deposit near Cum- 
berland, Maryland. Proc. U. S. Natl. Mus. 46:93- 
102, figs. l-8a. 

Goldman, E. A. 1937. The wolves of North Amer- 
ica. J. Mammal. 18:37-45. 

Hungerford, D. A., and R. L. Snyder. 1966. Chro- 
mosomes of a European wolf (Canis lupus) and a 
bactrian camel (Camelus bactrianus). Mam- 
malian Chromosomes Newsletter No. 20, arranged 
by the Section of Cytology, The Univ. of Texas, 
M. D. Anderson Hospital and Tumor Institute, 
Houston, Texas, p. 72-73, 1 fig. 

Jolicoeur, P. 1959. Multivariate geographical vari- 
ation in the wolf Canis lupus L. Evolution 13: 
283-299. 

Kendall, M. G. 1951. The advanced theory of sta- 
tistics, Vol. II. Hafner House, New York. 521 p. 

McCarley, H. 1962. The taxonomic status of wild 
Canis (Canidae) in the South Central United 
States. The Southwestern Naturalist 7:227-235. 

Pocock, R. I. 1935. The races of Canis lupus. Proc. 
Zool. Soc. London, part 3:647-686, 2 pis. 



80 



232 Barbara Lawrence and William H. Bossert 

Rao, C. R. 1952. Advanced statistical methods in tute, xx -f 636 p., illustr. 

biometric research. John Wiley, New York. 390 Young, S. P., and H. H. T. Jackson. 1951. The 

p. clever coyote. The Stackpole Co., Harrisburg, 

Young, S. P., and E. A. Goldman. 1944. The wolves Pa., and The Wildlife Management Institute, 

of North America. The American Wildlife Insti- Washington, D. C. xv -\- 411 p., illustr. 



81 



CHROMOSOME STUDIES OF POCKET GOPHERS, 

GENUS THOMOMYS. I. THE SPECIFIC STATUS OF 

THOMOMYS UMBRINUS (RICHARDSON) IN ARIZONA 

James L. Patton and Ross E. Dingman 

Abstract. — The complexities of morphology and, hence, taxonomy of pocket 
gophers (genus Thomomtjs) in southern Arizona are reflected by extreme 
interpopulation chromosomal variation in both T. hottae ( 2n = 76 ) and T. 
umhrinus (2n = 78). The variation consists of differing numbers of morpho- 
logical types of chromosomes for nearly each population karyotype. The known 
range of variation in either species is less than the amount of difference between 
the two. A somewhat strict ecological separation exists between T. hottae and 
T. umbrinus in areas of sympatry or near sympatry, with the former preferring 
the more friable soils of the valley floors and mountain tops and the latter 
confined to the indurate soils of the oak zones at intermediate elevations. 
Chromosomal and ecological concordance support the interpretation that T. 
hottae and T. umhrinus are distinct species. Limited hybridization between the 
two species at one locality of sympatric contact, however, is known. 

The taxonomy of Thomomys umbrinus (Richardson) has been the subject 
of considerable confusion in recent years. This problem centers primarily 
around isolated gopher populations inhabiting montane woodlands in south- 
eastern Arizona. These gophers have been allocated to three subspecies of 
T. umbrinus by Goldman ( 1947 ) and to two subspecies by Cockrum ( 1960 ) . 
Lange ( 1959 ) also recognized only two subspecies but used a different 
combination of names than did Cockrum ( 1960 ) . We follow this latter 
interpretation and recognize T. u. intermedins Mearns as occurring in the 
Santa Rita, Patagonia, and Huachuca mountains, and T. u. quercinus Burt 
and Campbell as occurring in the Pajarito Mountains. 

Hoffmeister and Goodpaster (1954:95) felt that ". . . perhaps in all of 
southern Arizona, gophers regarded as T. umbrinus by Goldman ( 1947 ) are 
best referred to T. bottae." This was finalized with their arrangement of T. 
burti proximus Burt and Campbell ( = T. umbrinus proximus auct. ) as a 
synonym of T. bottae hueyi Goldman. On the basis of this interpretation, Hall 
and Kelson (1959) regarded all populations of T. umbrinus and T. bottae 
as conspecific. Subsequently, Lange ( 1959 ) and Anderson ( 1966 ) have 
recorded sympatry or near sympatry for some populations of T. bottae and 
T. umbrinus, and Hoffmeister ( 1963 ) has revised his opinion of 1954 and 
implied that the populations of T. umbrinus in the Huachuca, Patagonia, 



82 



2 JOURNAL OP^ MAMMALOGY Vol. 49, No. 1 

and Pajarito mountains of southern Arizona are not conspecific with T. bottae. 

As recognized here, T. umbrinus {sensu stricto) is essentially limited to 
the Mexican Plateau (see Anderson, 1966) whereas T. bottae has a more 
northern and western distribution including most of the southwestern United 
States and northwestern Mexico. The two species are sympatric, or nearly so, 
in at least six localities, all in the extreme northwestern part of the range of 
T. umbrinus (i.e., the Pajarito, Patagonia, Santa Rita, and Huachuca mountains 
of Arizona, the Animas Mountains of New Mexico, and the Sierra de la 
Breiia of northwestern Chihuahua). In the first five of these areas, T. 
umbrinus occurs as "insular" populations, surrounded by intervening popula- 
tions of T. bottae. 

The systematic status of the Arizona populations has been a difficult 
problem to approach by use of conventional characters, and it still remains 
the subject of considerable debate. Many authors (Baker, 1953; Hoffmeister 
and Goodpaster, 1954; Lange, 1957; and Anderson, 1966) have pointed out 
the lack of a single, definable character that can be used consistently to 
separate T. umbrinus from T. bottae throughout the areas of sympatry or 
near sympatry. The karyotypic analysis reported herein may supply such a 
"diagnostic character," for in studies thus far conducted consistent differences 
exist between T. umbrinus and T. bottae in Arizona. 

Chromosomal characters in the future will aid in the "purification" of 
samples so that other characters, including standard morphological ones, 
may be better evaluated, and the ecologic, geographic, and genetic limits 
of gopher populations more clearly ascertained. At present, and until such 
"purified" collections are available, analysis of this type is difficult. 

Materials and Methods 

The animals studied (N = 65) were trapped alive using traps designed by Howard 
(1952). Specimens were initially assigned to species on the basis of pelage characters 
(see Goldman, 1947; Lange, 1957; Hoffmeister and Goodpaster, 1954). Such initial 
identification was later substantiated by the karotypes. Allocations of specimens to 
subspecies were based primarily on geography and gross morphology (Goldman, 1947; 
Hall and Kelson, 1959; Cockrum, I960; Lane, 1965). Conventional museum skins and 
skulls were saved of all animals examined and these are deposited in the collection of 
mammals of the Department of Biological Sciences (Zoology), University of Arizona, 
Tucson. See the list of specimens examined below for museum catalogue numbers and 
localities. 

Karyotype anulysis. — Metaphase chromosomes of bone marrow cells were analyzed 
using the in vivo colchicine-hypotonic citrate sequence described elsewhere (Patton, 1967). 
For the present analysis, the preparation of karyotypes from photomicrographs was based 
on the number of biarmed (metacentric, submetacentric, and subtelocentric ) and uniarmed 
(acrocentric or telocentric) autosomes present in the complement, and on the morphology 
of the X-chromosome. 

Sampling procedure. — Interpopulation variation was analyzed by comparing 16 popula- 
tions of gophers in Arizona, 13 of T. bottae and three of T. umbrinus (see Fig. 1). 
Intrapopulation variation was assessed by examining at least two individuals from all 
but one population sampled. The largest samples from a single population of both species 



83 



February 1968 PATTON AND DINGMAN— CHROMOSOMES OF THOMOMYS 




\i) Affs. 



10 



20 MILES 



Nogoles 



Fig. 1. — Map of southeastern Arizona showing locaHties of gophers analyzed (soHd 
circles = T. hottae; solid triangles = T. iiinhrinus); 5000-ft contour line shown. 



were 16 T. iimbrinus and 11 T. hottae, both from the Patagonia Mountains. These 
represent the most critical samples in the present analysis. Although the samples are 
relatively small, they do indicate no chromosomal variation within any single population. 

Results 

Extensive variation in the chromosomal complements between populations 
of T. hottae {i.e., subspecies or demes) and slight variation between popula- 
tions of T. umhrinus was found. No intrapopulation variation was found in 
either species. 



(} 



X X 



}i Si i-i A* h^ 

Fig. 2. — Karyotype of Thonwrmjs hottae modicus Goldman ($, UA 14992). Yerba 
Buena Ranch, Santa Cruz Co., Arizona. 



84 



JOURNAL OF MAMMALOGY 



Vol. 49, No. 1 



Table L — Siininuiry of kdnjottjpic variation in i)oi)ulation.s of Thomomys bottae in 

.wuihcrn Arizona. 



Subspecies 



d 



Locality 



Number of 
acrocentrics 



Morphology 

of X-chromo- 

some* 



V. 


b. 


alicnus 


- 


1 


St. David, San Pedro 
River, Cochise County 


9 


pairs 


ST** 


T. 


h. 


coll inns 


2 


4 


Turkey Creek and Rucker 
tanyons, Chiricahua Mts., 
Cochise Countv 


8 


pairs 


M 


T. 


h. 


collinus 


1 


1 


Rustlers Park, Chiricahua 
Mts., Cochise County 


6 


pairs 


M** 


T. 


b. 


ixtciitiatii.i 


1 


1 


Sulfur Springs Valley, 
Cochise County 


8 


pairs 


M 


T. 


b. 


proxinitis 


1 


3 


C'arr Canyon, Huachuca 
Mts., Cochise County 


4 


pairs 


SM** 


r. 


b. 


cdtdlinac 


2 


3 


Mt. Lemnion, Santa 
Catalina Mts. Pima County 


1 


pair 


SM 


r. 


b. 


iiioclictis 


3 


2 


vie. Tucson, Pima County 


o 


pairs 


ST 


r. 


b. 


niodicus 


4 


7 


Patagonia Mts., Santa 
Cruz County 





pairs 


SM 


r. 


b. 


inisillus 


1 


1 


Kit Peak, Quinlan Mts., 
Pima County 





pairs 


SM** 



* M = metacentric; SM = submetacentric; ST = subtelocentric. 
**Indicates probable designation of X-chromosomes. 

Thomomys bottae. — Although all T. bottae studied to date have a diploid 
number of 76 and a low number of acrocentric autosomes, seven different 
population karyotypes have been discovered. These populations differ in 
the number of acrocentric chromosomes and in the morphology of the 
X-chromosome (see Table 1). Samples of T. bottae modicus Goldman (Fig. 
2), with no acrocentric elements present, and of T. bottae aliemis Goldman 
(Fig. 3), with nine pairs of acrocentrics, represent the extremes of inter- 
population chromosomal variation known for the species. This great varia- 
tion contrasts to chromosomal variation known for other mammals, but it 
does parallel (and perhaps correlates with) the great variation in other 
morphological characters of this species (see Goldman, 1947; Durrant, 1946; 
Hall and Davis, 1935). Indeed, the populations sampled represent seven 
different subspecies to some workers (see Hall and Kelson, 1959). 

Thomomys umbrinus. — Populations of only one of the two subspecies 
recognized in Arizona by Lange (1959) have been sampled. This subspecies. 

Table 2. — Summary of kanjotijpic variation in population- of Thomomys umbrimis 
intermedins from the Santa Rita and Patagonia mountains, Arizotm. 

















Minute 


Morphology 


of 


Populatior 


1 
Canyon, 


? 


c^ 


M and SM* 


ST* 


A* 


chromosomes 


X-chromosome 


\ I adera 
















Santa 


Rita Mts. 


1 


.3 


10 


12 


.54 


6 


ST 




Gardner 


Canyon, 


















Santa 


Rita Mts. 


2 


- 


s 


12 


56 


6 


ST 




Svcamorc and 


















Italiar 


1 canyons, 


6 


10 


10 


10 


56 


6 


ST 




Patagonia Mts. 



















M = metacentric; SM = submetacentric; ST = subtelocentric; A = acrocentric. 



85 



February 1968 PATTON AND DINCMAN— CHROMOSOMES OF THOMOMYS 5 

ii(i XH KV) ^i*« 

Rfi U Af) ftn XA^MKKis Hl^ 

?SR ft?* Aft 1^^ Mr\ 4A A'^ /»^ x x 
/\(\ n<\ /^O 00 n(K f\Q AO 

Fig. 3. — Karyotype of Tlioniomys bottae alienus Goldman (9, UA 14989). About 
4.5 mi S St. David, San Pedro River Vallev, Cochise Co., Arizona. 

T. u. intermedins Mearns, is represented by three sampled populations that 
are characterized by a diploid number of 78, a high number of acrocentrics 
in the autosomal complement, and the presence of three pairs of minute 
acrocentrics (these latter elements are absent in all karyotypes of T. bottae). 
Slightly different karyotypes were found for each of these samples (see 
Table 2 and Figs. 4, 5, and 6). Again, the samples differ in the number of 
acrocentrics and in the relative number of each type of biarmed chromosomes. 
Unlike T. bottae, the X-chromosomes of all T. urnbrinus are subtelocentric 
and do not vary in morphology. 

The various population karyotypes of T. bottae have little similarity with 
those of T. urnbrinus. These two species differ noticeably in the number 
of biarmed and uniarmed chromosomes present in their respective comple- 
ments (see Table 3). From Table 3 it is also apparent that the total known 
range of variation within each species is less than the difference between 
them. 

T. bottae x T. urnbrinus hybrids. — The number of differences between 
the karyotypes of the two species facilitates the determination of any gene 
flow between them, since hybrids can be readily detected by the number 
of acrocentric chromosomes present in their complements. In the sample 
of both species from the sympatric locality in the Patagonia Mountains, a 

Table 3. — Chromosome features of populations of Thomomys bottae and Thomomys 
urnbrinus in southern Arizona, induding total known range of variation for each species. 



Feature T. bottae T. urnbrinus 



Diploid number 76 78 

Number of metacentrics and 

submetacentrics 22-32 8-10 

Number of subtelocentrics 32-46 10-12 

Number of acrocentrics 0-18 54-56 

Number of minute chromosomes 6 



86 



JOURNAL OF MAMMALOGY 



Vol. 49, No. 1 



Table 4. — Summary of chromosome features between sampled populations of Thomomys 

bottae niodicus and T. umbrinus intennedius from the Patagonia MountainSy Santa Cruz 

Co., Arizona, and of the four proposed hybrids. 





r. bottae 


Fi hybrids 
(UA15158) 




Backcross hybrids 






Feature 


UA14991 


UA15424 


UA15935 


T. umbrinus 


Diploid nunihcr 


76 


77 


76 


76 


77 


78 


Number of 














metacentrics and 


32 


21 


31 


33 


16 


10 


submetacentrics 














Number of 














subtelocentrics 


42 


26 


40 


40 


13 


10 


Number of 














acrocentrics 





28 


3 


1 


48 


56 


Number of minute 














chromosomes 





3 








4 


6 


Morphology of 














X-chromosome* 


SM 


SM/ST 


? 


p 


? 


ST 



* SM = submetacentric; ST = subtelocentric. 

single individual examined (UA 15158) possessed a diploid number of 77, 
and in all aspects of the karyotype it was intermediate between the two 
species (see Fig. 7 and Table 4). Such total intermediacy when compared 
to both species karyotypes from this locality (see Figs. 2, 6, and 7) leaves 
little doubt but that the specimen represents a first generation hybrid 
between T. bottae and T. umbrinus. The animal was a pregnant adult female 
with three nearly full-term and apparently normal embryos. The hybrid is 
thus judged to be fertile, and backcrossing to either parental species pre- 
sumably occurs, at least to a limited degree. 

« n u «K 

nh j)j& a u Ah »» (' 

X Y 

fiA OA Oo on 00 Oft ocv 

nrt ftn nn no ao on na 

|lf\ An tx€\ fyi\ H/^ 1^^ ^^ 

^(1 4\ ^ Af> /t^ .#.- •«'> 

Fig. 4. — Karyotype of Thomomys umbrinus intermedins Mearns {S, UA 14987). 
Gardner Canyon, Santa Rita Mts., Santa Cruz Co., Arizona. 



87 



February 1968 PATTON AND DINGMAN— CHROMOSOMES OF THOMOMYS 7 

X X 

^^ Aft Aft ftO ^^ ^^ 
^^ HA A^ Ail o^ A^ 

'"'ft ll#\ A^ -^^ ll<l #v*-» 
AM A^ A^ ^-^ -*•• «^* 

Fig. 5. — Karyotype of Thomomys umbrinus intermedins Mearns (9, UA 15343). 
Madera Canyon, Santa Rita Mts., Santa Cruz Co., Arizona. 



Three additional specimens examined from this population are judged 
to be backcross hybrids on the basis of the number of acrocentric elements 
in their respective karyotypes (Table 4). Two of these (UA 14991, 9, and 
UA 15424, S ) are the probable results of backcrossing to parental T. hottae, 
and one ( UA 15935, 9 ) the result of backcrossing to parental T. umbrinus. 
A more detailed analysis of this hybridization is presently under investigation 
and will be presented in the future. 

Discussion 

Ecological considerations. — Correlated with the karyotypic distinctness of 
the two species of Thomomys is a somewhat marked ecological separation in 
areas where the two are found in sympatry or near sympatry. Thomomys 
umbrinus was found only in the oak woodland through oak-pine woodland 
in the intermediate elevations of the Santa Rita and Patagonia mountains. 
These are two of the four mountain ranges in Arizona where presumed 
specimens of T. umbrinus were reported by Cockrum (1960). The other 
two populations allocated to T. umbrinus inhabit equivalent habitats in the 
Pajarito and Huachuca mountains. We have not yet sampled these popula- 
tions for karyotypic analyses, but have examined specimens from these areas. 

In the Huachuca Mountains, specimens obtained from what could be 
considered typical habitat for T. umbrinus {i.e., oak woodland) in Carr 
Canyon were found to be T. bottae, referable to the subspecies T. b. proximus 
Burt and Campbell. These specimens lack the somewhat distinctive dark, 
purplish-hued dorsum characteristic of T. umbrinus, and even without karyo- 
types they would not be confused with that species. Hoffmeister and Good- 
paster ( 1954 ) correctly allocated all of the specimens they examined from 



88 



8 JOURNAL OF MAMMALOGY Vol. 49, No. 1 



nt 



mumux. K 




X Y 



u^th (^H A6 ftfi on An 

Afi AA t\f\ 00 r\tk AA A/> 

Al* Aft ^SifN An ti ft A/4<»«* 



Fig. 6. — Karyotype of Thomomys timbrimis intermedins Mearns (6, UA 14990). 
Sycamore Canyon, Patagonia Mts., Santa Cruz Co., Arizona. 

the Huachuca Mountains to T. hottae. However, they incorrectly identified 
the material from Carr Peak as T. umhrinus intermedius Mearns, and on this 
basis, in part, assumed that only T. hottae occurred in the mountain range. 
Lange (1959) examined the type of T. u. intermedius and considered this 
name as valid and specifically distinct from the Carr Peak material examined 
by Hoffmeister and Goodpaster. Moreover, both Lange ( 1959 ) and Cockrum 
(1960) consider specimens from Brown Canyon and the vicinity of Panama 
Mine (near the west gate of Fort Huachuca) as T. umhrinus. Specimens 
examined by one of us (JLP) through the courtesy of Dr. Seth B. Benson 
from the Peterson Ranch, Sunnyside Canyon, definitely are referable to 
this species. Thomomys umhrinus is unquestionably present in the Huachuca 
Mountains, therefore, but additional specimens must be collected and karyo- 
typed to enable assessment of their ecological as well as genetical relation- 
ships to T. hottae in this same mountain range. 

Thomomys hottae is not known from the higher elevations of the Patagonia 
and Santa Rita mountains, although the latter supports well-developed pine 
forests similar to those occupied by T. hottae on more northern mountains 
in Arizona as well as the adjacent Huachuca Mountains. 

Gophers occurring in oak woodland habitats in other mountain ranges in 
southern Arizona, namely the Santa Catalina, Quinlan, and Chiricahua 
mountains, have karyotypes identical or similar to those of nearby popula- 
tions of T. hottae. These animals have been considered to be T. hottae and 
not T. umhrinus by most authors. 

The ecological separation of the two species is quite apparent in Sycamore 
and Italian canyons of the Patagonia Mountains. Generally, samples of T. 
hottae were obtained only at lower elevations in desert grassland or riparian 



89 



February 1968 PATTON AND DINGMAN— CHROMOSOMES OF THOMOMYS 

kit*' «**•••«• 



Fig. 7. — Karyotype of Fi hybrid between T. bottae modicus and T. umbrinus inter- 
medius (9, UA 15158). The proposed parental genomes are separated, with that 
of r. bottae on the left and that of T. umbrinus on the right. 

habitats (3600^800 ft), while T. umbrinus was found in open oak or juniper- 
oak woodlands (4500-6000 ft). Unlike the spatial separation of T. bottae 
and T. umbrinus at two localities in northwestern Chihuahua (Anderson, 
1966), the two species are sympatric along a narrow zone in the flat ground 
bordering the stream beds of Sycamore and Italian canyons {ca. 4400-4850 
ft; see Fig. 8). The floors of the canyons in this area consist of a mesquite- 
desert willow-grassland association with a few riparian elements {e.g., cotton- 
woods and sycamores) in Sycamore Canyon and a narrow desert riparian 
woodland community in Italian Canyon. Although both species were trapped 
on the canyon floors in such communities, T. umbrinus appears more limited 
to the open, rockier hillsides where Emory and Mexican blue oaks {Quercus 
emoryi and Q. oblongifoUa) predominate. 

Hijbridization. — At present, little more than speculative remarks can be 
made concerning the natural hybridization between T. bottae and T. umbrinus 
in Sycamore and Italian canyons of the Patagonia Mountains. The single Fi 
hybrid and the three individuals considered by their karyotypes to be back- 
cross hybrids all were trapped within the narrow zone of sympatry (see Fig. 
8, note localities of hybrids), an indication that the main populations of both 
species are not affected to a great extent by the hybridization. Although the 
Fi hybrid was fertile and backcrossing to both parental species is, therefore, 
judged to occur, lack of extensive introgression coupled with the narrowness 
of the hybrid zone indicates restricted gene flow between T. bottae and 
T. umbrinus at this single locality. 

Historical considerations. — The present distributions of many species in 
the inland Southwest have been explained in part by the shifting climatic 
and vegetational events of the late Pleistocene (summarized by Martin and 
Mehringer, 1965). Some populations that were continuous during late glacial 
to post-glacial times became disjunct, and interconnections were formed 
between other previously disjunct populations. This is apparent in the cases 



90 



10 



JOURNAL OF MAMMALOGY 



Vol. 49, No. 1 




Miles 



Fig. 8. — Map of Sycamore and Italian canyons, Patagonia Mountains, Santa Cruz Co., 
Arizona, showing area of sympatric contact between T. hottae and T. umbrinus (shaded 
area) and locahties where gophers were trapped in relation to zone of contact. SoHd circles 
= T. hottae; solid triangles = T. umbrinus; solid square = Fi hybrid; half-filled circles = 
hybrids backcrossed to T. bottae; half-filled triangle = hybrid backcrossed to T. umbrinus. 
(Additional specir^ens of T. bottae were trapped from outside the area indicated on map.) 

of T. bottae and T. umbrinus. Their present distributional pattern with 
"islands" of T. umbrinus in a "sea" of T. bottae, and the increased contact 
between the two species in Recent times, have been accompanied by repro- 
ductive isolating mechanisms that were inadequate to prevent limited hybrid- 
ization between the two species in the restricted area of the Patagonia 
Mountains. Presumably this occurred as the two species came into contact 
following changes in the vegetation in the present area of sympatry. Present 
hybridization between other groups of vertebrates (for example, Cnemi- 
dophorus — Zweifel, 1962; Lowe and Wright, 1966) and plants (for example, 
oaks — Tucker, 1963) in the same general area has been attributed to these 
factors also. 

Much of the current vegetation between the Santa Rita, Huachuca, and 
Patagonia mountains is desert grassland with scattered oaks and mesquites. 
A more well-developed oak woodland is present between the Patagonia and 
Pajarito mountains, following elevational contours into and out of Sonora. 
If the oak woodland were lowered 400 m during the late Pleistocene ( Wiscon- 
sin glaciation), as suggested by Martin and Mehringer (1965), all of these 
ranges would have been connected by well-developed oak woodland. Such 
habitats appear ideal for T. umbrinus in these mountain ranges today. 



91 



February 1968 PATTON AND DIXGMAX— CHROMOSOMES OF THOMOMYS 11 

Thomomys umbrinus is presently widespread on the Mexican Plateau, 
and was once undoubtedh' more widely spread in southern Arizona. The 
area that T. umbrinus now inhabits is known to contain the greatest degree 
of Mexican floral influence anywhere in Arizona ( Marshall, 1957; Martin, 
1963; Lowe, 1964); this applies especially to the vegetation at the lower and 
intermediate elevations. The two main factors contributing to the presently 
isolated state of T. umbrinus populations in Arizona were, then, the withdrawal 
of the extensive woodlands of the late glacial period to their present positions 
during the past 10,000 years (Martin and Mehringer, 1965), and the spread 
of r. bottae through the lower elevations in recently invaded desert scrub 
and desert grassland communities. 

In areas where T. bottae is present in the higher pine forests and the lower 
valley floors (for example, in the Huachuca Mountains). T. umbrinus, so far 
as is known, is restricted to the intermediate elevations in the oak zones. 
However, in mountain ranges where no T. bottae are found in upper eleva- 
tions (for example, in the Santa Rita Mountains), T. umbrinus inhabits both 
the oak woodland and the pine forests. It is apparent, therefore, that the 
present restriction of T. umbrinus to the oak zone is due in part to dis- 
placement through inability to compete with T. bottae. In all cases where 
T. bottae and T. umbrinus approach or meet in Arizona, the former occupies 
the more friable soils of the valley floors and mountain tops, whereas T. 
umbrinus is restricted more to the harder soils of the somewhat steeply 
inclined middle elevations. Thomomys bottae probably does not compete 
with T. umbrinus for these somewhat marginal habitats, for even in mountain 
ranges where T. umbrinus is absent, T. bottae populations are scarce in the 
indurate soils of the oak zones. The ability of T. umbrinus to survive in 
these habitats appears to have resulted in the present spatial and ecological 
relationships of the two species of gophers in southern Arizona. 

Taxonomic conclusions. — A basic problem to systematics has arisen from 
the above discussion — that is, whether to consider T. bottae and T. umbrinus 
in Arizona as distinct species that infrequently hybridize, or to consider them 
subspecies that intergrade. At the present time, it would appear more im- 
portant not to overshadow the biological findings with nomenclatorial 
problems. In this respect, we judge that consideration of the two forms as 
distinct species is in greater accord with the biological inferences. This 
interpretation allows for a greater appreciation and understanding of the 
past historical events, present distributional and ecological discordance, and 
great chromosomal distinction between T. bottae and T. umbrinus. 

Acknowledgments 

We are considerably grateful to Drs. Sydney Anderson, ^^'illiam B. Heed, T. C. Hsu, 
and John W. Wright for critically evaluating the manuscript. Special appreciation is 
due Dr. Wright for his sound biological advice and for aid in the field, to Dr. Anderson 
for clarifying the confusion of names apphed to the gophers of the Huachuca Mountains, 
and to Dr. E. L. Cockrvim for providing equipment and encouragement throughout this 



92 



12 JOURNAL OF MAMMALOGY Vol. 49, No. 1 

study. The field assistance of Robert J. Baker, Charles Drabek, and Oscar H. Soule is 
also ackno\%ledged. 

Specimens Examined 

Specimens prefixed by UA refer to those catalogued in the mammal collection, Depart- 
ment of Biological Sciences (Zoology), University of Arizona, Tucson. Other numbers 
refer to the personal field catalogue of one of us (JLP). 

Thomomys bottae catalinae {2$, 3 9 )• — Arizona. Pima Co.: Snow Bowl, Mt. Lemmon, 
Santa Catalina Mts. (JLP 737); Bear Wallow, Santa Catalina Mts. ( UA 15411-14). 

Thomomys bottae modicus (8$, 9 9). — Arizona. Pima Co.: Tucson (UA 1.5149-50, 
JLP 688); Molino Basin, Santa Catalina Mts. ( UA 1.5415-16). Santa Cruz Co.: 1.1 mi 
E Amado ( UA 15410); Verba Buena Ranch ( UA 14992, UA 15144, UA 15154); mouth 
of Italian Canyon, Patagonia Mts. ( UA 14988, UA 15409, UA 15943-44); Chamberlain 
Tank, Patagonia Mts. (UA 14993, UA 14906-07); Sycamore Canyon, Patagonia Mts., 
9.3 mi E Jet Arizona 82 and Washington Camp Road (UA 15942). 

Thomomys bottae extenuatus (l $ , 19). — Arizona. Cochise Co.: 0.2 mi E Jet 
Arizona 181 and Turkey Creek Canyon Road, Sulfur Springs Valley ( UA 15145); 3.9 mi 
E Jet Arizona 181 and Turkey Creek Canyon Road, Sulfur Springs Valley (UA 15151). 

Thomomys bottae collinus {Z$, 5 9). — Arizona. Cochise Co.: El Coronado Ranch, 
West Turkey Creek Canyon, Chiricahua Mts. (UA 15154, UA 15147); 1.7 mi E El 
Coronado Ranch, West Turkey Creek Canyon, Chiricahua Mts. (UA 15152, UA 15148); 
Rucker Canyon, Chiricahua Mts., ca. 5600 ft (UA 15146, UA 15153); 1 mi below Rustlers 
Park, Chiricahua Mts. (UA 15406-07). 

Thomomys bottae proximus (1$, 3 9). — Arizona. Cochise Co.: Carr Canyon Ranch, 
Huachuca Mts. (UA 15404-05); 0.5 mi N Clark Spring, Carr Canyon, Huachuca Mts. 
(UA 1.5417-18). 

Thomomys bottae alienus (19). — Arizona. Cochise Co.: ca. 4.5 mi S St. David on 
US 80 (UA 14989). 

Thomomys bottae pusillus (1$, 19)- — Arizona. Pima Co.: ca. 1.5 mi below Kit 
Peak National Observatory, Quinlan Mts. (UA 15419-20). 

Thomomys umbrinus intermedius {\0 i , 12 9). — Arizona. Santa Cruz Co.: Madera 
Canyon, Santa Rita Mts. ( UA 15343, UA 15163, UA 15403, UA 15001); Gardner Canyon, 
Santa Rita Mts. (UA 14986-87); Sycamore Canyon, Patagonia Mts., ca. 9.9 mi E Jet 
Arizona 82 and Washington Camp Road ( UA 14985 ) and ca. 9.3 mi E Jet Arizona 82 
and Washington Camp Road (UA 15937-41); ca. 1.2 mi E Crescent Spring (UA 15156, 
UA 15012); ca. 0.4 mi E Crescent Spring (UA 15160); ca. 0.6 mi E Crescent Spring 
(UA 14990); Crescent Spring (UA 15159); ca. 8.7 mi E Jet Arizona 82 and Washington 
Camp Road (UA 15408); mouth of Italian Canyon, Patagonia Mts. (UA 15157, UA 14983); 
Italian Canyon, Patagonia Mts. (UA 14984, UA 15936). 

Thomomys bottae x Thomom,ys umbrinus hybrids (15, 3 9). — Arizona. Santa Cruz 
Co.: Italian Canyon, Patagonia Mts. (UA 15158, UA 15424); Sycamore Canyon, Patagonia 
Mts., ca. 8.7 mi E Jet Arizona 82 and Washington Camp Road (UA 14991) and ca. 9.3 
mi E Jet Arizona 82 and Washington Camp Road (UA 15935). 

Literature Cited 

Antjerson, S. 1966. Taxonomy of gophers, especially Thomomys, in Chihuahua, Mexico. 

Syst. Zool., 15: 189-198. 
Baker, R. H. 1953. The pocket gophers ( genus Thomomys ) of Coahuila, Mexico. 

Univ. Kansas Publ., Mus. Nat. Hist., 5: 499-514. 
CocKRUM, E. L. 1960. The Recent mammals of Arizona. Univ. Arizona Press, Tucson, 

vii -^- 276 pp. 



93 



February 1968 PATTON AND DINGMAN— CHROMOSOMES OF THOMOMYS 13 

DuRRANT, S. D. 1946. The pocket gophers (genus Thomomys) of Utah. Univ. Kansas 

Publ, Mus. Nat. Hist., 1: 1-82. 
Goldman, E. A. 1947. The pocket gophers (genus Thomomys) of Arizona. N. Anier. 

Fauna, 59: 1-39. 
Hall, E. R., and W. B. Davis. 1935. Geographic distribution of pocket gophers (genus 

Thomomys) in Nevada. Univ. Cahfornia Publ. Zool., 40: 387-402. 
Hall, E. R., and K. R. Kelson. 1959. The mammals of North America. Ronald Press, 

New York, 1: xxx + 546 + 79. 
HoFFMEisTER, D. F. 1963. The yellow-nosed cotton rat, Sigmodon ochrognathus, in 

Arizona. Amer. Midland Nat., 70: 429-441. 
HoFFMEiSTER, D. F., AND W. W. GooDPASTER. 1954. The mammals of the Huachuca 

Mountains, southeastern Arizona. iHinois Biol. Monogr., 24: v -f 1-152. 
Howard, W. E. 1952. A live trap for pocket gophers. J. Mamm., 33: 61-65. 
Lane, J. D. 1965. Taxonomy of the pocket gopher, Thomomys haileyi. Ph.D. disserta- 
tion, Univ. Arizona, Tucson. 80 pp. 
Lange, K. I. 1957. Taxonomy and distribution of pocket gophers (genus Thomomys) 

in southeastern Arizona. M.S. thesis, Univ. Arizona, Tucson. 68 pp. 
. 1959. Taxonomy and nomenclature of some pocket gophers from southeastern 

Arizona. Proc. Biol. Soc. Washington, 72: 127-132. 
Lowe, C. H. 1964. The vertebrates of Arizona. Univ. Arizona Press, Tucson, vii + 

259 pp. 
Lowe, C. H., and J. W. Wright. 1966. Evolution of parthenogenetic species of 

Cnemidophorus (whiptail lizards) in western North America. J. Arizona Acad. 

Sci., 4: 81-87. 
Marshall, J. T., Jr. 1957. Birds of the pine-oak woodland in southern Arizona and 

adjacent Mexico. Pacific Coast Avifauna, 32: 1-125. 
Martin, P. S. 1963. The last 10,000 years, a fossil pollen record of the American 

Southwest. Univ. Arizona Press, Tucson, 87 pp. 
Martin, P. S., and P. J. Mehringer, Jr. 1965. Pleistocene pollen analysis and bio- 
geography of the Southwest. Pp. 433-451, in The Quaternary of the United 

States (H. E. Wright and D. G. Frey, eds.). Princeton Univ. Press, New 

Jersey. 
Patton, J. L. 1967. Chromosome studies of certain pocket mice, genus Perognathiis 

(Rodentia: Heteromyidae ) . J. Mamm., 48: 27-37. 
Tucker, J. M. 1963. Studies in the Quercus undulatus complex. Ill, The contribution 

of Q. arizonica. Amer. J. Bot., 50: 699-708. 
Zweifel, R. G. 1962. Analysis of hybridization between two subspecies of the desert 

whiptail lizard, Cnemidophorus tigris. Copeia, 1962: 749-766. 

Department of Biological Sciences, University of Arizona, Tucson, 85721, and Depart- 
ment of Biology, University of San Diego, San Diego, California 92110. Accepted 30 
October 1967. 



94 



Comp. Biochem. Physiol., 1966, Vol. 18, pp. 639 to 651. Pergamon Press Ltd. Printed in Great Britain 

SERUM PROTEIN ELECTROPHORESIS IN THE 

TAXONOMY OF SOME SPECIES OF THE GROUND 

SQUIRREL SUBGENUS SPERMOPHILUS* 

CHARLES F. NADLER and CHARLES E. HUGHES 

Department of Medicine, Northwestern University Medical School, 

Chicago, Illinois 

{Received IS January 1966) 

Abstract — 1. Serum protein patterns of Spermophilus undulatus, Spermophilus 
columbianiis and Spermophilus beldingi were analyzed by two-dimensional 
starch-gel electrophoresis. 

2. The patterns, although generally similar, exhibited variation in nine 
fractions or groups of fractions and these fractions had taxonomic significance 
at the level of population, subspecies or species. Intraspecific variability of two 
unidentified protein fractions was observed in S. undulatus kennicotti and S. 
beldingi and a third protein polymorphism involving transferrin was also 
observed in S. undulatus kennicotti. Intraspecific divergence between Arctic 
and sub-Arctic subspecies of S. undulatus was found and proteins from the 
latter show a closer resemblance to S. columbianus . 

3. The protein characters support present taxonomic concepts of the species 
of Spermophilus that indicate a close relationship between all three species and a 
closer relationship between S. undulatus and S. columbianus. 

4. Protein characters, as observed in the genus Spermophilus, appear to 
offer great promise as a method for systematic investigation at intraspecific 
levels where gross morphologic characters are least definitive. 

INTRODUCTION 
The concept that protein synthesis is dependent on rigid genetic control and is 
therefore a reflection of the genotype has provided a sound theoretical basis for 
utilizing physico-chemical characteristics of proteins in taxonomic studies. Among 
the simpler and more reliable techniques for study of serum protein fractions are 
paper electrophoresis and starch-gel electrophoresis. The more recent use of 
starch-gel electrophoresis provides an increased resolving power that results in 
patterns containing as many as thirty protein fractions in some human sera 
(Smithies, 1959), in comparison to the usual five fractions observed with paper 
electrophoresis. 

Many different vertebrates including primates (Goodman, 1963) and Rodentia 
(Blumberg et al., 1960) of the class Mammalia, Reptilia and Amphibia (Dessauer 
et al., 1962) and fishes (Sanders, 1964) have been investigated with electrophoretic 
techniques and the data applied to the taxonomy of groups within the respective 

* This investigation was supported by National Science Foundation Grant GB-3251. 

639 



95 



640 Charles F. Nadler and Charles E. Hughes 

classes. In their excellent review, Dessauer and Fox (1964) concluded that starch- 
gel electrophoresis showed greatest taxonomic promise at infraspecific and specific 
levels where the probability was high that proteins of identical mobility had 
identical structure. Certain proteins have been demonstrated to be polymorphic 
within a species and under genetic control. In the case of transferrin, which binds 
serum iron, gene frequencies can be calculated and successfully used to evaluate 
species and population relationships (Goodman et al., 1965). 

In the present investigation the serum proteins of Spermophilus undulatus, 
Spermophilus columbianus and Spermophilus beldingi were analyzed by two- 
dimensional starch-gel electrophoresis (Poulik & Smithies, 1958). These species 
constitute three of the eight species presently classified in the ground squirrel 
subgenus Spermophilus (Hall & Kelson, 1959) and they are of taxonomic interest for 
several reasons. First, Spermophilus is considered the most specialized of the 
ground squirrel subgenera (Bryant, 1945) and most recently evolved (Black, 1963) 
yet there is a paucity of gross morphological characters for convincing definition 
of interspecific relationships. Second, other lines of evidence have been applied 
to the latter problems that have yielded differing conclusions; zoogeographic 
evidence (Rand, 1954; MacPherson, 1965) and host-parasite observations (Holland, 
1958) indicate a close affinity between S. undulatus and S. columbianus whereas 
chromosomal evidence (Nadler, 1963, 1966) suggests an equal degree of divergence 
between S. undulatus, S. columbianus and S. beldingi. Because introducing evidence 
from additional characters might resolve these interspecific problems, the present 
study was undertaken with the following aims: 

(1) to determine whether the number and mobilities of fractions comprising 
the total serum protein pattern can be analyzed to yield reliable taxonomic charac- 
ters; (2) to determine the appropriate taxonomic level at which the protein 
characters are applicable; and (3) to test the validity of these characters by correlat- 
ing and comparing them with known systematic data of Spermophilus. 

MATERIALS AND METHODS 

Serum was obtained from the following animals : 

Spermophilus undulatus kennicotti (Ross). Alaska: 30 miles E. of Anaktuvuk 
Pass, 9 males and 5 females; 6 miles E. of Anaktuvuk Pass, 15 males and 7 females. 

Spermophilus undulatus kodiacensis (Allen). Alaska: Kodiak Island, 1 male and 
2 females. 

Spermophilus beldingi crebrus (Hall). Idaho: Twin Falls Co.; 10 miles N.W. of 
Buhl, 3 males and 3 females. 

Spermophilus beldingi oregonus (Merriam). Oregon: Harney Co.; Malheur 
Valley, 2 males and 1 female ; Burns, 6 males and 4 females. 

Spermophilus columbianus columbianus (Ord). Idaho: Adams Co.; Brundage 
Mountain, 4 males and 10 females. 

Blood was drawn from the heart using sterile equipment and the serum was 
stored at 4°C. Serum proteins were analyzed using a technique for horizontal, two- 
dimensional, starch-gel electrophoresis (Poulik & Smithies, 1958) combined with a 



96 



SERUM PROTEIN PATTERNS OF THE GROUND SQUIRREL 641 

tris-discontinuous buffer system (Poulik, 1957). The procedure was modified as 
reported by Goodman (1963). Starch blocks were bisected, stained with Nigrosin 
for 2-5 min (1 g Nigrosin, 30 cc acetic acid, 135 cc methyl alcohol and 135 cc 
distilled water) and decolorized for 24 hr using the same solution without the dye. 
Two to three separations of each serum specimen were performed on different days 
and all runs were carefully compared before recording the protein pattern of an 
individual animal as a scale indian ink drawing. Fractions with staining density 
equal to albumin or transferrin were recorded in black, those with faint staining 
reaction were drawn with open lines and fractions of intermediate intensity were 
stippled. When question arose regarding the presence or absence of a given 
fraction, additional runs were made to clarify the problem. 

The densely staining fraction with fastest mobility on paper and starch is 
tentatively labeled albumin and the fraction with slowest migration rate is labeled 
gamma globulin. Transferrins {Tf) were identified in several animals of each 
species by Fe^^ radioautography (Smithies, 1959). Transferrin was investigated 
at the interspecific level by simultaneously running serum samples from each 
species in one-dimensional starch-gel separations. 

RESULTS 

The serum protein patterns of S. undulatus, S. columbianus and S. beldingi show 

an overall similarity in the number of protein fractions and their respective 

mobilities (Figs. 2-8). However, a careful comparison shows nine major differences, 

illustrated in Fig. 1, that are exhibited in one or more species or populations and 

Alb 

<£-3 *"" A 




Fig. 1. A hypothetical separation of ground squirrel serum proteins illustrating 
fractions with taxonomic significance. The inital separation on paper results in a 
horizontal separation from left to right, followed by starch-gel electrophoresis 
which produces a vertical separation. The labeled fractions correspond with the 
following characters: Albumin (Character I), Fraction Group A (II), Fraction 
B (IV), Fraction C (V), Transferrin or T/(III), Fraction D (VI), Fraction E (VII) 
and Fraction F (VIII). The number of arc-like fractions constitute Character IX. 
Gamma globulin, y, has the slowest mobility on both paper and starch. 



22 



97 



642 Charles F. Nadler and Charles E. Hughes 

they may be evaluated as possible taxonomic characters. Other differences in the 
protein patterns were observed in some of the figures, but were inconsistent or 
difficult to evaluate because of faint staining properties. Because fractions other 
than transferrin were not characterized with regard to chemical structure or 
function, they are given a letter designation from A through F. It is recognized 
that similarity in mobility and configuration, as determined by a single technique, 
does not necessarily indicate identical chemical structure and it should be emphas- 
ized that no individual studied contained all nine characters. 



*is:i 





Fig. 2. A protein pattern from S. undulatus kemiicotti (30 mile population). The 
albumin is homogeneous. Fraction Group A contains four fractions; Fractions B 
and C are both present; two transferrins are present; Fractions D and E are 
absent; and Fraction Group F is not separated. One arc fraction is observed. 

For clarity, the nine protein characters observed in S. undulatus, S. columbianus 
and S. heldingi will be described individually and later comparisons made between 
taxa. The same data are presented in tabular form for each species in Table 1. 

Character I. This character consists of the presence or absence of a homogene- 
ous serum albumin fraction. S. undulatus (Figs. 2-6) and S. beldingi (Fig. 8) have a 
homogeneous serum albumin while S. columbianus (Fig. 7) showed an indication of 
two fractions migrating with nearly identical mobilities on starch. 

Character II. This character, designated Fraction Group A, is composed of 
three to four fractions that migrate slightly slower than albumin (Fig. 1). Both 
populations of S. undulatus kennicotti are characterized by Fraction A containing 
four individual fractions having an identical group configuration (Figs. 2, 3, 4, 5). 
In contrast, S. undulatus kodiacensis has only three fractions and these assumed a 
different configuration (Fig. 6). This pattern seen in S. undulatus kodiacensis is 
found to be identical to Fraction Group A in S. columbianus (Fig. 7). Fraction 
Group A of S. beldingi (Fig. 8) contains three fractions that exhibit a configuration 
different from the other taxa. Therefore, Character II shows both interspecific 
and intraspecific variability without individual variation. 



98 



SERUM PROTEIN PATTERNS OF THE GROUND SQUIRREL 



643 



.^ 



CO 

o 

< 

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644 



Charles F. Nadler and Charles E. Hughes 



Character ///consists of the number of transferrin fractions and their mobilities 
(Fig. 1). The population of S. undulatus kennicotti from 30 miles E. of Anaktuvuk 
Pass is polymorphic with respect to transferrin because 8 of 14 animals have two 
darkly staining bands with nearly identical mobility (Figs. 2, 3), both of which 



Z253. 



Tf 



^ 





Fig. 3. A protein pattern from S. undulatus kennicotti (30 mile population). This 
animal differs from the animal in Fig. 2 by an absence of Fractions B and C. Two 
transferrins are present. Fraction Group F is continuous. 



\^^ 




<=> Ci> 



Tf 




^*i!il^ 





Fig. 4. A protein pattern from S. undulatus kennicotti (30 mile population). This 

specimen lacks Fraction B, but Fraction C is present and only one transferrin {Tf) 

is observed. Note the absence of a separation within Fraction Group F. 

bind Fe^^. At present, the slower fraction is designated as a second molecular 
form of transferrin. The population of S. undulatus kennicotti from 6 miles E. of 
Anaktuvuk Pass is homogeneous with respect to transferrin, and only one fraction, 
migrating with a mobihty identical to the faster fraction from the 30 mile population, 



100 



SERUM PROTEIN PATTERNS OF THE GROUND SQUIRREL 



645 



is observed in each of the 22 animals (Fig. 5). On the basis of the transferrin 
polymorphism it is possible, when the populations are considered as a whole, to 
differentiate the two by this character. 




Fig. 5. A protein pattern from S. undulatus kennicotti (6 mile population). Fraction 

B is absent which is characteristic of all specimens from the 6 mile population. A 

single transferrin {Tf) is present. Fraction F is continuous. 



O 




Fig. 6. A protein pattern from S. undulatus kodiacensis. Fraction Group A 
contains three fractions with a configuration similar to S. columbianus (Fig. 7). Frac- 
tions B and C are present and a single transferrin (77) with a mobility identical to 
the faster fraction of 5. undulatus kennicotti is observed. A darkly staining Fraction 
D is present whereas Fraction E is absent. The two fractions comprising F are 

separated. 

All 3 specimens of S. undulatus kodiacensis (Fig. 6) have a single transferrin 
fraction that migrates at the same rate as the faster transferrin of both population 
samples of S. undulatus kennicotti, which suggests a common relationship between 
the three populations studied. 



101 



646 Charles F. Nadler and Charles E. Hughes 

S. columbianus (Fig. 7) and S. beldingi (Fig, 8) each have a single transferrin 
fraction and the transferrins of both species have an identical mobility that is faster 
than the mobility of S. undulatus transferrin. 

Character IV consists of a single fraction that migrates slightly more slowly, 
on both paper and starch-gel, than the fastest arc-like fraction, and it is designated 
Fraction B (Fig. 1). It stains with moderate or strong intensity. Fraction B was 
present in 4 of the 14 specimens of S. undulatus kennicotti (Fig. 2) from the 30 mile 
population and absent in all animals from the 6 mile population (Fig. 5). 

Fraction B was present in all 3 specimens of S. undulatus kodiacensis (Fig. 6), 
8 of 19 specimens of S. beldingi (Fig. 8) and all 10 specimens of S. columbianus 
(Fig. 7). 




Fig. 7. A protein pattern from S. columbianus columbianus. The albumin is 
notched, indicating a heterogeneous fraction. Three fractions comprise Fraction 
Group A and their configuration resembles .S. undulatus kodiacensis (Fig. 6). Both 
Fractions B and C are present and a single transferrin {Tf) migrates more rapidly 
than Fraction C and the Tf of S. undulatus (Figs. 2-6). Fractions D and E are 
present and Fraction Group F is separated. Three arc fractions are observed, a 

characteristic feature of the species. 

Character V. Fraction C constitutes Character V, It migrates faster than 
transferrin, slower than Fraction B and is located diagonally between the two 
fractions on the two-dimensional separation (Fig. 1). Staining intensity varies 
between individual specimens from moderate to strong. 

Among specimens of S. undulatus kennicotti, from the 30 mile population 
Fraction C was observed in 8 of 14 specimens (Fig. 2, 4) and 15 of 22 specimens 
from the 6 mile population (Fig. 5). All specimens of S. undulatus kodiacensis 
(Fig. 6), S. columbianus (Fig. 7) and S. beldingi (Fig. 8) had patterns containing 
Fraction C, and no geographic variation was seen. 

Character VI is a strongly staining fraction, designated Fraction D, that 
migrates faster than gamma globulin on paper but slower in starch (Fig. 1). Frac- 
tion D is absent in both populations of S. undulatus kennicotti (Figs. 2, 3, 4 and 5) 



102 



SERUM PROTEIN PATTERNS OF THE GROUND SQUIRREL 647 

and present in 5. undulatus kodiacensis (Fig. 6), S. coliimbianus (Fig. 7) and S. 
beldingi (Fig. 8). There is no intrapopulational variation. 

Character VII consists of a small lightly or moderately staining fraction, 
Fraction E, that migrates slightly faster than Fraction D on both paper and 
starch-gel (Fig. 1). Fraction D is absent in both populations of S. undulatus 
kennicotti (Figs. 2-5) and in S. undulatus kodiacensis (Fig. 6). It is present in S. 
columbianus (Fig. 7) and S. beldingi (Fig. 8). 




Fig. 8. A protein pattern from 5. beldingi crebriis. Fraction Group A contains 
three fractions with different configuration from S. undulatus and S. columbianus. 
Fractions B, C, D and E are present. A single transferrin {Tf) with mobility 
more rapid than Fraction C and similar to Tf oi S. columbianus is present. Fraction 

Group F is separated. 

Character VIII consists of two fractions that migrate more slowly than Fraction 
E on starch but at the same or faster rate on paper, and they are designated Fraction 
Group F (Fig. 1). The two fractions are separated by a gap in S. undulatus kodia- 
censis (Fig. 6), S. columbianus (Fig. 7) and S. beldingi (Fig. 8) that is produced by 
more rapid migration of one fraction during the initial paper run. Conversely, 
Fraction Group F is not separated by a gap in either population of S. undulatus 
kennicotti (Figs. 2, 3, 4, 5). 

Character IX. The number of arc-like fractions observed in the protein pattern 
varies. S. undulatus kennicotti, S. undulatus kodiacensis and S. beldingi patterns are 
characterized by one arc fraction whereas S. columbianus patterns (Fig. 7) contain 
three arc fractions. 

DISCUSSION 
The present study demonstrates that serum protein patterns from three related 
ground squirrel species can be analyzed to provide nine potential taxonomic 
characters. The theoretical basis for the valid use of proteins as characters rests 
upon the assumption that they are under genetic control and differences in genotype 
will be reflected by an alteration in chemical structure and behavior. However, 



103 



648 Charles F. Nadler and Charles E. Hughes 

before accepting these characters as rehable indicators of taxonomic relationships, 
it is important to attempt to exclude protein differences influenced by the stage of 
development or physiologic state of the animal (Dessauer & Fox, 1964). In this 
study, no juvenile or pregnant animals were studied and no differences in pattern 
could be attributed to the sex of the animal. With respect to seasonal influences, 
S. undulatus kodiacensis specimens were obtained in late April 1965, S. beldingi 
specimens were collected from 27 May-25 June 1965, and S. columbianus specimens 
were collected on 19 August 1965. The two populations of S. undulatus kennicotti 
that showed the greatest intraspecific variation in proteins were collected between 
20-30 August 1965. Animals were not examined just before or after hibernation. 
These observations, we believe, indicate that the proposed protein characters are 
not due to non-genetic variation. 

Protein characters appear definitive at the species level where Characters I, II, 
III, VI, VII, VIII and IX may be used alone or in combination (Table 1) to 
distinguish individual species, and these characters appear fully as diagnostic as 
such gross morphological characters as pelage color, size, etc. (Howell, 1938). 
Two taxonomic conclusions at the species level are suggested by the protein 
characters derived from this investigation. First, S. undulatus, S. beldingi and S. 
columbianus all show a certain general similarity in their protein patterns that 
suggests a common ancestral relationship, although each exhibits a number of 
characteristic features. 5. beldingi is unique in its manifestation of Character II, 
by a combination of Characters I and IX it can be distinguished from S. columbian- 
us, and utilizing Characters III and VII it can be distinguished from S. undulatus. 
S. columbianus has two unique characters, I and IX, yet it exhibits a similarity and 
presumably close relationship to S. beldingi with respect to Characters III, VI, VII 
and VIII. 

Second, it is pertinent that S. undulatus kennicotti and S. undulatus kodiacensis, 
which share a number of characters that distinguish them from the other species 
(Table I), also differ with respect to Characters II, VI and VIII. In fact, these 
latter characters suggest a close relationship between S. undulatus kodiacensis and 
S. columbianus whereas S. undulatus kennicotti might be considered more divergent. 
The validity of these seemingly paradoxical observations receives support from 
zoogeographic and ectoparasite studies. Rand (1954) suggests that S. undulatus 
and S. columbianus originated from the same stock which became separated by 
continental glaciation. One part survived in the Beringia refugium during the 
Wisconsin phase of the Pleistocene and differentiated during the separation to 
become undulatus and the other survived in a refugium south of the ice and became 
what is now columbianus. Holland (1958) compared samples of fleas from S. 
undulatus of Western Alaska and Northern British Columbia with samples from S. 
columbianus and regarded the fleas only weakly differentiated at the subspecies 
level. These observations suggested the ranges of the two ground squirrels were 
at one time contiguous (Holland, 1963) and the possibility that they evolved from 
a single ancestral stock is also strongly suggested by protein data from the present 
study. MacPherson (1965) also accepts the thesis offered by Rand (1954) and 



104 



SERUM PROTEIN PATTERNS OF THE GROUND SQUIRREL 649 

supported by Holland (1958). Therefore, among the three species we have 
examined, the kodiacensis population of S. iindulatus exhibits a closer degree of 
relationship to 5. columbiamis than that found between any other two species. 

Analysis of mitotic chromosomes from species of the genus Spermophilus has 
provided evidence for an equal degree of kar^otypic divergence between 5. 
beldingi with diploid number {In) of 30, S. columbianus 2n = 32 and S. undulatus 
with 2n = 34 (Nadler, 1966). Comparison of their chromosomes did not suggest 
a particularly close relationship between 5. undulatus and S. columbianus because 
several relatively uncommon types of rearrangements had to be postulated as the 
mechanisms responsible for their kar^'otypic divergence. The chromosome data 
might be interpreted to indicate that the two species diverged less recently than 
other lines of evidence suggest, but it is generally recognized that no one line of evi- 
dence invariably provides unequivocal evidence for satisfying taxonomic decisions. 

The subspecific divergence between S. undulatus kennicotti and S. undulatus 
kodiacensis, which is suggested by protein Characters II, VI and VIII, correlates 
with Holland's (1958, 1963) observations that Arctic and sub-Arctic populations of 
S. undulatus are parasitized by different species of fleas. He postulated a possible 
intraspecific divergence within these ground squirrels, although it was recognized 
that the differences could be explained by a dependence of the fleas upon ecologic 
factors other than the host. Perhaps these three lines of evidence, mammalian 
morpholog}', Siphonapteran morphology and protein analysis, may be interpreted 
as indicating differing rates of evolutionary divergence from what must have once 
been a common ancestral gene pool. The Arctic subspecies of S. undulatus may 
have diverged farther from the ancestral genotype than sub-Arctic subspecies 
which appear to share a greater number of common characteristics w^ith S. 
columbianus. It should, of course, be emphasized that the several evidences of 
divergence manifested by S. undulatus are of a low degree of magnitude and do not 
imply achievement of species status, although they do suggest the probability of 
incipient speciation within S. undulatus. 

The two subspecies of 5. beldingi that were studied could not be differentiated 
by trenchant protein characters. However, the frequency of Fraction B in two 
populations of S. beldingi oregonus was 1/10 and 1/3 and in S. beldingi crebrus, it was 
6/6. This fraction, constituting Character IV, appears to be a genetically controlled 
protein that exists in a polymorphic state similar to, but distinct from, transferrin 
and haptoglobin. As such, its gene frequency might be determined in larger samples 
from additional populations and thereby serve as a means for distinguishing these 
tw'o subspecies of S. beldingi. 

Differences in protein pattern between populations of S. undulatus kennicotti 
are quite striking and they involve two apparently unrelated fractions (Table 1). 
First, 8 of 14 specimens of kennicotti from the 30 mile population exhibit two 
transferrin fractions as judged by the ability of both to bind Fe^^. In contrast, 
sera from the 22 animals obtained 6 miles from Anaktuvuk Pass contain only one 
transferrin. Thus, the two populations can be differentiated on the basis of the 
frequency of one versus two transferrins ; similar observations have been reported 



105 



650 Charles F. Nadler and Charles E. Hughes 

in primates (Goodman et ai, 1965) and reptiles (Dessauer et ai, 1962). A second 
population difference consists of the presence of a low frequency of Fraction B 
(4/14) in the 30 mile kennicotti population and a complete absence in the 6 mile 
population (0/22). The chemical identity and function of this fraction are not 
known: it exists in a polymorphic state in both S. undidatus kennicotti and S. 
beldingi, whereas it is present in all samples of ^S. undulatus kodiacensis and S. 
columbianus. As mentioned in the discussion of this fraction in S. beldingi, calcula- 
tion of its frequency in larger population samples might provide an additional 
reliable indicator of population composition that could be employed with transferrin 
in the study of kennicotti populations. A third protein, Fraction C, exhibits a 
nearly equal degree of variation in the two kennicotti populations and therefore this 
fraction does not aid in their differentiation, although the fact that all three speci- 
mens of 5. undulatus kodiacensis manifested this fraction suggests that Character V 
might be applicable at the subspecies level if larger samples were studied. 

Because of the differences shown to exist between the proteins of ground 
squirrels from the 30 and 6 mile localities, it is necessary here to consider the 
taxonomic status of specimens from the Anaktuvuk Pass region and the geographic 
distribtuion of animals examined in the present study. Concerning taxonomic 
status, Bee & Hall (1956) examined a large sample of S. undulatus from the entire 
Arctic slope of Alaska, including specimens from Anaktuvuk Pass and Tulugak 
Lake located 12 miles N. of Anaktuvuk Pass, and concluded that all were referable 
to a single subspecies, kennicotti. Specimens analyzed in the present study were 
taken from a locality on the Anaktuvuk River (Arctic slope Brooks Range) 6 miles E. 
of Anaktuvuk Pass and are probably also referable to kennicotti. The second 
population we studied, however, was taken 30 miles E. of Anaktuvuk Pass on 
Ernie Creek, which is a tributary of the Koyukuk-Yukon River Drainage (south 
slope Brooks Range). Since animals from the south slope of the Brooks Range 
have not yet been studied in detail, our sample from the 30 mile population can be 
only tentatively regarded as kennicotti and the possibility that they are referable to a 
different subspecies, perhaps osgoodi, is open to consideration. 

There are no obvious physical barriers at the divide that might separate the two 
populations of S. undulatus we studied, although we did observe that the terrain 
even in mid-August was wet and poorly drained for about 2 miles on either side 
and that area may be unsuitable for burrow construction. Future studies might be 
profitably directed toward analysis of proteins from larger samples and examination 
of additional north and south slope colonies in an attempt to further characterize 
and explain the mechanisms responsible for the divergence we observed within 
S. undulatus kennicotti. 

Acknoiuledgements — We thank Doctor Robert L. Rausch and Russell Pengelly for 
generously providing some of the specimens studied. Nancy W. Nadler, Bob Ahgook and 
Johnny Rulland rendered invaluable service to the senior author during field work in Alaska. 
Doctors Joseph Curtis Moore and Roy Patterson offered valuable suggestions and reviewed 
the manuscript. Doctor Morris Goodman offered encouragement and advice concerning 
methodology. 



106 



SERUM PROTEIN PATTERNS OF THE GROUND SQUIRREL 651 

REFERENCES 

Bee J. W. & Hall E. R. (1956) Mammals of northern Alaska on the Arctic slope. Univ. 

Kans. Pubis Mus. nat. Hist. 8, 1-309. 
Black C. C. (1963) A review of the North American Tertiary Sciuridae. Bull. Mus. comp. 

Zool. Harv. 130, 109-248. 
Blumberg B. S., Allison A. C. & Garry B. (1960) The haptoglobins hemoglobins and 

serum proteins of the Alaskan fur seal, ground squirrel and marmot. J. cell. comp. 

Physiol. 55, 61-71. 
Bryant M. D. (1945) Phylogeny of Nearcac Sciuridae. Am. Midi. Nat. 33, 257-390. 
Dessauer H. C. & Fox W. (1964) Electrophoresis in taxonomic studies illustrated by 

analyses of blood proteins. In Taxonomic Biochemistry and Serology (Edited by Leone 

C. A.), pp. 625-647. Ronald Press, New York. 
Dessauer H. C, Fox W. & Hartwig Q. L. (1962) Comparative study of transferrins of 

Amphibia and Reptilia using starch-gel electrophoresis and autoradiography. Comp. 

Biochem. Physiol. 5, 17-29. 
Goodman M. (1963) Serological analysis of the systematics of recent Hominoids. Human 

Biol. 35, 377^36. 
Goodman M., Kulkarni A., Poulik E. & Reklys E. (1965) Species and geographic differ- 
ences in the transferrin polymorphism of macaques. Science, N.Y 147, 884-886. 
Hall E. R. & Kelson K. R. (1959) The Mammals of North America, Vol. 1, pp. 1-546. 

Ronald Press, New York. 
Holland G. P. (1958) Distribution patterns of northern fleas (Siphonaptera). Proc. \Oth 

int. Congr. Ent. 1, 645-658. 
Holland G. P. (1963) Faunal affinities of the fleas (Siphonaptera) of Alaska: With an 

annotated list of species. In Pacific Basin Biogeography (Edited by Gressitt J. L.), 

pp. 45-63. Bishop Museum Press, Honolulu. 
Howell A. H. (1938) Revision of the North American ground squirrels. A'^. Am. Fauna 56, 

l-25o. 
MacPherson a. H. (1965) The origin of diversity in mammals of the Canadian arctic 

tundra. Systematic Zool. 14, 153-173. 
Nadler C. F. (1963) The application of chromosomal analysis to taxonomy of some North 

American Sciuridae. Proc. XVI int. Congr. Zool. 4, 111-115. 
Nadler C. F. (1966) Chromosomes and systematics of the ground squirrel subgenus 

Spermophilus. To be published. 
Poulik M. D. (1957) Starch-gel electrophoresis in a discontinuous system of buffers. 

Nature, Lond. 180, 1477-1479. 
Poulik M. D. & Smithies O. (1958) Comparison and combination of the starch-gel and 

filter-paper electrophoretic methods applied to human sera: two-dimensional electro- 
phoresis. Biochem. J. 68, 636-643. 
Rand A. L. (1954) The ice age and mammal speciation in North America. Arctic 7, 31-35. 
Sanders B. G. (1964) Electrophoretic studies of serum proteins of three trout species and 

the resulting hybrids within the family Salmonidae. In Taxonomic Biochemistry and 

Serology (Edited by Leone C. A.), pp. 673-679. Ronald Press, New York. 
Smithies O. (1955) Zone electrophoresis in starch-gels: Group variations in the serum 

proteins of normal human adults. Biochem. J. 61, 629-641. 
Smithies O. (1959) Zone electrophoresis in starch-gels and its application to studies of 

serum proteins. Adv. Protein Chem. 14, 65-113. 



107 



\'oL SO, pp. 22-3-226 1 December 1967 

PROCEEDINGS 
OF THE 

BIOLOGICAL SOCIETY OF WASHINGTON 

THE SYSTEMATIC POSITION' OF THE BATS DESMODUS 

AND CHILOXYCTERIS. BASED OX HOST-PAK\SITE 

RELATIONSHIPS (MAMMALIA: CHIROPTEIL\)i 

By C. E. Machado-Allisox 

Instituto de Zoologia Tropical, Universidad 

Central de Venezuela 

Patterson (IGSe^i has pointed out that the fossils and ecto- 
parasites of bats pro\ide ver\- Little e\idence which can be 
used in clarif>"ing the problems of phylogem' in the order 
Chiroptera. Indeed, chiropteran fossils are scarce, and the 
majorit}- of chiropteran ectoparasites belong to groups that, 
ha\ing a Hfe histon- stage off the body of the host do not 
show notable specificit>". Another factor detracting from the 
use of ectoparasites is the intimate ecological association 
existing betvveen bats of different groups, particularly those 
found in caves, holes in trees, etc., where, occasionally, several 
species roost together. This beha\'ior favors, without doubt, 
polyhaematophag>", and there are striking cases of this such 
as the presence of fleas of the family IschnopsylHdae on bats 
of the distantly related famHies Molossidae (Tadarida Raf- 
inesque) and Xoctihonidae {ycctilio Linnaeus). However, 
host-parasite relationships may yet prove to be of value in 
shedding new hght on phylogenetic problems in Chiroptera. 
It must be realized that we still know httle about such relation- 
ships in the majorit>- of bats and that only in the last few 
years have careful well-documented collections of the ecto- 
parasites been made. 

In \iew of these facts, it becomes particularly important 
to study a group of ectoparasites, such as the Spintumicidae 
(Acarina. Mesostigmata) which apparently show great host 



-A eor-tribntion of the S~/.:':.-. -;in Venezuelan Project, supported by a 
• - DA-49-193-MD-27SS, of the Medical Research and Development 

_ ---r. i, Office cf the Siirgeon General, U. S. Army. 

35— Pp.oc. Biol. Soc. W.\sh., Vol. SO, 1967 (223) 



108 



224 Proceedings of the Biological Society of Washington 

specif icit\' (Rudnick, 1960; Macbado-Alli'soD. 1965a), and also 
show peculiar modifications in their life c\'cle (Baer, 1952; 
Rudnick, op. cit.), for instance, ovo\i\~iparit>- and reduction 
in number of n)Tnphal stages. 

In the past few years I have been stud>ing the taxonomy 
of the Neotropical Spintumicidae, especially of the genus 
Perighschrus Kolenati ( Machado-.Allison, 1965b), which is 
intimately related to the bats of the familv PhvUostomidae. 
Comparing the arrangement of the genera and subfamilies of 
Phyllostomidae, based on the work of Miller (1907) and 
Simpson (1945), now acc-epted by most mammalogists, with 
certain data offered by the relationships of Spintumicidae and 
the bats, I find some significant disagreements which I want 
to point out. 

According to Simpson (op. cit.^, the superfamily Phyl- 
lostomoidea includes the families Phyllostomidae and Des- 
modidae. Simpson di\ided the family Phyllostomidae into 
seven subfamilies: Chilonycterinae, PhyUostominae, Glos- 
sophaginae, CaroUiinae, Stumirinae, Stenodermatinae, and 
PhyUonycterinae. Among these subfamilies, only one, Phyl- 
lon\cterinae, is not known to be parasitized by the Spin- 
tumicidae (there are no pubhshed data on the CaroUiinae, 
but I have recently found a new spintumicid on Rhinophylla 
pumilio Peters), 

The Chilon>"cterinae occupy a special position in the Phyl- 
lostomidae. The absence of a noseleaf and the lack of articula- 
tion of the trochiter with the scapula clearly differentiate these 
bats from those of the other subfanulies. These features led 
Winge (1923) to associate the Chilonycterinae \^-ith the 
Noctihonidae in a section of the Phyllostomidae that he called 
"Mormopini." Xo\ick (1963) found the orientation sounds 
and associated anatomical features of the Chilonycterinae to 
differ sharply from those of other phyUostomids. 

Spintumicidae have not been found on the Xoctilionidae. 
and the only South .American form that I have found on 
ChiJonycterls Gray presents morphological characteristics so 
peculiar that I have considered it to belong to a genus Camer- 
onieta Machado- Allison, distinct from Periglischrus (Machado- 
-AlHson. 1965a). The other subfamilies of PhvUostomidae are 



109 



Host-Parasite Relationships of Bats 



225 



Table 1. Host-parasite relationships of Phyllostomidae with 

Spinturnicidae. 



Spintumicid 
species 


Chiropteran 
genera 


Present subfamilial 
assignment 


Cameronieta ihomasi 


Chilonycteris 


Chilonycterinae 


Periglischrus acutisternus 
Periglischrus torrealbai 
Periglischrus parvus 


Phyllostomus 
Phyllostomus 
Microntjcteris 


Phyllostominae 


Periglischrus setosus 
Periglischrus squamosus 
Periglischrus hopkinsi 


Glossophaga 

Anoura 

Lionycteris 


Glossophaginae 


Periglischrus ojastii 


Sturnira 


Stumirinae 


Periglischrus iheringi 


Artiheus, 

Vampyrops, etc. 


Stenodennatinae 


Periglischrus sp. 


Rhinophylla 


Carolliinae 


Periglischrus herrerai 


Desmodus 


Desmodidae 



parasited by species of Periglischrus (three species on Glos- 
sophaginae, three on Phyllostominae, one on Carolliinae, one 
on Stumirinae, and one on Stenodermatinae; see Table 1). 

Desmodus rotundus E. Geoffrey, family Desmodidae, is the 
host of the species Periglischrus herrerai Machado-AlHson, 
which clearly belongs to the genus Periglischrus. In orienta- 
tion behavior Desmodus resembles phyllostomid genera 
( Novick, op. cit. ) . 

The evidence presented here indicates that a reappraisal 
of the familial relationships of the Chilonycterinae and the 
Desmodidae is in order. I would suggest that rather than 
being a subfamily of the Phyllostomidae, the chilonycterines 
may form a distinct family. The desmodids, on the other hand, 
may be no more than a subfamily of the Phyllostomidae. 

Literature Cited 

Baer, J. 1952. Ecology of Animal Parasites. The University of 
Illinois Press, Urbana, 223 pp. 

Machado- Allison, C. E. 1965a. Notas Sobre Mesostigmata Neo- 
tropicales III. Cameronieta Thomasi: Nuevo Genero y 
Nueva Especie Parasita de Chiroptera (Acarina, Spin- 
turnicidae). Acta Biol. Ven., 4(10): 243-258, 15 Figs. 



110 



226 Proceedings of the Biological Society of Washington 

. 1965b. Las Especies Venezolanas del Genero Periglischrus 

Kolenati, 1857, (Acarina, Mesostigmata, Spintumicidae ) . 
Acta Biol. Ven., 4(11): 259-348, 46 Figs. 

Miller, G. S. 1907. The Families and Genera of Bats. Smithsonian 
Inst., U. S. Nat. Mus., Bull. no. 57, 282 pp., 14 pis. 

Nov^CK, A. 1963. Orientation in Neotropical bats. II Phyllostomatidae 
and Desmodontidae. Journ. Mamm., 44: 44-56. 

Patterson, B. 1956. Mammalian Phylogeny. ler. Symp. Specif. 
Parasit., Neufchatel, pp. 15-49. 

RuDNiCK, A. 1960. A Revision of the Mites of the Family Spin- 
tumicidae (Acarina). Univ. Calif. Publ. Entomol., 17(2): 
157-284, pis. 18-48. 

Simpson, G. G. 1945. The principles of classification and a classifica- 
tion of mammals. Bull. Amer. Mus. Nat. Hist., vol. 85, 
350 pp. 

Wince, H. 1923. Pattedyr-Slaegter. Kjobenhavn, H. Hagerups F. 
vol. 1, 360 pp. 



Ill 



SECTION 2— ANATOMY AND PHYSIOLOGY 

Form and function are intimately related. It is difficult to consider one for 
long or at all thoroughly without considering the other. 

In comments elsewhere we apply a concept of organizational levels. In 
taxonomy, classification begins with individuals and proceeds through local 
aggregates or populations, geographic variants, subspecies, and species, and 
on to groupings at the level of higher categories. In ecology, the individual 
organism is the basic unit, then progressively more inclusive and more com- 
plex levels are local populations of single species, local communities of many 
species, larger ecosystems, and finally the entire biosphere of life-supporting 
parts of the surface of the Earth. Similarly in anatomy and physiology there 
are organizational levels. However, in these fields the individual is the largest 
unit instead of the smallest, except as we may speak of the anatomical charac- 
ters of a species or other taxon. Form or function may be studied at the bio- 
chemical or molecular level, or at progressively higher levels through more 
complex molecules, mixtures and solutions, organelles, cells, tissues, organs, 
systems, and finally to the organism in its entirety. 

The study of anatomy began at the gross level and only after the invention 
of the microscope and development of special techniques of preparing mate- 
rials did histological and cytological studies become possible. The recent 
development of the electron microscope has added several orders of magnitude 
to the possibilities of studying fine structure. Physiology developed later than 
gross anatomy and in many ways paralleled chemistry and physics. 

Our selection of examples is a modest one, drawn from a rich field, and we 
will have to be content with the above mention of the broad scope of anatomy 
and physiology, inasmuch as none of our selections has electron photomicro- 
graphs or histochemical analyses. The selections do, nevertheless, serve to 
illustrate some fundamental biological concepts. 

The concept of homeostasis was conceived and broadly applied in physiol- 
ogy. The concept is relevant, at least by analogy, in ecology under the guise of 
the "balance of nature," recently expanded to include a sizable vocabulary of 
terms such as "feedback regulatory mechanism" and "damped cycles." We 
judge that homeostasis or the tendency of an organism to maintain internal 
conditions at a dynamic equilibrium is the most general concept of physiology, 
and that homology is the most general concept of anatomy. 

The short paper by Hill that begins this section presents one simple ana- 
tomical problem, and at the same time presents the concept of homology and 
the problems of interpreting it. 

The subsequent contributions by Hooper, Hughes, and Mossman are com- 
parative studies within one family ( Cricetidae ) , one order (Marsupialia), and 
one class (Mammalia), respectively. Each author studied a different part of 
the animals concerned and attempted to relate his observations to existing 
knowledge within the systematic framework. 

The next paper, by Noback, treats hair, one of the unique features of the 
Class Mammalia, and theorizes about its adaptive and phylogenetic impHca- 



113 



tions. This article is from a symposium that contains other interesting papers 
on hair. 

The two reprinted papers by Vaughan and Rabb treat form and function 
together, the former at the level of a taxonomic family, the latter in terms of 
one set of glands in one species. 

Among the classic works in mammalian anatomy is Weber's Die Sdugetiere 
(1927, 1928). English mammalogists dating back to Richard Owen and earlier 
have published many comparative papers on mammalian anatomy (see for 
example Pocock's The External Characters of the Pangolins, 1924 ) . One of the 
most productive American mammalian anatomists was A. B. Howell, whose 
Anatomy of the Wood Rat (1926) and Aquatic Mammals (1930) both have 
much to offer. Four good recent works of a comparative nature are Rinker's 
( 1954 ) study of four cricetine genera, Vaughan's ( 1959 ) paper on three kinds 
of bats, Klingener's (1964) treatment of dipodoid rodents, and D. Dwight 
Davis' major work (1964) on the greater panda. Hildebrand's (1959) paper 
on locomotion in the cheetah and the horse should be consulted by any student 
interested in functional anatomy or locomotion. The Anatomical Record and 
Journal of Morphology are two of the more important serial pubHcations 
containing papers on anatomy. 

Among the environmental influences that are important to organisms, and 
whose effects within the organism must be mitigated, are water, oxygen and 
other gases, energy sources (food), ions, temperature, and radiation. Most of 
these factors are touched upon in one or more of the last four papers in this 
selection in ways that help clarify the adaptive nature of internal, behavioral, 
and ecological responses. In addition to these aspects of physiology, some 
areas of special mammalogical interest are hibernation, estivation, thermo- 
regulation, and sensory physiology. Examples appear in Section 4 (Ecology 
and Behavior ) as well as in this section. 

A recent paper by Brown ( 1968 ) , too long to include among our selections, 
is an excellent example of how physiological adaptations, related in this case 
to environmental temperature, can be studied comparatively. Other important 
contributions in mammalian physiology can be found in such journals as Com- 
parative Biochemistry and Physiology, Journal of Applied Physiology, 
Journal of Cell and Comparative Physiology, and Physiological Zoology. 



114 



THE HOMOLOGY OF THE PRESEMIMEMBRANOSUS 
MUSCLE IN SOME RODENTS 

JOHN ERIC HILL 
Museum of Vertebrate Zoology, University of California 

ONE FIGXTBE 

Appleton ('28) has distinguished between the caudofemo- 
ralis muscle and the presemimembranosus muscle (of Leche, 
1883) on the basis of their respective relations to the 'nerve 
to the hamstring muscles.' At the same time he has empha- 
sized the importance of considering topographical relations 
in any discussion of the homologies of muscles. The caudo- 
femoralis, according to this author, crosses over the nerve to 
the hamstring muscles, dorsal and lateral to this, while the 
presemimembranosus is medial to the nerve. 

In many rodents (Parsons, 1894, 1896) the caudofemoralis 
arises from the caudal vertebrae and inserts on the medial 
epicondyle of the femur and the caudal surface of this bone. 
This is the condition in the white rat (Rattus norvegicus) 
where I found the muscle dorsal to the nerve. In this rodent, 
and in the others mentioned below, the caudofemoralis is sup- 
plied by the most cephalic branch of the nerve to the ham- 
string muscles. In the pocket gophers (Thomomys bulbivorus 
and Geomys bursarius), in the kangaroo rat (Dipodomys 
spectabilis), and in a specimen of the wood rat (Neotoma 
fuscipes), I found that the caudofemoralis arises from the 
ischial tuberosity and inserts on the medial epicondyle. 
Howell ('26) found that, in some specimens of the wood rat, 
the muscle originates from the caudal vertebrae, and in all 
these cases the caudofemoralis is dorsal (that is superficial) 
to the nerve to the hamstring muscles; so there is no doubt 
of its identity. In Dipodomys a few fibers of the muscle were 
medial to the nerve. 

311 

THE ANATOMICAL RECORD, VOL. 59, NO. 3 



115 



312 



JOHN ERIC HILL 



However, in two specimens of a ground squirrel (Citellus 
richardsonii) and in a mountain beaver (Aplodontia rufa) I 
found a muscle which originated from the ischium medial 
(that is deep) to the nerve to the hamstrings, but which other- 
wise presented the same topographical relations as the caudo- 
femoralis in the other rodents. Like the latter muscle in 
these other forms, it was supplied by the most cephalic branch 



dorsal hjscia 
gluteus maximus (cut) 
aluleus medius 



iensc fasciae lahe 



uashis lalefalis 



qtuheus maximus 
' (cuO 

Quadfatus femon's 



femorvcoccf^g e us 
(cut) 



Fascia la la- 




ienuissimua (cut) 
piriforinis 

nefi/e {o hamsifing mascJts 
■femo''ococcu<^eiAS (cut) 
N. ^udendus 

Nfernoralis cuhneus posiethr 
I'endon of caudo^emofal/s 
caudal head of seniilendinasus 
c audofemorali s 
-ischial head of semiiendinosus 

adduclor ma^nus 

-N ischiadicus 
biceps femon's 
somimambrano Sus 
gracilis 
M Surae lateralis 

ienuissimus fculj 

vV peroneus communis 

biceps femoris Icuti 

fascia lafa 



Fig. 1 The muscles of the thigh of Sciurus griseus showing the relations of 
the caudofemoralis (presemimembranosus). 

of the nerve to the hamstrings. According to the views of 
Appleton ('28) and Leche (1883), however, this muscle would 
be a presemimembranosus and not a caudofemoralis. 

The condition of this muscle in the gray squirrel (Sciurus 
griseus) suggests a solution to the problem of its homology, 
in rodents at least. In the specimen dissected, the muscle 
arose by tendinous and fleshy fibers from the ischial bone 
and, by a slender tendon (fig. 1), from the transverse process 



116 



HOMOLOGY OF PRESEMIMEMBRANOSUS MUSCLE 313 

of the first caudal vertebra. The tendon crossed superficial to 
the nerve to the hamstring muscles, while the part of the 
muscle arising from the ischium lay medial and deep to the 
nerve. Alezais ( '00) described the muscle in Sciurus vulgaris 
as the 'ischio-condylien.' In this animal it is apparently 
identical with the muscle described above in Sciurus griseus, 
but that author did not perceive the significance of the peculiar 
relation between the muscle and the nerve to the hamstrings. 
This relation may be considered a stage intermediate between 
the typical position of the caudofemoralis and that of the so- 
called presemimembranosus. 

It may be concluded that muscles do, in rare instances, 
change their topographical relations to nerves; and that the 
caudofemoralis and the presemimembranosus are homologous 
muscles. Consequently, when the muscle in question is con- 
tinuous with the semimembranosus, the condition should not 
be considered primitive or undifferentiated, but rather as a 
secondary fusion of the caudofemoralis and the semimem- 
branosus. Also, since it is generally accepted by workers in 
comparative myology (Alezias, '00; Parsons, 1892; Leche, '00) 
that the presimimembranosus forms part of the great ad- 
ductor in man, the identification of the former muscle as a 
modified caudofemoralis seems to fill a gap between the known 
morphological history of the sciatic part of the adductor 
magnus and the phylogeny of the caudofemoralis as traced 
by Appleton ('28). ' 



117 



314 JOHN EEIC HILL 

LITERATURE CITED 

Alezais, H. 1900 Contribution a la myologie des rongeurs. Theses presentees 

a la faculte des sciences de Paris. 
Appleton, a. B. 1928 The muscles and nerves of the post-axial region of the 

tetrapod thigh. J. Anat., vol. 62, pp. 364-438. 
Howell, A. B. 1926 Anatomy of the wood rat. Baltimore : Williams & Wilkins 

Company. 
Leche, W. 1883 Zur Anatomie der Beckenregion bei Insectivora. Kongl. 

Svensk. Vetensk.-Akad. Handl., vol. 20, pp. 1-112. 

1900 Muskulatur. Saugethiere: Mammalia. In Bronn: Klassen 

und Ordnungen des Thier-Reichs, Bd. 6 : 5 : 1 : 2, S 649-919. 

Parsons, F. G. 1892 Some points in the myology of rodents. J. Anat. and 
Physiol., vol. 26, Proc Anat. Soc. Gt. Britain and Ireland. 

1894 On the myology of the sciuromorphine and hystricomorphine 

rodents. Proc. Zool. Soc. London, pp. 251-296. 

■ 1896 Myology of rodents. Part II. An account of the myology of 

the Myomorpha, together with a comparison of the muscles of the 
various suborders of rodents. Proc. Zool. Soc. London, pp. 159-192. 



118 



Number 625 May 10, 1962 

OCCASIONAL PAPERS OF THE MUSEUM OF 

ZOOLOGY 
UNIVERSITY OF MICHIGAN 

Ann Arbor, Michigan 

THE GLANS PENIS IN SIGMODON, SIGMOMYS, AND 
REITHRODON (RODENTIA, CRICETINAE) 

By Emmet T. Hooper 

Cotton rats {Sigmodon and Sigmomys), marsh rats, (Holochilus), 
coney rats (Reithrodon), and red-nosed rats (Neotomys) compose an 
assemblage which Hershkovitz (1955) considers to be natural and 
which he designates as the "sigmodont group." This group contrasts 
with or)zomyine, ichthyomyine, phyllotine, akodont, and other 
supraspecific assemblages which various authors (e.g., Thomas, 1917; 
Gyldenstolpe, 1932; Hershkovitz, 1944, 1948, 1955, 1960; and Voront- 
sov, 1959) have recognized in analyzing the large cricetine fauna of 
South America. While all of these groups are tentative, at least in 
regard to total complement of species in each, nevertheless some are 
strongly characterized and probably natural; and all, whether natural 
or not, are useful in that they constitute conveniently assessable seg- 
ments of an unwieldly large South American cricetine fauna, now 
disposed in approximately 40 nominal genera. New information re- 
garding three of those genera is provided below. It is derived from 
fluid-preserved and partially cleared glandes (procedures described by 
Hooper, 1959) as follows: 

Reithrodon ciiniculoides: Argentina, Tierra del Fuego, 1 adult. 
Sigmodon alleni: Michoacan, Dos Aguas, 3 adults. 5. hispidus: 
Arizona, Pima Co., 1 subadult. Florida, Alachua and Osceola coun- 
ties, 3 adults. Michoacan, Lombardia, 2 adults. 5. minimus: New 
Mexico, Hidalgo Co., 1 juvenile. 5. ochrognathus: Texas, Brewster 
Co., 1 subadult. Sigjnomys alstoni: Venezuela, Aragua, 1 subadult. 

I am indebted to Elio Massoia for the specimen of Reithrodon and 
to Charles O. Handley, Jr., for the example of Sigmomys. Figures 1 
and 2 were rendered by Suzanne Runyan, staff artist of the Museum of 
Zoology. The National Science Foundation provided financial aid. 

Listed below in sequence are representative measurements (in mm.) 

1 



119 



2 Emmet T. Hooper Occ. Papers 

of Sigmodon hispidus (averages of five adults), Sigmomys ahtoni (one 
subadult), and Reithrodon cuniculoides (one adult). Length of hind 
foot: 34, 30, 33; greatest lengths of glans, 7.6, 6.6, 7.8; greatest diam- 
eter of glans, 6.2, 4.0, 5.0; length of main bone of baculum, 5.5, 4.9, 
4.1; length of medial distal segment of baculum, 2.8, 2.0, 2.7; total 
length of baculum, 8.3, 6.9, 6.8. 

DESCRIPTION OF GLANDES 

Sigmodon hispidus.— In Sigmodon hispidus the glans is a spinous, 
stubby, contorted cylinder (Fig. 1), its length one-fourth to one-fifth 
that of the hind foot and its greatest diameter approximately three- 
fourths its length (see measurements). The spines which densely stud 
almost all of the epidemiis, except tJiat of the terminal crater, are 
short and thick-set; each is recessed in a rhombic or hexagonal pit. The 
glans is somewhat swayback and potbellied, yet in its basal one-half 
or tAvo-thirds it is essentially plain and cylindrical, without lobes or 
folds other than a short midventral frenum which, as an indistinct 
raphe, continues distad to the rim of the crater. The distal third or 
half of the glans is conspicuously hexalobate, the six lobes separated 
from each other by longitudinal troughs or grooves which increase in 
depth distad. The lobes are unequal in size and shape; the ventral 
pair is largest and the least convex, the lateral pair smallest, and the 
dorsal pair the most convex; the latter is a key item in the swayback 
appearance of the glans. These lobes converge distally, and tJieir 
crescentic lips form the scalloped, overhanging rim of the terminal 
crater. 

The largest structure in the crater is the mound which houses the 
medial distal segment of the baculum. Nestled between the lips of the 
ventral lobes, it projects outside the crater approximately to the limits 
of the dorsal lobes. The two smaller lateral mounds, housing the 
lateral processes of the baculum, are closely appressed to the medial 
mound, and the tip of each is distinctly pointed, rather than gently 
rounded like the medial mound. Immediately ventral to the medial 
mound is the meatus urinarius which is guarded ventrally by a ure- 
thral process. This process consists of a pair of rather thick arms each 
of which is out-curved and tapers to an obtuse tip (Fig. 1); in one 
specimen the ventral face of the process is studded with spines. Dorsal 
to the medial mound is the dorsal papilla, which is a single distensible 
cone of soft tissue dotted with spines both dorsally and laterally. Two 
additional pairs of crater conules, here termed "dorsolateral and 
lateral papillae," are particularly noteworthy because, insofar as known 



120 



No. 625 



Glans Penis in Sigmodont Rodents 



3 





I I 



foot glans bac. bone 



Fig. 1. Views of glans penis of Sigmodon hispidus: a, dorsal; b, lateral; c, incised 
midventrally exposing urethra; d, epidermal spines, enlarged; e, urethral process, 
enlarged, ventral aspect; UMMZ 97270, Florida. 



121 



4 Emmet T. Hooper Occ. Papers 

in the New World cricetids studied to date, they are peculiar to 
Sigmodon and Sigmomys. All four of these are spine-studded, stubby, 
and smoothly rounded terminally. Each dorsolateral papilla is situated 
just below the crater rim at the junction of the dorsal and lateral 
lobes. Each lateral papilla is partly recessed in a pocket on the lower 
flank of the crater wall alongside a lateral bacular mound. 

There is no ventral shield (a large mass of tissue between the 
urethral process and the ventral lip of the crater) as seen in most 
microtines, and the bacular mounds are relatively free within the 
crater, there being no partitions connecting the lateral mounds with 
the crater walls; the urethra empties onto the crater floor, not into a 
partition-encircled secondary crater within the larger crater, an 
arrangement seen in some rodent species. 

Below the crater floor is a right and left pair of bilobed sacs (Fig. 
1), each ovoid ventral lobe about 1.5 mm. in length, and each atten- 
uate dorsal lobe approximately a millimeter longer, its tip extending 
distad almost to the limits of the main bone of the baculum. These 
sacs or sinuses emerge from tissues situated beside the corpora 
cavernosa penis and they extend alongside the baculum and the corpus 
cavernosum urethra, but they apparently are not parts of either of 
those structures. Composed entirely of soft tissues and engorged with 
blood in some specimens, they appear to be continuous with the deep 
dorsal vein and, thus, they seem to be part of the vascular system. 
Similar sacs, as illustrated in Phyllotis by Pearson (1958:424) for ex- 
ample, occur in all of those New World cricetids studied to date that 
have a four-part baculum; they have not been observed in Peromyscus, 
Neotoma, or other cricetid groups which are characterized by a simple 
baculum and glans. 

The four-part baculum is at least as long as the glans and is one- 
fourth the hind foot in length (see measurements). The main bone, 
one-sixth the length of the hind foot, is angular and gross. The dorsal 
face of its wide and angular base is deeply concave between prominent 
lateral and proximal condyles to which the corpora cavernosa attach, 
while the ventral surface is almost flat except for a midventral keel of 
either cartilage or bone which, spanning approximately four-fifths the 
length of the bone, terminates at the cartilage of the digital junction. 
The shaft is oval in cross-section, the dorsoventral diameter exceeding 
the transverse one; as viewed laterally it is slightly bent and is con- 
stricted terminally, while in ventral view it is gently tapered distad 
before expanding to form a distinct terminal head. 

The three distal segments of the baculum are subequal in length. 



122 



No. 625 Glans Penis in Sigmodont Rodents 5 

the lateral pair slightly shorter than the medial one. They differ con- 
siderably in shape and amount of ossification. In one breeding adult 
they are entirely cartilaginous, while in four other adults they con- 
tain various amounts of osseous tissue in addition to cartilage; proba- 
bly in very old animals they are entirely osseous. The medial segment, 
attached to the ventral sector of the main bone, projects distad and 
slightly ventrad, then it bends abruptly dorsad before terminating in 
a rounded tip. It is approximately oval in cross section in its distal 
three-fourths, but in its proximal fourth it is much wider than deep 
and is keeled ventrally; moreover, at the digital junction it bears a 
pair of lateral processes and a medial flange, the continuation of the 
midventral keel, w'hich extends over the ventral face of the head of 
the main bone. In all specimens at hand these three processes are 
cartilaginous; furthennore, the osseous tissue of the three distal seg- 
ments is restricted to, or concentrated in, the distal parts of each seg- 
ment, indicating that ossification apparently proceeds from the tip 
proximad in S. hispidus. 

The lateral segments, situated dorsolateral to the medial unit, 
attach onto the dorsal and lateral parts of the head of the main bone- 
dorsal to the flanges of the medial segment. Each is pointed and blade- 
shaped, the dorsoventral diameter exceeding the transverse one; and 
as viewed ventrally each curves gently distad and slightly laterad. 
Whether cartilaginous or osseous, they are situated in the lateral parts 
of each bacular mound, while the medial and distalmost parts of each 
mound consist entirely of soft tissue, a large part of which is vascular 
and appears to be instrumental in distention of the mounds. In some 
examples, the basal parts of the three distal segments of the baculum 
are more or less coalesced; this is particularly true of the two lateral 
units, and the two have been interpreted as a single horn-shaped 
structure (Hamilton, 1946). However, as indicated by Burt (1960) they 
are separate units (Fig. 1); their individual limits are clear in speci- 
mens at hand. 

Sigmodon minimus, S. ochrognathus, and 5. alleni.—l recognize no 
interspecific differences in the specimens of minimus and ochrognathus, 
both examples of which are young and rather unsatisfactory. Each 
closely resembles specimens of hispidus of like age in external size and 
shape, and in conformation of the six exterior lobes, dorsal papilla, 
dorsolateral papillae, lateral papillae, urethral process, crater mounds, 
and baculum. If there are interspecific differences, they are not clearly 
evident in the materal at hand. 

The three adults from Dos Aguas, Michoacan, which are labeled S. 



123 



6 Emmet T. Hooper Occ. Papers 

alleni, are also like adults of hispidus. The two series differ slightly 
in regard to size of glans and shape of baculum, but these are small 
differences and doubtfully interspecific. 

A few remarks regarding the identification of the specimens from 
Dos Aguas are needed. Until variation in Sigmodon is better under- 
stood, .S. alleni seems to be the most appropriate name to apply to 
these specimens and, as well, to others like them from the vicinity of 
Autlan, Jalisco, and Angahuan and Uruapan, Michoacan. Cranially 
and externally distinguishable from specimens of 5. hispidus and S. 
mclanotis from nearby localities in the same states, they appear to 
represent a species other than either hispidus or melanotis. They 
agree well with the description of alleni, but they have not been com- 
pared directly with the type specimen of that form. 

Sig7nomys alstoni.—The specimen of Sigmomys alstoni resembles 
examples of Sigmodon of comparable age in length (relative to hind 
foot), in external configuration (hexalobate, swaybacked and pot- 
bellied in lateral view, and covered with proximally directed, thickset, 
sharp, entrenched spines), shape of dorsal papilla (single, spine-stud- 
ded cone), appearance of urethral process (two outcurved arms with a 
longitudinal row of spines on the ventral face of each), shape of the 
bacular mounds (the medial one large and rounded, each lateral one 
smaller and rounded laterally but acute medially), position of digits 
of baculum with respect to the main bone, presence of ventral keel 
and lateral arms on the medial digit, and occurrence of a midventral 
keel on the main bone. The specimen differs from examples of 
Sigmodon in characters as follows: glans smaller in diameter (diam- 
eter-length ratio approximately 60 per cent, compared with 70-88 per 
cent in Sigmodon); the six external lobes, particularly the dorsal pair, 
less prominent; dorsolateral papillae smaller, scarcely more than the 
spine-studded infolding of the dorsal and lateral lobes; crater more 
extensively spinous (spines studding most of inner wall of each lateral 
lobe); medial digit of baculum projecting principally distad, its tip 
not sharply flexed dorsad; and the osseous proximal segment flatter 
and wider for a larger fraction of its length. 

The lateral papillae and baculum warrant additional comment. It 
is uncertain whether lateral papillae are present in the specimen. Two 
papillose vascular cores occur at sites where papillae are to be ex- 
pected, but in the present damaged specimen the overlying crater 
floor is not correspondingly papillose, although it is strongly spinous; 
the spiny area occupies most of the inner face of the lateral lobe and 
of the adjoining crater floor. On the left side of the specimen this 



124 



No. 625 Glans Penis in Sigmodont Rodents 7 

roughly circular spiny area is plate-like, while on the right side it is 
buckled distad and, thus, resembles a large papilla. If, in undamaged 
specimens, these areas are papillose, then the lateral papillae in 5. 
alstoni are relatively larger than any yet seen in Sigmodon. 

In ventral view, the main bone of the baculum is shaped roughly 
like an isosceles triangle— wide basally and tapered rather evenly dis- 
tad (without pronounced incurve) almost to the slight constriction 
which subtends the small, round, terminal head. Its wide basal part 
is concave dorsally (between low lateral condyles) and almost fiat 
ventrally; but farther distad the bone is deeper than wide and, some- 
what triangular in cross section, it bears a slight midventral ridge to 
which a cartilaginous keel is attached. The distal segments are entirely 
cartilaginous. The medial one is deeper than wide in its distal half 
and blunt terminally; basally it bears a medial process and two lateral 
flanges. Each lateral segment, also deeper than wide and blunt termin- 
allv, is situated dorsolateral to the medial unit. 

Reithrodon cimiculoides— The glans of R. cuniciiloides (Fig. 2) is 
stubby (diameter-length ratio 64 per cent), subcylindrical, and indis- 
tinctly lobate, the lobes defined by four, shallow, longitudinal troughs. 
Two of these depressions, one situated middorsally and the other 
mid\entrally, extend approximately the full length of the glans and 
thereby divide the surface of the glans into right and left halves; the 
distal limit of each is a notch in the crater rim. The shorter third pair 
of troughs is situated dorsolaterally in the distal half of the glans, but 
each tenninates short of the rim. All of the epidermis as far distad as 
the crenate, membranous, overhanging rim of the crater is densely 
studded with small, conical, recessed tubercles. 

The three bacular mounds, together with the underlying baculum, 
resemble a fieur-de-lis in ventral aspect (Fig. 2); the erect medial part 
extends beyond the crater, while each of the truncate lateral pair 
sends off an attenuate lateral segment which curves laterad and then 
distad before terminating in an acute tip. These lateral processes con- 
tain no cartilage or bone; they consist entirely of soft tissues, a large 
part of which is vascular and apparently erectile. The spine-tipped 
dorsal papilla is unusually small and slender; it is a single cone, but a 
slight cleft near its tip suggests that the papilla may consist of two 
conules in other specimens. The urethral process is a bilobed flap 
with two attenuate and erect (not outcurved) arms; it bears two longi- 
tudinal rows, each of eight tubercles, on its ventral face. There are no 
lateral or dorsolateral papillae, and the crater walls and floor are 
smooth and non-spinous. 



125 



Emmet T. Hooper 



Occ. Papers 




I I I 

foot glans bac. bone 



Fig. 2. Views of glans penis of Reithrodon cuniculoides; UMMZ 109233, Argen- 
tina. For explanation see Fig. 1 and text. 



126 



No. 625 Glans Penis in Siemodont Rodents 



Q' 



The baculum is shorter than the glans (see measurements). Its prox- 
imal, osseous segment consists of a wide basal part and a slender shaft. 
The basal part, which bears large, proximally directed condyles (these 
separated medially by a deep notch), is broadly concave ventrally and 
narrowly and shallowly concave dorsally. The relatively straight shaft 
is slightly deeper (dorsoventrally) than wide and it bears a slight 
ventral keel; its terminal portion is slightly expanded laterad and 
slightly constricted dorsoventrally (Fig. 2). The three distal segments 
are cartilaginous. The long medial one (its length two-thirds that of 
the bone) is rod-like for much of its length, but it is enlarged basally 
and is tapered distally to a pointed tip. The lateral units are disc- 
shaped in cross section, the dorsoventral diameter of each much great- 
er than the transverse one. From its attachment on the head of the 
bone (the attachment dorsal and lateral to that of the medial unit) 
each lateral segment curves gently laterad and distad before it termin- 
ates at the base of the laterally projecting process of its lateral mound. 

DISCUSSION 

To judge from specimens at hand, the glandes of Sigmodon alleni, 
S. hispidus, S. minimus, and 5. ochrognathus are fundamentally alike, 
although they may differ interspecifically in details which can not be 
appraised in present samples. In each species the stubby, swayback, 
tubercle-invested glans bears six prominent exterior lobes which sur- 
round the terminal crater and divide its rim into six corresponding 
parts. Within the crater there are five spine-studded papillae consist- 
ing of dorsolateral and lateral pairs in addition to a single cone mid- 
dorsally. The urethral process bears two attenuate, outcurved arms. 
The bacular mounds are truncate except for a small, acute medial 
crest on each lateral mound, and the medial distal segment of the 
four-part baculum bears a medial keel and a pair of lateral processes 
on its base, while its tip is flexed sharply dorsad. These characters, 
together with others, distinguish Sigmodon from the other New World 
cricetid genera which have been studied to date, with the possible 
exception of Sigmomys. Sigmomys alstoni, the only species of Sig- 
momys about which there is information on the glans, appears to be 
closely similar to species of Sigmodon, but its characters are not yet 
adequately known. 

In contrast to the phalli of Sigmodon and Sigtnomys, the glans of 
Reithrodon cuniculoides is comparatively slim and simple. There are 
only four exterior lobes, and these are less prominent than the lobes 
of Sigmodon or Sigmomys. The membranous, crenate, and non-spiny 



127 



10 Emmet T. Hooper Occ. Papers 

crater rim is not divided into six distinct lobes. The crater, also 
smooth and spineless, has no dorsolateral or lateral papillae. The 
slender dorsal papilla bears spines only at its tip. Each lateral mound 
has an attenuate lateral process, and the entire configuration of the 
three crater mounds as well as of the underlying baculum is distinc- 
tive. The three, long, erect distal segments of the baculum, all car- 
tilaginous insofar as known, are essentially rod-like in form, without 
prominent keels or processes. These and other contrasting characters 
indicate that the glans of R. cuniculoides is morphologically quite 
different from that seen in Sigmodon and Sigmomys. Preliminary 
comparisons suggest that it may be more similar to glandes of phyllo- 
tine or other species which are not now included in the sigmodont 
group of rodents. 



128 



No. 625 Glans Penis in Sigmodont Rodents 11 

LITERATURE CITED 

Burt, William H. 

1960 Bacula of North American mammals. Miscl. Publ. Mus. Zool. Univ. Mich., 
113:1-76,25 pis. 

Gyldenstolpe, Nils 

1932 A manual of Neotropical sigmodont rodents. Kungl. Svenska Veten. 
Hand., Ser. 3, no. 3: 1-164, 18 pis. 

Hamilton, William J., Jr. 

1946 A study of the baculum in some North American Microtinae. Jour. 
Mamm., 27:378-87, 1 pi., 3 figs. 

Hershkovttz^ Philip 

1944 A systematic review of the neotropical water rats of the genus Nectornys 
(Cricctinae). Miscl. Publ. Mus. Zool. Univ. Mich., 58:1-88, 4 pis., 5 figs. 

1948 Mammals of northern Colombia, preliminary report No. 3: water rats 
(genus Nectornys), with supplemental notes on related forms. Proc. U.S. 
Natl. Mus., 98:49-56. 

1955 South American marsh rats, genus Holochilus, with a summary of sig- 
modont rodents. Fieldiana: Zoology, 37:639-73, 13 pis., 6 figs. 

1960 Mammals of northern Colombia, preliminary report No. 8: arboreal rice 
rats, a systematic revision of the subgenus Oecomys, genus Oryzomys. 
Proc. U.S. Natl. Mus., 110:513-68, 12 pis., 6 figs. 

Hooper, Emmet T. 

1959 The glans penis in five genera of cricetid rodents. Occ. Pap. Mus. Zool. 
Univ. Mich., 613:1-10, 5 pis. 

Pearson, Oliver P. 

1958 A taxonomic revision of the rodent genus Phyllotis. Univ. Calif. Publ. 
Zool., 56:391-496, 8 pis., 21 figs. 

Thomas, Oldfield 

1917 On the arrangement of the South American rats allied to Oryzomys and 
Rhipidomys. Ann. Mag. Nat. Hist., ser. 8, 20:192-8. 

Vorontsov, N. N. 

1959 The system of hamster (Cricetinae) in the sphere of the world fauna 
and their phylogenetic relations. Bull. Mosk. Obsh. Ispyt. Prirody, Biol. 
Sec. (Bull. Moscow Soc. Naturalists), 64:134-7. 

Accepted for publication February 5, 1962 



129 



COMPARATIVE MORPHOLOGY OF SPERMATOZOA FROM FIVE 

MARSUPIAL FAMILIES 

By R. L. Hughes* 

[Manuscript received April 8, 1965] 
Summary 

The spermatozoa of 18 marsupial species derived from five families have been 
examined and of these only the spermatozoon of the bandicoot Perameles nasuta 
has previously been described adequately. 

The spermatozoon morphology within the families Macropodidae, Dasyuridae, 
Phascolarctidae, and Peramelidae was relatively homogeneous. A distinctive 
morphology occured between these families. Within the family Phalangeridae 
spermatozoa were morphologically diverse, however, as a group they were relatively 
separate from those of the other families studied. 

The spermatozoa of the Phascolarctidae (koala, Phascolarctos cinereus, and 
wombat, Phascolomis mitchelli) have a unique, somewhat rat-like morphology which 
clearly separates them from those of the other marsupial sperm studied. This finding 
is of considerable taxonomic interest as most authorities consider the koala to be more 
closely related to the phalangerid marsupials than to the wombat. 

I. Introduction 

Previous descriptions of marsupial spermatozoon morphology cover six of the 
major marsupial groups. A considerable proportion of these accounts is devoted to 
a study of the spermatozoon morphology of three species, each belonging to separate 
marsupial families. (1) Family Didelphidae: Didelphis [Selenka (1887), Fiirst (1887), 
Waldeyer (1902), KorflF (1902), Retzius (1909), Jordan (1911), Duesberg (1920), 
Wilson (1928), McCrady (1938), Biggers and Creed (1962)]; (2) family Phalangeridae: 
Phalangista vulpina ( = Trichosurus vulpecula) [Korff (1902), Benda (1897, 1906), 
Retzius (1906), Bishop and Walton (I960)]; (3) family Peramehdae: Perameles nasuta 
[Benda (1906), Cleland (1955, 1956, 1964), Cleland and Rothschild (1959), Bishop and 
Austin (1957), Bishop and Walton (I960)]. 

The spermatozoon morphology of two Dasyuridae, Phascogale albipes ( = Smin- 
thopsis murina) and Dasyurops maculatus, was studied by Fiirst (1887), Bishop and 
Austin (1957), and Bishop and Walton (1960). 

Benda's (1906) description of an epididymal sperm from the koala, Phascolarctos 
(family Phascolarctidae), is, as he admits, inadequate. 

Spermatozoon morphology studies on members of the family Macropodidae 
include those of an unknown Macropus sp. (Benda 1906), Macropus billardierii 
( = Thylogale billardierii), Petrogale penicillata, Onychogale limata ( = Onychogalea 
lunata), Bettongia cimiculus (Retzius 1906), Macropus giganteus ( = Macropus canguru) 
(Binder 1927), and Potorous tridactylus (Hughes 1964). 

* Division of Wildlife Research, CSIRO, Canberra. 

Aust. J. ZooL, 1965, 13, 533-43 



130 



534 R. L. HUGHES 

The spermatozoa examined in the present study were obtained from members 
of the five Australasian marsupial families: Phalangeridae, Peramelidae, Dasyuridae, 
Phascolarctidae, and Macropodidae. The present series of observations has been 
viewed with reference to those of earlier workers and this has permitted at least an 
elementary discussion of the comparative aspects of spermatozoon morphology 
between the marsupial families examined. 

II. Material and Methods 

The testes together with the attached epididymis were removed from the scrotum 
soon after death and fixed in 10% neutral formalin or, more rarely, Bouin's fluid or 
Carnoy fixative. 

(i) Method for Adhering Spermatozoa to Microscope Slides 

The slides were labelled at one end with a diamond pencil and a 15-mm square 
was marked out at the opposite end. The entire surface of the slide was liberally 
smeared with Mayer's albumen. A small piece of epididymal tissue was placed in a 
drop of 10% neutral buifered formalin within the marked square and extensively 
teased with dissecting needles. Filter paper circles of 5-5 cm diam. were saturated 
with 10% formalin, drained, and placed over the specimen by a rolling action. Air 
bubbles were punctured with a needle. The filter paper was kept moist with 10% 
formalin for at least 30 min and then permitted to dry until free fluid between the 
slide and the filter paper had disappeared. The filter paper was then removed by a 
rolling action, excess tissue was removed with fine forceps, and the preparations rinsed 
and stored in water for staining. 

(ii) Staining of Spermatozoa 

(1) Heidenhains Iron Haematoxylin. — Slides containing adhering spermatozoa 
were transferred from water to a 5 % solution of iron alum and kept in a warm place 
for 2-3 days. They were then stained with Heidenhain's haematoxylin for a similar 
period. The area not containing the specimen was thoroughly cleaned with paper 
tissues during a 10-15 min rinsing period in running tap water. The preparations were 
then diff'erentiated in 5% iron alum under a staining microscope at 30 sec intervals. 
The preparation was washed in water and re-examined after each differentiation inter- 
val. Difl'erentiation times of between 30 sec and 5 min proved satisfactory to show the 
desired range of structures. The preparations were upgraded to absolute ethyl alcohol, 
placed in two changes of xylol, and mounted in euparal. 

(2) Periodic Acid-Schijf {with saliva controls). — Slides containing the mounted 
spermatozoa were removed from water and placed horizontally in two groups on a 
flat tray. One group was flooded with water and the other with saliva for 1 hr at a 
temperature of 37°C. The slides were then thoroughly rinsed in distilled water and 
stained by a method described by Carleton and Drury (1957, p. 143). The SchiflF's 
reagent used was de Tomasi (for preparation see Pearse 1961, p. 822). The prepara- 
tions were mounted in euparal. 

(3) Feulgen (with and without fast green counterstain). — Slides containing the 
adhering spermatozoa were removed from water and stained by a method described 



131 



MORPHOLOGY OF SPERMATOZOA 535 

by Pearse (1961, p. 823). The Schiff' s solution used was de Tomasi. Half the Feulgen 
preparations were stained with fast green counterstain (0-5% solution in 70% ethyl 
alcohol) for 15-20 min. Both Feulgen and Feulgen-fast green preparations were 
quickly passed through three changes of 90% alcohol (dips only) to absolute ethyl 
alcohol and then cleared in xylol and mounted in euparal. 

Slides were stored until dry in an oven at a temperature of 37°C after mounting 
in euparal. Preparations were not permitted to dry out during any of the earlier stages 
in preparation. 

The drawings of spermatozoa shown in Figure 1 are based on camera lucida 
outlines using a Xl2 eyepiece in conjunction with a x 100 oil-immersion objective. 

The spermatozoon dimensions shown in Table 1 are means of 25 observations 
and were obtained with a special Leitz x 12 -5 screw micrometer eyepiece and a X 100 
oil-immersion objective. The preparations used were fixed in 10% neutral formalin 
or, more rarely, Bouin's fluid or Carnoy and were stained with Heidenhain's iron 
haematoxylin. 

During the course of the observations on sperm it became apparent that the 
efferent ducts connecting the testis and epididymis were either multiple or single 
within each marsupial family. This was investigated further from frozen transverse 
sections stained with haematoxylin and eosin. The sections were prepared from the 
efferent duct or ducts at the point of their emergence from the testis and also approxim- 
ately midway between the testis and epididymis. 

The author follows Cleland and Rothschild (1959) in considering for the purpose 
of description that the flagellum is inserted into the ventral surface of the sperm head 
and the opposite surface is taken as dorsal. 

in. Results 

The mature epididymal spermatozoa of 1 8 marsupial species have been examined. 
The dimensions of 13 of these spermatozoa are shown in Table 1. The gross morphol- 
ogy of 14 of the spermatozoa is shown in Figure 1. 

Spermatozoa of each of the five marsupial families studied (Macropodidae, 
Phalangeridae, Dasyuridae, Peramelidae, Phascolarctidae*) exhibited sufficient 
homogeneity in morphology and dimensions of the head, flagellum, and fine structure 
to be of taxonomic value. 

The heads of all marsupial spermatozoa examined showed some dorsoventral 
flattening. This was most marked in the Dasyuridae and Peramelidae. It was least 
evident in the Phascolarctidae and the genus Pseudocheirus of the Phalangeridae. 
Macropod and the other phalangerid spermatozoa exhibited an intermediate con- 
dition. The distal extremity of the head of all species when viewed dorsally was 
relatively rounded while the shape of the lateral margins and proximal tip varied 
considerably. In the Dasyuridae the spermatozoon heads of up to 12-7 /a in length 
in Dasyuroides byrnei are among the longest known for mammals (Table 1). The 

* The author follows Sonntag (1923) in grouping the wombat and koala in the family 
Phascolarctidae. 



132 



536 



R. L. HUGHES 



lateral head margins of dasyurid sperm are slightly convex in dorsal view and taper 
gradually to a proximal point. Macropod sperm heads are considerably shorter than 
those of the Dasyuridae and in dorsal outline are elongated ovoids bluntly pointed 
proximally. The sperm head of the macropod Megaleia rufa (Figs. 1^ and 1/?) is 
rapidly tapering, a condition typically found in the Phalangeridae. Phalangerid 
sperm, when viewed dorsally, exhibit considerable variability in the convexity of the 
lateral head margins. The proximal region of the head is typically semicircular, 
although sometimes bluntly pointed as in Pseudocheirus cupreus (Figs. \n and \o). 

Table 1 
marsupial spermatozoon dimensions 









Mean ±SD (/a) 




Family and Species 


Head 


Middle 


-piece 


Flagellum 




Length 


Width 


Length 


Diameter 


Length 


Macropodidae 












Macropus canguru 


7-3±016 


2-2 + 011 


10-7±0-24 


1-5±014 


111-6+ 3-60 


Megaleia rufa* 


5-l±0-2I 


2-4±009 


7-9±0-25 


l-4i:012 


1040± 4-74 


Protemnodon rufogrisea 


8-5±0-22 


2-3±018 


Il-7±0-34 


l-6±0-14 


115-4± 8-85 


Protemnodon agilis] 


7-l±0-38 


1-8±012 


110±0-28 


1-4±013 


— — 


Thylogale stiginatica* 


7-2±009 


2-2±0Il 


10-9±0-22 


1-5±012 


1031± 4-43 


Dasyuridae 












Dasyuroides byrnei 


12-7±0-41 


2-5±015 


40-7 il -26 


3- 1+0- 19 


242- 1± 6-77 


Sarcophilus harrisii 


llliO-45 


2-2±0-I7 


34-4:rO-84 


2-6±013 


207-4±1202 


Phalangeridae 












Petaurus brevicepsX 


5-9±019 


2-5±018 


8-3 :L0-27 


1-4±011 


101-3± 4-96 


Pseudocheirus cupreus% 


5-4±016 


2-6±011 


6-2^016 


1-5±017 


84-7± 2-47 


Pseudocheirus peregrinus 


5-9iO-38 


3-8±018 


6-9±0-21 


21±0-22 


106-9± 5-31 


Phascolarctidae 












Phascolomis mitchelli 


5-7±0-33 


l-7x009 


180±l-56 


0-9±010 


87-9± 8-23 


Peramelidae 












Perameles nasuta 


5-7±015 


30±013 


140±0-32 


20±011 


1941± 5-25 


Isoodon macrourus 


60±013 


3-3±018 


10-7±0-19 


1-8±014 


1651± 3-64 



* Fixed in Bouin's fluid; t Carnoy fixative; % from New Guinea. 

Peramelid spermatozoon heads have concave lateral margins when seen in dorsal 
view and are relatively square proximally with a median cap. In phascolarctid sperm 
the proximal portion of the spermatozoon head of both the wombat Phascolomis 
mitchelli, and the koala, Phascolarctos cinereus, bears a strongly recurved hook. 

In all sperm, a positive Feulgen reaction for nuclear material (DNA) was given 
by almost the entire head mass. The DNA-negative areas that took up a fast green 
counterstain in Feulgen preparations were the acrosome (Fig. 1 ; AC) and basal 
granule complex which is located at the proximal tip of the flagellum. The acrosome 



133 



MORPHOLOGY OF SPERMATOZOA 



537 




20; 



Fig. 1. — Marsupial epididymal spermatozoa: the drawings are all at the same scale and are based 
on camera lucida outlines of formalin-fixed Heidenhain's iron haematoxylin preparations. A xl2 
eyepiece was used in conjunction with a x 100 oil-immersion lens. Fam. Phascolarctidae: Phascolomis 
mitchelli, {a) lateral view; Phascolarctos cinereus, (b) lateral view of spermatozoon head with flagellum 
outline. Fam. Macropodidae: /'ro/f/?;Aio^o/7r///o^m£'fl, (c) ventral view, (^) lateral view; Protemnodon 
agilis*, (e) lateral view, (/) ventral view; Megaleia rufaj, (g) lateral view, (/;) ventral view; Macropus 
canguru, (/) lateral view; Thyiogale stiginaiica't, (/) lateral view; (A) ventral view. Fam. Dasyurinae: 
Dasyuroides byrnei, (I) dorsolateral view; Sarcophilius harrisii, (m) ventral view. Fam. Phalangeridae: 
Pseudocheirus cupreus, (n) dorsal view, io) lateral view; Pseudocheirus peregrinus, (p) lateral view, 
(q) dorsal view; Petaurus breviceps, (r) ventral view. Fam. Peramelidae: Isoodon macrourus, {s) 
ventral view; Peranieles nasuta, (t) ventral view. Key: AC, acrosome; AF, axial filament; CD, 
cytoplasmic droplet (middle-piece bead) ; CM, cortical helix of main-piece sheath ; MH, mitochondrial 
helix of middle-piece; A'G, neck granule; i?C, ringcentriole; FG, ventral groove. 
* Fixed in Carnoy fixative, t Fixed in Bouin's fluid. 



134 



538 R. L. HUGHES 

was also variably positive to periodic acid-Schiff (P.A.S.) between species and the basal 
granule complex was invariably strongly P.A.S. -positive. Neither acrosome nor basal 
granule complex exhibited any reduction in P.A.S. activity in saliva controls. A faint 
tinge of green over the entire head surface in Feulgen-fast green preparations pre- 
sumably represents a limiting membrane. 

A "nuclear rarefaction" of vacuole-like appearance results from a minute 
superficial nuclear indentation. The nuclear rarefaction was most conspicuous in the 
Dasyuridae and Peramelidac and least evident in the Macropodidae. This structure 
is located on the mid-median aspect of the ventral nuclear surface of all sperm with 
the exception of those of the Phascolarctidae, where its occurrence is also ventral and 
median but distal. 

In most of the marsupial sperm examined acrosomal material (Fig. 1 ; AC) was 
apparently confined to a relatively small surface area of the head. In the Macropodidae 
the acrosome is relatively small and is a discrete ovoid structure embedded super- 
ficially in the extreme proximal portion of the dorsal head surface. In some of the 
Phalangeridae it has a definite structure as in Pseudocheinis (Figs, \n-\q) where 
it occupies all but a marginal annular zone of the dorsal head surface and is rather 
deeply embedded. In other phalangerids, such as Petaurus breviceps (Fig. \r), the 
dorsal head surface in Feulgen-fast green preparations gives a diffuse acrosomal 
reaction and bears a shallow depression which extends to all but the margins. A 
similar diffuse acrosomal reaction of at least the proximal half of the dorsal head 
surface occurred in the Dasyuridae. The proximal dorsal tip of the dasyurid sperm 
has a concentration of acrosomal material situated in a minute groove. The acrosomal 
material in the Peramelidae was found in a small distally flanged proximal cap which 
covered a minute nuclear protuberance. In the Phascolarctidae the acrosome is a 
small "comma-shaped" structure. The body of the acrosomal "comma" is embedded 
superficially in about the middle of the dorsal head surface and the tail of the comma 
extends throughout the greater portion of the inner curvature of the head hook. 

In marsupial sperm the ventral surface of the head (by convention that bearing 
the flagellum) is typically grooved (Fig. 1 ; VG) or bears a shallow distal notch as in 
the case of the Phascolarctidae. At the distal extremity of the head the groove is broad 
and deep so that the head is here relatively broad and has the form of an extremely 
thin curved plate. The groove becomes shallow and narrow towards its proximal 
extremity; in the Macropodidae and Phalangeridae it terminates at about the mid- 
median portion of the ventral head surface. The groove is most extensive in the 
Peramelidae involving the whole of the ventral aspect of the nucleus, only the proximal 
acrosomal head cap is excepted. In the Dasyuridae it extends throughout the distal 
four-fifths of the head. 

Spermatozoa are immature when they enter the head of the epididymis and 
were characterized by the orientation of the long axis of the head at 90° to the 
flagellum which was directed towards the nuclear rarefaction. The ventral surface of 
the spermatozoon head was supported by a somewhat cone-shaped cytoplasmic 
droplet (Fig. 1 ; CD) of characteristic morphology for each species. Phascolarctid 
sperm from the head region of the epididymis differed from the other marsupial 



135 



MORPHOLOGY OF SPERMATOZOA 539 

species examined in that tiie flagellum was most frequently observed not to meet the 
head at right angles and cytoplasmic droplets were small and often absent. On 
entering the epididymis the head hook of the phascolarctid spermatozoa were only 
slightly recurved or of an irregular spiral configuration. During the passage of 
spermatozoa through the epididymis the head hook became simple (vv'ithout spiral) 
and more tightly recurved. 

Maturation of spermatozoa is completed during their passage through the 
epididymis and is accompanied by shedding of the cytoplasmic droplet and rotation 
of the long axis of the head parallel to that of the flagellum. The neck of the 
flagellum of mature epididymal sperm in all species was inserted in the vicinity of the 
nuclear rarefaction. In the Dasyuridae the neck was inserted rather deeply into the 
proximal margin of the nuclear rarefaction. In the Peramelidae the proximal tip of 
the flagellum was also deeply inserted and extended from the proximal margin of the 
nuclear rarefaction to a point about midway between the anterior rim of the nuclear 
rarefaction and the most proximal extremity of the nucleus. 

The flagellum is traversed throughout its entirety by an axial filament (Fig. 3; 
AF). The size of the flagellum varies from species to species. The smallest flagellum 
was that of Pliascolomis mitchelli with a maximum diameter of 0-9 /^ and a minimum 
length of 87-9^ (Table 1). The giant flagella of dasyurid sperm are among the 
largest known for mammals. Dasyiiroides byrnei has a minimum flagellum length 
of 242 • 1 /Li and a maximum flagellum thickness of 3 • 1 /x. In an old museum specimen 
of the testes of the now possibly extinct dasyurid Thylacinus cynocephalus (Tasmanian 
wolf or tiger) the flagellum of epididymal sperm in wax sections had a maximum 
diameter of 3 0/x and comparable morphology to that of other dasyurids; the 
sperm heads, although degenerate, were in the form of a long narrow plate, dorso- 
ventrally flattened and with the flagellum inserted at about the mid-median ventral 
aspect. Peramelid sperm flagellae were also relatively large, having a maximum 
diameter of as much as 2 ;li and a minimum length of up to about 200 ^ (Table 1). 
Macropod and phalangerid sperm flagellae were of intermediate dimensions rarely 
varying from a maximum diameter of 1 -5 /m and a minimum length of a little over 
100 /x. 

The basal granule complex located at the proximal end of the flagellum consists 
of at least fused proximal and distal components in the Dasyuridae and Peramelidae. 

The neck region of the flagellum is a slender proximally pointed cone with a 
smooth contour, and a small neck granule (Fig. 1 ; NG) is situated at approximately 
half its length. It was only possible to identify the neck granule with certainty in the 
Peramelidae, Dasyuridae, and Macropodidae. In the Peramelidae and Dasyuridae 
it seemed to be a more deeply stained, modified portion of the ground substance of 
the neck rather than the discrete granule found in the Macropodidae. The sperm of 
the dasyurids Dasyuroides byrnei, Sarcophilus harrisii, and Thylacinus cynocephalus 
had a neck length of about 3-5 /j. in comparison with 2-7 fi for the peramelids 
Isoodon macrourus and Perameles nasuta. Macropod sperm necks ranged in length 
from 1 • 8 /x in Thylogale stigmatica to 2 • 6 /x in Protemnodon rufogrisea. The neck 
lengthsof the Phalangeridae and Phascolarctidae were somewhat reduced in compari- 
son to those of other marsupial families. 



136 



540 R. L. HUGHES 

The proximal portion of the middle-piece in all species examined tapered gradu- 
ally to the diameter of the neck and was particularly firmly clasped by the lateral 
margins of the sperm head in the Peramelidae and Dasyuridae. The remainder of 
the middle-piece was relatively cylindrical. A mitochondrial helix (Fig. 1 ; MH) of 
spiral configuration gave the entire surface of the middle-piece sheath a slightly 
uneven contour. The mitochondrial helix is a relatively fine structure in the Dasyuridae 
and Peramelidae, of moderate thickness in the Macropodidae and Phascolarctidae 
and Petaiirus breviceps of the Phalangeridae. It was quite thick and granular with 
relatively few gyres in the genus Pseudocheirus of the Phalangeridae. The middle- 
piece is terminated distally by a ring centriole (Fig. 1 ; RC). 

The flagellum undergoes an abrupt reduction in diameter on the main-piece 
side of the ring centriole in both the Pseudocheirus species and to a moderate degree 
in Petaurus breviceps and the Macropodidae, but not to any appreciable extent in the 
Dasyuridae, Peramelidae, and Phascolarctidae. 

The main-piece of the flagellum tapers distally and in twisted specimens appears 
not to be circular in cross section in Pseudocheirus peregrinus, Peramelidae, Dasyuridae, 
and Macropodidae. Striations of the sheath of the main piece in all sperm indicate 
the presence of a fine spiral cortical helix (Fig. 1 ; CH). The tail sheath also gave a 
strong impression of two lateral thickenings in transverse axis in Macropus canguru, 
Protemnodon rufogrisea, Pseudocheirus peregrinus, Perameles nasuta, and Isoodon 
macrourus. 

The axial filament protruded beyond the terminal portion of the sheath of the 
main-piece in apparently complete sperm of all species but this cannot be positively 
taken to represent a true end-piece for in all preparations terminal breakage of the 
main-piece was prevalent. 

IV. Discussion 

Spermatozoa from three other Peramelidae, Perameles gunnii, Isoodon obesulus, 
and Echymipera rufescens have also been exam.ined superficially and it can be stated 
that they are comparable in morphology to other peramelid sperm. The spermatozoa 
of marsupial mice, Antechinus flavipes flavipes, A. f. leucogaster, A. swainsonii, A. 
stuartii, and Sminthopsis crassicaudata, have a morphology typical of other dasyurids 
(Woolley, personal communication). This similarity in morphology also extends to 
two other dasyurids, Phascogale albipes ( = Sminthopsis murina) (Fiirst 1887) and 
Dasyurops maculatus (Bishop and Austin 1957; Bishop and Walton 1960). The 
spermatozoon morphology of the macropod species examined in the present study 
varies in only minor details from that of six other macropods previously described 
by Benda (1906), Retzius (1906), and Hughes (1964). 

The phenomenon of conjugate spermatozoa (pairing of relatively numerous 
epididymal spermatozoa) redescribed and reviewed by Biggers and Creed (1962) for 
the American opossum, Didelphis, has not been observed in any of the sperm pre- 
parations from Australian marsupials; however, fresh unfixed material has been 
examined only for Potorous tridactylus (Hughes 1964) and Phascolomis mitchelli. 



137 



MORPHOLOGY OF SPERMATOZOA 541 

Another feature worth mentioning is that the head of the epididymis was not 
fused with the testis in any marsupial examined, including Thylacinus cynocephalus 
and Dendrolagus lumholtzi. In the Dasyuridae and Peramelidae a relatively long 
single efferent duct together with associated blood vessels links the epididymis to 
one pole of the testis long axis by way of an extensive membrane, the mesorchium. 
A tract of relatively long multiple efferent ducts serves the same function in the 
Phalangeridae, Phascolarctidae, and Macropodidae. A ligament was inserted by 
way of the mesorchium into the opposite pole of the testis. 

In both the wombat and the koala the morphology of the sperm, particularly 
the head, differs strikingly from that of any marsupial sperm previously described. 
In both species the proximal portion of the spermatozoon head bears a strongly 
recurved hook not described for other marsupial sperm, and the flagellum is inserted 
into a notch on one side of the distal portion of the head (Plate 1, Fig. 1 ; and Figs. \a 
and \b). These features, although somewhat resembling those of certain murid 
sperm, are not strictly comparable (Plate 1, Fig. 2) (Friend 1936). The hook in the 
wombat sperm resembles that of Microtus hirtus, Lemmus lemmus, and several other 
members of the murid subfamily Microtinae in that the hook contains no supporting 
"rod" and its tip like that of Lemmus lemmus is typically extremely reflected so that 
it lies against the distal portion of the head (Friend 1936). The position of the hook 
in Phascolomis is not an artefact of fixation for it was observed in living spermatozoa 
from the epididymis of several specimens. In sperm from the head of the epididymis 
the curvature of the hook frequently approximated to that of rats and mice. It can 
be seen from Plate 1, Figure 1, and Figures \a and \b that the insertion notch of 
the flagellum of the wombat and koala sperm is located on the opposite side of the 
head to the hook, whereas in the hooked types of murid sperm both structures occur 
on the same side of the head (Plate 1, Fig. 2). A head hook is absent in at least the 
murine, Micromys mmutus and in the microtine Ondatra zibethica (Friend 1936). 
In Heidenhain's iron haematoxylin preparations the head length of the wombat sperm 
measured from the distal extremity to the most proximal point of the curvature of 
the hook (i.e. excluding the recurved portion of the hook) is about 5-7 /x in contrast 
to 8-0 /x and 11-7/x for mouse and rat, respectively (Friend 1936). Feulgen pre- 
parations (with or without fast green counterstain) of wombat and koala sperm have 
shown that nuclear material (DNA) extends to the tip of the hook and occupies all 
but a small comma-shaped acrosomal portion of the head. Herein lies the greatest 
departure of wombat sperm from the hooked varieties of murid sperm. In several 
microtine species the hook is formed entirely from a proximal extension of the nuclear 
cap (acrosome). In murine sperm a hooked portion of the nucleus bearing a rod 
extends into the hooked nuclear cap and follows its contour almost to its proximal 
extremity (Friend 1936). 

On the basis of skeletal and dental structure most workers consider the koala 
to be more closely related to the ringtail possums of the genus Pseudocheirus than the 
wombat (Wood Jones 1924; Simpson 1945). Comparisons of sperm morphology on 
which selection pressure would presumably be lower than that for external characters 
of an animal such as skeletal or dental characters, is therefore of considerable interest 
as a possible basis for taxonomic classification. 



138 



542 R. L. HUGHES 

Tt can be seen from the previous descriptions that the spermatozoon oi Pseudo- 
cheirus peregrinus is not intermediate in structure between the more typical marsupial 
types (Macropodidae and Dasyuridae) and those of the highly divergent wombat and 
koala. On the contrary, it deviates in quite a difTerent manner from the typical 
marsupial patterns. The head is broad (3-8/x) in comparison to its length (5-9/^), 
the anterior end lacks a hook and is semi-circular in dorsal view (Plate 1, Figs. 3 and 4). 
Other distinguishing features are the shape and position of the acrosome previously 
mentioned and a relatively short middle-piece (6-9 /x). The view that the koala is 
more closely related to the ringtail possum than the wombat is not supported by 
comparisons of sperm morphology. On the contrary, the findings reported here 
support the observations of Sonntag (1923) and Troughton (1957) who considered 
that the koala shares sufficient characters with the wombat for its classification along 
with the phalangers to be rejected. 

V. Acknowledgments 

The author wishes to express his sincere thanks to Dr. E. H. Hipsley, Director, 
Institute of Anatomy, Canberra; to J. T. Woods, Queensland Museum; to J. A. 
Thomson, Zoology Department, University of Melbourne; to Dr. M. E. GriflSths, 
W. E. Poole, K. Keith, M. G. Ridpath, Division of Wildlife Research, CSIRO, for 
material; to J. Sangiau and L. S. Hall for technical assistance; to E. Slater for 
photography; and to Professor K. W. Cleland and Dr. A. W. H. Braden who offered 
helpful criticism. 

VI. References 

Benda, C. (1897). — Neuere Mittheilungen iiber die Histiogenese der Saugethierspermatozoen. Verh. 

berl. physiol. Ges. 1897. [In Arch. Anat. Physiol. (Physiol. Abt.) 1897: 406-14.) 
Benda, C. (1906). — Die Spermiogenese der Marsupialier. Denkschr. med.-naturw. Ges. Jena6: 441-58. 
BiGGERS, J. D., and Creed, R. F. S. (1962). — Conjugate spermatozoa of the North American opossum. 

Nature, Lond. 196: 1112-3. 
Binder, S. (1927). — Spermatogenese von Macropus giganteus. Z. Zellforsch. 5: 293-346. 
Bishop, M. W. H., and Austin, C. R. (1957). — Mammalian spermatozoa. Endeavour 16: 137-50. 
Bishop, M. W. H., and Walton, A; (1960). — Spermatogenesis and the structure of mammalian 

spermatozoa. In "Marshall's Physiology of Reproduction". (Ed. A. S. Parkes.) 3rd Ed. 

Vol. 1, Pt. 2, pp. 1-129. (Longmans, Green and Co.: London.) 
Carleton, H., and Drury, R. A. B. (1957). — "Histological Technique." (Oxford University Press.) 
Cleland, K. W. (1955). — Structure of bandicoot sperm tail. Aust. J. Sci. 18: 96-7. 
Cleland, K. W. (1956). — Acrosome formation in bandicoot spermiogenesis. Nature, Lond. Ill: 

387-8. 
Cleland, K. W. (1964). — History of the centrioles in bandicoot (Perameles) spermiogenesis. J. Anat. 

98:487. 
Cleland, K. W., and Lord Rothschild (1959). — The bandicoot spermatozoon: an electron 

microscope study of the tail. Proc. R. Soc. B 150: 24-42. 
Duesberg, J. (1920). — Cytoplasmic structures in the seminal epithelium of the opossum. Carnegie 

Institute Contributions to Embryology. Vol. 9, pp. 47-84. 
Friend, G. F. (1936).— The sperms of the British Muridae. Quart. J. Micr. Sci. 78: 419-43. 
Furst, C. M. (1887). — Ueber die Entwicklung der Samenkorperchen bei den Beutelthieren. Arch. 

mikrosk. Anat. EntwMech. 30: 336-65. 
Hughes, R. L. (1964). — Sexual development and spermatozoon morphology in the male macropod 

marsupial Potorous tridactylus (Kerr). Aust. J. Zool. 12: 42-51. 



139 



MORPHOLOGY OF SPERMATOZOA 543 

Jordan, H. E. (1911). — The spermatogenesis of the opossum {Didelphis virginiana) with special 

reference to the accessory chromosome and the chondriosomes. Arch. Zellforsch. 7: 41-86. 
KoRFF, K. VON (1902). — Zur Histogenese der Spermien von Phalangista vulpina. Arch, mikrosk. 

Anat. EntwMech. 60: 233-60. 
McCrady, E. (1938). — The embryology of the opossum. Am. Anat. Mem. 16: 1-233. 
Pearse, a. G. E. (1961).— "Histochemistry." (J. & A. Churchill: London.) 
Retzius, G. (1906). — Die Spermien der Marsupialier. Biol. Unlers. (N. F.) 13: 77-86. 
Retzius, G. (1909).— Die Spermien von Didelphis. Biol. Unfers. (N. F.) 14: 123-6. 
Selenka, E. (1887). — Studien ijber Entwickelungsgeschichte der Thiere. Das Opossum (Didelphis 

virginiana). Wiesbaden 1887, pp. 101-72. 
Simpson, G. G. (1945). — Principles of classification and a classification of mammals. Bull. Am. 

Mas. Nat. Hist. S5: 1-350. 
Sonntag, C. F. (1923). — On the myology and classification of the wombat, koala and phalangers. 

Proc. Zool. Soc. Lond. 1922: 683-895. 
Troughton, E. (1957). — "Furred Animals of Australia." 6th Ed. (Angus and Robertson: Sydney.) 
Waldeyer, W. (1902). — Die Geschlechtszellen. In "Handbuch der vergleichend und experimentellen 

Entwickelungsgeschichte der Wirbelthiere". Vol. 1, Pt. 1, pp. 86-476. 
Wilson, E. B. (1928). — "The Cell in Development and Heredity." (Macmillan: New York.) 
Wood Jones, F. (1924). — "The Mammals of South Australia." Pt. II. (Govt. Printer: Adelaide.) 



Explanation of Plate 1 

Figures 1 and 2 are photographs of Heidenhain's iron-haematoxylin preparations from formalin-fixed 

epididymal material 

Fig. 1. — Phascolomis mitchelli, mature epididymal spermatozoon, lateral view. 

Fig. 2. — Rattus norvegicus, mature epididymal spermatozoon, lateral view. 

Fig. 3. — Pseudocheirus peregrinus, spermatozoon head, showing centrally placed acrosomal pit, 

dorsal view. 
Fig. 4. — Pseudocheirus peregrinus, epididymal spermatozoon, lateral view. 



140 



Hughes 



MORPHOLOGY OF SPERMATOZOA 




A 



Aust. J. ZooL, 1965, 13, 533-43 



Plate 1 



s 



141 



THE GENITAL SYSTEM AND THE FETAL MEMBRANES 
AS CRITERIA FOR MAMMALIAN PHYLOGENY AND 

TAXONOMY 

By H. W. Mobsman 

All systems of classification of natural phenomena are admittedly imperfect 
because these phenomena differ from one another in such infinitely variable de- 
grees that it is impossible to divide them into a system of groupings which do 
not frequently overlap or intergrade. It is also absolutely impossible consistently 
to select morphological criteria for a scheme of classification that will lend them- 
selves to the assignment of a series of ranks such as species, genera, and famiUes, 
in one group that ^vill be of parallel value to a similar series assigned to another 
related group. Yet in spite of these obviously insurmountable barriers to perfec- 
tion, convenience and orderliness in science demand that classifications be made, 
and that their categories be of as nearly parallel value as possible. 

Most biologists believe that the best basis for classification is phylogeny, that 
is, the evolutionary or genetic relationships within and of the group. This is so 
widely accepted that practically all other forms of classification are considered 
"artificial." Although artificial classification is often temporarily necessary, as 
in tentatively fitting a poorly understood entity into a general scheme, still a 
natural or phylogenetic classification should always be the ultimate aim. 

Criteria for classification of any group should therefore be characters of 
phylogenetic significance. Furthermore there should be some way to evaluate 
the relative significance of one set of criteria in relation to another set; for in- 
stance, dentition as compared to skull proportions; or pelage as compared to 
baculum. There should also be some method for determining whether a given set 
of characters is suitable for separating the lower categories such as species and 
genera, or the higher categories such as famihes and orders. 

The more conservative characters obviously will be of greater value in char- 
acterizing the higher categories, while the less conservative will only be of use 
in the lower categories. The presence of the fetal membranes (amnion, chorion, 
yolk sac, and allantois) is a highly conservative character appearing in all Am- 
niota. Yet certain aspects of the finer morphology of the placenta, such as 
whether it is villous, trabecular, or labyrinthine, are of use only in characterizing 
the families within a suborder, for example the Anthropoidea. This is true be- 

289 



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290 JOURNAL OF MAMMALOGY Vol. 34, No. S 

cause parallel transitions in placental morphology are known to occur inde- 
pendently in other orders not closely related to the Anthropoidea or to one 
another. These same aspects of finer morphology are, however, too conservative 
to be of much use in separating genera or species, there being very slight or no 
differences in this character within single families or genera. 

The relative conservatism of biological characters is based on two entirely 
distinct and independent thhigs. The first is the human factor, or simply the 
question of generality versus particularity of concept. The greater the breadth 
or inclusiveness of a character concept the more conservative it is within its 
particular field. For example, the character "bony skeleton" is much broader 
and therefore much more conservative than the character "cranium", w'hile 
the latter is in turn much broader and more conservative than "zygoma." We 
can and do quite properly select the generalized and broader characters as 
criteria for separating the higher categories, and the more narrow and particular 
ones for the lower subdivisions. 

Superimposed on this, much more complex, and equally as important, is the 
second or biological factor in determining conservatism. This may be expressed 
as the degree to which a character has been subjected to natural selection. 

Assuming equal, intrinsic genetic factors, it is certainly true that the more 
intimately a character is related to the environment the more rapid and exten- 
sive will be its environmental adaptations during the course of evolution. The 
main thesis of this discussion rests on this assumption. It is maintained that 
the structural characters of the reproductive tracts and fetal membranes of 
mammals, because they have been largely independent of environmental selec- 
tion, show relatively little evolutionary divergence as compared to most other 
organ systems. This is not the place to discuss, statistically, results to be ex- 
pected in the evolution of a genetically variable system subjected to environ- 
mental selection in contrast to one subjected to very little and indirect en- 
vironmental action. However, it can be readily understood that without the 
selective effects of differing environments, variations would tend to be submerged 
because of continuous selection for one constant set of environmental conditions. 
A race under these conditions would become more and more stabilized and 
specialized, but no new divergent races would arise from it. But this is not the 
situation in regard to a genetically variable system, such as the fetal membranes 
that are practically isolated from any direct selective effects of external environ- 
ment. In such a system, in this case the fetal membranes, evolution is free to 
proceed along almost any line so long as it meets certain vital requirements: 
(1) the supplying of a means of maintaining an embryo within the mother's 
uterus until mature enough to be bom; (2) structural conditions which will 
allow the uterus to resume a normal nonpregnant state after delivery, so that 
another pregnancy may ensue. 

Certainly these fundamental requirements are far from simple in either a 
structural or physiological sense; they involve extremely complex mechanisms. 
But the point is that not only is the intrauterine en\'ironment relatively con- 
stant in mammals generally, but so are the requirements for maintenance of an 



143 



Aug., 195S MOBSMAN— TAXONOMIC CRITERIA 291 

embryo and for restorability of the uterus to the condition for beginning another 
pregnancy. 

What then should one expect of the evolution of an organ system, such as the 
fetal membranes, largely isolated from the external environment and charged 
with a highly complex job to do, but one which is fundamentally the same in all 
members of the group, in this case the Subclass Eutheria? It seems that, regard- 
less of rate of genetic variation of the system, divergence would be relatively 
slow and narrow, and that intergradation would be the rule, there being slight 
environmental selection, and little race isolation due directly to adaptive varia- 
tions in this system itself. But while this type of evolution would be taking 
place in an environmentally independent organ system, the group of organisms 
in which the organ system existed could nevertheless be undergoing the usual 
evolutionary course in its other organ systems: diverging widely in adaptation 
to environmental niches old or new; losing species or whole major groups by 
extinction; in short, becoming the widely divergent, often aberrant or isolated 
groups that are characteristic of mammals at the present time. 

Such an environmentally isolated system must then be very conservative in 
its characters as compared to those organ systems related closely to the environ- 
ment and therefore subject to intense, adaptive evolution. The characteristics of 
such a system should vary relatively little between major groups, and almost 
none between closely related minor categories. This lack of divergence should 
make it possible to detect common characteristics among groups widely sepa- 
rated from one another in other characteristics, whether this be due to adapta- 
tions to divergent environments, or to extinction of intergrading groups. Con- 
versely, dissimilarity in characters of a conservative organ system should be good 
evidence of lack of close phylogenetic relationship. 

It is generally conceded that similarity of more conservative characters be- 
tween two forms is better evidence of close relationship than similarity of less 
conservative characters. Whether lack of conservatism is due to more intensive 
environmental selection or to a combination of this with such things as more 
intensive sexual selection, or greater innate potential of genetic variability, there 
is more chance that similarities in less conservative characteristics are due to 
evolutionary parallelism or convergence. In estimating phylogenetic relation- 
ship it is therefore extremely important to know which are the more conserva- 
tive organ systems and to give their characters the greater weight. It is also im- 
portant to evaluate the various characters of such an organ system to determine 
which are the more conservative within the system. The more conservative will 
serve to characterize the higher categories, the less only the lower ones. 

The foregoing discussion largely reiterates generally recognized principles 
which have been used for years by students of evolution and taxonomy. How- 
ever it seemed best to restate them here since the chief purpose of this paper is 
to point out that the reproductive tracts and fetal membranes of mammals are 
conservative systems which have never been adequately used in phylogenetic 
and taxonomic studies of this group. It will be shown that the relative conserva- 
tism of the various features of these organ systems can be estimated and the 



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292 JOURNAL OF MAMMALOGY Vol. S4, No. S 

characters used as criteria in proper relation to their significance. It is now best 
to proceed to specific examples. The first concerns the male genital tract of the 
Sciuridae. 

In 1923, Pocock pointed out the marked difference between the male external 
genitalia of Tamiasciurus and Sciurus and separated the two genera on this 
basis. In 1932, Mossman, Lawlah, and Bradley published a more detailed study 
of the tracts of Sciurus carolinensis, S. niger, Tamias striatus, Citellus tridecem- 
lineatus, Glaucomys volans, and Tamiasciurus hudsonicus. They showed that the 
typical sciurid male tract as seen in all these genera (except Tamiasciurus), and 
as also described by KroUing (1921) in Sciurus vulgaris, is characterized by a 
unique arrangement of the ducts of the bulbo-urethral glands. Tullberg (1899) 
gave enough information on several other genera to indicate the probability 
that they also have this same character, and Oudemans (1892) made it fairly 
clear that Petaurista petaurista is essentially like Sciurus. So, with the exception 
of Tamiasciurus, other sciurids so far as known have a pair of large bulbo- 
urethral glands drained by a pair of voluminous ducts which, upon entering the 
sheath of the corpus cavernosum urethrae in the bulb region, become highly 
modified to form another accessory organ, the bulbar gland. This whole com- 
plex is then drained by a single long glandular duct, the penile duct, w^hich lies 
ventral to the urethra throughout almost the entire length of the corpus cav- 
ernosum urethrae, finally entering the urethra at approximately the base of the 
glans. The author has examined some other genera, including Marmota and 
Heliosciurus and has found them also fundamentally like this. 

At the same time we showed that Tamiasciurus, the red squirrel or chickaree, 
possesses an entirely different type of bulbo-urethral gland and duct. It has no 
bulbar gland and no penile duct. It does have a urethral sinus in the bulb much 
like that of some Muridae. Later it was shown that the female tract of the 
chickarees is also unique, the vagina being extremely long and coiled while that 
of all other Sciuridae studied is short and broad (Mossman, 1940). Other peculiar 
features of the male tract of the chickarees, such as the long filiform penis and 
the absence of a baculum, were also pointed out at that time. (Layne (1952) has 
shown that Tamiasciurus does possess a minute baculum averaging only .26 mm, 
in length in adults. Pocock and the author both failed to note this structure.) 

A recent, and as yet unpublished manuscript by Mr. M. R. N. Prasad of 
Central College, Bangalore, India entitled, "Male genital tract of two genera of 
Indian squirrels," presents excellent descriptions of the palm squirrel, Funam- 
bulus palmarum palmarum Linn., and of the giant Malabar squirrel, Ratufa 
indica maxima Schreb. Ratufa has the typical sciurid tract, but F. palmarum 
is hke Tamiasciurus in having minute Cowper's glands and no bulbar gland or 
penile duct. Obviously this indicates close relationship between this species and 
the Tamiasciurinae, and poses a number of interesting questions in regard to 
sciurid phylogeny and geographic distribution, to say nothing of the doubt it 
throws on the present taxonomy of the whole group. 

Although the nature of the reproductive tracts of most of the genera of squir- 
rels is still unknown, enough knowledge is available to make it seem very prob- 



145 



Aug., 195S MOBSMAN— TAXONOMIC CRITERIA 293 

able that instead of a wide range of types within the family, there are at least 
two fundamentally different types. This seems probable as it is definitely known 
that at least one genus of three of the six tribes that Simpson (1945) includes 
under the subfamily Sciurinae has the typical male sciurid tract; and that two 
genera of his second subfamily, Petauristinae, also are typical. One can raise 
the question then as to the logic in placing the chickarees and Funambulini as 
tribes of the subfamily Sciurinae when the reproductive tracts of Tamiasciurus 
and F. p. palmarum are so different from others of this group. Also, in view of 
Prasad's work, F. p. palmarum and Ratufa should not be in the same tribe with 
one another. Furthermore, it is illogical to place the chickarees and Funambulus 
in these subgroups and at the same time to put Petaurista and Glaucomys in a 
separate subfamily, although their genital tracts are almost identical to that 
of Sciurus. Obviously the flying squirrels (Petauristinae) have been separated 
on the basis of petagial characters; but these must be highly subject to environ- 
mental selection, hence nonconservative. Very similar petagial characters have 
been developed in certain marsupials (Acrohates and Petaurus), and in other 
Eutheria, namely in the Dermoptera, and in the Anomaluroidea among the ro- 
dents. Of course one could ask if similar reproductive tract characters may not 
also have developed in widely unrelated groups. There is no evidence that this 
is true, but it must be admitted that the data are insufficient. This in itself should 
be a challenge, to those who ask the question, to make an effort to gather the 
information. 

There may be those who will still fall back on the fundamental question of 
whether the genital tract characters are more conservative than others in the 
Sciuridae. If they will allow the ruling out of the genus Tamiasciurus and the 
species Funambulus p. palmarum as members of the family, then one can cite 
the fact that the genital tracts of Sciurus, Tamias, Citellus, Marmota, Ratufa, 
and Glaucomys are the same in fundamentals, and indeed very similar even in 
details, while there is great divergence between these various genera in body 
form, pelage, feet, ears, skeleton, skull, and teeth. If one is not willing to allow 
the ruling out of the chickaree group, and F. p. palmarum, then in the face of 
the apparent aberrance of these he is bound to withhold judgment until someone 
can show whether or not there are intergrading forms, so far as male genitals 
are concerned, between them and the typical sciurids. If there are, then perhaps 
the genitals are not as conservative as they now seem. 

There are a few minor characters of male genital tracts that are variable 
enough in some groups to be of use in separating species of a single genus. Howell 
(1938) pubhshed a plate showing the bacula of several species each from the 
genera Eutamias, Citellus, and Sciurus. There are fairly obvious intrageneric 
differences between these bones within each of the three genera, although oc- 
casionally in two species they are practically identical (Sciurus carolinensis and 
niger). It is probable that there are other features of the male genitals which 
would show intrageneric differences: certainly differences in the glans penis cor- 
related with those of the bacula would be expected. However, appreciable intra- 
generic, species differences in the internal genitaha of either the male or female 



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294 JOURNAL OF MAMMALOGY Vol. S4, No. S 

have never been noted by the author in the sciurids or other groups, but inter- 
generic differences are the rule, and are often rather extensive; for example 
between Tamias, Citellus, and Sdurus (Mossman, Lawlah and Bradley, 1932). 

To the author's knowledge, no attempt has ever been made to compare the 
reproductive tract at the level of the higher categories. It seems doubtful that 
such clearcut indications of relationship would be found as occur in the case of 
the fetal membranes, where, for example, considerable affinity is shown be- 
tween the Artiodactyla, Perissodactyla, and Cetacea; and between the Fis- 
sipedia and Pinnipedia. Before such a study would be sound, a thorough investi- 
gation of the various genera and families of several well-defined orders should be 
made, in order to evaluate the conservativeness of the various genital tract 
features. 

The female genital tract characters are probably about as equally conserva- 
tive as those of the male, but those of the female are in general more difficult to 
observe and define. A good example of this is the os clitoridis or baculum, which 
in recent years has been demonstrated in females of several species, leading one 
to expect that, where present in the male, it probably also occurs in the female. 
This female element may show intrageneric differences like its male homolog, 
but the fact that it is usually so small and so obviously rudimentary argues 
against its value as a character for taxonomic purposes. The other characters of 
the female external genitalia are also relatively indefinite and difficult to ob- 
serve. Female internal genitalia show a few very definite features which could 
be of considerable use, but they are almost always too conservative for intra- 
generic taxonomy, in fact in most cases they are of use only in separating groups 
higher than genera. For instance, the form of the uterus, oviduct, and ovary is 
almost identical in the Cervidae and Bovidae. The Mustelidae, Procyonidae, 
and Ursidae have a peculiar configuration of the oviduct in relation to the 
ovary and ovarian bursa that is highly characteristic and differs very little be- 
tween the three families. The Heteromyidae and Geomjddae likewise have a 
characteristic oviduct pattern which is practically identical in the two groups. 
By and large then, it may be said that the characters of the female internal 
genitalia are very conservative, but usually rather obscure and difficult to 
observe. 

Comparative studies of the microscopic anatomy of the ovaries have revealed 
no case where obvious intrageneric differences exist, except those due to differ- 
ences in body size of the species. However some intergeneric differences in 
microscopic structure do occur: for example; ovaries of mature females of Syl- 
vilagus and Lepus are rather easily distinguished from one another, but those of 
Lepus and Oryctolagus would be difficult; Citellus and Sdurus are separable, 
but Sdurus and Tamias are alike, except for size. When one reaches the higher 
categories such as families and orders, then microscopic features become char- 
acteristic for each group. All the mustelids examined have a very similar and 
tjrpical interstitial cell pattern: this includes Maries americana, Taxidea taxus, 
Mephitis mephitis, Spilogale interrupta, and Mustela vison, dcognani, frenata, and 
putorius. There are even examples of striking similarity in microscopic structure 



147 



Aug., 1953 MOBSMAN— TAXONOMIC CRITERIA 295 

between related families, at least so far as the few genera of each studied are an 
indication. Examples of this are Ursidae and Procyonidae, Cervidae and Bovidae, 
and Erethizontidae and Dasyproctidae. 

Let us now turn our attention briefly to the fetal membrane characters of the 
Sciuridae (Mossman, 1937; Mossman and Weisfeldt, 1939). It is not necessary 
to enter into a detailed description of the sciurid membranes and placentation, 
as the main point to be made is that these are even more conservative characters 
than the male genital system of the group. So it is not surprising that in all the 
genera studied, including Tamiasciurus, the fetal membranes are practically the 
same, differing only in minor details. These include all the genera mentioned in 
connection with the male genitals, except Heliosciurus and Petaurisia, and two 
others in addition, Cynomys, Xerus (Rau, 1925). In fact the membranes and 
placenta of Aplodontia are distinctly sciuroid, although the male genitals lack 
the bulbar gland and penile duct. 

It appears then that the criteria of the male and female reproductive tracts 
and the fetal membranes could be applied to advantage in determining the 
phylogenetic relations of the Sciuridae, and consequently in estabhshing a more 
logical taxonomy of this group. The fetal membrane characters are even 
more conservative criteria than those of the male or female genital tracts. 

The application of the genital tract and fetal membrane criteria in the phy- 
togeny and taxonomy of the Sciuridae has been discussed first, since it is the 
only group in which the author has made reasonably comprehensive studies of 
both systems. Little has been said thus far of the evaluation of specific criteria, 
as the studies of the male tract in such a small group do not lend themselves to 
adequate analysis. The author has however made extensive comparative studies 
of mammalian fetal membranes and believes, that for them, the basis is broad 
enough to enable clearly reliable estimates to be made of the relative value of 
the different characters involved. Since this subject was presented fully in his 
1937 monograph, it is not necessary to repeat the details here. Suffice it to point 
out that all the descriptions of the fetal membranes of specific species which 
have appeared in the literature since then, and all of the numerous additional 
observations of the author, bear out the thesis proposed at that time. The facts 
derived from these studies can be stated very simply. 

1. In every group of mammals, high or low in category, in which the members 
can be clearly related to one another on the basis of total anatomical similarity, 
their fetal membranes are fundamentally similar, showing far less divergence 
than do other characters. These groups are perhaps best illustrated by the orders 
Lagomorpha, Rodentia, Carnivora, and Artiodactyla; by the suborders Micro- 
chiroptera, Lemuroidea, and Anthropoidea; by the families Tenrecidae, Sorici- 
dae, Talpidae, Cebidae, Cercopithecidae, Pongidae, Das5T)odidae, Sciuridae, 
Heteromyidae, Geomyidae, Muridae, Canidae, Mustelidae, Felidae, Cervidae, 
and Bovidae; and by numerous genera in these and some other families. All 
these groups consist of anatomically closely related forms and all have even 
closer fetal-membrane affinities. They are used as illustrations because enough 
is known about the fetal membranes of enough members of each group to make 



148 



296 JOURNAL OF MAM^IALOGY Vol. S4, No. S 

it reasonably certain that the above statement is true. There are other ana- 
tomically homogeneous groups such as the Megachiroptera, Cetacea, and Peris- 
sodactyla where the limited data available points in the same direction. This is 
particularly true of the data on the species of numerous genera of the groups 
already mentioned. 

2. In many groups of mammals made up of subgroups widely divergent or of 
uncertain affinities there are fundamental differences in the fetal membranes. 
This is true of the Insectivora; the Chiroptera, where there is wide divergence 
between the membranes of the two suborders (Microchiroptera and Mega- 
chiroptera); the Primates, where the membranes of Lemuroidea and Tarsoidea 
differ widely from one another and from the Anthropoidea; and the Edentata, 
where the Bradipodidae and Myrmecophagidae are probably much alike, but 
differ markedly from the Dasypodidae. The Pholidota, often included in the 
order Edentata, differ fundamentally from all others of this order. 

3. The membranes of certain groups commonly separated on anatomical 
grounds, but known to be somewhat related, are often so similar that the wide- 
ness of separation does not seem justified. This is true of the Pongidae and 
Hominidae, the Lagomorpha and Rodentia, and of the Perissodactyla and 
Artiodactyla. 

4. There are fundamental similarities between certain aberrant groups and 
other groups to which they have not been supposed to be clearly related. Strik- 
ing examples of this are the strong resemblances between the membranes of the 
Brady podidae and the Anthropoidea; between the Lemuroidea, Pholidota, Ceta- 
cea, and Sirenia and those of the Perissodactyla and Artiodactyla; and between 
the Dasypodidae, Rodentia, Microchiroptera and Soricoidea. 

More data than are at present available are certainly necessary to warrant 
drawing more than very tentative conclusions as to the significance or non- 
significance of these facts, but it is interesting to note that there are many 
points of anatomical resemblance between lemurs and the hoofed animals, and 
between the sloths and anthropoids. Certainly taxonomists should not close 
their minds to the possibility that lemurs are an arboreal line derived from stock 
ancestral to the hoofed animals, and that their relatively slight resemblance to 
anthropoids is due to retention of primitive characters in both lines, and to 
convergence and parallelism effected by adaptation of both to an arboreal 
habitat. Nor should one close his mind to the possibility that the sloths repre- 
sent highly specialized edentulous forms derived from the same ancestral stock 
as the anthropoids. 

Now that the general method of application of the reproductive tract and 
fetal membrane criteria to the taxonomy and phylogeny of mammals has been 
described and illustrated, one must clear up the important point of the evalua- 
tion of the criteria used. The basis for this is the observation described as number 
1 above ; namely, that in every group of mammals in which the members can be 
clearly related to one another on the basis of total anatomical similarity their 
fetal membranes are fundamentally similar, showing far less divergence than 
do other characters. This makes it possible to compare the variability of differ- 



149 



Aug., 19BS MOSSMAN— TAXONOMIC CRITERIA 297 

ent features of the membranes within the group as a whole and within its various 
lesser taxonomic categories, as was done by the author some years ago (Moss- 
man, 1937). Those characters which are consistently constant throughout all 
the subgroups of a major category certainly are the more conservative ones of 
that group. If the same characters are also constant, but not necessarily alike, 
throughout several well established orders, then they are certainly characters 
conservative enough to be used for establishing phylogenetic relationships be- 
tween orders. If they are constant within single families, but vary between differ- 
ent families of an order, then they are only conservative enough to establish 
relationship between families. This general principle can be applied to all cate- 
gories. Obviously one must choose test groups in which the taxonomy is quite 
clear and definite, and must compare parallel, major groups in which the minor 
categories are also reasonably parallel in value. This is obviously arguing in a 
circle, and thus a dangerous practice if not tempered with good judgment and a 
reasonable scientific conservatism on the part of the person using it. However 
it is the best method available, and far superior to making no attempt at evalua- 
tion. 

One further argument in favor of the fetal membranes as criteria for phy- 
logeny must be stated. This point seems even more important than that of their 
conservatism. In fact, coupled with their conservatism, it makes them the most 
ideal of all anatomical criteria for recent forms. This is the fact that the history 
of the development of the fetal membranes of a species is the history of a com- 
plete, complex, and, structurally, highly independent organ system, from its 
inception during cleavage to its complete functional maturity, old age, and death 
at the time of birth of the young. We are therefore dealing with the complete 
life history of an organ system carried out in the relatively constant environment 
of the uterus, thus almost completely isolated from adaptational demands of 
the varying external environment. Other criteria conmionly used do not offer 
this overall picture of the individual. The fetal membranes and their develop- 
ment are comphcated, but far less so than the total history of all the organ sys- 
tems ordinarily used as criteria. Their conservatism, and the total develop- 
mental picture that they give, render them the most ideal of all organ systems 
for phylogenetic and taxonomic studies of recent mammals, 

SUMMARY 

When compared with the organ systems ordinarily employed as criteria for 
taxonomic and phylogenetic studies of manmials, the characters of the male 
and the female reproductive systems and of the fetal membranes are the more 
conservative. This is apparently due to the relatively minor role that adaptation 
to external environment has played in the evolution of these systems. 

Little effort has ever been made to apply male and female genital tract char- 
acters to such studies of mammals, but a limited consideration of them by the 
author indicates that they are less conservative than the fetal membranes. They 
furnish characters that are of use in the study of the interrelationships of genera 
and families, and, in some cases, even of species. Whether or not they would be 



150 



298 JOURNAL OF MAMMALOGY Vol. S4, No. S 

reliable in showing affinities between higher categories, such as orders and sub- 
orders, is unknown. 

On the contrary, the fetal membranes are so conservative that clear-cut inter- 
specific or even intergeneric differences seldom exist. Furthermore interorder 
and interfamily fetal-membrane similarities often demonstrate relationships 
between these major groups. This conservatism, plus the fact that the complete 
life cycle of the fetal membranes takes place during embryonic development 
and is therefore much more easily studied than that of any other organ-system 
ontogeny, makes this system the most ideal of all criteria for the study of phy- 
logenetic interrelationships of recent mammals. 

Acknowledgement. — This study was aided by grants from the Wisconsin Alumni 
Research Foundation. 

LITERATURE CITED 

Howell, A. H. 1938. Revision of the North American ground squirrels with a classifica- 
tion of the North American Sciuridae. U. S. D. A., N. Amer. Fauna, No. 56: 
1-256. 

Kbolling, O. 1921. Die akzessorischen Geschlechtsdriisen und mannlichen Kopula- 
tionsorgane von Sciurus vulgaris. Zeitschr. f. Anat. u. Entwick., 61: 402-438. 

Layne, J. N. 1952. The os genitale of the red squirrel, Tamiasciurus. Jour. Manam., 
33: 457-459. 

Mobsman, H. W. 1937. Comparative morphogenesis of the fetal membranes and ac- 
cessory uterine structures. Contribs. Embry., 158; Publ. 479, Carnegie Inst, 
Washington, 129-246. 

1940. What is the red squirrel? Trans. Wis. Acad. Sci., Arts & Letters, 32: 

123-134. 

Mobsman, H. W., J. W. Lawlah, and J. A. Bradley. 1932. The male reproductive tract 
of the Sciuridae. Amer. Jour. Anat., 51: 89-155. 

MossMAN, H. W., AND L. A. Weisfeldt. 1939. The fetal membranes of a primitive ro- 
dent, the thirteen-striped ground squirrel. Amer. Jour. Anat., 64: 59-109. 

Oudemans, J. T. 1892. Die accessorischen Geschlechtsdriisen der Saugetiere. Natuurkun- 
dije Verhandelingen van de Hollandsche Maatschappij der Wetenschappen. 
3de Verz., Deel 5, 2de Stuk., 1887-1892. 

PococK, R. I. 1923. The classification of the Sciuridae. Proc. Zool. Soc. Lond., 1: 209- 
246. 

Rau, a. S. 1925. Contributions to our knowledge of the structure of the placenta of 
Mustelidae, Ursidae, and Sciuridae. Proc. Zool. Soc. London, 1925: 1027-1070. 

Simpson, G. G. 1945. The principles of classification and a classification of mammals. 
Bui. Amer. Mus. Nat. Hist., 85: 350 p. 

Tullberg, T. 1899. Ueber das System der Nagetiere. Nova Acta Reg. Soc. Upsala, ser. 
3, 18: 1-514. 

Department of Anatomy, University of Wisconsin, Madison. Received December 26, 1952. 



151 



MORPHOLOGY AND PHYLOGENY OF HAIR 

By Charles R. Noback* 

Department of Anatomy, College of Physicians and Surgeons, Columbia University, 

New York 

Hair is a structure found exclusively in mammals. With this in mind, 
Oken named the Mammalia, Trichozoa (hair animals), and Bonnet (1892) 
named them Pilifera (hair bearers). 

Of the many aspects of morphology and phylogeny of hair, only four will 
be discussed. These include (1) the principle of the arrangement of hairs in 
group patterns, (2) the types of hair and their relation to the principle of 
the group pattern, (3) a brief analysis of the structural elements of hair and 
their relation to the types of hair, and (4) the phylogeny of hair, with some 
remarks on (a) the relation of hair to the epidermal derivatives of other 
vertebrate classes and (b) aspects of the phylogeny of the hair and wool of 
sheep to illustrate that marked dififerences in hair coats exist between closely 
related animals. 

Hair is the subject of a voluminous literature. Toldt (1910, 1912, 1914, 
and 1935), Danforth (1925a), Pinkus (1927), Pax and Arndt (1929-1938), 
Trotter (1932), Lochte (1938), Smith and Glaister (1939), and Stoves 
(1943a) discuss the problem of mammalian hair in general. Wildman 
(1940), von Bergen and Krause (1942), and the American Society for 
Testing Materials (1948) discuss the problem of fiber identification as 
applied to textiles. 

Principle of the Group Pattern of Hairs 

In the only extensive survey of the grouping of hair in mammals, DeMei- 
jere (1894) documented the concept of the group pattern of hair (figures 
1-6). Unfortunately, the few studies on this phase of the problem since 
that time have not fully exploited the implications of this concept. DeMei- 
jere concluded that hairs are mainly arranged in groups with the pattern of 3 
hairs — with the largest hair in the middle — as the basic pattern. The 
concept of the basic trio as the primitive condition is accepted as an ade- 
quate working hypothesis by Wildman (1932), Galpin (1935), Hofer (1914), 
Gibbs (1938), Hardy (1946), and others. DeMeijere described 8 patterns: 
(1) 3 or less hairs behind each scale of the tail (as in the opossum, Didelphis 
marsupialis), (2) more than 3 hairs behind each scale of the tail (as in the 
rodent, Loncheres [Echimys] cristata), (3) 3 hairs (as in the back of the 
marmoset, Midas rosalia), (4) more than 3 hairs arranged in a regular 
pattern with some of greater diameter than others (as in the back hairs of 
Loncheres [Echimys] cristata in figure 3), (5) several hairs composed of a 
number of fine hairs and one coarse hair (as in the back of the dog, Canis 
familiaris, in figure 5D), (6) several hairs composed of a number of fine 
hairs and one isolated coarse hair (as in the back hairs of the mouse, Mus 
decumanus, in figure 6D), (7) scatterings of fine hairs with no apparent 

* The author wishes to thank Dr. Margaret Hardy, Division of Animal Health and Production, Sydney, 
Australia, for her valuable suggestions. 

476 



152 



Noback: Morpholog}^ and Phylogeny 477 

arrangement and a few intermingled coarse hairs (as in the back hairs 
of the cat, Felis domesticus in figure 4D), and (8) hairs in irregularly 
scattered groups (as in the back hair of the raccoon, Procyon cancrivorus) . 

Dawson (1930) does not completely agree with DeMeijere's pattern in 
the guinea pig. She found variations in the pattern and no correlation be- 
tween the size of hair and the arrangement of the hairs in each group. 
Histological study frequently shows follicle grouping which was not appar- 
ent to DeMeijere when he was examining only the skin surface, e.g., in 
Felis domesticus (see Hofer, 1914). This indicates that analyses of the 
group pattern of hairs are needed in both common laboratory mammals and 
mammals in general. 

In addition, DeMeijere analyzed the formation of the patterns by ex- 
amining the skins of animals during their development (figures 4-6). 
This phase of the problem has been extended to include a study of the ontog- 
eny of the arrangement of hair follicles in sheep (Wildman, 1932, Galpin, 
1935, and Duerden, 1939), in the cat (Hofer, 1914), in marsupials (Gibbs, 
1938, Stoves, 1944b, and Hardy, 1946), in the mouse (Calef, 1900, Dry, 
1926, and Gibbs, 1941) in the rat (Frazer, 1928), and in a number of mam- 
mals (Duerden, 1939). The terminology used by these authors in this 
problem is summarized in table 1 (adapted from Wildman and Carter, 
1939 and Carter, 1943). 

UtiHzing the terminology of Wildman and Carter, 1939, the following is a 
brief statement of the relation of the fiber generations. The first follicles 
to differentiate are the central trio follicles (figure 7). If these follicles 
appear at two different times as in the opossum (Gibbs, 1938), then the 
follicles are called "primary X" and "primary Y." The essential point is 
that each of these primary follicles will be the central follicle of different hair 
groups. Later in development, other follicles of the hair group differentiate 
in relation to these central trio follicles. The trio is formed when two 
follicles are differentiated lateral to the primary follicles (figure 8). The 
lateral follicles associated with primary X and primary Y are called re- 
spectively "primary x" and "primary y." If only one lateral follicle is 
formed adjacent to a primary follicle (X or Y), then a couplet follicle 
is formed. If no lateral follicles differentiate, a primary follicle (X or Y) is 
called a "solitary follicle." Later, another generation of follicles is differ- 
entiated — the secondary follicles. In the opossum (figure 9), these 
secondary follicles are located between the central trio follicle and the lateral 
trio follicles. The ontogenetic studies of follicle arrangement have added 
confirmatory evidence to DeMeijere's basic concept that in mammals there 
is a universal and regular grouping of hair follicles (Hardy, 1946). 

In general, the early differentiating follicles (central trio follicles) form 
the coarse overhair, while the late differentiating follicles (lateral trio 
follicles and secondary follicles) form the fine underhair. Lateral trio 
follicles sometimes at least produce overhair like that of the central fol- 
licles {e.g. in sheep) or intermediate types such as awns, which are classified 
by Danforth (1925a) as overhair. In Ornithorhynchus analinus (Spencer 
and Sweet, 1899) and many marsupials (Gibbs, 1938, Bolliger and Hardy, 



153 



478 



Annals New York Academy of Sciences 



1945, Hardy, 1946), however, the lateral trio fibers are indistinguishable 
from those of secondary follicles, so it is difficult to place them in either the 
"overhair" or the "underhair" category. 




Figures 1-9 {see facing page). 



Spencer and Sweet (1899) claimed that, in monotremes, each group of 
follicles was differentiated by budding from the central follicle. This has 
not been described in marsupials or in eutherians, in which the follicles 
arise independently as epidermal downgrowths. Monotremes and mar- 



154 



Noback: Morphology and Phylogeny 479 

supials have in common the fact that a follicle group typically contains a 
large central follicle with a sudoriferous gland, and two or more clusters of 
smaller lateral follicles (Spencer and Sweet, 1899, Gibbs, 1938, Hardy, 1946). 
This arrangement is also found in some eutherians, such as the cat (Hofer, 
1914) and dog (Claushen, 1933). In the cat and a few other eutherians, the 
first-formed lateral follicles (primary x and y of the classification of Wild- 
man and Carter, 1939) produce hairs intermediate in type between those of 
the central and the other lateral follicles. There are other eutherians in 
which the lateral primary x and y fibers are still more like the central pri- 
mary X and Y fibers, as in the pig (Hofliger, 1931) and the sheep (Carter, 
1943). Except in the rodents, there is always a sudoriferous gland opening 
into the central primary X or Y follicle (Hardy, unpublished data). Many 
animals, such as the pig and sheep, also have a sudoriferous gland opening 
into each primary x and y follicle, but others do not (Duerden, 1939). 
Some of the eutherians have only primary follicles in their skin, each with 
a sudoriferous gland. Findlay and Yang (1948) showed that this is the 
arrangement in cattle, and the same is probably true in horses and in 
human head hair (Hardy, unpublished observations). 

Types of Hair 

DeMeijere's analysis leads to the classification of hair types by Toldt 
(1910 and 1935) and by Danforth (1925a). Many details of the hair types 
in many species of animals and the variations of the structure of these types 
are described, illustrated, and bibliographically annotated by Toldt (1935) 
and Lochte (1938). 

Types of Mammalian Hair 
(after Danforth, 1925a) 
1. Hairs with specialized folhcles containing erectile tissue. Large, stiff hairs that are 
preeminently sensory. They have been variously designated as feelers, whiskers, 



FiGDRES 1-9 (see opposite page) . 

Figure 1. The trio hair group pattern on the back and tail of the marmoset, Midas rosalia (after DeMei- 
jere, 1896). .Ml hairs have similar diameters. 

Figure 2. The hair group pattern of more than 3 hairs with some fibers of greater diameter than other 
fibers on the back of the paca, Coelogenys paca (after DeMeijere, 1896). 

Figure 3. The hair group pattern of more than 3 hairs with some fibers of greater diameter than other 
fibers on the back of the rodent, Loncheres (Echimys) cristata (after DeMeijere, 1896). 

Figure 4. Ontogeny of a hair group on the back of the cat, Felis domesticus. A, from a newborn animal; 
B and C, from an older animal; and D, from an adult animal (after DeMeijere, 1896). 

Figure 5. Ontogeny of a hair group on the back of the dog, Canis Jamiliaris. A, from an embryo dog; B, 
from a newborn animal; C, from a young dog; and D, from an adult animal (after DeMeijere, 1896). 

Figure 6. Ontogeny of a hair group on the back of the mouse, Mus decumanus. A, from a 7 cm. long ani- 
mal; B, from a 9 cm. long animal; C, from a 12.5 cm. long animal; and D, from an adult animal. 

(Figures 4, 5, and 6 illustrate that the follicle of the first hair to erupt (A) will be the follicle of the coars- 
est hair of the hair group in the adult. The type of hair group pattern in the adult (D) in each figure is noted 
in the text. The X in the diagrams marks the location of erupting follicles.) 

Figure 7. The primary follicles X (the more differentiated follicles) and the primary follicles Y (the less 
differentiated follicles) in the transverse section of skin of a 12.5 cm. Australian opossum embryo [Tricliosurus 
vulpecula). Follicles are scattered irregularly. (After Gibbs, 1938.) 

Figure 8. Two new follicles (primary x or primary y) have become grouped with each previously differen- 
tiated follicle (primary X or primary Y) to form the typical trio arrangement. The trio would be either 
primary x, primary X, primary x or primary y, primary Y, primary y. Transverse section of skin of a 15.0 
cm. Australian opossum embryo (Trichosurus vulpecula). (After Gibbs, 1938.) 

Figure 9. Two secondary follicles have added to each ffio group to form a 5 follicle group. The secondary 
follicles differentiate between the primary X (or Y) follicle and the primary x (or y) follicles. The five group 
would be either primary x, secondary follicle, primary X, secondary follicle, primary x or primary y, second- 
ary follicle, primary Y, secondary follicle, primary y. Transverse section of skin from 20.0 cm. Australian 
opossum emciryo (Trichosurus vulpecula). Note presence of a dermal capsule surrounding each 5 follicle 
group. (After Gibbs, 1938.) 

(In figures 7, 8, and 9, the terminology of Wildman and Carter (1939), noted in the text, is used.) 



155 



480 



Annals New York Academy of Sciences 



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156 



Noback: Morphology and Phylogeny 481 

sensory hairs, sinus hairs, tactile hairs, vibrissae, etc. They occur in all mammals 
except man, and are grouped by Botezat (1914) (Pocock, 1914) essentially as follows: 

(1). Active tactile hairs — under voluntary control. 

(2) Passive tactile hairs — not under voluntary control. 

(a) Follicles characterized by a circular sinus. 

(b) Follicles without a circular sinus. 

2. Hairs with follicles not containing erectile tissue. The remaining types of hair, most 
of which are more or less defensive or protective in function. In many cases, the 
follicles have a good nerve supply, endowing the hair with a passive sensory function 
as well. These hairs are grouped here according to their size and rigidity. 
(1). Coarser, more or less stiffened "overhair," guard hair, top hair. 

(a) Spines. Greatly enlarged and often modified defensive hairs, quills. 

(b) Bristles. Firm, usually subulate, deeply pigmented, and generally 
scattered hairs. "Transitional hairs" (Botezat, 1914), "Leithaare" 
(Toldt, 1910), "protective hair," "primary hair," "overhair." This 
group also includes mane hairs. 

(c) Awns. Hairs with a firm, generally mucronate lip but weaker and 
softer near the base. "Grannenhaare" (Toldt, 1910), "overhair," "pro- 
tective hair." 

(2). Fine, uniformly soft "underhair," "ground hair," "underwool." 

(a) Wool. Long, soft, usually curly hair. 

(b) Fur. Thick, fine, relatively short hair — "underhair," "wool hair." 

(c) Vellus. Finest and shortest hair — "down," "wool," "fuzz," "lanugo." 
(Danforth, 1939). 

The following comments supplement the above classification. The guard 
hairs are listed in a series from greater to lesser rigidity (in order: spines, 
bristles, and awns). There are many intergrade hairs between the typical 
bristle and the typical awn and between the typical awn and the typical 
fur hair (figures 10, 11, and 12). 

The tactile hairs have a rich nerv^e supply, while the roots of some are 
encircled by large circular sinuses containing erectile tissue. When the 
pressure in the circular sinus is increased the hair becomes a more efficient 
pressure receptor. The overhairs have a definite nerve supply, while the 
underhairs have no direct nerve supply. As a general but not absolute 
rule, the coarser hairs appear ontogenetically earlier than the finer hairs 
(Gibbs, 1938, Danforth, 1925a, Duerden, 1937 (reported by Wildman, 
1937), Hofer, 1914, and Spencer and Sweet, 1899). 

The contour, diameter, and shape of a hair fiber changes from its root to 
its tip (Note awns, figures 16-18). The cross-sectional outline of hairs 
may vary from the thick rounded porcupine quill to the eccentric flattened 
hairs of seals. The former serves a protective function, while the latter is 
adapted to hug to the skin so as not to hinder aquatic locomotion. Many 
details of the anatomy of hair form are noted by Stoves (1942 and 1944a), 
Toldt (1935), and Lochte (1938). 

It is possible for a hair follicle to differentiate one type of hair at one stage 
and another type at another stage. The follicle of a bristle (kemp) of the 
Merino lamb may become the follicle of wool in the adult sheep (Duerden, 
1937, reported by Wildman, 1937). A fine lanugo hair of the human 
fetus is associated with a follicle which will later be the follicle of a coarser 
hair. 

The theories of hair curling are reviewed by Herre and Wigger (1939). 
The curling of hair in primitive sheep is independent of the arrangement of 
hair, existence of hair whorls, or the cross section of the hair (Pfeifer, 1929). 



157 



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Annals New York Academy of Sciences 



Wildman (1932) suggests that the shape of the foUicle, especially the curve 
in its basal portion, is a possible factor in hair curling. Reversal of the 
spiral in some wool fibers may be explained according to Wildman as due to 
a shift in the growing point of the follicle and inner root sheath. Spiral 
reversal occurs in human hair (Danforth, 1926). Pfeifer (1929) doubts 
that curHng is determined by a curve of the follicle alone and suggests that 
Tiinzer's (1926) contention that the follicle must be saber-shaped is im- 





12 





14 



s. 



"D. 



c.T=is.ne 



Figures 10-15. 







Figure 10. The hair of the fox, Canis vulpes (after Toldt, 1935), illustrating intergrade hairs. From the 
left to the right, Toldt named the fibers Leithaar (bristles), Leit-Grannenhaar, thick Grannenhaar (awns), 
thin Grannenhaar, Grannen-WoUhaar, and WoUhaar (fur). 

Figure 11. The hair of the chinchilla. Chinchilla laniger (after Toldt, 1935) illustrating an animal hair 
coat with hairs of appro.ximately the same length. The 2 hairs on the left are awns, and the rest, either 
intergrade hairs or fur hairs. 

Figure 12. The hair of the wild pig, Sus scrofa (after Toldt, 1935) illustrating bristles on the left and 
underhair on the right with some intergrade hairs between them. Note the brushlike distal ends of the 
bristles. 

P'igure 13. The scale index (S. I.), according to Hausman (1930), is equal to the ratio of the free proximo- 
distal length of a scale (F) to the diameter of the hair shaft (E)). 

Figure 14. The thickness of the cuticle (C. T.), according to Rudall (1941), is equal to the length of a 
cuticular scale (1) times the sine of angle (sin 9) the scale makes with the cortex (X). 

Figure 15. Cross sections of several regions of a fur hair (left) and an awn (right) of the rabbit (after 
Toldt, 1935). The sections, at the top of the figure, are from the base of the hair and, at the bottom of the 
figure, from the tip of the hair. Illustrates general uniformity of the diameters of the fur haii and differences 
in diameters and contour of awn hairs throughout their lengths. 

portant. Waving of all compact wools is due at least in part to the flat- 
tening of the primary spiral and to the unequal lateral growth of the fiber 
(Duerden, 1927). The curling of hair in karakul sheep fetuses may be 
associated with the differences in the rates of growth in the various skin 
layers (Herre and Wigger, 1939). 

The factors responsible for curling and crimping of hair are as yet not 
completely known. 



158 



Noback : Morphology and Phylogeny 483 

Structural Components of Hair 

The cuticle, cortex, and medulla are the three structural components in 
hair. They will be discussed in order. 

Cuticle. The cuticle consists of thin, unpigmented, transparent over- 
lapping scales, whose free margins are oriented toward the tip of the hair 







20 




Figures 16-21. 

KiGi'FE 16. Diagram of the fiber components of coat of a generalized non-wooled animal fafter Duerden, 
1929). Note presence of bristles (coarse fibers), awns (fibers with fine basal segments and coarse distal 
segments) and fur fibers (fine fibers). 

Figure 17. Diagram of the fibers of the wild sheep (after Duerden, 1929). Note the presence of bristles 
(kemp), awns (heterotypes), and wool. 

Figure 18. Diagram of the fibers of British mountain breeds (after Duerden, 1929\ The fibers are 
mainly awns and wool. Few bristles are present. 

Figure 19. Diagram of the fibers of the British luster breeds (after Duerden, 1929). F'ibers on the left 
are wool fibers which are coarser than the wool fibers of wild sheep. The fibers on the right are modified 
awns with fine pro.ximal segments and slightly coarse distal segments. All fibers are elongated and spiraled. 

Figure 20. Diagram of fibers of adult Merino sheep (after Duerden, 1929). All fibers are wool. Note 
uniformity of all fibers as to size, length, and waviness. These wool fibers are coarser than wool fibers from 
wild sheep. Unlike the fibers of other breeds, the fibers of the adult Merino sheep grow from persistent germs 
and do not shed. 

Figure 21. Diagram of the fibers of the Merino lamb. Note the presence of bristles (kemp), awns (hetero- 
types), and wool. During later development, the bristles are shed and the distal coarse segments of the 
awns are lost. The adult coat is formed by the persistent growth of the wool fibers of the lamb, by the re- 
placement of wool in the follicles of the shed kemp, and by the persistence of the growth of the proximal seg- 
ments of the awns. 

(figure 22). Within the follicle, the free margins of the hair cuticular 
scales interlock with the inner root sheath cuticular scales, which are oriented 
in the opposite direction toward the papilla. This interlocking of scales 
helps to secure the hair in place (Danforth, 1925a). The cuticle functions 
as a capsule containing the longitudinally splitable corte.x (Rudall, 1941). 
This explains why the cortex of a hair frays at its severed end. In addition, 
the cuticle, with its oily layer, prevents the transfer of water (Rudallj 1041). 



159 



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Annals New York Academy of Sciences 



The cuticular scales vary in thickness from 0.5 to 3 micra (Frolich, Spotel, 
and Tanzer, 1929). Since the scales overlap, the number of overlapping 
scales at any point on the hair surface determines the thickness of the 
cuticle. The cuticular thickness may be expressed as being equal to the 
length of the scales times the sine of the angle the scale makes with the 
cortical surface (figure 14, Rudall, 1941). 

The cuticular scales may be classified into two types: coronal scales and 
imbricate scales (Hausman, 1930). A coronal scale completely encircles 
the hair shaft. They are subdivided according to the contour of the free 
margins as: simple, serrate, or dentate (figure 23). Mliller (1939) con- 
tends that a coronal scale is in reality several scales whose lateral edges are 



HAIR SHAFT IN MICR0N5 




;oronal I 



ICORONAl I ACUMINATE 

EL0N6ATE OVATE 



CRENATE 1 

FLATTENED 



Figure 22. Graph illustrating the relation of the diameter of the hair to the tjmes of cuticular scales. 
The finest hairs (with small diameters) have a high-scale index and coronal scales. The coarsest hairs (with 
large diameters) have a low-scale index and flattened scales. Diameters of hair shafts are plotted on the 
ordinate. General regions of the occurrence of scale forms are shown along the abscissa, the average scale 
indices along the curve. The figures of the scale types beneath the graph are not drawn to scale. (After 
Hausman, 1930.) 

fused. For example, a dentate coronal scale with 5 processes in its free 
border is the fused product of 5 elongated pointed scales. 

An imbricate scale does not completely surround the hair shaft. They 
are classified as ovate, acuminate, elongate, crenate, and flattened (figure 
22, Hausman, 1930). 

Hausman (1930) devised a scale index to express the relation between the 
diameter of the hair shaft and the free proximo-distal dimension of the 
scales (figure 13). The free proximo-distal dimension is actually a means 
of expressing the type of scale. For example, coronal scales have a large 
proximo-distal dimension, while crenate scales have a small dimension 
(figure 22). An analysis of the scale indices indicates that a relation exists 
between the types of scales and the shaft diameters. In general, the finest 



160 



Noback: Morphology and Phylogeny 



485 



hairs have large scale indices and coronal scales, while the coarsest hairs 
have small scale indices and crenate or flattened scales. On the basis of 
the above, it is concluded that the types of cuticular scales present on hair 
are related not to the taxonomic status of the animal possessing the hair 
but rather to the diameter of the hair shaft (Hausman, 1930). In hairs 
with both thick and thin segments, the thick segments have the scale types 
of large diameter hairs while the thin segments have the scale types of small 
diameter hairs. 

A coarse guard hair has scales with free lips that are closely applied to the 
cortex and are scarcely raised. As a result, these hairs have a high luster 
(due to unbroken reflection of light from the hair surface) and do not inter- 
lock with other hairs. A fine underhair has scales with lips that have raised 
margins. As a result, these hairs are dull (due to broken reflection of light) 
and interlock with other fine hairs. Thus, mohair has a high luster but 
makes poor felt, while wool is dull but makes good textiles. 





C. 




Figure 23. Figures illustrating the types of coronal cuticular scales. A. simple scales, B. serrate scales, 
C. dentate scales, (after Hausman, 1930). Note raised nurgins on the free lips of scales. 

Many details of the cuticle, in many species of animals are presented and 
illustrated by Lochte (1938). 

Cortex. The cortex usually forms the main bulk of a hair. It is a column 
of fusiform keratinized cells which are coalesced into a rigid, almost homoge- 
neous, hyaline mass (Hausman, 1932). Damaged hairs tend to split length- 
wise because the elongated cortical cells are oriented longitudinally. The 
cortex has such a low refractive index — due to the degree of cornification^ 
that, in the absence of pigment, it is translucent. Since cortical scales have 
not been analyzed in such detail as cuticular scales, no statement can be 
made of a relation between cortical scale morphology and hair size. The 
form and distribution of the pigment in the cortex and the medulla is noted 
by Lochte (1938), Toldt (1935), and Hausman (1930). 

Hausman (1932 and 1944) analyzed the cortical air spaces known as 
cortical fusi — cortical in location and fusiform in shape — air vacuoles, air 
chambers, air vesicles, or vacuoles. As the irregular-shaped cortical cells 
located in the bulb rise to the follicular mouth, they carry between them 
cavities filled with tissue fluid. As the hair shaft dries out, the cavities lose 



161 



486 Annals New York Academy of Sciences 

the fluid, and air may fill the resulting spaces — the fusi. The shape of the 
fusi vary. They are largest, most numerous, and most prominent near 
the base of the hair, and they are fihform and thin or lost in the distal seg- 
ments of the hair. Seldom do they persist to the tip of a hair. As a rule, 
they are visible only under a microscope. Hausman implies that there is 
a relation between fusi and hair size. Presumably, the coarser a hair seg- 
ment is, the more numerous the fusi. 

Ringed hair results when the fusi appear in masses at regular intervals in 
the shaft. Fractured fusi result when hairs are damaged sufficiently to 
separate the cortical cells enough to allow air to collect between them. 
Fusi can be distinguished from pigment granules, for they are fusiform, 
whereas pigment granules have blunt ends. 

The presence of a thin membrane located between the cuticle and the 
cortex has been assumed by Lehmann (1944). Observations of pigment 
granules, cell nuclei, and submicroscopic fibrils are presented by Mercer 
(1942), Hausman (1930), and others. 

Medulla. The medulla (pith), when present, is composed of shrunken and 
variably shaped cornified remnants of epithelial cells connected by a fila- 
mentous network. In contrast to the cortex, the medulla is less dense and 
has fewer and larger cells, which are more loosely held together. In the 
medulla are air cells or chambers, which are filled by a gas, probably air. 
These air cells may be intracellular (deer) or intercellular (dog, weasel, 
and rat) (Lochte, 1938). The intercellular air cells are classifiable accord- 
ing to their coarseness and arrangement (Lochte, 1934 and 1938). 

Medullas are classified by Hausman (1930) as follows: absence of medulla, 
discontinuous medulla (air cells separate), intermediate medulla (several 
separate air cells of the discontinuous type arranged into regular groups), 
continuous medulla (air cells arranged to form a column), and fragmental 
medulla (air cells arranged into irregular groups). These types are illus- 
trated in FIGURE 24 and are arranged in the order of the sizes of hairs in 
which they are located. In the finest hairs (underfur), the medulla is either 
absent or of the discontinuous type. In the coarsest hairs, the medulla is 
either of the continuous or the fragmental type (figure 24). If a hair 
varies in thickness, its medulla will vary. For example, in the awns of 
sheep, the distal thickened segment has a medulla, while the fine proximal 
segment may have no medulla. The arrangement of the medullary air 
cells is related not to the taxonomic group of the animal possessing the hair 
nor the age of the hair, but rather to the diameter of the hair shaft (figure 
24) (Hausman, 1930; Wynkoop, 1929; and Smith, 1933). The sheens 
and colors of hairs are largely determined by the light reflected from the 
medulla (Hausman, 1944). 

Although the cortex forms the bulk of the shaft in most hairs, the medulla 
assumes large proportions in some hairs. In rabbit hair (figure 15), the 
medulla is composed of large air cells separated by little more than a frame- 
work of cortex (Stoves, 1944c). 

The significance of the cuticle, cortex, and medulla in the commercial 
aspects of fur is presented by Bachrach (1946). Although many of the 



162 



Noback : Morphology and Phylogeny 



487 



details of the structural elements of hair cannot be detinitely utilized to 
identify an animal species (Hausman, 1944), it is possible that some morpho- 
logical features of hair can be used (Williams, 1938). 

Some chemical and physical aspects of the morphological elements of 
hair have been analyzed. Not only do the cuticle, cortex, and medulla 
exhibit different chemical and physical properties, but various segments of 
these structural elements may have different chemical and physical proper- 




FiGURE 24. Graph illustrating the relation of the diameter of the hair to the types of medullas. The 
finest hairs have no medulla, and the coarsest hairs have a fragmental medulla. Diameters in micra of the 
hair shafts are plotted on the ordinate. The figures of the types of medullas beneath the graph are not drawn 
to scale. (After Hausman, 1930.) 

ties (Rudall, 1944; Stoves, 19436, 1945; Lustig, Kondritzer, and Moore, 
1945; Leblond, 1951; and Giroud and Leblond, 1951). 

Some Phylogenelic Aspects of Hair 

The relation of hair to the epidermal structures in non-mammalian ani- 
mals has been discussed by many authors and has been summarized by 



163 



488 Annals New York Academy of Sciences 

Botezat (1913 and 1914), Danforth (1925b), and Matkeiev (1932). No 
direct relation between hair and non-mammalian epidermal elements has 
been established. Hair is most probably an analog to these structures. 
Danforth (1925b) and others conclude that hair is probably a de novo morpho- 
logical entity in mammals. 

Broili (1927) reports that he identified hair and hair follicles in a fossil 
aquatic reptile, Rhamphorynchus. This animal is a specialized reptile, 
removed from those reptiles in the evolutionary line to mammals. If 
established, this observation would alter the concept that only mammals 
produce hair. 

The phylogeny of hair in related groups of animals has not been analyzed 
extensively. Because of the economic importance of wool, several studies 
of the hair types in the coat of a number of breeds of sheep have been made. 
One significant aspect of these studies is that they illustrate how the hair 
coat may vary in closely related forms. 

This statement is adapted primarily from Duerden (1927 and 1929). 
The generalized wild animal hair coat consists of an overcoat of bristles and 
awns and an undercoat of fur (figure 16). In the wild sheep and the 
black-headed Persian sheep, the hair coat is similar to that of the wild 
animal. These sheep have an overcoat of bristles (called kemp) and awns 
(called heterotypes) and an undercoat of wool (figure 17). The British 
mountain breeds have a hair coat consisting of awns and wool (figure 
18). In these breeds, kemp formation is negligible. The coat of the 
British luster breeds have evolved in another direction. The awns retain 
their fine proximal segments. Their distal segments are still thicker than 
the proximal segments, but are thinner than the distal segments of the awns 
of primitive sheep. The wool undercoat fibers have thickened. Both fiber 
types are elongated and spiraled (figure 19). The adult Merino sheep, 
the most efficient wool-producing sheep, has a coat consisting of elongated, 
regularly crimped fibers of uniform diameters and lengths (figure 20). 
An analysis of the coat of the Merino lamb is essential for the identification 
of the types of fibers that form the coat of the adult sheep. The Merino 
lamb coat has bristle, awn, and wool fibers (figure 21). During ontogeny, 
the bristles are shed and then replaced by wool fibers. The awn fibers 
lose their distal thickened segments, but the thin proximal segments persist. 
The wool fibers are retained, but are coarser than the wool of primitive 
sheep. Hence, the adult Merino sheep coat consists of wool fibers differ- 
entiating from follicles which produced kemp in the lamb, of awns deprived 
of their distal segments, and of wool fibers differentiating from follicles 
which produced wool in the lamb. A major difference between the Merino 
sheep and other sheep is in the nature of the hair follicles. Whereas the 
coat of other breeds is shed periodically and then new hairs differentiate 
from the follicles, the fibers of the adult Merino sheep grow from persistent 
germs and are not shed. 

In the evolution of the sheep coat from primitive wild sheep to the various 
domestic breeds, several changes have occurred. As summarized by Duer- 
den (1927), the domestic wooled sheep has evolved in the direction of the 



164 



Noback : Morphology- and Phylogeny 489 

loss of the protective coat both of bristles (kemp) and awns (heterotypes), 
the increase in length, density, and uniformity of the fibers, and the tend- 
ency of the retained bristles to become finer but still capable of being shed. 
In addition, the Merino sheep has developed persistently growing hair 
follicles. 

Important implications of the evolution of the sheep coat are that the 
types of hair in the hair coat may differ (1) in closely related animals and 
(2) at various stages of ontogeny with the same animal. Hence, data 
derived from a study of the coat of one animal species may not always apply 
to another animal species. 

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Stoves, J. L. 1944a. The appearance in the cross sections of the hairs of some car- 
nivores and rodents. Proc. Roy. Soc. Edinburgh 62B: 99-104. 



166 



Noback: ]\Iorphology and Phylogeny 491 

Stoves, J. L. 19446. A note on the hair of the South American opossum {Didelpliix 

caranopliaga). Proc. Leeds Phiios. Soc. 4: 182-183. 
Stoves, J. L. 1945. Hislochemical studies of keratin fibres. Proc. Roy. Soc. Kdin- 

burgh. 62: 132-136. 
Taxzer, E. 1926. Haul und Haar l)eim Karakul im rassenanahtischem V'ergleich. 

Halle a.d.S. (cited i)y: Pfeifer, 1929). 
TOLDT, K., Jr. 1910. Uber eine beachtenswerte Haarsorte und iiber das Haarformen- 

svstem der Saugetiere. Annalen d. K. K. Naturhistorischen Hofmuseums in \\ ien. 

24: 195-265. 
ToLDT, K., Jr. 1912. Betrage zur Kenntnis der Behaarung der Saugetiere. Zool. 

Jahrb. Abt. Syst. 33: 9-86. 
ToLDT, K., Jr. 1935. Aufbau untl naturliche Fiiriiung des Haarkleides der VVildsiiuge- 

tiere. 291 pp. Deutsche Gesellschaft fur Kleintier- und Pelztierzucht. Leipsig. 
Trotter, M. 1932. The hair. Special Cytology (Cowdry, E. ed.) 1: 39-65. P. 

Hoeber. New York. 
VonBergen, W. & W. Krauss. 1942. Textile fiber atlas. Amer. Wool Handbook 

Co. Xew York. 
WiLDMAX, A. B. 1932. Coat and fibre development of some british sheep. Proc. Zool. 

Soc. London 1: 257-285. 
WiLDMAX, A. B. 1937. Non-specificitv of the trio follicles in the Merino. Nature, 

Lond. 140: 891-2. 
VViLDM.AX, A. B. 1940. Animal fibres of industrial importance: their origin and identi- 
fication. 28 pp. Wool Industries Research Assoc. Torridon, Headingley, Leeds. 
WiLDMAN, A. B. & H. Carter. 1939. Fibre-follicle terminology in the mammalia. 

Nature 144: 783-784. 
W'lLLiAMS, C. 1938. Aids to the identification of mole and shrew hairs with general 

comments on hair structure and hair determination. J. Wildlife Management 2: 

239-250. 
Wynkoop, E. M. 1929. A study of the age correlations of the cuticular scales, meduUae 

and shaft diameters of human head-hair. Am. J. Phys. .\nthrop. 13: 177-188. 

Discussion of the Paper 

Doctor M. H. H.jirdy {McM aster Laboratory, Glebe, X. S. W., Austra- 
lia): I am glad Dr. Noback mentioned sheep, because the study of the ar- 
rangement of folUcles in groups on these animals has disclosed some im- 
portant principles. Terentjeva,^ Duerden,' and Carter^ showed that de 
Meijere's trio group is the basic unit in the follicle population of sheep. 
The trio (primary) follicles develop first and have accessory structures 
(sudoriferous gland, arrector pili muscle) which are absent from the later 
developing (secondary) follicles of the group.'' In the young lamb, it is the 
primary follicles which produce the coarse, and frequently meduUated, 
kemp fibers and the secondary follicles which produce the fine and usually 
non-meduUated wool fibers. These correspond respectively to the 'over- 
hair' and 'underhair' in Danforth's classification. The primary follicles 
may produce kemp in the lamb and wool in the adult sheep, as Dr. Xoback 
has mentioned. 

The size of the follicle groups, i.e., the number of secondary follicles to 
each trio of primary follicles, varies greatly between breeds* and individuals^ 
and also between body regions.® The breeds and, to some extent, indi- 
viduals with the largest group size have also the greatest number of fibers 
to the square inch and the greatest uniformity of fiber thickness and length.^ 
In the midside region, at least, the potential group size (including second- 
ary follicle rudiments in the young lamb) is strongly inherited, but the 
actual group size (number of active follicles) in the mature animal varies 



167 



492 Annals New York Academy of Sciences 

according to the food intake in the first year of lifeJ Thus, it is possible 
to alter the group size experimentally. Varying the food intake in the 
second and third year of life had no marked effect on group size.^'^ 

It seems that many properties of the coat of the sheep depend on the 
inherited follicle group pattern and the modifications of this superimposed 
by the environment. Perhaps the same principles apply to other mammals. 

1. Terentjeva, a. a. 1939. Pre-natal development of the coat of some fine-wooled 

breeds of sheep. C. R. Acad. Sci. U.R.S.S. (N.S.) 25: 557. 

2. DuERDEN, J. E. 1939. The arrangement of fibre follicles in some mammals, with 

special reference to the Ovidae. Trans. Roy. Soc. Edin. 59: 763. 

3. Carter, H. B. 1943. Studies in the biology of the skin and fleece of sheep. 1. 

The development and general histologv of the follicle group in the skin of the Merino. 
Coun. Sci. Ind. Res. (Aust.) Bull. 164: 7. 

4. Carter, H. B. & P. Davidson. Unpublished data. 

5. Carter, H. B. 1942. "Density" and some related characters of the fleece in the 

Australian Merino. J. Coun. Sci. Ind. Res. (Aust.) 15: 217. 

6. Carter, H. B. & M. H. Hardy. 1947. Studies in the biology of the skin and fleece 

of sheep. 4. The hair follicle group and its topographical variations in the skin 
of the Merino foetus. Coun. Sci. Ind. Res. (Aust.) Bull. 215: 5. 

7. Carter, H. B., H. R. Marston, & A. W. Peirce. Unpublished data. 

8. Ferguson,K. A., H.B. Carter & M.H.Hardy. 1949. Studies of comparative fleece 

growth in sheep. Aust. J. Sci. Res. B 2: 42. 

9. Ferguson, K. A., H. B. Carter, M. H. Hardy, & H. N. Turner. Unpublished 

data. 



168 



MORPHOLOGY AND FLIGHT CHARACTERISTICS OF 

MOLOSSID BATS 

By Terry A. Vaughan 

Abstract: Selected aspects of the morphology of bats of the family Molossidae 
are described and the functional significance of these features are discussed. The 
structure and proportions of the ears and the wings are considered to reflect 
primarily the rapid enduring fUght typical of molossids. Comparisons of some 
characteristics of the wings of three molossids and of four bats of the family 
Vespertilionidae were made, and several aerodynamic relationships were applied 
to a consideration of the styles and speeds of flight of these bats. Molossid bats in 
general seem adapted to fast flight in open areas, whereas the vespertihonids 
studied are apparently suited to slower flight fairly low to the ground, near vege- 
tation and other obstacles. 

Bats of the family Molossidae form a distinctive and anatomically peripheral 
group, and their flight probably surpasses that of all other bats in speed and 
endurance. Repeated mention in the literature has been made of the mode of 
flight of these bats (H. W. Grinnell, 1918; A. B. Howell, 1920; Orr, 1954; 
Vaughan, 1959; Hall and Dalquest, 1963); and Miller (1907), Vaughan (1959) 
and Struhsaker ( 1961 ) have described selected aspects of the postcranial 
morphology of molossids. 

MATERIALS AND METHODS 

Specimens in alcohol representing the following species and famiUes were examined for 
this study: Macrotus californicus ( Phyllostomidae ) ; Myotis lucifugus, M. yumanensis, M. 
velifer, M. evotis, Lasiurus horealis, L. cinereus, Plecotus townsendii, Antrozous pallidus 
( Vespertilioiiidae ) ; Tadarida hrasiliensis, T. molossa, Eumops perotis (Molossidae). The 
specimens are in the collection of the author. 

Measurements of areas and proportions of wings were made from tracings of wing 
outhnes. Although care was taken to pin each wing in the same fuUy spread position, the 
wing measurements of preserved specimens probably differ from those of fresh animals. 



169 



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,,.^L^'^.^t^ 




Fig. L — Front and side views of the heads of Eumops perotis (above) and Tadanda 
molossa (below). In tlie front view of Eumops the anterior part of the left ear is removed 
to show the structure of the ear. 

All wing measurements were taken as follows from fully outstretched wings: the length 
of the distal segment of the wing ( chiropatagium ) was measured from the base of the 
thumb to the wing tip; the length of the proximal segment of the wing ( plagiopatagiimi ) 
was measured from the middle of the base of the wing where it joins the body to the 
middle of the fifth digit; the width of the wing was measured across the flattened airfoil 
from the base of the thumb to the tip of the fifth digit; the length of the wing was 
measured from the center of the base of the wing to the vdng tip. Wing areas were 
measured as if the wings were continuous through the interf emoral membrane ( uropatagium ) 
and the body. Ear lengths were measured from the crown, and ear widths were measured 
across the base of the pinna where it joins the head, or, as in the case of molossids, from 
the posterior base of the pinna to where the anterior base joins the fold of tissue connecting 
the anterior edges of the pinnae. 

RESULTS AND DISCUSSION 

Head. — The heads of all molossid bats are similar in basic design: the 
braincase and rostrum are broad and the muzzle is truncate; the lips are 
thick and frequently wrinkled; the ears are usually broader than long, have 
thickened and reinforced borders, and face more nearly downward or to the 
side than forward (Fig. 1). The design and position of the ears is of con- 
siderable aerodynamic importance in a bat with rapid, sustained flight, and 
with this in mind the ears of molossid bats merit close attention. 

The shape and proportions of the ears of molossids are distinctive and fairly 
uniform. The ears are characteristically very broad, relative to their length, 
and have squared-off tips. In Eumops perotis and Tadarida molossa the ears 
are 1.6 times as wide as high. The corresponding figure for T. brasiliensis is 
1.2. The ears of most vespertilionid bats, in contrast, are longer than wide. 
In the vespertilionid bats listed in Table 1, for example, the ratio of ear width 
to ear length is from 0.39 to 0.70. 

In molossid bats the anterior and ventral borders of the pinnae are generally 



170 



May 1966 VAUGHAN— MORPHOLOGY AND FLIGHT OF MOLOSSIDS 



251 



Table 1. — Sizes of heads of bats and birds and proportions of the ears of bats. All figures 
are averages; the numbers of specimens measured are given in parentheses 







Weight of head 


Ear width 




Species 




Total weight 


Ear length 




Sturnus vulgaris 


(9) 


0.11 


— 




Turdus migratorius 


(13) 


0.11 


- 




Mijotis yumanensis 


(10) 


0.15 


0.58 




M. velifer 


(10) 


0.17 


0.70 




Plccotus townsendii 


(10) 


0.16 


0.39 




Tadarida brasiliensis 


(10) 


0.16 


1.15 




T. molossa 


(3) 


0.20 


1.56 




Eumops perotis 


(5) 


0.23 


1.61 





strongly braced by connective tissue. Viewed from the side, the pinna arches 
dorsad and resembles a crude airfoil of high camber (Fig. 1). The base of 
the leading edge of the pinna is almost directly anterior to the base of the 
trailing edge, thus furthering the resemblance of the ears to short, broad wings. 
During flight the thickened ventral borders of the ears lie against the side of 
the head and cover the eyes in some molossids. Short, broad ears which lie 
against the head and do not directly face the airstream during flight are found 
also in Lasiurus. Here, as in the molossids, this type of ear is associated with 
rapid flight. 

In both birds and bats there has been a trend toward the concentration of 
weight near the center of gravity. The heads of most birds are light; they 
carry no teeth and generally have only light jaw musculature. In a series of 13 
robins {Turdus migratorius) and 9 starlings (Sturnus vulgaris) from Colorado 
the head comprised on the average 10.9% and 11.2% of the total weight, re- 
spectively. Relative to total body weight, bats have heavier heads than those 
of birds. In the bats studied the weight of the head comprised from approxi- 
mately 15 to 23% of the total weight (Table 1). The heads of two of the 
molossid bats are relatively considerably heavier than the heads of the ves- 
pertilionid bats. When in flight most bats carry the occipital portion of the 
head against the interscapular depression, thus compensating for the weight 
of the head by bringing it fairly close to the center of gravity. 

The unique design of the ears of molossid bats probably developed in re- 
sponse to fast, sustained flight, and serves to minimize drag and to brace the 
ears against the force of the airstream. In addition, the ears probably develop 
some lift during flight, allowing the heavy head to be supported as least in 
part by the airstream. During long flights this could result in an important 
conservation of energy which would otherwise be expended in supporting 

the head. 

A further characteristic of the molossid head which has probably been de- 
veloped in response to rapid flight is the loose or wrinkled lips. It remains 
for high-speed photography to demonstrate the operation of the lips in catching 
insects, but it seems probable that when the mouth is wide open during flight 



171 



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JOURNAL OF MAMMALOGY 



Vol. 47, No. 2 



r""Coraco-cutaneus 



• occipito-pollicalis 

■•humeropatagialis 




Fig. 2. — The wings of Eumops perotis (top), Lasiurus borealis (middle), and Myotis 
evotis (bottom), showing the muscles and networks of elastic fibers that tighten and brace 
the wing membranes. 

the lips spread outward, away from the teeth, thus increasing the area of the 
mouth. The wrinkled or loose lips of molossids seem functionally homologous 
to the rictal bristles around the bills of caprimulgiform birds; in both groups 
the increase in the effective area of the mouth may partially compensate for 
the sacrifice of maneuverability attending rapid flight. 



172 



May 1966 VAUGHAN— MORPHOLOGY AND FLIGHT OF MOLOSSIDS 253 

Wings. — Molossids possess many advanced chiropteran characteristics as- 
sociated with efficient flight, such as the well-developed humeroscapular lock- 
ing device (Vaughan, 1959: 54); but in addition they are obviously highly 
specialized for fast flight, with a resulting sacrifice in maneuverability and 
lifting power. Davis and Cockrum ( 1964 ) have shown by experimentally 
attaching weights to bats that, although the animals are roughly equal in 
weight, Macrotus calif ornicus ( Phyllostomidae ) can take flight with approxi- 
mately five times the additional load lifted by Tadarida brasiliensis (Molossi- 
dae). Differences in the ability to take off with extra loads reflect, in part, 
differences in wing design. 

The long, narrow wings of molossid bats are unique in several ways. The 
fifth digit is unusually short, making the plagiopatagium narrow. The first 
phalanges of the third and fourth digits flex posteriorly instead of ventrally 
as in most other bats. This allows the long part of the wing distal to the third 
and fourth metacarpals to be folded compactly against the posterior surfaces 
of these bones when the wing is at rest or is used in terrestrial locomotion. In 
molossid bats the third metacarpal, the longest bone in the hand, is almost 
exactly the same length as the radius. Consequently, because of the pattern of 
flexion of the third and fourth digits, the long chiropatagium folds into a bundle 
no longer than the radius. 

In considering the form and function of wings, the amount of camber (an- 
teroposterior curvatiu-e) is of basic importance. The amount of camber is a 
major factor in determining the ability of a wing to develop lift. Airfoils with 
high camber develop high lift at low speeds, but create considerable drag. 
Relative to airfoils of high camber, those of low camber are effective at pro- 
ducing lift at higher speeds and produce little drag. The airfoils of most bats 
are of high camber, whereas those of molossids are of relatively low camber. 
In terms of function, the latter design creates relatively little drag but forces 
molossid bats to fly fairly rapidly to enable the airfoils to produce sufficient 
lift to maintain flight. An aerodynamic refinement occurring in bats but not 
in birds is the ability to vary the camber of the wing. Flexion of the phalanges 
of the fifth digit and lowering the hind limbs increases the camber of the wing 
by curving the trailing edge of the plagiopatagium downward and causing it 
to function like a flap on an airplane. Such a flap enables either bats or air- 
craft to increase the camber of an airfoil for higher Hft at low speeds and to 
flatten the airfoil and reduce the drag at higher speeds. Thus, a wing with 
flaps can operate effectively under a greater range of speeds than that within 
which the same wing could function if it had a fixed airfoil. The ability to 
change the amount of camber of the wings is probably important in enabling 
small, broad-winged bats such as Myotis evotis and Plecotus townsendii to fly 
at a great variety of speeds. The camber of the narrow molossid wing seems 
less variable than that of broad-winged vesperitilionids. 

The flight membranes of molossids are leathery and elastic and seem much 
stronger than those of other bats. In molossids the wing membranes are braced 



173 



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JOURNAL OF MAMMALOGY 



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•biceps brachii 




acromiodeltoideus 

clavodeltoideus 

■ occipito-pollicalis 

■ omocervicalis 

V i^vi$^^' pectoralis 



Fig. 3. — Front view of the right shoulder of Eumops perotis showing the attachment of 
the occipito-poUicahs muscle to the pectorahs muscle. 



by cartilaginous extensions of the distal ends of the third, fourth and fifth 
phalanges and by complex meshworks of connective tissue in the plagiopa- 
tagium and in the interdigital membranes ( Fig. 2 ) . The elasticity of the wing 
membranes may be of considerable aerodynamic importance. When the wings 
are partially flexed, as they are during dives or in rapid level flight, the tension 
on the plagiopatagium is partially relaxed and this membrane narrows sharply, 
reducing its area and the drag it creates. This narrowing is probably caused by 
both the elastic network and by the humeropatagialis muscle. The high-speed 
dives made by Eumops perotis, and sometimes made by Tadarida brasiliensis, 
when approaching a roosting place in a cliff (see Vaughan, 1959: 20) may be 
made possible partly by the narrowing of the plagiopatagium when the wing 
is partly flexed. 

In all bats the wing membranes are strengthened by muscles not present in 
other mammals, but in molossids there has been a greater development of these 
muscles than in any other group of bats. The occipito-pollicalis muscle in 
most bats originates on the lambdoidal crest, extends along the leading edge 
of the propatagium ( the membrane anterior to the humerus and radius ) , and 
inserts along the anterior surface of the second metacarpal. This muscle keeps 
the propatagium taut during flight, pulls this membrane slightly ventrad, and 
thereby helps give camber to the plagiopatagium. This improves the effective- 
ness of this segment of the wing as an airfoil. This narrow muscle is attached 
by fascia to the front of the shoulder in most bats. In molossids, however, the 
muscle is relatively large and is more complex: it is divided into a proximal 
and a distal part, and the junction of these parts is attached strongly by a 
tendon-like fascial bundle to the pectoralis muscle (Fig. 3). The coraco-cutane- 
ous muscle, which occurs in all bats, originates on the humerus and passes 
into the proximal part of the plagiopatagium. This muscle helps maintain the 
tautness of the axillary portion of the plagiopatagium. Two additional muscles, 
serving to tense the plagiopatagium, are present only in molossid bats and are 



174 



May 1966 VAUGHAN— MORPHOLOGY AND FLIGHT OF MOLOSSIDS 255 

probably adaptations to fast flight. The first, the tensor plagiopatagii, origi- 
nates on the tibia and tarsus and inserts into the part of the plagiopatagium 
adjoining the shank and into the connective tissue tliat reinforces the trailing 
edge of the plagiopatagium. This muscle not only tenses this part of the wing 
but is of importance in strengthening the attachment of the plagiopatagium 
to the shank and tarsus. The second muscle, the humeropatagialis, originates 
on the distal end of the humerus and inserts into the elastic fibers in the distal 
part of the plagiopatagium (Fig. 2). The most important function of the 
muscles and connective tissue which reinforce and tense the plagiopatagium 
is to maintain this proximal segment of the wing as an efficient airfoil during 
flight and to keep the membrane from being distorted by the force of the air- 
stream. In fast-flying bats considerable distortion could occur and this would 
reduce sharply the effectiveness of the plagiopatagium as a lifting surface. Be- 
cause the plagiopatagium supplies the major share of lift during flight, this 
is of critical importance. An additional function of the plagiopatagialis may 
be to narrow the plagiopatagium during dives or when the wings are partially 
flexed during rapid flight. 

The morphology of the scapula varies considerably within the order Chirop- 
tera and reflects, in part, degrees of specialization for various modes of flight. 
One variable structure is the long coracoid process, which, because it extends 
ventral to the plane of the scapula, allows the biceps brachii and coraco- 
brachialis muscles to serve as adductors of the wing. In most bats the coracoid 
curves laterad (toward the wing), whereas in all molossids the coracoid is di- 
rected sharply mediad (Fig. 4). This "molossid" type of coracoid is found also in 
Miniopterus (Miller, 1907), and to a lesser degree in Lasiurus. Attending this 
difference are differences between the brachial musculature of molossid bats 
and most other bats. In the latter the coracobrachialis and the biceps brachii 
muscles are the important members of the flexor group of the arm. The 
glenoid head of the biceps originates on the lateral base of the coracoid process 
and is the larger division of the biceps. The smaller coracoid head originates 
along the distal part of the coracoid process. Both divisions insert into a slit 
in the anteromedial surface of the radius just distal to its head. Molossids, in 
contrast, have lost the coracobrachialis muscle; and the coracoid head of the 
biceps, rather than the glenoid head, is the largest division of this muscle 
(Fig. 4). Because of the medial curvature of the coracoid process in molossids, 
during the lower part of the downstroke of the wing the coracoid head of the 
biceps can act as a far more effective adductor than can this muscle in most 
nonmolossid bats (Vaughan, 1959: 90). In molossids, due partly to the modi- 
fications of the scapula and biceps mentioned above, occurs the most perfect 
development of the basic chiropteran trend toward dividing the labor of the 
downstroke of the wing between a number of muscles. This division of labor 
was probably developed in response to the demands of the enduring flight 
typical of most molossids. 

The shapes and aerodynamic characteristics of the wings considered in this 



175 



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Vol. 47, No. 2 



••humerus 




acromion process 



coracoid process 



>■• biceps brachii 
(glenoid head) 



•biceps brachii (coracoid head) 




Fig. 4. — Front views of the right shoulders of Antrozous pallidus (above), showing the 
lateral curvature of the coracoid process of the scapula typical of most vespertilionid bats, 
and of Eumops perotis (below), showing the medial curvature of the coracoid process 
typical of molossid bats. 

study differed widely (Fig. 2, Table 2), but certain differences between the 
molossid and vespertilionid wings are readily apparent and are indicative of 
functional contrasts. The ratios based on wing proportions illustrate that, com- 
pared to the vespertilionid wing, the molossid wing is narrow, has a long distal 
segment, a high aspect ratio (the ratio of length to width of a wing; for ir- 
regularly shaped wings it is considered to be the ratio of the wing span^/wing 
area), and a high wing loading (weight in pounds/wing area in feet^). 

For the molossid bats considered here the length of the chiropatagium 
averaged 154.1% of the length of the plagiopatagium, and the width of the 
wings averaged 36.8% of the length. In the vespertilionids measured the cor- 
responding figures were 138.5% and 48.7%. The aspect ratios reflect these 
differences and are higher for the molossids (8.60-9.98) than for the ves- 
pertilionids (5.99-6.74). In general, the higher the aspect ratio the more ef- 
ficient the wing because of the reduction of drag at the wing tip. The wing 



176 



May 1966 VAUGHAN— MORPHOLOGY AND FLIGHT OF MOLOSSIDS 



257 



Table 2. — Proportions of wings of bats. All figures are averages; the numbers of 
specimens measured are given in parentheses 



Species 


Area of 
chiropatagium 

Area of 
phigiopatagium 


Length of 
chiropatagium 

Length of 
plagiopatagium 


Greatest width 
of wing 
Length 
of wing 


Aspect ratio: 
Wing span^ 

Area of wings 


Myotis yumanensis 


(5) 


0.95 


L32 


0.47 


6.74 


M. evotis 


(5) 


0.80 


L35 


0.51 


6.48 


M. lucifugus 


(5) 


0.69 


L41 


0.48 


6.47 


Plecotus townsendii 


(5) 


0.86 


L46 


0.50 


5.99 


Tadarida brasUiensis 


(5) 


0.93 


1.58 


0.38 


8.60 


T. molossa 


(3) 


0.86 


L47 


0.36 


9.71 


Eumops perotis 


(5) 


0.83 


1.58 


0.36 


9.98 



loadings of the molossid bats (0.325-0.546) are considerably higher than those 
of the vespertilionids (0.157-0.202). As a rule, the higher the wing loading 
the greater the speed necessary to produce adequate lift for sustained flight. 
Usually the smaller the bat the lower the wing loading because in small bats 
the ratio of mass to surface is small ( the volume and mass vary as the cube 
of the linear dimensions whereas the surface area varies as the square). 

Instructive comparisons can be made between habitat and wing form in 
both bats and birds and between the characteristics of the wings of certain 
bats and those of the wings of birds with well-known modes of flight. The 
plan form of the wing of Myotis evotis ( Fig. 2 ) is similar to that of many small 
passerine birds. This roughly elliptical wing is fairly efficient for low speed 
flight, and occurs in birds adapted to flight through brush or woods, or where 
numerous obstacles make long wings unmanageable (Savile, 1957). The 
short, broad wing of Myotis evotis is seemingly well suited to flight near the 
ground in the wooded or brushy areas the bat inhabits. A markedly different 
adaptation is Illustrated by the wings of molossid bats which are similar to 
the "high-speed" wings of many birds known to be strong enduring fliers or 
to feed on the wing ( falcons, plovers, sandpipers, swifts and swallows ) . Such 
birds characteristically fly in open places with few obstructions, a situation 
"allowing" the development of long, aerodynamically efficient wings. The 
wings of these birds have the following characteristics according to Savile 
( 1957 ) : low camber; high aspect ratio; taper to a slender, elliptical tip; pro- 
nounced sweepback of the leading edge; and wing root fairing. These same 
features describe well the molossid wing. Thus, in wing design and foraging 
habits the molossids appear to be chiropteran counterparts of the swdfts and 
swallows, whereas the smaller vespertilionids seem to most nearly resemble the 
smaller flycatchers in wing design, but differ from the latter in flying con- 
tinuously while feeding. 



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Table 3. — Sizes, aerodynamic characteristics and computed minimum flight speeds of 
seven species of bats. All figures are averages; the numbers of specimens measured are 

given in parentheses 



Species 



Weight 

(g) 



Wing span 
( cm ) 



Wing area 
(cm2) 



Wing loading 



lbs/ft2 



g/cm2 



Minimum 
flight 
speed 
(mph) 



Myotis yumanensis 


(5) 


5.2 


20.26 


60.95 


0.173 


0.084 


8.3 


M. evotis 


(5) 


6.2 


22.80 


80.20 


0.157 


0.077 


7.9 


M. lucifugus 


(5) 


8.1 


23.30 


83.41 


0.202 


0.099 


8.8 


Plecotus townsendii 


(5) 


9.1 


24.52 


100.41 


0.184 


0.090 


8.5 


Tadarida hrasiliensis 


(5) 


12.2 


25.08 


73.14 


0.339 


0.165 


11.6 


T. molossa 


(3) 


16.2 


31.33 


101.12 


0.325 


0.159 


11.7 


F.umops perotis 


(5) 


53.5 


44.58 


199.22 


0.546 


0.266 


14.7 



From the weight of a bat and the area of its wing surfaces the speed it must 
fly to sustain level flight can be approximated by the equation 

(von Mises, 1945) where V is velocity (in feet per second); 2 gc is a unit- 
conversion constant; W is the total weight; A is the area of the wings; C^ is 
the coefficient of lift; and V is the density of air in pounds per cubic foot. 
The coefficient of lift is derived from the size, camber, aspect ratio, angle of 
attack and other characteristics of the wing, and for the present study was 
assumed to be 1.0, which probably approximates the actual values closely 
enough to cause little error. These calculations are based on the further as- 
sumption that each bat has its wings fully and rigidly outstretched. Although 
the calculated speeds may not correspond closely to the actual flight speeds 
of the bats, they probably reflect accurately the relative flight speeds. Except 
for the molossids, flight speeds arrived at by the above equation (Table 3) 
are fairly close to those found experimentally by Hayward and Davis ( 1964 ) . 
As these authors mention, the speeds shown for the molossids in their study 
are probably too low because the bats could not fly normally under their 
experimental conditions. 

The speeds calculated on the basis of the figures for total weight and wing 
area shown in Table 3 suggest that in order to maintain level flight the 
molossids must fly faster than do the vespertilionids. The speed for Myotis 
evotis (7.9 mph), for example, is roughly half that of Eumops perotis (14.7 
mph). The calculated speeds probably approximate the relative speeds of 
the bats under study in level flight, but all of these bats seem to be capable 
of a wide range of flight speeds. Judging from my own observations, M. evotis 
can hover briefly and can fly at very low speeds; at the other extreme, some 
molossids are capable of rapid dives and of level flights at speeds far greater 
than those listed here. A complicating factor, but one of critical importance 
when considering the flight capabilities of a bat, is the animal's ability to 



178 



May 1966 VAUGHAN— MORPHOLOGY AND FLIGHT OF MOLOSSIDS 259 

vary the camber, angle of attack and the areas of the membranes. A fm-ther 
complexit>' is the fact that the wings are in nearly constant movement dur- 
ing flight, and supply both the lift and the thrust necessary for flight. 

Various aerodynamic relationships are pertinent to the problem of relative 
flight speeds and differences in morphology in bats. For example, because 
drag increases in proportion to surface area and as the square of the speed, 
E. perotis is probably subject to about three times the drag faced by M. evotis. 
This explains why features which tend to minimize drag, such as low camber 
of the wing and short ears which present their most streamlined aspect to 
the airstream, are of vastly greater importance in the large E. perotis, and in 
most molossid bats, than in smaller, relatively slow-flying bats. Even the 
short, velvety fur of molossids may be an adaptation to reduce drag caused 
by the body during flight. 

Miscellaneous considerations. — The family Molossidae is unique in having 
developed the most rapid, enduring flight occurring in bats while retaining 
(or developing) the most accomplished terrestrial locomotion. Consequently, 
molossids offer many trenchant examples of a single morphological character 
serving diverse functional ends. 

One such character is the posterior flexion of the first phalanges of digits 
three and four. Because of this modification the long tip of the narrow wing is 
manageable when the bats are not flying, an important feature in a group 
including many species which take daytime refuge in narrow crevices. This 
unusual pattern of flexion may have developed prior to the lengthening of 
the wing tip and may have "allowed" the evolution of this typically molossid 
character. The part of the wing distal to the carpus folds into a bundle no 
longer than the radius, facilitating a lateral action of the forelimb during 
quadripedal locomotion which enables molossids to move remarkably rapidly 
and easily within the confines of narrow crevices. Thus, the pattern of 
phalangeal flexion in molossids has probably played a role in both terrestrial 
and aerial locomotion. 

The small uropatagium of these bats slips forward along the tail freeing 
the hind limbs to move in a wide arc when the animals run. Also, the re- 
duced drag during flight resulting from the small size of the uropatagium is 
probably aerodynamically important in furthering the cause of fast flight. 
The well-braced flight membranes of molossids may also serve two ends, 
for in addition to resisting effectively the force of the airstream during rapid 
flight, they are better able than are the delicate membranes of most bats to 
withstand the occasional rough treatment resulting from crawling between the 
irregular and abrasive surfaces of rock crevices. 

Perhaps the strong adductors and flexors of the hind limbs represent the 
best example of a dual-puipose molossid character. These limbs are re- 
markably robust and strongly muscled and account in large part for the ac- 
complished terrestrial locomotion typical of the group. Of equal importance, 
however, is their function in serving as a rigid anchor for the posterior portion 



179 



260 JOURNAL OF MAMMALOGY Vol. 47, No. 2 

of the plagiopatagium. This function requires strong flexors and adductors 
of the shank to resist the powerful lateral and dorsal pull exerted by the flight 
membranes during the downstroke of the wing, and is of basic importance 
in maintaining the proper angle of attack and camber of the plagiopatagium. 

Considering the evolution of the family Molossidae, the sturdiness of the 
hind limb and the complete fibula suggest that the basal molossid stock 
may have diverged early from the rest of the Chiroptera, before the hind 
limbs had been greatly modified from their primitive structure and propor- 
tions. By contrast, in many members of the family Phyllostomidae the hind 
limbs have become so highly specialized that they no longer function effec- 
tively in quadripedal locomotion. But in molossids, probably because the 
primitive hind limbs suited the demands of both terrestrial and aerial locomo- 
tion, the hind limbs have remained basically primitive through a period of 
time that saw the evolution of the highly specialized molossid wing of today. 

Some vespertilionid bats and one rhinolophid bat have been shown to use 
the flight membranes in capturing insects (Webster and Griffin, 1962), In 
these species most modifications tending to reduce the dexterity of the 
phalanges were probably disadvantageous, and the evolution of the hand 
was probably influenced by its use in capturing insects, as well as by the de- 
mands of aerial and terrestrial locomotion. 

ACKNOWLEDGMENTS 

This study was supported in part by a grant from The Society of Sigma Xi and RESA 
Research Fund. For critically reading the manuscript and for helpful discussions of 
aerodynamics I am grateful to Dr. P. H. Baldwin and Dr. R. D. Haberstroh. 

LITERATURE CITED 
Davis, R. and E. L. Cockrum. 1964. Experimentally determined weight lifting capacity 

in individuals of five species of western bats. J. Mamm., 45: 643-644. 
Grinnell, H. W. 1918. A synopsis of the bats of CaHfomia. Univ. California Publ. 

Zool., 17: 223-404. 
Hall, E. R. and W. W. Dalquest. 1963. The mammals of Veracruz. Univ. Kansas 

Publ., Mus. Nat. Hist., 14: 165-362. 
Hayward, B. and R. Davis. 1964. Fhght speeds in western bats. J. Mamm., 45: 236-242. 
Howell, A. B. 1920. Contribution to the hfe history of the California mastiff bat. J. 

Mamm., 1: 111-117. 
Miller, G. S. 1907. The famihes and genera of bats. U. S. Nat. Mus. Bull., 57: 

xvii -I- 282 pp. 
Orr, R. T. 1954. Natural history of the pallid bat, Antrozous pallidus. Proc. CaUfomia 

Acad. Sci., 28: 165-246. 
Savtle, D. B. O. 1957. Adaptive evolution in the avian wing. Evolution, 11: 212-224. 
Struhsaker, T. T. 1961. Morphological factors regulating flight in bats. J. Mamm., 

42: 152^159. 
Vaughan, T. a. 1959. Functional morphology of three bats: Eumops, Myotis, Macrotus. 

Univ. Kansas Publ, Mus. Nat. Hist., 12: 1-153. 
von Mises, R. 1945. Theory of flight. McGraw-Hill Book Co., New York. 629 pp. 
Webster, F. A. and D. R. Griffin. 1962. The role of the flight membranes in insect 

capture by bats. Animal Behavior, 10: 332-340. 

Colorado Agricultural Experiment Station, Colorado State University, Fort Collins. 
Accepted 23 September 1965. 



180 



NATURAL HISTORY MISCELLANEA 

Published by 

The Chicago Academy of Sciences 

Lincoln Park - 2001 N. Clark St., Chicago 14, Illinois 

No. 170 October 30, 1959 



Toxic Salivary Glands in the Primitive Insectivore Solenodon 

George B. Rabb* 

In 1942 0. P. Pearson demonstrated the toxic property of the saliva 
of Blarina brevkauda, a common shrew of the eastern United States, 
and identified its principal source as the submaxillary gland. Compara- 
tive studies at that time and subsequently revealed that similar poison- 
ous factors were not present in the salivary glands of other soricid and 
talpid insectivores (Pearson, 1942, 1950, 1956). I had an unexpected 
opportunity to make a crude check on the salivary glands of Solenodon 
paradoxus, a remote relative of the shrews, when three of these animals 
died at the Chicago Zoological Park within two months after their 
arrival in 1958 from the Dominican Republic. 

Parts of the submaxillary and parotid glands of one animal that 
had died one to two hours beforehand were ground separately with 
sand, diluted to 10 per cent by weight solutions with 0.9 per cent XaCl 
solution, and filtered, following the procedure of Pearson (1942). These 
solutions were injected into a small series of male white mice that 
ranged in weight from 29 to 44 grams. 

All of the mice injected with extract from submaxillary gland 
showed some reaction — at least urination and irregular or rapid 
breathing for several minutes. Five that received intravenous doses of 
extract of .09 to .38 mg. submaxillary gland per gram of body weight 
did little more than this and recovered within 30 minutes. Five that 
received intravenous doses of .38 to .55 mg. per gram additionally ex- 
hibited protruding eyes, gasping, and convulsions before dying within 
two to six minutes. Two animals that had intraperitoneal injections of 
extract of .56 and .66 mg. per gram died in about 12 hours, and one 
injected at the level of 1.02 mg. per gram died in 13 minutes. Urination, 
cyanosis, and depression were observed in these animals. Three "con- 
trol" mice injected intravenously with extract of 1.02, 1.68, and 1.87 



♦Chicago Zoological Park, Brookfield, Illinois 



181 



No. 170 The Chicago Academy of Sciences, Natural History Miscellanea 

mg. of parotid gland per gram of body weight showed no distress except 
for initially very rapid breathing in the last case. 

In general these results are very like those described for Blarina 
extracts. It may be noted that the twentyfold lesser potency evident 
here of Solenodon extract as compared to that of Blarina may be due 
to postmortem inactivation of the toxic principle as reported by EiLs 
and Krayer (1955) for fresh Blarina material. Further tests with tne 
refined techniques of these authors using acetone treated glands will 
be necessary for a fairer assessment of the potency of Solenodon toxin. 

Sections were made of the submaxillary glands and stained w-th 
hematoxylin and eosin and also with a modification of Mallory's triple 
stain. These sections showed some large cells with coarse acidophilic 
granules and small nuclei in the secretory ducts. Pearson (1950) sus- 
pected that such cells in Blarina might be concerned in the production 
of the saliva's toxic principle, although somewhat similar cells are 
found in other soricids. 

The submaxillary glands of Solenodon are rather enormous and con- 
spicuous structures (see fig. 47 in Mohr, 1938). Each gland weighs 
three to four grams in adult animals. According to Allen (1910), the 
duct of the submaxillary gland ends at the base of the large deeply 
channeled second incisor tooth of the lower jaw (see fig. 19D in Mc- 
Dowell, 1958). Presumably toxic saliva would be conducted thereby 
into a wound. I could not induce Solenodon to bite live mice and there- 
fore have no direct evidence on this point. However, in 1877 Gundlach 
reported inflammatory effects of bites by Cuban Solenodon to himself 
and a mountaineer (although he dismissed the possibility of venomous 
action on the basis of authority!). Of his hand bite he said: "... I 
was bitten by the tame individual, which gave me four wounds cor- 
responding to the [large] incisors: those from the two upper incisors 
healed well, but those from the lower ones inflamed." 

Moreover, there are indications that Solenodon is not immune to its 
own venom. Autopsy of the third animal disclosed multiple bite wounds 
on the feet and no obvious internal evidence of other causes of death. 
Sections of the liver show considerable congestion in that organ. The 
snout, lips, limbs, and tail were very pale the afternoon preceding death. 
Mohr (1937, 1938) gave accounts of several cases in which death was 
the outcome of fighting with cage mates although only slight foot 
wounds were inflicted. Pearson (1950) reported that Blarina was rela- 
tively immune to its own venom, although the single test animal died 
and the interpretation was problematical. The utility of the venom for 



182 



Rabb: Toxic Salivary Glands of Solenodon 1959 

Solenodon in its natural environment is unknown and is certainly not 
indicated by its insectivorous habits. The explanation may be phylo- 
genetic and historical rather than one of present-day function. 

I wish to acknowledge the help of the park's veterinarian, W. M. 
Williamson, and medical technician, Ruth M. Getty. 

Literature Cited 

Allen, Glover M. 

1910. Solenodon paradoxus. Mem. Mus. Comp. Zool., 40: 1-54. 
Ellis, Sydney and Otto Krayer 

1955. Properties of a toxin from the salivary gland of the 
shrew, Blarina brevicauda. Jour. Pharmacol, and Exptl. 
Therap., 114: 127-37. 

Gundlach, Juan 

1877. Contribucion a la mamalogia Cubana. Havana, G. 
Monteil, 53 pp. 
McDowell, Samuel B., Jr. 

1958. The Greater Antillean insectivores. Bull. American Mus. 
Nat. Hist., 115(3): 113-214. 

Mohr, Erna 

1937. Biologische beobachtungen an Solenodon paradoxus 
Brandt in Gefangenschaft. HI. Zool. Anz., 117: 233-41. 

1938. Biologische beobachtungen an Solenodon paradoxus 
Brandt in Gefangenschaft. IV. Ibid., 122: 132-43. 

Pearson, Oliver P. 

1942. On the cause and nature of a poisonous action produced 

by the bite of a shrew {Blarina brevicauda). Jour. 

Mamm., 23: 159-66. 
1950. The submaxillary glands of shrews. Anat. Record, 107; 

161-69. 

1956. A toxic substance from the salivary glands of a mammal 
(short-tailed shrew), pp. 55-58 in Venoms, ed. E. E. 
Buckley and N. Porges, American Assoc. Adv. Science 
Publ. No. 44, xii + 467 pp. 



183 



466 JOURNAL OF MAMMALOGY Vol. 48, No. 3 

SOME ASPECTS OF THE WATER ECONOMICS OF TWO SPECIES OF CHIPMUNKS 

The water economics of chipmunks have not received much attention from physiological 
ecologists. Allen (New York State Mus. Bull., 314: 1-122, 1938) wrote of Tamias striatus: 
"Unlike many of the western ground squirrels, the Eastern chipmunk requires a great deal 
of water to drink." Panuska and Wade (J. Mamm., 38: 192-196, 1957) found that water 
consumption of captive T. striatus decreased from 33.4 ml per day just after capture to 
29.2 ml per day after the animals had been confined for a time. Davis ( Murrelet, 15: 20-22, 
1934) wrote that water was not a factor in determining the distribution of the cliff chip- 
munk, Eutamias dorsalis, in Nevada. Seton (Lives of game animals, 4: 184-215, 1929) 
observed that west and south of Manitoba the least chipmunk, E. minimus, is found in 
desert environments far from permanent water. ManviUe (Misc. Publ. Mus. Zool., Univ. 
Michigan, 73: 1-83, 1949) thought water to be of httle importance in the distribution of 
E. minimus in the Huron Mountains of Michigan. 

In the Itasca region of Minnesota the ranges of the gray eastern chipmunk, T. striatus 
griseus, and the least chipmunk, E. minimus neglectus, overlap. Since striatus and minimus 
apparently have markedly different water economics in the extremes of their ranges, I 
wondered if the two species, in the mesic, forested Itascan habitats, would differ from each 
other in their gross and weight-relative water consumption and in their responses to water 
deprivation. 

These studies were conducted in August and September 1963. Chipmunks of both species 
were captured in National Live Traps, 5^/4 X 5^2 X 16 inches, set within 3 miles of Itasca 
State Park, Hubbard and Clearwater counties, Minnesota. The chipmunks were transferred 
to an animal room in the zoology building at the University of Minnesota, Minneapohs. 
There were no provisions for regulating light, temperature, or humiclit; in the room. 

Nine striatus and nine minimus were confined individually in cages 18 X 18 X 12 inches 
with wood shavings provided for htter, and were fed only sunflower seeds. The seeds 
contained water amounting to about 12% of their weight. Tap water was provided ad 
libidum in 30 cc or 100 cc graduated drinking tubes. One tube of each size, hung on the 
rack of cages, permitted assessment of evaporative water loss from the tubes. For 36 days, 
daily records were kept of the change of water level in each tube. On 18 days, at least 
one of the striatus spilled water, indicated by wet litter below the tube. Least chipmunks 
were not known to spiU water. Records of water consumption for the 18 days on which no 
spillage was noted were used to calculate each animal's gross water consumption. Each 
animal's mean daily water consumption was calculated by dividing gross water consump- 
tion by 18. Each animal's water consumption per g of body weight was estimated by 
dividing gross water consumption by the mean value of the animal's body weight as 
recorded on the first and thirty-sixth days. The arithmetic mean, standard deviation, 
standard error of the mean, and coefficient of variation ( V ) were computed for each of the 
foregoing variables for each species. 

Following the studies of water consumption, seven individuals of each species were 
deprived of water for five consecutive days. Two individuals of each species served as 
controls and were allowed unrestricted access to drinking water. The chipmunks were 
weighed daily during the five days of water deprivation and for seven days after ad 
libidum access to water was restored. Each animal's daily weight was recorded as a 
percentage of its body weight at tlie outset of the experiment. Mean daily percentages were 
calculated for each species. 

Statistical procedures followed were those of Simpson, Roe, and Lewontin (Quantitative 
zoology, 1960). The level of significance used for tests of hypotheses was 95%. 

Data on water consumption are summarized in Table 1. Although the gross water 
requirement of minimus was about one-third that of striatus, there was no significant 
difference in the weight-relative water consuimptions of the two species. The coefficients 



184 



August 1967 



GENERAL NOTES 



467 



Table 1. — Summary of data on water constimption of confined chipmunks. 







1'. striatus 




E. minimus 




Variable 


Mean 
Range 


SE 


V 


Mean 

Range se 


V 



Weights of 
animals (g) 

Total HaO 
consumed ( ml ) 

Mean HaO consumed 
per day (ml) 

Mean H2O consumed 
per g body weight 



115.0 
102.8-132.8 

296.1 
208-471 

16.4 
11.6-26.2 

2.52 
1.98-<3.60 



3.4 8.9 
26.5 26.8 

1.5 

0.18 20.8 



46.2 



42.0-50.2 



97.8 



76-150 

5.4 
4.2-8.3 

2.16 
1.62r-2.96 



0.8 
7.6 
0.4 
0.17 



5.1 
23.2 



23.6 



of variation show that individual variation in water consumption was very large. There are 
individual and specific differences in the adjustments of the animals to captivity. As a 
group, eastern chipmunks were more sedentary in their cages than were least chipmunks, but 
activity among individual striatus was quite variable. 

The two species did not differ significantly from each other in their abilities to resist 
weight loss during water deprivation or to regain weight once access to water was restored 
(Table 2). When experimental animals were deprived of water, they first became more 
active than usual. Their activity decreased markedly during the last three days of water 
deprivation. Normally, a lively chase ensued before an animal could be caught by hand 
for weighing, but by the fifth day of water deprivation one could easily pick up a 
dehydrated chipmunk from its cage. Control animals remained quick and alert. Their 
weights varied only a few grams on either side of their pre-experimental weights during this 
study. The mean weights of rehydrating striatus are distorted by the weights of one 
individual that continued to lose weight even after access to water was restored. Ultimately, 



Table 2. — Percentages of pre-experimental weights of experimental chipmunks during 

dehydration and rehydration. 



Day 


n 


T. striatus 
Range Mean 


SD 




E. minimus 




number 


n 


Range 


Mean 


SD 


1 


7 


89.9-95.5 


93.0 


1.8 


7 


89.5-95.4 


93.4 


1.8 


2 


7 


85.5-91.6 


88.2 


2.2 


7 


85.6-91.6 


88.6 


1.9 


3 


7 


80.0-86.7 


83.6 


2.6 


7 


79.2-S5.2 


82.9 


2.2 


4 


7 


74.6-82.5 


78.6 


3.4 


7 


74.8-83.7 


78.8 


3.1 


5 


7 


70.4-79.4 


75.7 
Access 


4.0 
to water 


7 
restored 


69.4-79.2 


74.9 


3.7 


6 


7 


76.6-85.4 


82.5 


2.9 


7 


80.7-92.0 


84.7 


4.5 


7 


6* 


67.8-85.5 


81.1 


6.6 


7 


77.3-95.0 


84.9 


6.2 


8 


6 


63.6-92.8 


83.3 


10.1 


6* 


79.1-96.5 


88.1 


6.3 


9 


6 


62.8-94.3 


85.7 


11.6 


6 


80.7-100.0 


89.1 


7.0 


10 


6 


59.4-97.4 


87.0 


14.1 


6 


79.9-100.0 


89.1 


7.1 


12 


6 


57.9-100.0 


89.1 


16.3 


6 


82.7-100.0 


90.6 


6.0 



* One experimental animal found dead. 



185 



468 JOURNAL OF MAMMALOGY Vol. 48, No. 3 

this animal lost half of its pre-experimental weight, but the pre-experimental weight was 
eventually regained and siupassed. 

The literature suggests that striatus is somewhat more dependent upon a plentiful supply 
of drinking water than are minimus and its relatives. The present experimental evidence 
suggests that this is so. The gross water requirements of minimus are small. With some 
insects and fruit of high water content, and a morning supply of dew, Itascan minimus can 
probably keep themselves in good condition with no permanent source of drinking water. 
When raspberries ( Rubus minnesotanus ) are in fruit at Itasca, minimus is found in greatest 
abundance around raspberry thickets. Often, several chipmunks at a time can be seen 
eating the fruit, the seeds of which the animals carry away in their cheek pouches. While 
such a diet would supplement a marginal water supply, I think the chipmunks take the fruit 
as much for the seeds as for the moist, pulpy parts. 

It was surprising to me that m,inimus — a small, active species with high metabolic and 
breathing rates — did not require more water per g of body weight than did the larger, 
seemingly less active striatus whose metabohc and breathing rates are lower. Nor did 
comparison of rates of dehydration and rehydration suggest any significant difference 
between the water economics of the two species. At Itasca, as in other parts of its range, 
minimus is most common in exposed habitats such as the margins of slash piles and gravel 
pits. Exposure to wind and solar radiation is maximal in such situations; daytime tempera- 
tures, consequently, are often high and relative humidity is often low. In contrast, striatus 
remains beneath tree and shrub cover where, since insolation and wind are reduced, daytime 
temperatures are lower and relative humidity is higher than in open habitats. In view of 
the morphologic, physiologic, and behavioral differences between the two species, the 
similarities found in their water economics may represent the existence of physiologic 
adaptations in minimus to its somewhat more xeric Itascan microhabitats. 

A thorough analysis of the water economics of these and other chipmunks could, in 
addition to testing these results, provide information relevant to habitat preferences among 
the many species of Eutamias. In addition, Nadler (Amer. Midland Nat., 72: 298-312, 
1964) has suggested that physiologic and ecologic study may shed light on phylogenetic 
problems involving Eutamias. I have found chipmunks to be difficult subjects for experi- 
ments of this sort. They are active and often hard to catch for weighing. Some individuals 
invariably shake water out of their drinking tubes; others are inclined to pack Htter into the 
tubes, but use of cedar tow as litter reduces this. Control of temperature, light, and hu- 
midity, and selection of experimental animals of about the same size and age, should reduce 
the variability in performance. 

Part of this work was done while I held an NSF Summer Fellowship for Teaching 
Assistants, awarded through the University of Minnesota. — Richard B. Forbes, Department 
of Biology, Portland State College, Portland, Oregon 97207. Accepted 30 January 1967. 



186 



THE OXYGEN CONSUMPTION AND BIOENER- 
GETICS OF HARVEST MICE 

OLIVER P. PEARSON 
Museum of Vertebrate Zoology, University of California, Berkeley 



R\TES of metabolism or of oxygen 
consumption have been reported 
k, for many species of small mam- 
mals, but little effort has been made to 
relate such measurements to the energy 
economy of small mammals in the wild. 
Such efifort has been avoided because the 
rate of metabolism varies so much with 
changes of the ambient temperature and 
with activity of the animal. I believe, 
however, that these variables can be 
handled with sufficient accuracy so that 
one can make meaningful estimates of 
the 24-hour metabolic budget of free-liv- 
ing mice in the wild. In this study I have 
measured the oxygen consumption of 
captive harvest mice under different con- 
ditions, and from these measurements I 
have estimated the daily metabolic ex- 
change of wild harvest mice living in 
Orinda, Contra Costa County, Califor- 
nia. 

The harvest mice used in the study 
{Reithrodontomys megalotis) are noctur- 
nal, seed-eating rodents living in grassy, 
weedy, and brushy places in the western 
half of the United States and in Mexico. 
In Orinda they encounter cool wet win- 
ters (nighttime temperatures frequently 
slightly below 0° C.) and warm dry sum- 
mers (daytime temperatures sometimes 
above 35° C, but nights always cool). 
They do nothibernate. 

MATERIAL AND METHODS 

Five adult harvest mice were caught 
on January 29 and 30, 1959, and were 
kept in two cages in an unheated room 
with open windows so that the air tem- 



perature would remain close to that out- 
side the building. They were fed a mix- 
ture of seeds known as "wild bird seed." 
Metabolic rates were tested between Jan- 
uary 29 and April 1 in a closed-circuit 
oxygen consumption apparatus similar to 
the one described by Morrison (1947) but 
without the automatic recording and re- 
filling features. All tests except the 24- 
hour runs were made during the daytime 
and without food. Since harvest mice are 
strongly nocturnal, several hours had 
usually elapsed between their last meal 
and the measuring of their oxygen con- 
sumption. When placed in the apparatus, 
the mice usually explored the metabolic 
chamber and groomed their fur for about 
half an hour and then went to sleep on 
the wire mesh floor of the chamber. One 
hour or more was allowed for the animals 
to become quiet and for the system to 
come to temperature equilibrium. The 
animals usually were left in the chamber 
until from five to ten determinations of 
oxygen consumption had been made, 
during which they had remained asleep 
or at least had made no gross movements. 
Each determination lasted between 9 and 
24 minutes. The mice were weighed when 
they were removed from the apparatus. 
Oxygen consumptions are reported as 
volume of dry gas at 0° C. per gram of 
mouse. 

RESULTS 
SIZE X RATE OF METABOLISM 

Adult harvest mice weigh between 7 
and 14 grams. Larger individuals con- 
sume oxygen at a lower rate per gram of 



152 



187 



A'lETABOLISM OF HARVEST MICK 153 

body weight (I'ig. 1). I'or example, at with restful surroundings, as in a nest, 
12° (\ a 12-gram mouse would use only the animals probably relaxed their tcm- 
1.17 times as much oxygen per hour as an perature control temporarily. This ex- 
8-gram mouse, although it is 1.5 times as planation seems plausible in view of the 
heavy. The various points in the regres- known lability of the body temperature 
sion of body weight against rate of oxy- of some rodents such as Peromyscus 
gen consumption can be fitted ade- (Morrison and Ryser, 1959), Dipodomys 
quately with a straight line, and from the (Dawson, 1955), and Perognathus (Bar- 
slopes of such lines illustrating the re- tholomew and Cade, 1957) under similar 
gression at different ambient tempera- circumstances. Birds permit their body 
tures it may be seen (Fig. 1) that at cold temperature to drop about 2° C. when 
temperatures a variation of 1 gram in they sleep at night, and this is accom- 
body weight causes a greater change in panied by a drop of as much as 27 per 
metabolic rate than at 30° C. At 1°, 12°, cent in rate of metabolism (De Bont, 
and 24° a change of 1 gram in weight is 1945). The 40 per cent drop shown by 
associated with a change in oxygen con- some of the mice may have been accom- 
sumption of 0.98, 0.48, and 0.35 cc/g/hr, panied by a drop in body temperature of 
respectively. several degrees. 

At warm and moderate temperatures 
there was little variation in the measure- resting met.^bolism at different 
ments of each mouse during any one run temperatures 
(Fig. 1), but at 1° C. the variation was Since the weights of adult harvest mice 
sometimes enormous. Since each meas- vary so much, it is desirable to eliminate 
urement was made over a period while the the size variable by adjusting all rates of 
mouse was inactive, the variation must metabolism to a single average size (9 
stem from a real difference in the resting grams) . This has been done by using the 
metabolism of each mouse at different series of regression lines in Figure 1. 
times. I believe that lability of body tem- Where each of these lines crosses the 9- 
perature is the cause. Harvest mice ex- gram ordinate, that value is taken as the 
posed to cold and hunger in box traps appropriate rate for a "standard" 9-gram 
sometimes are found to be torpid and harvest mouse and is used in Figure 2. 
with a cold body temperature. If they The middle curve in Figure 2 shows 
are tagged and released, they can be re- that the minimum rate of oxygen con- 
captured in good health at subsequent sumption of harvest mice (2.5 cc/g/hr 
trappings, demonstrating that harvest ^or a 9-gram mouse) is reached at the 
mice have a labile body temperature and relatively high ambient temperature of 
can recover trom profound hypothermia. ^^° or 34° C. and that there is almost no 
During the metaboUc tests at 1° C, espe- zone of thermal neutrality. Rate of me- 
cially those with the mouse in a nest, tabolism almost certainly begins to in- 
there was a tendency for most of the crease before 36° C. is reached so that the 
measurements to lie at one level; but zone of minimum metabolism could not 
there would be a few very low readings include more than 3°. The critical tem- 
and a few intermediate readings, pre- perature (33-34°) is remarkably close to 
sumably as the animal entered and the upper lethal temperature. The single 
emerged from the low-metaboUc condi- animal tested at 37° died after two hours 
tion (best shown by the U^-gram mouse at this temperature but provided several 
in Fig. 1). In response to cold coupled good measurements before entering the 



188 



12 

II 
^ 10 

(T 

I 

o 
B 8 

z 
9 7 

I- 

Q. 

2 6 

3 

in 

§5 
o 

z 4 

UJ 

o 

^ 3 

o 




\ 



^"^'f^ONEST 



•NONESr 




8 



9 10 

WEIGHT IN GRAMS 



II 



12 



Fig. 1.— The relation beUveen body weight and rale of oxygen consumption under different conditions, 
showing also the variation in individual measurements. Each cluster or vertical array of points represents 
a series of values obtained from a single individual. 



189 



METABOLISM OF HARVEST MICE 



155 



final coma. Because of the large exposed 
surface of calcium chloride and soda lime 
in the metabolic chamber, relative hu- 
midity was probably low; heat death 
would probably occur at an even lower 
temperature under humid conditions in 
which cooling by evaporation would be 
limited. 



ercd body temperature. Inclusion of 
these low values causes the apparent de- 
crease of the slope of the two curves be- 
tween 12° and 1°. No body temperatures, 
however, dropped to the torpid level. 
Rcithrodontomys megalotis is able to main- 
tain its temperature well above the tor- 
pid level even when sleeping in cold sur- 



I I I I I 



T— r 



10 



_9 

O ' 

z6 

o 

Q. ^ 

z 



THREE MICE 
HUDDLED 



uj ^ 

>• 

X 

o 



r I 






I I I I 
- NOT 
HUDDLED 



r 




p 



•XX 



• 



Xf 



'■■■'■■'■ 



■ ■ ' ■ 



X 



I I I 



BODY 
TEMR^< 
■'''''■■*' 



8 12 16 20 24 

TEMPERATURE °C 



28 



32 



36 



Fig. 2. — The rate of oxygen consumption of resting harvest mice at different temperatures in a nest, 
without nest, and without fur. All three curves have been adjusted, on the basis of the regression Hnes shown 
in Fig. 1, to represent a 9-gram mouse. Triangles indicate rate of oxygen consumption of three mice huddled 
together without a nest compared with the expected rate for the same three mice singly (average weight 
8.5 grams). I am grateful to Martin Murie for supplying the value for deej) body temperature, which was 
the average of manj^ determinations made during the day and night at ambient temperatures between 
14° and 27° C. 



The increase in rate of metabolism at 
cool temperatures is almost linear be- 
tween ?>i° and 12°; each drop of 1° C. 
causes an increase in the rate of oxygen 
consumption of 0.27 cc/g/hr. This rate of 
change, possibly because of the small size 
of harvest mice, is greater than that of 
any of the rodents listed by Morrison and 
Ryser (1951) and by Dawson (1955). The 
averages used for the two points at 1° C. 
include several low values obtained while 
the animals probably had a slightly low- 



roundings. In this respect it differs from 
the pocket mouse {Perognathus longi- 
membris), a mouse with which it should 
be compared because of its similarly 
small size. When pocket mice are caged 
at cold temperatures with adequate 
food, they either drop into torpor or are 
continually awake and active. They may 
even be unable to maintain a high body 
temperature during a prolonged period 
of sleep at cool temperatures (Bartholo- 
mew and Cade, 1957). 



190 



156 



OLRER P. PEARSON 



The only other report on the rate of 
oxygen consumption of harvest mice lists 
a rate of 3.8 cc/g/ hr at 24° C. for mice 
with an average weight of 9.6 grams 
(Pearson, 1948a). This rate is almost 10 
per cent lower than the comparable rate 
obtained from I'lgure 1 and is below the 
range of variation obtained at this tem- 
perature. The difference may be ac- 
counted for by the fact that the mice 
used in the earlier study were acclimated 
to a warmer temperature (for discussion 
of the effect of acclimatization on me- 
tabolism see Hart, 1957). 

INSl'LATING EFFECTIVENESS OF FL'R 

Figure 2 shows also the metabolic ef- 
fect of removing all the fur (277 mg. in 



cent at intermediate temperatures and 24 
per cent at 1° C. (lowest curve in Fig. 2). 
To obtain these measurements, individ- 
ual mice placed in the metabolic chamber 
were provided with a harvest mouse nest 
collected from the wild (shredded grass 
and down from Compositae), and this 
the mouse ciuickly rebuilt into an almost- 
complete hollow sphere about tliree 
inches in diameter. Metabolic rates were 
counted only when a mouse was resting 
Cjuietly deep in the nest. 

THERMAL ECONOMY OF IIIDDLINC, 

The metabolic economy of huddling 
was measured on one occasion with three 
mice at an environmental temperature of 
1° C. without nesting material. The rate 



10 



o 

o 

7 

eh 



/\r~. 



\j 



-VA..AA J V ^V,__ _^ /-v.A/.-/\/v.7 



v^- 



\/ 



\/"^v 



12 I 2 3 4 5 6 7 e 9 10 II 12 I 2 3 4 5 6 7 8 9 10 II 12 

PM AM 

Fig. 3. — Rale of oxygen consumption of a 9-gram harvest mouse for 24 hours at 12° C. 



the single 8.8-gram specimen used) with 
an electric clipper. When calculating the 
points for the curve in Figure 2, 0.28 
grams was added to the naked weight 
and then this rate was adjusted to that 
for a 9-gram animal on the basis of the 
regression lines shown in I'lguie 1. The 
rate of metabolism of the naked mouse 
was about 35 per cent higher at each of 
the temperatures used, and the rate in- 
creased 0.38 cc/g/hr for each 1° C. drop 
in air temperature. 

INSULATING EFFECTIVENESS OF NESTS 

When normal, fully furred mice were 
given an opportunity to increase their in- 
sulation by constructing nests, their met- 
abolic rates were lowered about 17 per 



of metabolism per gram of huddled mice 
was 28 per cent less than it would have 
been for a single one of the mice (Fig. 2). 
The metabolic saving would probably be 
greater when more mice were huddled to- 
gether and less when only two mice were 
huddled, as is true for feral Mus (Pear- 
son, 1947) and laboratory mice (Prychod- 
ko, 1958). 

24-HOUR OXYGEN CONSUMPTION IN CAPTIVITY 

Figure 3 illustrates the rate of oxygen 
consumption of a mouse kept in the ap- 
paratus at 12° C. without nesting mate- 
rial but with food and water for 24 hours. 
The mouse consumed 1,831 cc. of oxygen 
to give an average rate of 8.48 cc/g/hr. 
This is equal to a heat production of 



191 



METABOLISM OF HARVEST MICE 



157 



about 8.8 Calories per day. In agreement sumed during rest and during activity is 
with the fact that activity of harvest proportionately great at warm tempera- 
mice in the wild is greatest shortly after tures and small at cold temperatures, 
dusk (Pearson, 1960), the oxygen con- 
sumption was greatest at that time. The ^^^^^'^ °^- activity on metabolfsm 
prolonged low i)eriod lasting from aljout An athlete is able, for short periods, to 
8:30 to 10:0:) p.m. was unexpected in raise his rate of metabolism to a level 15 
this nocturnal animal. to 20 times his basal rate, but small 
Pearson (1947) used as an indicator of mammals do not match this effort. The 
the noctuvnality of different species the peak metabolic effort of mice running in 
ratio of the total amount of oxygen con- ^ wheel is only 6 to 8 times their basal 
sumed at ni.uht (6:00 p.m. to 6:00 A.m.) rate (Hart, 1950). At (f C. lemmings run- 
to that consumed in the daytime. I'or the ning in a wheel at a speed of 15 cm/sec 
harvest mouse described in Mgure 3, the increase their o.xygen consum[)tion less 
ratio is low- -1.02- but it should be than 35 per cent above the level of rest- 
pointed out that the record was made at ing lemmings (Hart and Heroux, 1955). 
12° C, which is colder than the tempera- At cool ambient temperatures, such as 
ture used for the species in the earlier re- this, small mammals ex[-)end so much 
port. Temperature affects the night/day energy at rest that a considerable amount 
ratio of oxygen consumption because the of activity causes only a proi)ortionately 
ditterence in amount of oxygen con- small increase in oxygen consumption ; 

T.VHLK 1 

'rill'; 24 iiouK ()XV(;i;\ coxsu.nu' rnix fix (( .) of a 9-(;r.\m harv i:si' 

Mousi'. nuKixc; DkckmuI'R axi) Junjc at (:)KIX|)A, Camiokxia 









Willi 






Wilh 






Willi- 


Undcr- 




With- 


Undct- 






out 


.1,'iounci 




out 


{^round 






Xc^l 


Xest 




Xesl 


Xest 


Noclur- 














nal 














haljit 


4 hr. above grouiul 
at l°C.* 


367 


367 


4 hr. above ground 
at 12°C.t 


297 


297 




20 hr. under ground 


1,548 


1,296 


20 hr. under ground 


1,152 


954 




at ]0°C.t 






at 18°C.§ 








Activity correction |! 


+ 119 
2,034 


+ 119 
1,782 cc. 


Activity correction | 


+ 119 
1,568 


+ 119 




1 ,370 cc. 








(8.55 Ca].)# 






(6.58 Cal.),f 


i^iunial 














lialiit 


20 hr. under ground 
at 10°C.| 


1,.548 


1,296 


20 hr. under grounel 
at 18°C.§ 


1,152 


954 




4 lir. above ground 


M3 


3M 


4 hr. above ground 


155 


155 




at6°C.** 






at 25° C. ft 








Activity correctionjl 


+ 119 
2,000 


+ 119 


Activit}' correction] 


+ 119 
1,426 


+ 119 




1 , 748 cc. 


1,228 cc. 








(8.39 Cal.)# 






(5.89 Cal.)# 



* ^fcaii tcniiicrature in runways at time of passage of harvest mite in December. 

t Mean temperature in runways at time of passage of harvest mice in June. 

X Underground temperature in December. 

§ Underground temperature in June. 

II Add 40 per rent of the oxygen consumption on the surface at a temperature of 12° C 

// Assunii-d 4..S ( al. per liler of oxygen. 

*'■ .Mean half-hourly temperature in runways l>etwcen 6 a.m. and 6 P.M. in DeLtmbcr. 

tt Mean half-hoiiily temperature in runways between 6 a.m. and 6 p.m. in June. 



192 



158 OLIVER P. PEARSON 

and at cold temperatures the metabolic 24-hour metabolism in the field 
cost of keeping warm may be so high as The preceding observations indicate 
to leave little or no capacity tor exercise that ambient temperature is a much 
(Hart, 1953). During measurement of the more important variable than activity in 
resting metabolism of harvest mice, nu- the 24-hour energy budget of harvest 
meious measuring periods had to be dis- mice in the wild. By use of automatic de- 
carded because the mouse was moving vices that record the temperature in 
around in the metabolism chamber. Such mouse runway? whenever a mouse passes 
activity rarely raised the oxygen con- by, the temperature encountered by har- 
sumption more than 40 per cent above vest mice during their nightly periods of 
the level of a resting animal at the same activity are known (Pearson, 1960). I 
temperature. During the 24-hour run at have also recorded throughout the year 
12° C, the highest metabolic rate oc- the temperature five inches below the 
curred during an 11-minute period when surface of the ground. This gives an ap- 
the average oxygen consumption was proximation of the temperature encoun- 
10.36 cc/g/hr. This is only 40 per cent tered by the mice while they are in their 
greater than the lowest rate recorded for retreats during the daytime. Some of 
that mouse during any one measuring these surface and underground tempera- 
period. The maximum metabolic effort ture measurements have been used m the 
recorded for any harvest mouse was that calculations summarized m Table L 
of an 8.6-gram mouse at 1° C. This ani- ^ To complete the calculations m Table 
, • ^ 1 • • 1 • J 1, it has been necessary to estimate how 
mal persisted in gnawing, exploring, and , , , ^/^, , 
. , , , , r many hours of each 24 the mouse spends 
trying to escape from the chamber tor /, . r .lu i i u 

•^ ^, V T^ • 1^ • ori the surface of the ground and how 

more than two hours. During one lO-mm- ^^^^ ^^^^^ ^^^ ^^^^^^^ ^^ ^^^^ ^^^^ 

ute period its oxygen consumption aver- ^^^^^^ ^^ j ^^^^ ^^^^ ^^ estimate based 
aged 15.8 cc/g/hr, which is 50 per cent ^^ ^^^ behavior of captive animals and 
higher than the rate of a resting mouse at ^^ automatic recordings made at the exit 
the same air temperature and six times of ^n underground nest box being used by 
the minimum value for the species at ^ild harvest mice. Admittedly this esti- 
thermal neutrahty. This is probably not mate (4 hours on the surface each night) 
far from the peak metabolic effort of the could be wrong by 50 per cent or more, 
species. but it should be noted that an error of 
On several occasions I have watched two hours in this estimate would only 
undisturbed harvest mice carrying on alter the answer (the total 24-hour me- 
their normal activities in the wild, and I tabolism) by about 25 per cent. Assum- 
have been impressed by their leisurely ing that the rate of oxygen consumption 
approach to life. Hard physical labor and during above-ground activity is 40 per 
strenuous exercise must occur quite in- cent higher than the rate of a mouse rest- 
frequently. Most normal activities of ing at 12° C. (see above), the activity 
harvest mice are probably accomplished correction used in Table 1 can be calcu- 
without a rise in metabolic rate more lated. 

than 50 per cent above what it would be In 24 hours in December a harvest 

in a resting animal at the same air tem- mouse uses 8.55 Calories, and in June, 

perature. 6.58 Calories (Table 1), assuming that 



193 



METABOLISM OF HARVEST MICE 



159 



the mouse has the benefit of a nest. A 
nest reduces his daily energy budget by 
about 12 per cent. These estimates of 
daily metabolic demands seem reason- 
able when compared with the values ac- 
tually obtained by measuring the 24-hour 
oxygen consumption of captive animals, 
as reported above. The average metabol- 
ic impact, or daily degradation of en- 
ergy, by a single harvest mouse should be 
somewhere between that in December 
and that in June, perhaps 7.6 Calories. 
This is about the same as that of a hum- 
mingbird in the wild (Pearson, 1954)— 
less than half that of a much heavier 
English sparrow (Davis, 1955). 

BIOENERGETICS 

In seasons when harvest mice are abun- 
dant, there may be twelve of them per 
acre (Brant, 1953). At that population 
density, the species would be dissipating 
at the rate of 91 Calories per acre per day 
the solar energy captured by photosyn- 
thesis, or something like ^ of 1 per cent 
of the energy stored each day by the 
plants in good harvest-mouse habitat in 
the Orinda area. This percentage was cal- 
culated using a net productivity of 
20,000 Cal/acre/day, which was esti- 
mated by assuming 4 Calories per gram 
of dry vegetation (based on data in Brody, 
1945, pp. 35, 788) and an annual crop 
of 1,800 kg. of dry vegetation per acre 
(based on Bentley and Talbot, 1951). 
The harvest mice on this hypothetical 
acre are causing about the same caloric 
drain on the environment as all the small 
mammals in the acre of forest described 
by Pearson (19486). 

By using caloric units, direct compari- 
son can be made of the metabolic impact 
of different species, as in the example 
above. Similarly, the metabolic cost of 
different activities and different habits 
can be compared (Pearson, 1954). For 



example, harvest mice are strongly noc- 
turnal (Pearson, 1960), in spite of the 
fact that air temperatures are much 
colder at night and force mice to con- 
sume more oxygen and more food than if 
they were diurnal. Since evolution has 
permitted nocturnahty to persist, it 
seems logical to assume that the value of 
nocturnality to harvest mice is greater 
than the metabolic cost. I estimate that 
during a 24-hour period in December a 
9-gram harvest mouse uses 0.16 more 
Calories by being nocturnal than it 
would if it were diurnal (Table 1). In 
summer, the difference is even greater, 
0.69 Calories. The average is 0.42 Cal- 
ories, or about 3| grains of wheat. This is 
a rough estimate of the price each har- 
vest mouse pays for nocturnality. Some 
environmental pressure makes harvest 
mice remain nocturnal, and this pressure 
must be more than 0.42 Calories per 
mouse per day. If harvest-mouse noc- 
turnality evolved for one reason only— to 
avoid predation by hawks — -then we 
would have discovered a minimum esti- 
mate of the predation pressure of hawks 
on harvest mice. Surely the situation is 
not this simple; nevertheless, it is inter- 
esting to measure the pressure that 
makes harvest mice nocturnal even if the 
cause of the pressure is not known. 

SUMMARY 

Oxygen consumption of harvest mice 
reaches a minimum of 2.5 cc/g/hr at an 
ambient temperature of 33° C, and the 
zone of thermal neutrality is not more 
than 3°. Each drop of 1° in ambient tem- 
perature causes an increase in the rate of 
metabolism of 0.27 cc/g/hr. Removing 
the fur raises the rate of metabolism 
about 35 per cent, and use of a nest 
lowers it 17 to 24 per cent. Huddling by 
three mice at 1° reduces the rate 28 per 
cent. 



194 



160 



OLIVER P. PEARSON 



Jvxcrcise at cool tcm{)eraturcs causes a 
relatively small increase in the rate o£ 
metabolism, whereas change of ambient 
temperature has a great effect! Making 
use of the temperatures that harvest mice 
are known to encounter in the wild, the 
24-hour oxygen consumption of a wild 
harvest mouse was calculated to be 1,782 
cc. in December and 1,370 cc. in June. 
The average (1,576 cc.) is equivalent to 



about 7.6 Calories per day. A dense p(Jp- 
ulation of harvest mice would dissipate 
about 91 Calories per day per acre, which 
is about ^ of 1 per cent of the energy 
stored by the plants each day. 

By being nocturnal, harvest mice en- 
counter cooler temperatures, and this 
habit increases the daily energy budget 
of each mouse by 0.42 Calories, or about 
3| grains of wheat. 



LITERATURE CITED 



Bartholomew, G. A., and C.a.de, T. J. 1957. Tem- 
])erature regulation, hibernation, and aestivation 
in the little pocket mouse, Perognatlnts longintem- 
bris. Jour. Mammal., 38:60-72. 

Bentley, J. R., and T.^lbot, M. W. 195L Efficient 
use of annual plants on cattle ranges in the 
California foothills. U.S. Dept. .Agriculture, Cir- 
cular No. 870, 52 pp. 

Brant, D. H. 1953. Small mammal populations near 
Berkeley, California: Reithrodontomys, Peromys- 
cus, Microtus. Doctoral thesis, University of Cali- 
fornia, Berkeley. 

Brody, S. B. 1945. Bioenergetics and growth. New- 
York: Reinhold Publishing Corp. 

D.xvis, E. A., Jr. 1955. Seasonal changes in the 
energy balance of the English Sparrow. Auk, 
72:385-411. 

Dawson, VV. R. 1955. The relation of oxygen con- 
sumption to temperature in desert rodents. Jour. 
Mammal., 36:543-53. 

De Bont, A.-F. 1945. Metabolisme de repos de 
quelques es])eces d'oiseaux. .Ann. Soc. Roy. Zool. 
Belgique, 75 (1944) :75-80. 

Hart, J. S. 1950. Interrelations of daily metabolic 
cycle, activity, and environmental temperature 
of mice. Canadian Jour. Research, D, 28:293- 
307. 

. 1953. The influence of thermal acclimation 

on limitation of running activity by cold in 
deer mice. Canadian Jour. Zool., 31:117-20. 



. 1957. Climatic and temperature induced 

changes in the energetics of homeotherms. Revue 
Canadienne de biol., 16:133-74. 

Hart, J. S., and Heroux, O. 1955. Exercise and 
temperature regulation in lemmings and rabbits. 
Canadian Jour. Biochem. & Physiol., 33:428-35. 

Morrison, P. R. 1947. An automatic api)aratus 
for the determination of oxygen consumption. 
Jour. Biol. Chem., 169:667-79. 

Morrison, P. R., and Ryser, F. .\. 1951. Tempera- 
ture and metabolism in some Wisconsin mam- 
mals. Federation Proc, 10:93-94. 

. 1959. Body temperature in the white-footed 

mouse, Peromyscus leiicopus noveboracensis. Phvs- 
iol. Zool., 32:90-103. 

Pearson, 0. P. 1947. The rate of metabolism of some 
small mammals. Ecology, 28:127-45. 

. 1948a. Metabolism of small mammals, with 

remarks on the lower limit of mammalian size. 
Science, 108:44. 

. 19486. Metabolism and bioenergetics. Sci- 



entific Monthly, 66:131-34. 

. 1954. The daily energy requirements of 

a wild Anna Hummingbird. Condor, 56:317-22. 
1960. Habits of harvest mice revealed by 



automatic photographic recorders. Jour. Mam- 
mal, (in press). 
Prychodko, W. 1958. Effect of aggregation of labo- 
ratory mice {Mus musculus) on food intake at 
different temperatures. Ecology, 39:500-503. 



Reprinted for private circulation from 
PHYSIOLOGICAL ZOOLOGY 

Vol. XXXIII, No. 2, April 1960 

Copyright 1960 by the University of Chicago 



195 



OXYGEN CONSUMPTION, ESTIVATION, AND HIBERNATION IN 
THE KANGAROO MOUSE, MICRODIPODOPS PALLIDUS^ 

GEORGE A. BARTHOLOMEW AND RICHARD E. MacMILLEN 

Departments of Zoology, University of California, Los Angeles, 
and Pomona College, Claremont, California 

THE pallid kangaroo mouse occurs material and methods 
only in the desert parts of western Experimental animals— The twenty- 
Nevada and extreme eastern Call- ^^iree kangaroo mice used were trapped 
fornia. Its habitat is restricted to areas of ^^ ^^^^ ^^^^^ f^^^ rniles south of Arle- 
fine sand which support some plant ^^^^ Ranch, Esmeralda County, Neva- 
growth. Like its relatives, the kangaroo ^^^ j^^ ^pj.-^^ ^959^ ^nd May, 1960. They 
rats (Dipodomys) and the pocket mice ^^^^ housed individually in small ter- 
{Perognathus) , it is nocturnal, fossorial, ^^^^^ p^^^^y ^^g^j ^ith ftne sand, kept in a 
and gramnivorous and can under some ^indowless room on a photoperiod of 12 
circumstances live indefinitely on a dry j^^^j.^^ ^^^ f^^ ^^ ^ ^i^^ of j^ixed bird 
diet without drinking water. The genera] ^^^^ supplemented occasionally with 
life history (Hall and Linsdale, 1929) of ^^^-^^ p^g^g^ ^f cabbage. Survival was 
this kangaroo mouse and the details of excellent, and some of the animals were 
its distribution (Hall, 1946) are known, ^^^^ f^j. ^^gj. ^g^^ months, 
but virtually no quantitative data on its ^^^y temperatures— AW temperatures 
physiology are available. ^g^g measured with 30-gauge copper- 
The present study was undertaken to gonstantan thermocouples connected to 
compare the thermoregulation of Micro- ^ recording potentiometer. All body tem- 
dipodops with that of the better-known pg^atures were taken orally by inserting 
genera, Dipodomys and Perognathus. ^ thermocouple to a depth of at least 
These three genera belong to the family 2 cm 

Heteromyidae, which has been more sue- Ambient temperatures— The ambient 

cessful in occupying the and parts of tgn^pg^atures were monitored with ther- 

Tof'of mTmrnalT''''^ ^^^"^ ^""^ *'^^'' "^«^«^P^^^ ^^^ controlled by insulated 
^ P ^ ■ chambers equipped with automatic heat- 

1 This study was aided in part by a contract be- ing and cooling units, blowers, and 
tween the Office of Naval Research, Department of Uahts 
the Navy, and the University of California (Nonr ° ' • r\ 

266[3ll). Oxygen consumption. — Oxygen con- 

177 



196 



178 



GEORGE A. BARTHOLOMEW AND RICHARD E. MacMILLEN 



sumption was measured by placing a 
mouse in an air-tight 500-cc. glass con- 
tainer equipped with a thermocouple and 
ports for the introduction and removal 
of air. The bottom of the container was 
covered to a depth of about 1 cm. with 
fine dry sand. The glass container with 
animal inside was placed in a tempera- 
ture-control chamber, and dry air was 
metered through the container at a rate 



the response of body temperature {Tb) 
to moderately low ambient temperatures 
{Ta), kangaroo mice were placed at Ta 
of 7°-9° C. for five days starting May 11, 
1959, with food available in excess; 
measurements of Tb were made at 24- 
hour intervals. There were no apparent 
changes in Tb during the test period, nor 
was the mean Tb significantly different 
from that of animals maintained at room 



42 
o 

o 

q: 40 
iij 



i 38 

ffi 



36 



o 

o 
I 



o 

o 

I 
^. 

OJ 
CO 



B 



o 

o 

in 

in" 

to 

I 

If) 

^" 
ro 



D 



o 

o 
lO 

d 

I 
m 

ro 



42 



40 



38 



36 



Fig. 1. — Body temperatures of M. pallidus at various ambient temperatures. A, 47 measurements on 
twelve animals; B, 38 measurements on thirteen animals; C, 7 measurements on four animals; D, 9 measure- 
ments on four animals (three other animals tested at this temperature died). The horizontal lines indicate 
the means {M). The rectangles inclose M ± a^- The vertical lines indicate the range. 



of 250 cc/min and then delivered to a 
Beckman paramagnetic oxygen analyzer 
which, used in conjunction with a re- 
cording potentiometer, gave a continu- 
ous record of oxygen consumption. All 
data used were from post-absorptive 
animals. 

RESULTS 

Body temperature during normal ac- 
tivity. — Normally active animals kept at 
room temperature (22.4°-25.4° C.) had 
body temperatures ranging from slightly 
less than 37° to as high as 41° C, with 
a mean of 38.8° C. (Fig. 1). To determine 



temperature. The animals appeared nor- 
mally active and unaffected by the 
change in environmental temperature. 

Animals were maintained at Ta of 
37.5°-40.5° C. for 24 hours to test their 
response to moderately high environ- 
mental temperatures. They showed a 
conspicuous elevation in Tb with a mean 
almost 2° C. higher than that of animals 
at room temperature. Animals main- 
tained at Ta close to 35° C. also became 
hyperthermic and showed a mean Tb in- 
termediate between that of animals held 
at room temperatures and those held at 
39° C. There was no mortality in animals 



197 



THERMOREGULATION IN THE KANGAROO MOUSE 



179 



held at 35° C, but exposure to 39° C. for 
more than a few hours killed three out of 
the seven animals tested. At a high Ta 
the kangaroo mice did not salivate or 
pant; they merely sprawled out fiat on 
the sand with legs extended and lower 
jaw and neck prone on the substrate. 
This prone posture alternated with brief 
bursts of intense activity characterized 
by repeated shifts in position and much 
digging and moving of sand. 



gm.) is 1.8 cc 02/gm/hr when the for- 
mula M = 3.811^-'' " jg ygg(j (^ggg Brody, 

1945, and Morrison, Ryser, and Dawe, 
1959). The observed basal metabolism 
of our kangaroo mice (mean, 1.3 ± 0.2 
cc 02/gm/hr) was about three-fourths 
of the predicted value. This relatively 
low figure is consistent with the obser- 
vation on some other heteromyids (Daw- 
son, 1955). 

The only comparative data on the 



a: 

X 



o 
o 



-|4 



•• 












• • 



• • • 

• • • 

• • • 



10 



20 



30 



40 



Fig. 2. — The relation of oxygen consumption to ambient temperature. Data obtained from ten animals. 
Each point represents the minimum level of oxygen consumption maintained by an animal for half an hour. 
Oxygen volumes are corrected to 0° C. and 760 mm. (Hg.) pressure. 



Oxygen consumption. — The relation of 
oxygen consumption to Ta is summarized 
in Figure 2. There is no clearly defined 
zone of thermal neutrality, but oxygen 
consumption is minimal at about 35° C. 
The increase in oxygen consumption at 
temperatures above 35° C. is relatively 
more rapid than is the increase below 
this point of thermal neutrality. No dif- 
ferences in oxygen consumption were ap- 
parent between males and females. 

The calculated metabolism of Micro- 
dipodops paUidus (mean weight, 15.2 



energy metabolism of Microdipodops is 
that of Pearson (1948) on M. megacepha- 
lus. Pearson's data, obtained at tempera- 
tures near 24° C. from animals that were 
not post-absorptive, gave oxygen con- 
sumptions of 3.4-3.7 cc 02/gm/hr. Pear- 
son's measurements, as might be expect- 
ed from the fact that he was not using 
post-absorptive animals, are higher than 
our determinations of 2.7 cc 02/gm/hr 
at 25° C. 

Hibernation and estivation. — No infor- 



198 



180 



GEORGE A. BARTHOLOMEW AND RICHARD E. MacMILLEN 



mation on hibernation or estivation is 
available for Microdipodops. Hall (1946, 
p. 386) pointed out that kangaroo mice 
are often active above ground in temper- 
atures many degrees below freezing, and 
Ingles (1954, p. 214) suggested that 
kangaroo mice probably do not hiber- 
nate. 

Under laboratory conditions we found 
that kangaroo mice at any time of year 



40 r 



there are no conspicuous physiological 
differences between arousal from spon- 
taneous dormancy and that from induced 
dormancy. 

Animals dormant at room tempera- 
tures (estivating) started to arouse im- 
mediately upon being handled. The rate 
of increase in Tb varied but usually fell 
between 0.5° and 0.8° C. per minute. 
Usually within 20 minutes of the onset 



-.40 




10 20 30 40 50 

MINUTES FROM START OF AROUSAL 

Fig. 3. — Increases in oral temperatures in nine kangaroo mice during arousal from torpor. All arousals 
took place in ambient temperatures between 23° and 26° C. Temperatures taken manually with thermo- 
couples. The five upper animals were dormant at room temperature (22°-25° C); the four lower animals 
were dormant at 5°-8° C. 



will spontaneously become dormant at 
ambient temperatures ranging at least 
from 5° to 26° C. and can readily be in- 
duced to hibernate (or estivate) over this 
range of temperatures by reduction of 
food for 24 hours or less. 

Body temperature and behavior dur- 
ing entry into torpor were not recorded, 
but the animals apparently entered tor- 
por in the crouching posture normally 
used in sleeping. Dormant animals had 
body temperatures l°-2° C. above am- 
bient. Judging from the course of body 
temperature during arousal from torpor, 



of arousal the animals attained their nor- 
mal operating temperature, and within 
as little as 12-15 minutes from the start 
of arousal they appeared to behave nor- 
mally, even though Tb approximated 
30° C. Arousal from low temperatures 
was essentially the same as arousal from 
high temperatures (Fig. 3). However, 
animals arousing from low temperatures 
attained maximal body temperatures 
about 1° C. higher than did those arous- 
ing from room temperature. 

Incidental to the measurement of Tb 
the relations of various types of behavior 



199 



THERMOREGULATION IN THE KANGAROO MOUSE 181 

to body temperature were noted during mals the ability to become dormant and 

nine arousals. Mice unsuccessfully at- to decrease body temperature and meta- 

tempted to right themselves when turned bolic activity may be more useful in the 

over at Tb between 16.1° and 18.2° C. summer than in the winter, and it may 

and successfully righted themselves at be as important for water conservation 

Tb between 19.0° and 22.0° C. The first as for energy conservation, 

vocalizations were given at Tb between Kangaroo mice are unique among 

24.7° and 28.6° C. Grain was available heteromyids in having conspicuous de- 

to the animals during arousal, and seven posits of adipose tissue in the proximal 

of the nine animals ate during arousal, third of the tail, which is considerably 

The lowest Tb for eating was 25.5° C, larger than either its base or its distal 

and three animals ate at temperatures half. Hall (1946, p. 379) suggests that the 

between 25° and 29.4° C. The mean Tb fleshiness of the tail permits it to func- 

for onset of visible shivering for seven tion in balancing. However, since these 

animals was 25.5° C. Two of the nine mice hibernate but do not show conspicu- 

animals observed did not visibly shiver ous seasonal deposits of subcutaneous fat 

during arousal. Shivering usually stopped over the body as a whole, it seems reason- 

at a Tb of 34°-35° C . able to suggest that the fat tail serves as 

a reserve of energy for use during periods 

DISCUSSION q£ torpor. In the laboratory with food 

The general features of thermoregula- available in excess, many of the kangaroo 

tionin Microdipodops pallidus dirtsirmlzr mice showed a marked increase in tail 

to those of the related genus Perognathus diameter. 

in that both show well-developed pat- Our data (Fig. 1) show almost no in- 
terns of hibernation and estivation, es- dication of a discrete zone of thermal 
sentially normal behavior at Tb below neutrality for the kangaroo mouse. Its 
35° C, obligate hyperthermia at Ta critical temperature is unusually high for 
above 35° C, and no apparent salivary an animal living in an area characterized 
response to elevated body temperature, by cold winters. For months on end kan- 
Microdipodops differs from the related garoo mice can be active only at tempera- 
genus Dipodomys in that the latter does tures below thermal neutrality. Presum- 
not readily become dormant at either ably, their energetic and thermal prob- 
high or low temperatures and does use lems are reduced in cold weather by pe- 
salivation as an emergency thermoregu- riodic episodes of torpor. It is of interest 
latory response (Schmidt-Nielsen and that we captured our animals on nights 
Schmidt-Nielsen, 1952). when environmental temperatures went 

In kangaroo mice, as in Perognathus below —10° C, and Hall (1946, p. 396) 

longimemhris (Bartholomew and Cade, reports that these animals are often "ac- 

1957) and Citellus mohavensis (Bartholo- tive on nights when the temperature is so 

mew and Hudson, I960-), there appears to low as to freeze to a state of stiffness the 

be no sharp physiological differentiation bodies of mice caught in traps." Thus, al- 

between hibernation and estivation. This though they can hibernate, they are 

underscores the point that the faculta- also commonly active during subfreezing 

tive hypothermia shown by mammals weather. 

should not be thought of only as an adap- This species has remarkably shallow 

tive response to low environmental tem- burrows, often no deeper than 4 inches 

peratures; at least for small desert mam- (Hall, 1946, p. 396). Consequently, when 



200 



182 GEORGE A. BARTHOLOMEW AND RICHARD E. MacMILLEN 

high daytime temperatures occur, at in Microdipodops correlates nicely with 
least some members of the population its strong tendency toward hyperthermia 
may be exposed to temperatures near at high ambient temperatures. For ani- 
35° C. It is possible, therefore, that the mals living in a desert environment 
high point of thermal neutrality of this where water is usually in short supply, 
species allows a significant metabolic hyperthermia is a more advantageous re- 
economy and a significant reduction in sponse to heat than is evaporative cool- 
pulmocutaneous water loss during the ing. 
severely hot desert summers. summary 

Extrapolation of the plot of metabo- Microdipodops pallidus occurs only on 
lism against ambient temperature below gp^^g^iy vegetated sand dunes in the 
thermal neutrality does not intersect the ^^^^^^ ^^^^^ ^^ western Nevada and 
abscissa within the usual range of body ^^^^^^^ California. In the absence of 
temperature (38°-39°C.) of kangaroo ^-gj^pei-ature stress body temperature, 
mice (Fig. 2). This means that, unlike j^ averages 38.8°C. There is no diminu- 
some of the species considered by Scho- ^j^^ ^^ j.^ ^^-^^^ decreasing ambient tem- 
lander et al. (1950), and unlike the perature, T^, at least to 8° C. However, 
masked shrew, Sorex cinereus (Morrison, hyperthermia is apparent at a Ta of 
Ryser, and Dawe, 1959), the kangaroo 350 ^ ^^^ ^^ 390 ^ j^^ averages 40.5° C. 
mouse does not follow Newton's empiri- E^pos^re for more than a few hours to 
cal law of cooling in a simple and direct 390 ^ j^ ^^^^^ lethal. At high ambient 
manner. The failure to follow the pattern temperatures kangaroo mice neither 
predicted by Newton's law of cooling p^^^ ^^^ ^^^^^ ^j^^y ^^^^ no clearly de- 
may be related to the fact that kangaroo ^^^^ ^^^^ ^f thermal neutrality; oxygen 
mice start to become hyperthermic as consumption is minimal at 35° C. and in- 
they approach their critical temperature ^^^^^^^ ^lore rapidly at temperatures 
(Fig. 1), and it suggests that the relation ^^^^^ ^^^^ ^^-^^^ ^^^^ ^^i^^ it. Basal 
between skin and ambient temperature ^letabolism is 25 per cent less than that 
in this species differs from the usual pat- pj-g^i^ted on the basis of body size. Kan- 
tern. It is of interest that Pearson's data ^^^^^ ^^^^ ^^^ capable of both estivation 
(1960) for Reithrodontomys show a situa- ^^^ hibernation. In the laboratory they 
tion similar to that reported here for ^^^^^ become dormant at ambient tem- 
Microc^z>(^o^5, that is, almost no zone of pg^atures ranging at least from 5° to 
thermal neutrality, a high critical tem- 25° c. The rate of temperature increase 
perature, and a failure of the curve of ^^^j^^g arousal at room temperature is 
metabolism against ambient temperature 5o__0.8°C. per minute. Terminal body 
to intersect the abscissa at the usual body temperatures after arousal from low tem- 
temperature. Although Pearson does not pej-^tures averaged about 1° C. higher 
comment on this point, it appears that in ^^iQ^n after arousal from room tempera- 
Reithrodontomys as in Microdipodops the ^^^.g gy ^^g time the Tb of arousing ani- 
curve of metabolism against ambient ^lals reaches 30° C, their behavior ap- 
temperature intersects the abscissa at a pears normal. The thermoregulatory re- 
point above the lethal temperature for sponses of kangaroo mice are compared 
the species. with those of other desert heteromyids. 
The apparent absence of a marked in- and the ecological significance of their 
crease in salivation at high temperatures physiological capacities is discussed. 



201 



THERMOREGULATION IN THE KANGAROO MOUSE 



183 



LITERATURE CITED 



Bartholomew, G. A., and Cade, T. J. 1957. Tem- 
perature regulation, hibernation, and aestivation 
in the Uttle pocket mouse, Perognatlms longimem- 
bris. Jour. Mamm., 38:60-72. 

Bartholomew, G. A., and Hudson, J. W. 1960. 
Aestivation in the Mohave ground squirrel, Citel- 
lus mohavensis. Bull. Mus. Comp. Zool., 124:193- 
208. 

Brody, S. 1945. Bioenergetics and growth. New 
York: Reinhold Publishing Co. 

Dawson, W. R. 1955. The relation of oxygen con- 
sumption to temperature in desert rodents. Jour. 
Mamm., 36:543-53. 

Ingles, L. G. 1954. Mammals of California and its 
coastal waters. Stanford, Calif.: Stanford Univer- 
sity Press. 

Hall, E. R. 1946. Mammals of Nevada. Berkeley: 
University California Press. 

Hall, E. R., and Linsdale, J. M. 1929. Notes on 
the life history of the kangaroo mouse {Microdi- 



podops). Jour. Mamm., 10:298-305. 

Lyman, C. P., and Chatfield, P. 0. 1955. Physiol- 
ogy of hibernation in mammals. Physiol. Rev., 
35:403-25. 

Morrison, P., Ryser, F. A., and Dawe, A. R. 1959. 
Studies on the physiology of the masked shrew 
Sorex cinereus. Physiol. Zool., 32:256-71. 

Pearson, 0. P. 1948. Metabolism of small mam- 
mals, with remarks on the lower limit of mam- 
malian size. Science, 108:44. 

. 1960. The oxygen consumption and bio- 
energetics of harvest mice. Physiol. Zool., 33: 
152-60. 

Schmidt-Nielsen, K., and Schmidt-Nielsen, B. 
1952. Water metabolism of desert mammals. 
Physiol. Rev., 32:135-66. 

Scholander, p. F., Hock, R., Walters, V., John- 
son, F., and Irving, L. 1950. Heat regulation in 
some arctic and tropical mammals and birds. 
Biol. Bull., 99:237-58. 



Reprinted for private circulation from 
PHYSIOLOGICAL ZOOLOGY 

Vol. XXXIV, No. 3, July 1961 
Copyright 1961 by the University of Chicago 

PRINTED IN U.S.A. 



202 



Counter-Current Vascular Heat Exchange in the Fins of Whales^ 



p. F. SCHOLANDER and WILLIAM E. SCHEVILL. From the Woods Hole 
Oceanographic Instilution, Woods Hole, Afassaclmsetts 



IT MAY BE a source of wonder that whales 
swimming about in the icy waters of the 
polar seas can maintain a normal mam- 
malian body temperature. What prevents 
them from being chilled to death from heat loss 
through their large thin fins?- These are well 
enough vascularized to justify the question 
(fig. i). One may conjecture that a whale may 
be so well insulated by its blubber that it needs 
such large surfaces to dissipate its heat. On the 
other hand, if heat conservation is at a pre- 
mium, there must be some mechanism whereby 
the fins can be circulated without losing much 
heat to the water. One may point to two 
circulatory factors which would reduce the heat 
loss from the fin: a) slow rate of blood flow 
and, 6) precooling of the arterial blood by veins 
before it enters the fin. 

Bazett and his coworkers (i) found that in 
man the brachial artery could lose as much as 
3°C/decimeter to the two venae comitantes. 
This simple counter-current exchange system 
is a mere rudiment compared to the multi- 
channelled arteriovenous blood vascular bun- 
dles which we find at the base of the extremities 
in a variety of aquatic and terrestrial mammals 
and birds. These long recognized structures 
have most recently been studied by Wislocki 
(2), Wislocki and Straus (3) and Fawcett (4). 

The function of these bundles has long been 
a mystery. No matter what else they do, they 
must exchange heat between the arteries and 
veins, and it has been pointed out that they 
very likely play an important role in the pres- 
ervation and regulation of the body heat of 
many mammals and birds (5). 

In the present study we describe a conspic- 
uous arteriovenous counter-current system in 
the fins and flukes of whales, which we interpret 
as organs for heat preservation. 

Received for publication July 21, 1955. 

' Contribution Number 807 from the Woods Hole 
Oceanographic Institution. 

^ In 'fin' we include the structures more specifically 
called flippers (pectoral fins), flukes (caudal fins) and 
dorsal fin. 



MATERIAL 

Two species of porpoises have been studied : Lageno- 
rliynclius aculits: dorsal fin, tail-fluke, and flipper of 
an adult female collected 50 miles east of Cape Cod; 
Tursiops tnmcatus: dorsal fin and tail-fluke of a 4- 
month-old calf from Florida, supplied through the 
courtesy of the Marineland Research Laboratory. 

Lagenorhynchiis is a genus of fairly high latitudes, 
the southern limit of L. acutns being about latitude 
4i°N. on the New England coast and about 55°N. in 
the British Isles. It has been caught at least as far 
north as latitude 64°N. in west Greenland and Nor- 
wegian waters. Tursiops is found in lower latitudes, 
T. truncalus overlapping slightly with L. aciihts and 
occurring south into the tropics. 

DESCRIPTION 

Figure 2 illustrates the vascular supply at 
the base of the dorsal, pectoral and caudal fins. 
It may be seen that all major arteries are 
located centrally within a trabeculate venous 
channel. This results in two concentric con- 
duits, with the warm one inside. In addition 
to the circumarterial venous channels there are 
separate superficial veins, as seen in figure 2. 
The circumarterial venous channels are con- 
spicuously thin walled compared to the simple 
veins, as may be seen in figure 3. When an 
artery was perfused with saline, the solution 
returned through both of these venous systems. 

INTERPRETATION 

Based on the anatomical findings and on the 
perfusion experiments, we interpret the artery- 
within-vein arrangement as a heat-conserving 
counter-current system, as schematically pre- 
sented in fig. 4. In such an arrangement the 
warm arterial blood is cooled by the venous 
blood which has been chilled in the fin. The 
result is a steep proximodistal temperature 
drop from the body into the appendage. The 
heat of the arterial blood does not reach the 
fin, but is short-circuited back into the body in 
the venous system. Body heat is therefore 
conserved at the expense of keeping the appen- 
dage cold. There is reason to believe that the 
analogous blood vascular bundle in the proxi- 



279 



203 



28o 



p. F. SCHOLANDER AND WILLIAM E. SCHEVILL 



Volume S 




Fig. I. Arterial supply to the flukes in the common 
porpoise {Plincoena phocnena), drawn from an x-ray 
l^icture by Braun (6). 

mal part of the extremities of sloths serves a 
similar function, inasmuch as these animals 
can barely keep warm even in their warm 
environment (5). Cold extremities have been 
described in many arctic mammals and birds 
as important factors for conservation of body 
heat (7), but to what extent arteriovenous 
counter-current structures are present in these 
animals is not known. 

The efficiency of heat exchange in a system 
like that diagrammed in figure 4 is related to 
the blood flow. The slower the flow, the more 
nearly identical will be the arterial and venous 
temperatures along the system, and the more 
efficient will be the heat conservation. At high 
rates of flow, warm blood will reach the periph- 



ery and cool venous blood will penetrate into 
the body.'' 

It was shown by perfusion experiments on 
the detached fins that the arterial blood may 
return via the concentric veins, and/or through 
the separate superficial veins. As pointed out 
above, the concentric vein channels are very 
thin walled and weak compared to the thick- 
walled superficial veins (fig. 3). One may inter- 
pret these anatomical facts in the following 
way. If the animal needs maximal heat con- 
servation, blood circulation through the fins 
should be slow, and the venous return should 
preferentially take place through the counter- 
current veins. But a slow rate of blood flow 
would need only weak venous walls, as actually 
found. If, on the other hand, the animal needed 
maximal cooling, as during exercise in rela- 
tively warm water, this would be most effec- 
tively accomplished by a high rate of blood 
flow through the fins, with venous return 
through the superficial veins and the least 
possible flow through the concentric veins. 
This would require the strong and thick walls 
of the superficial veins. One may even see the 
likelihood of a semiautomatic regulatory func- 
tion in the concentric system, for when the 
artery is swelled by increased blood flow, the 
concentric veins will be more or less obliterated, 



^ The theory for a multichannel counter-current 
system has been elaborated in connection with the 
swimbladder in deep sea fishes (8). 



L. CAUDAL 

„I1„„IIU. .1 iv II,,.. |i»i 



DORSAL 




r— 1 >— I 1 1 

O CEMTIMETERS .S 



TUR5I0P5 TRUhCflTUS 



L.PECTORflL 




mmumasssiiiiMsamm 



LAGEMORHYMCHU^ AOUTUS 



Fig. 2. Sections near base of 
fins and flukes of two species of 
jiorpoises. Each artery is sur- 
rounded by a multiple venous 
channel. Simple veins are near the 
skin (only the larger ones are indi- 
cated). 



204 



COUNTER-CURRENT HEAT EXCHANGE IN W HAEE FINS 



281 













Fig. 3. Sections from Tursiops Inincatus. (Courtesy of the Department of Anatomy. Harvard Medical School.) 
A. From tail-fluke. Upper: artery surrounded by thin-walled venous channels. Lower: superficial single thick- 
walled vein in the hypodermis. (X 9) B. From dorsal fin. Artery surrounded hy thin-walled venous channels (X 12) 



but will remain open when the diameter of the 
artery is reduced during decreased blood flow. 
Thus the anatomical findings fit logically into 
the simplest possible scheme of heat regulation 
in the fins. 

There are a few observations available in- 
dicative of heat regulation in the fins of por- 
poises. Tomilin (g) made some observations 
on an east Siberian 'white-sided dolphin' on 
deck, and found that the fins could vary be- 
tween 25° and 33. 5°C, while the body varied 
only 0.5°. Schevill observ^ed that the flukes in 
a Florida Tursiops out of water became about 
10° warmer than the body surface itself. In 
both of these cases the animals were probably 
resisting overheating. On the other hand, 
Scholander (5) has recorded cold flippers in 
water-borne common porpoises (Phocoena). 

The concentric counter-current system of 
an artery within a vein appears to be a pecu- 
liarly cetacean arrangement, and we have seen 
it only in the fins, flippers and flukes of these 
animals."* This is an impressive example of 
bioengineering, which, together with other 




TRUNK 



29" 






39° 



h;^////>//,',7/]///////////^/////////^;//7777. 
ARTERY-«4-iO° 20° 30° 40° -- 





■* The present material is from odontocetes, Ijut 
these structures have also been noted by Scholander 
in the tail flukes of a mysticete (fin whale). 



>:::^ TRUNK 



Fig. 4. Schematic diagram of hj^iothetical tempera- 
ture gradients in a concentric counter-current system. 

factors, adapts these homeotherms for a suc- 
cessful existence in a heat-hungry environment. 

SUMM.'^RY 

The vascular supply to the fins and flukes 
of two species of porpoises, Lagenorhynchus 
aciitus and Tursiops truncalus, is described. 
All major arteries entering the fins and flukes 



205 



282 



1'. F. SCHOLANDER AND WILLIAM E. SCHEVILL 



Volintie 8 



are surrounded by a trabeculate venous chan- 
nel. The arteries drain into these, but also into 
superlicial simple veins. The artery within the 
venous channel is interpreted as a heat-con- 
serving counter-current exchange system. The 
heat regulatory aspects of the two venous 
systems are discussed. 

We wish to express our appreciation to Dr. F. G. 
Wood, Jr., and the Marineland Research Laboratory, 
Marineland, Fla., for providing the material of Tur- 
siops tnmcatus, and to Dr. G. B. Wislocki of the Dept. 
of Anatomy, Harvard Medical School, Boston, Mass., 
for providing the histological sections and photographs. 



REFERENCES 

1. B.\ZETT, H. C, L. Love, M. Newton, L. Eisen- 
BERG, R. Day and R. Forster II. J. Appl. 
Pliysiol. 1 : 3, 1948. 

2. Wislocki, G. B. /. Morpliol. 46: 317, 1928. 

3. Wislocki, G. B. and W. L. Straus, Jr. Ball. Mus. 
Comp. Zool. Harvard 74: i, 1933. 

4. Fawcett, D. W. J Morphol. 71: 105, 1942. 

5. ScHOLANDER, P. F. Evolution 9: 15, 1955. 

6. Braun, M. Zool. Anz. 29: 145-149, 1905. 

7. Irving, L. and J. Krog. J. Appl. Pliysiol. 7: 355, 

1955- 

8. Scholander, p. F. Biol. Bull. 107: 260, 1954. 

9. ToMiLiN, A. G. Rybnoe Khozaistvo 26: 50, 1950. (In 

Russian.) 




206 



SECTION 3— REPRODUCTION AND DEVELOPMENT 

Just as animal structures must be adaptive, so must reproductive and devel- 
opmental patterns. In other words, the organism must be a functioning unit in 
its particular environment at all times. In our selections, Spencer and Steinhoff 
discuss the possible functional significance of geographic variation in litter 
size, and Sharman points out the adaptive value of some peculiarities of kan- 
garoo reproduction. The interrelationships of reproductive and developmental 
patterns in the fisher are evident in the account by Wright and Coulter. Super- 
fetation ( or the fertilization of new ova during gestation, known in kangaroos, 
rabbits, and some rodents), delayed implantation (which occurs in some 
mustelids), and delayed fertilization (through sperm storage, known in some 
bats) all are interesting variations of the reproductive theme, and all are 
adaptive in certain circumstances. A recent study of reproductive adaptations 
of the red tree mouse by Hamilton ( 1962, not reprinted here ) related small 
litters, long gestation, delayed implantation during lactation, and slow develop- 
ment of young with the limited amount of energy available in the food sources 
of the mice. The study here reproduced by Jones on the evening bat relates 
development to function, in this case flight, and also nicely illustrates some 
quantitative refinements that adequate data provide. 

The student of any field is well advised to learn what compilations, summa- 
ries, or collected works are available. Sometimes a summary is short, as is the 
paper by Hamilton included herein on reproductive rates of some small mam- 
mals. In the field of mammalian reproduction, the classic summary by Asdell 
(as revised in 1964), and recent collections of contributions edited by Enders 
( 1963) on delayed implantation and by Rowlands ( 1966) on comparative biol- 
ogy of mammalian reproduction will repay study. 

Two classic books in the field of development in which relative growth 
rates were considered at length are On Growth and Form by D'Arcy Went- 
worth Thompson (1942) and Problems of Relative Growth by Julian Huxley 
( 1932 ) . A comparative study of two related species ( Butterworth on Dipod- 
omys) is included here. A recent and detailed account (too long to include 
here) of one species in terms of relative growth and in comparison to several 
other species is the study by Lyne and Verhagen ( 1957 ) on Trichosurus vul- 
pecula, an Australian brush-tailed possum. 

A number of studies of single species may be found in the literature. Allen's 
paper (reprinted here) is of interest because it is one of the earliest to give 
serious consideration to variation as such and to possible relevance of variation 
to systematic and other problems. Hall (1926) described at greater length 
than could be included here and in detail uncommon at that time the changes 
during growth of the skull in the CaHfornia ground squirrel. Two among the 
many good recent studies of development of single species are by Layne ( 1960, 
1966) on Ochrotomys nuttalli and Peromyscus floridanus. 

Although we have not included examples of methods of determining age 
other than the report of Wright and Coulter on the fisher, we must comment 
that age determination is important in many practical problems of wildlife 
management as well as in studies of population composition or of growth as 



207 



such. Managers of deer herds, for example, can examine the teeth of hunter- 
killed animals using standards developed by Severinghaus (1949) and later 
workers. The formation of annuli in dental cement in various kinds of mam- 
mals provides another method for determining age — see Adams and Watkins 
(1967) on its application to ground squirrels. Epiphyseal growth as observed 
in X-ray photographs and the use of lens weights are other means ( see Wight 
and Conaway, 1962, on aging cottontails ) . 

A short paper on maturational and seasonal molt in the golden mouse con- 
cludes our selection for this section. Studies of molt in furbearers are, of 
course, of special economic import, and knowledge of pelage differences related 
to age, sex, or season are of obvious use in most studies of mammalian popula- 
tions. 



208 



THE REPRODUCTIVE RATES OF SOME SMALL MAMMALS 

By W. J. Hamilton, Jr. 

Students of cyclic mammal populations realize the necessity of properly evaluat- 
ing the breeding rate. A proper assessment of the reproductive rate is frequently 
essential for a correct interpretation of population levels. Without a satisfactory' 
estimate of breeding rate, conclusions regarding cyclic populations may be in- 
valid. Unfortunately, it is difl&cult to secure accurate data on the breeding rate 
in feral species; analogous observations on captive species may not give a true 
picture of the breeding behavior in wild species. Many field investigators be- 
lieve that small mammals have successive litters, one following another in rapid 
succession during the height of the breeding season. On the other hand, there 
are those who argue that a post-partus oestrus in wild species seldom occurs. 
They insist that mating during the lactation period is rare under natural condi- 
tions; captive individuals alone exhibit this phenomenon due to crowding or other 
factors imposed by laboratory conditions. Since the subject is an important one 
in population studies, I present such data as are available to demonstrate that 
certain shrews, mice, and other small mammals are not only capable, but do mate 
successfully following partus. Actively lactating species are upon occasion 
gravid. 



209 



258 JOURNAL OF MAMMALOGY Vol. SO, No. S 

In an important paper on discontinuous development in mammals, Hamlett 
(1935) remarks that in a fairly extensive series of mice of various kinds, including 
free living house mice, Norway rats, and wild species of deer mice and field mice, 
pregnant suckling females were never found. He concludes that copulation im- 
mediately after parturition in mice is a response to domestication, and is rare or 
lacking in free living races. Pearson (1944) examined early pregnant females of 
Blarina in which placental scars were visible and the manmiary glands greatly 
developed, indicating that these individuals had been nursing young recently. 
He suggests the possibility that the young may have been lost or destroyed a 
short time before, and that mating took place after the loss of the young. Pear- 
son believes that shrews with advanced mammary development merely indicate 
that it is possible for Blarina to produce more than one litter, but his data do not 
prove that there is a true post-partum oestrus. He concludes that true post- 
partum mating and pregnancy during lactation rarely, if ever, occur in Blarina; 
remating depends upon the loss of a litter. 

Several investigators have demonstrated a post-partum oestrus in captive 
cricetid rodents. Bailey (1924) observed that captive meadow voles, Microtus p. 
pennsylvanicus, mated immediately following parturition, one female producing 
seventeen litters in a year. The gestation of this species is twenty-one days; 
lactation does not lengthen the period. Svihla (1932) reports several species of 
captive Pcromyscus mating shortly after parturition. Practically all females of 
the European wild rabbit (Oryctolagus cuniculus) under natural conditions become 
pregnant again at each post-partum oestrus during the height of the breeding 
season (Brambell, 1943). Elsewhere (Hamilton, 1940), I have shown that the 
cottontail, Sylvilagus floridanus mearnsii, presumably has a post-partus oestrus, 
for actively nursing females have contained embryos, suggesting that mating 
occurs shortly following parturition. Vorhies and Taylor (1940), in their study 
of the white-throated wood rat, Neotoma albigula, suggest that it is highly prob- 
able that this species produces successive litters with only very short intervals. 
In one den they found a female with two newly bom young hanging to the teats, 
with three half-grown young in the same den. This presumptive evidence of 
rapid succession in litters is nevertheless suggestive. 

Obviously with the species discussed above there is a post-partum oestrus at 
which time the female is receptive to the male. It appears unlikely that the im- 
position of captivity would modify the reproductive cycle in a short time. The 
absolute proof of such should be studied under natural conditions, though posi- 
tive data are rather difficult to secure. 

A feral Norway rat will cease lactating within forty-eight hours after the loss of 
a litter. Gentle traction on the teats fails to produce milk following this period. 
Meadow voles usually cease to lactate a day after the young are removed. The 
short-tailed shrew, Blarina hrevicavda, will not produce a flow of milk in a similar 
length of time if the nursing young be destroyed. Since such is known of these 
three species, we may adduce the probability of pregnant females nursing a litter 
if a flow of milk is possible. The mammary glands and teats swell noticeably in 
many mammals shortly before parturition. Interpretation of data may be faulty 



210 



Aug., 1949 HAMILTON— REPRODUCTIVE RATES 259 

if such evidence is not considered with care. A colustral flow is evident in sev- 
eral cricetid rodents and some insectivores shortly before parturition. Inexperi- 
enced observers may mistake this secretion for milk and draw faulty conclusions. 
The following data lend support to the assumption that some small mammals, 
under natural conditions, successfully mate shortly after parturition and produce 
successive litters in rapid succession during part of the breeding season. Unless 
otherwise stated, the observations below relate to those of small mammals under 
conditions in the vicinity of Ithaca, New York. 

Blarlna brevicauda. Short-tailed shrew. — On July 23, 1947, E. W. Jameson, Jr. collected 
a nursing shrew. Under gentle pressure, milk could be drawn from the posterior teats. 
This shrew had four embryos, the uterine swellings measured 10 mm. in greatest width, sug- 
gestive of at least half-time pregnancy. A week later I trapped a nursing Blarina with five 
11-mm. embrj'os. The teats, on traction, produced milk. A Blarina with six 9-nim. em- 
bryos was taken on August 10, 1948. The teats were drawn out and produced milk under 
gentle traction. In my field notes from 1926 to 1941 I have recorded data on many hundreds 
of these shrews, and noted on numerous occasions the occurrence of lactating gravid females. 
I have always considered this condition a perfectly natural one in shrews. 

Sorex f. fumeus. Smoky shrew. — Mating may follow parturition in this species (Hamil- 
tion, 1940). Actively nursing females have been taken which contained well-developed em- 
bryos. Specimens of pregnant Sorex cinereus have likewise been collected with prominent 
mammary glands containing an abundance of milk. 

Peromyscus leucopus noveboracensls. White-footed mouse. — Many hundreds of adult 
females have been examined during the breeding season over a twenty-year period. Many 
of these were actively nursing and contained embryos of various sizes. Pregnant nursing 
individuals appear more frequently in May and June collections. It is possible that more 
lactating individuals were gravid than my notes indicate, since early pregnancy cannot be 
determined by macroscopic examination. 

Oryzomys palustrls. Rice rat. — This is a prolific species. Field data obtained in Vir- 
ginia demonstrates that actively nursing females are occasionally pregnant ; there is evidence 
that a high fertility, resulting in vigorous females actually producing nine litters in a breed- 
ing season, is quite possible. The females are capable of breeding when seven weeks old. 

Clethrionomys gapperi. Red-backed vole. — On October 10, 1941, 1 took a 35-gram nursing 
female with four 3-mm. embryos and recent placental scars. The mammary glands, when 
dissected out, weighed 2.5 grams. On May 29, 1940, a nursing individual contained five 
6-mm. embryos. Such data are admittedly fragmentary, but do suggest the rapidity of 
breeding in this species. Apparently many parous animals of the bank vole, Clethrionomys 
glareolus, are pregnant and lactating simultaneously. In such, pregnancies are prolonged 
by lactation causing a delay in implantation. This delay results in the blastocysts remaining 
in a resting state in the uterine lumen for a considerable period (Brambell and Rowlands, 
1936). 

Microtus pennsylvanlcus. Meadow vole. — The reproductive behavior of this species in 
the wild is similar to that of captives. Adult females give birth to one litter after another in 
rapid succession. Data on this high fecundity are readily obtainable by live trapping. 
Females approaching full term are readily recognized ; repeated captures of specific individ- 
uals indicate that in some instances young are produced at three-week intervals over a period 
of several successive months. The capture of numerous wild pregnant females with nest- 
young is indubitable proof that post-parous mating occurs normally from early spring to fall. 
I have obtained many records of such. 

Ondatra zibethica. Muskrat. — Arthur C. Cook of the New York Conservation Depart- 
ment informs me (personal letter) that on June 20, 1941, he dug out a muskrat den at How- 
lands' Island, Cayuga County, New York. From the den he recovered a pregnant muskrat 



211 



260 JOURNAL OF MAMMALOGY Vol. SO, No. 3 

with two litters of different size. In captivity, this gravid female suckled the smaller litter. 
This is presumptive evidence that the muskrat may mate following partus. 

Some polyoestrous rodents, in which two Htters a year are the rule, have the 
Htters widely spaced. Mating normally occurs in the late winter and midsum- 
mer. No post-partum oestrus occurs. Deanesly and Parkes (1933) indicate 
that there is no oestrus immediately after parturition or during lactation in the 
gray squirrel, Sciurus caroUnensis. A similar condition obtains with Tamiasdu- 
rus, Tamias, and Eutamias. 

Where populations of small mammals are sufficiently large, it appears prob- 
able that fruitful matings often occur following partus, at least during the height 
of the breeding season. If such a condition be generally true, it enables one to 
compute, in a measure, the probable reproductive rate. One may thus visualize 
the annual natural increment in a population during the breeding season. Such 
data are most useful to students of populations and animal behavior. 

LITERATURE CITED 

Bailey, Vernon. 1924. Breeding, feeding, and other life habits of meadow mice (Micro- 

tus). Journ. Agr. Research, 27: 523-536. 
Bbambell, F. W. Rogers. 1943. The reproduction of the wild rabbit Oryctolagua cuni- 

culu8 (L.). Proc. Zool. Soc. London, 114: 1-45. 
Brambell, F. W. R., and I. W. Rowlands. 1936. Reproduction in the bank vole (Evo- 

tomys glareolus Schreber). I. The oestrous cycle of the female. Phil. Trans. 

Royal Soc. London, Series B., No. 531, 226: 71-97. 
Deanesly, Ruth, and A. S. Parkes. 1933. 3. The reproductive process of certain 

mammals. Part 4. The oestrous cycle of the grey squirrel {Sciurus caroUnensis) 

Phil. Trans. Royal Soc. London, B. 222: 47-78. 
Hamilton, W. J., Jr. 1940. The biology of the smoky shrew {Sorex Jumeus fumeuiMiWQr) . 

Zoologica, 25(4) : 473-492. 
1940. Breeding habits of the cottontail rabbit in New York State. Jour. 

Mamm., 21: 8-11. 
Hamlett, G. W. D. 1935. Delayed implantation and discontinuous development in the 

mammals. Quart. Rev. Biol., 10: 432-447. 
Pearson, Oliver P. 1944. Reproduction in the shrew (Blarina brevicauda Say). Amer. 

Jour. Anat., 75: 39-93. 
SviHLA, Arthur. 1932. A comparative life history study of the mice of the genus Pero- 

myscus. Misc. Publ. Mus. Zool. Univ. Michigan, 24: 1-39. 
VoRHiES, Charles T., and Walter P. Taylor. 1940. Life history and ecology of the 

white-throated wood rat, Neotoma albigula albigula Hartley, in relation to 

grazing in Arizona. Univ. Ariz. Agr. Exp. Sta. Tech. Bull., 86: 456-629. 

Cornell University, Ithaca, New York. Received October 4, 1948. 



212 



AN EXPLANATION OF GEOGRAPHIC VARIATION IN LITTER SIZE 
Albekt W. SpexNCeh and Harold W. Steinhoff 

Absthact. — Our explanation of the latitudinal and altitudinal variation in litter 
sizes of small nianinials invokes the effect of length of season and parental mor- 
tality related to reproduction. It may be assumed that a portion of the maternal 
mortality rate varies directly as the size of litter produced. Short seasons limit 
the maximum number of times a female can reproduce in her lifetime and give an 
advantage to phenof\pes producing large litters. Long seasons favor producers of 
small litters. The contribution to the total rate of increase of the litters produced 
in the additional time afforded by long seasons is greater for producers of small 
litters because a larger proportion of parents of small litters survive to produce 
throughout the periods. The increment provided is sufficient to overcome the 
initial advantage of parents producing large numbers of young in their first litters. 

Variation in mean litter size related to latitude and altitude has been re- 
ported for several species of small mammals. Lord (1960) analyzed data on 
several species and concluded there was a regression of litter size on latitude 
in small nonhibernating prey species. Dunmire ( 1960 ) added the dimension 
of altitude when he reported an increase with elevation of mean litter sizes 
of deer mice from the White Mountains in California. Mean litter sizes in 
all cases were larger at northern locations and high elevations than at more 
southern or lower localities. 

Several explanations have been proposed to account for the observed varia- 
tion. Lord ( 1960 ) reviewed and rejected several hypotheses before proposing 
his own theory that higher mortality rates during northern winters required 
an increase in reproductive rate. We cannot accept this explanation because 
it contradicts established principles of population dynamics. 

The problem is part of the larger question of regulation of fecundity in all 
animals. Lack ( 1948, 1954 ) has explained the regulation of clutch size and 
litter size in terms of natural selection. The modal number in his view repre- 
sents the most consistently successful clutch or litter. Williams ( 1967 ) has 
presented a mathematical refinement of Lack's Principle. According to his 
concept, an allocation of parental energy between present and residual re- 
productive values that will maximize the total reproductive value is selectively 
advantageous. The cost of rearing a large or better nourished brood now is 
reduction of future reproduction. The litter size prevalent in a particular 
population represents the best investment possible for the particular situation 
of the population. 

Although Williams did not specifically consider intraspecific latitudinal 
variation in litter size, our own explanation, developed independently, sub- 
stantially parallels his general treatment. We believe the shorter seasons of 
more northern latitudes or higher altitudes limit the number of times an 
animal resident in those areas is able to reproduce in its lifetime compared 
to its relatives in lower or more southern regions. It therefore becomes ad- 

281 



213 



282 JOURNAL OF MAMMALOGY Vol. 49, No. 2 

vantageous for an animal to invest its energies in a few, large, early litters 
even though doing so reduces its life expectancy and total reproductive con- 
tribution below the maximum achievable by many small litters. This is so 
because short seasons make it impossible for the animal to realize the returns 
from the conservative approach within its life-span. The most productive 
strategy is the production of large litters. This idea is developed and illus- 
trated below. 

Results and Discussion 

Our interest in the problem began with the observations recorded in Table 
1. Feromyscus maniculatus had been collected at several sites in Colorado 
along a transect extending from the plains of central Weld County to timber- 
line in western Larimer County. The increase in mean potential litter size 
parallels the experience of Dunmire ( 1960 ) in the White Mountains of Cali- 
fornia. The regression of mean litter size on elevation is of the same order 
of magnitude as that on latitude as determined by Lord (1960). The data 
thus illustrate the general nature of the variation. 

The major factors influencing the potential rate of increase of a species are 
the number of female young per female per parturition and the length of the 
period from birth to first reproduction. However in realistically appraising 
the number of young per female per litter it is necessary to consider the 
actual contribution to the next generation represented by that litter (Lack, 
1948, 1954). If survival to maturity were a linear function of litter size and 
decreased 10% for each additional young, then only 2.5 (1.25 females) in a 
litter of five and only 2.4 ( 1.2 females ) in a litter of six would effectively be 
contributed on the average to the next generation. If these were the only 
factors influencing the rate of increase and time to maturation were uniform 
in the species, then a phenotype producing the greatest effective number (5) 
would have the highest potential rate of increase and thus the selective ad- 
vantage. 

Reproductive longevity and subsequent reproduction, however, also play 
a role in determining the rate of increase. Each successive litter contributes 
an increment to the total reproductive value. The value of each increment 
declines the later its production occurs in life, but the collective importance 
of the increments in influencing the rate of increase grows as the margin of 
difference between the effective numbers of different litter sizes diminish 
and as the length of the maturational period lengthens (Fisher, 1930; Birch, 
1948). This portion of the reproductive value is the major element involved 
in the phenomenon of latitudinal and altitudinal variations in litter size. 

The magnitude of the contribution to the rate of increase by successive 
litters depends in part on the survival of the parents (Birch, 1948). Bearing 
and rearing young constitutes a risk for the parent. The presence of the 
young reduces concealment of parents from, and adds to their vulnerability 
to, predators. Increased foraging activity also exposes the parents to greater 
dangers of predation. Physiological stresses such as nutritional deficiencies 



214 



May 1968 



SPENCER AND STEINHOFF"— LITTER SIZE 



283 



Table 1. — Fieciticncy distribution of embryo counts in Pcroinysciis nianiculatus from 

different elevations. 





Number 




















Mean 


Mean 




of 




















litter 


bod\' 


Site 


females 


1 


2 


3 


4 


•■D 


6 


7 


8 


9 


size 


length 



Plains (5100-5300 ft) 
Coal Creek 10 

Pierce 17 

Cobb Lake 29 



Subtotal 



56 



5 3 1 
2 9 4 
2 17 9 



1 



9 29 14 1 



4.0 



95.5 -0.7 



Foothills ( 5500-6500 ft ) 
Rist Canyon 22 

Siiltzcr Culch 15 



Subtotal 



37 



2 
2 



S 
10 



6 
2 



18 



4.1 



95.9 -0,9 



Mountains (8000-11,000 ft; 



Buckhorn R. S. 


7 




1 


3 


1 


I 




1 










Pennock Creek 


4 




1 


3 


















Cirques 


3 










1 


1 


1 




5.0 


94.2 




Subtotal 


14 




2 


6 


1 


2 


1 


2 




-2.2 


Pingree Park 


33 


1 


1 


6 


6 


11 


5 


2 


1 


5.6 






Mountain 






















subtotal 


47 


1 


O 


12 


7 


13 


6 


4 


1 


5.4 







and post partum diificulties impair the survival of the parents and damage 
their capabilities for reproduction in the future. It is reasonable to assume 
that the effects are proportional to the number of young produced ( Lack, 
1954, 1948). Such risk is incurred at each successive reproductive event. The 
greater the risk and the more times repeated, the more the survival rate is 
lowered and reproduction in later life is curtailed. Less drastic effects than 
actual death of the parents are probable and perhaps even more important. 
However the end result is the same and we feel justified in regarding these 
lesser effects as a form of mortalitv. 

The natural longevity (maximum physical reproductive longevity) of the 
organism and extrinsic factors such as climate impose an upper limit on the 
maximum number of opportunities for reproduction (hereafter designated 
MOR). For example if the season permitted four litters annually and the 
maximum reproductive longevity of the species were 2 years the MOR would 
be eight. Only a fraction of any age class would attain the maximum limit 
MOR. The actual proportion of the population that achieved the maximum 
would depend upon the mortality rates discussed above, and would be in- 
versely proportional to litter size. It follows, then, that any reduction in the 
MOR would have a relatively greater effect on the rate of increase of pheno- 
types producing smaller number of young per litter and having higher sur- 
vival rate than on phenotypes producing large litters. 



215 



284 JOURNAL iW MAMMALOGY Vol. 49, No. 2 

This is the Hne of reasoning that led to our conception of the connection 
between length of season and variation in litter size. Thus far we have ap- 
proached the problem strictly from the theoretical aspect by constructing 
models of the growth of idealized populations. We then studied the conse- 
quences for the potential intrinsic rate of increase of reducing the MOR and 
changing the length of the period of maturation. For simplicity, the relation- 
ships of survival of the young to maturity and survival of parents was as- 
sumed to be an inverse linear function of litter size. Consideration of avail- 
able data on guinea pigs (Lack, 1948), Peromysctis (McCabe and Blanchard, 
1950) and birds and lizards (Lack, 1954) indicated that these may be accept- 
able approximations. All effects of fecundity on future parental reproduction 
were combined under the heading of parental mortality. All mortality not 
related to litter size was ignored. Litter size was assumed to be a constant 
characteristic throughout the population and independent of age. Only female 
births were considered. The unit of time was taken to be the minimum in- 
terval between successive parturitions and each mature female was assumed 
to reproduce at each interval. Net reproductive ratios and rates of increase 
were evaluated by a combination of numerical integration and graphic methods. 
Lotka (1925), Fisher (1930), and particularly Birch (1948) were the main 
sources of inspiration and methods used in the computations. 

Fig. 1 summarizes the findings of our study. Observe that the size of the 
litter with the greatest potential rate of increase declines as the MOR in- 
creases. The shift reflects the relatively greater increase in the total repro- 
ductive value of producers of small litters as the number of late reproductions 
is allowed to increase. Note also that the shift is rather abrupt and little 
affected by further increase in MOR. The range of the shift increases as the 
period of maturation lengthens. Changes in the parameters of survival of 
parents and young also affect the locus and magnitude of the shift but these 
effects have not yet been thoroughly explored. Approximations of the varia- 
tion shown in Table 1 were achieved by substitution into the calculations for 
curve C (Fig. 1) of the following coefficients. The coefficient of regression 
for survival of young to maturity on litter size used was -.10 and of survival 
of parents on litter size was -.016. It of course would be possible to obtain 
the same approximation by an almost limitless number of combinations, but 
the important point is that the magnitude of the coefficients required is of 
plausible order. 

The analysis offers an explanation of the observed distribution of latitudinal 
variation in litter size among mammals considered by Lord ( 1960 ) . The 
fossorial and hibernating species investigated (Spermophilus and Thomomys) 
usually have one litter annually. Their period of development from birth to 
first reproduction is about 1 year or 6 months when two litters are produced 
(Asdell, 1964). The effect of shortening the annual season would thus have 
little effect on the reproductive opportunities of these organisms. Their pat- 
terns of reproduction are approximated by that shown in curve A in Fig. 1. 



216 



May 1968 SPENCER AND STEINHOFF— LITTER SIZE 285 



6- 



B 

3 

z 4 




Maturity at one reproductive interval 



Maturity at two reproductive intervals 



Maturity at ttiree reproductive intervals 

P ►€ 



2 4 8 16 

Maiimum number of opportunities for reproduction 

Fig. 1. — Change in the fitness of Htter sizes as the maximum number of opportunities fur 
reproduction is increased. The Hnes connect the htter sizes liaving the greatest potential 
rate of increase under the hmitations imposed. 



Only drastic differences in length of season would produce noticeable effects. 
Even then the magnitude of variation would be relatively small. On the other 
hand, the species of mice and shrews that display latitudinal variation can 
produce several (up to 12) litters annually and yet have a period of develop- 
ment from birth to first reproduction equal to several reproductive intervals. 
Many shrews begin reproducing at the age of 1 year. The reproductive pat- 
terns of these animals correspond to curve C. Effects of significant magnitude 
could be produced with relatively small changes in the length of the season. 
In the Colorado data, for example, the growing seasons on the plains (5000 
ft) and in subalpine areas (8000-10,000 ft) differ by almost a factor of two. 
An interesting aspect of the analysis is that the relative superiority of the 
favored phenotype is reduced directly as the MOR. Therefore, the genetic 
variance in the population would be correspondingly reduced. Attainment of 
maximum fitness in the population should be a long process; in two popula- 
tions, the one occupying the environment with the shorter season should 
have the greater variability in litter size after a given period. This would be 



217 



286 JOURNAL, OF MAMMALOGY Vol. 49, No. 2 

particularly true if gene flow between them were occurring. This condition 
is seen in Table 1. 

Intraspecific variation may originate in many ways. There is, however, 
only one agency, natural selection, regularly producing the directed sort of 
variation we are considering. Lord (1960) has suggested that the increased 
size of litters may be a compensating response to mortality among the small 
mammals during winter. However, if a population of a species were able to 
increase its reproductive potential in this manner, the ability would be just 
as adaptive in any environment. Variation would quickly disappear. If the 
variation is to be described in terms of fitness then the particular phenotypes 
characteristic of each locality must have the greatest fitness in that situation. 
Our explanation offers an hypothesis explaining how the differential in fitness 
may originate. 

Literature Cited 

AsDELL, S. A. 1964. Patterns of mammalian reproduction. Cornell Univ. Pre.ss, Ithaca, 

2ncl ed., viii + 670 pp. 
Bn^CH, L. C. 1948. The intrinsic rate of increase of an insect population. J. Anim. Ecol., 

17: 15-26. 
DuxMiRE, W. W. 1960. An altitudinal survey of reproduction in Pcronnj.scus niaiiictt- 

latus. Ecology, 41: 174-182. 
Fisher, R. A. 1930. The genetical theory of natural selection. Clarendon Press, O.xford, 

272 pp. 
Lack, D. 1948. The significance of litter-size. J. Anim. Ecol., 17: 45-50. 
. 1954. The natural regulation of animal numbers. Clarendon Press, Oxford, 

viii + .34.3 pp. 
Lord, R. D., Jr. 1960. Litter size and latitude in North American mannnals. Amer. 

Midland Nat., 64: 488^99. 
LoTKA, A. J. 1925. Elements of physical biology. Williams and Wilkins, Baltimore. 
McCabe, T. T., and B. D. Blaxchard. 1950. Three species of Peromyscus. Rood 

Associates, Santa Barbara, California, v -|- 136 pp. 
Williams, G. C. 1967. Natural selection, the costs of reproduction, and a refinement 

of Lack's principle. Amer. Nat., 100: 687-690. 

Division of Biological Science, Fort Lewis College, Durango, Colorado 81301, and 
Departmetit of Fishery and Wildlife Biology, Colorado State University, Fort Collins, 80521. 
Accepted 2 January 1968. 



218 



Sonderdruck aus Z. f. Saugetierkunde Bd. 30 (1965), H. 1, S. 10—20 

A!le Rechte, audi die der Cbersetzung, des Nadidrudts und der photomedianischen Wiedergabe, vorbehalten. 
VERLAG PAUL PAREY ■ HAMBURG 1 • SPITALERSTRASSE 12 

The effects of suckling on normal and delayed cycles of 
reproduction in the Red Kangaroo 

By G. B. Sharman 

Eingang des Ms. 23. 12. 1963 

Introduction 

In non-lactating female marsupials the occurrence of fertilization, followed by imme- 
diate gestation of the embryo, does not delay the onset of the following oestrus. In 
those marsupials in which the gestation period is considerably shorter than the length 
of one oestrous cycle, such as Didelphis virginiana (Hartman, 1923) and Trichosurus 
vulpecula (Pilton and Sharman, 1962), oestrus recurs at the expected time if the young 
are removed at birth. In several species of Macropodidae, sudi as Setonix brachyurus 
(Sharman, 1955), Potorous tridactylus (Hughes, 1962) and the Red Kangaroo (Shar- 
man and Calaby, 1964), the gestation period occupies almost the length of one oestrous 
cycle and oestrus is imminent at the time of parturition. Oestrus thus recurs just after 
the young reach the pouch (post-partum oestrus) presumably because pro-oestrus chan- 
ges are initiated before the onset of the suckling stimulus. In all marsupials suckling 
of young in the pouch is accompanied by a lengthy period during which oestrus does 
not occur. This period is called the quiescent phase of lactation or, simply, the quies- 
cent phase. It differs from seasonal anoestrus in that the ovaries and other reproduc- 
tive organs respond to the removal of the suckling stimulus by resuming cyclic func- 
tions. Those marsupials in which post-partum oestrus occurs exhibit discontinuous 
embryonic development analogous to the delayed implantation which occurs in some 
eutherian mammals. If fertilization takes place at post-partum oestrus the resulting 
embryo assumes a dormant phase, at the blastocyst stage, and is retained as a dormant 
blastocyst during the quiescent phase. In these marsupials pregnancy (the interval 
between copulation at post-partum oestrus and parturition) is long and gestation of 
the embryo is interrupted by the dormant phase. 

In the Red Kangaroo, Megaleia rufa (Desm.), the oestrous cycle averages 34 to 35 
days and the gestation period is 33 days in length (Sharman and Calaby, 1964). Post- 
partum oestrus occurs, usually less than 2 days afler the newborn young reaches the 
pouch, and a dormant blastocyst is found in the uterus of females, fertilized at post- 
partum oestrus, which are suckling young less than 200 days old in the pouch (Shar- 
man, 1963). If the young is removed from the pouch suckling ceases and the dormant 
blastocyst resumes development: the young derived from it being born about 32 days 
after removal of the pouch young (RPY). This birth is followed by another post- 
partum oestrus or, if the female was not carrying a blastocyst, by a normal oestrus. 
Oestrus recurs at the same number of days after RPY irrespective of whether a de- 
layed blastocyst was carried or not. The sequence of events from RPY to the next 
oestrus is called the delayed cycle of reproduction^ to distinguish it from the normal 
reproductive cycle which follows oestrus. The delayed reproductive cycle may be 
divided into delayed gestation and delayed oestrus cycle according to whether a dor- 



1 The term "delayed cycle of reproduction" or "delayed (reproductive) cycle", was introduced 
by Tyndale-Biscoe (1963) to describe the resumption of ovarian activity, and the features 
associated with it, following removal of pouch young (RPY). 



219 



Normal and delayed cycles of reproduction in the Red Kangaroo 11 

niant blastocyst does or does not complete development. If the young is retained in 
the pouch until it leaves in the normal course of events the delayed reproductive 
cycle occurs coincident with the latter stages of pouch life. The dormant phase of 
the blastocyst gives way to renewed development when the pouch young is a little 
over 200 days old and subsequent vacation of the pouch, at an average age of 235 days, 
is immediately followed by birth of another young (Sharman and Calaby, 1964). 
The young is suckled for another 130 days, that is until it is about a year old, after 
it leaves the pouch. During this period the normal reproductive cycle occurs if the 
pouch is not occupied. It is thus evident that, although the delayed reproductive cycle 
occurs after RPY and cessation af lactation, some factor other than the actual pro- 
duction of milk must be implicated for both delayed and normal cycles may also 
occur during lactation. 

The aim of the experiments reported below was to determine the effect of the 
suckling stimulus on both normal and delayed reproductive cycles. Additional suck- 
ling stimulus was provided by fostering an extra young on to females already suck- 
ling a young-at-foot. The experimental approach was suggested by chance obser- 
vations on a female Red Kangaroo which, while suckling her own young-at-foot, 
alternately fed the young of another female kept in the same enclosure. There are 
four teats in the pouch but the teat to which the young attaches after birth alone 
produces milk and its underlying mammary gland produces all the milk for the 
young from birth to weaning. The female's own young and the foster-young thus 
shared the products of a single mammary gland and used the same teat alternately. 
Some initial results, in so far as they were relevant to the theme of delayed implanta- 
tion, were reported earlier in a review of that subject (Sharman, 1963). 



Methods 

The results presented consist of observations on a minimum of five reproductive cyc- 
les in the female Red Kangaroo in each of the following categories: 

1. Normal cycle of reproduction, suckling one young-at-foot. 

2. Normal cycle of reproduction, suckling two young-at-foot. 

3. Delayed cycle of reproduction, suckling one young-at-foot. 

4. Delayed cycle of reproduction, suckling two young-at-foot. 

The results are compared with data on the normal and delayed cycles of reproduc- 
tion in non-lactating females most of which have been published elsewhere (Sharman, 
1963; Sharman and Calaby, 1964; Sharman and Pilton, 1964). In most cases the 
experimental females were pregnant or carrying dormant blastocysts so that cycles 
of normal or delayed gestation with subsequent post-partum oestrus were studied. 
The gestation periods and cycles were regarded as having been significantly lengthened 
when they occupied a time greater by the length of two, or more, standard deviations 
than similar cycles in control, non-lactating, females 

Some difficulty was experienced in getting females to accept foster-young and only 
six females readily did so. The experiments were therefore done serially one female 
being used in two and two females in three experiments. 

The animals were watched from a hide overlooking the enclosures and observed 
with binoculars. An initial watch was always done to find whether females accepted 
their potential foster-young. Thereafter prolonged watches were kept on some females 
to determine the amount of time spent suckling the young-at-foot. 

Vaginal smears for the detection of oestrus and copulation were taken as reported 
previously (Sharman and Calaby, 1964). 



220 



12 G. B. Sharman 

Results 

Effects of suckling on the normal cycle of reproduction 

In thirteen non-lactating female Red Kangaroos forty-two intervals from oestrus to 
the succeeding oestrus averaged 34.64 days with a standard deviation of 2.22 days 
(34.64 ± 2.22 days). Twenty gestation periods in fourteen females lasted 33.00 ± 0.32 
days (Fig. lA). In five females, each observed for a single reproductive cycle while 
suckling one young-at-foot, the intervals between two successive oestrous periods were 
not different from those in non-lactating females (Fig. IB). In another female (K32a) 



A 42 cycles 



K60 

K53a 

Kic 

K30c 

K12c 

K32q 

K3lQ 

K31b 

K36c 

K30a 

Kdd 

K4e 

K35c 




12 



16 



20 24 28 32 



36 



40 44 



48 



Intervals between successive oestrous periods 



Fig. 1. Intervals between successive oestrous periods in nonlactating (control) female Red 
Kangaroos (A), females sudiling one young-at-foot (B) and females suckling two young-at- 
foot (C). Black lines — continuous embryonic development, broken lines — approximate 
periods of dormant phase in embryo induced and maintained by suckling young-at-foot, open 
lines — no embryos present, bars inserted in A — standard deviations either side of mean. 

the gestation period was not significantly different from that of control females but 
oestrus did not occur until 5 days post-partum. This was the longest interval between 
parturition and post-partum oestrus recorded but it is not regarded as significant. Two 
cycles in female K31, one lasting 41 days and one 47 days, were abnormally long. The 
41-day cycle is of special significance since the interval between copulation and birth 
was 40 days. This differs so much from the gestation period in the control, non-lacta- 
ting, females that it must be assumed that suckling of the single young-at-foot induced 
a short quiescent phase in the uterus accompanied by a dormant phase of about 7 days 
in the embryo. The 47-day cycle was over 12 days longer than the mean normal cycle 
length and 7 days longer than the maximum cycle length. The female copulated at 
oestrus but did not give birth so it is presumed that fertilization did not occur. 

In three females already suckling one young-at-foot, which had another young-at- 
foot fostered on to them at about the time of fertilization, the lengths of the repro- 
ductive cycles were not significantly different from those in control females. Two 
females had significantly longer cycles than in control females. One of these (K36) was 
used in three successive experiments while suckling the same two young-at-foot. In the 
first of these (K36a) the extra suckling stimulus had no significant effect on the length 
of the reproductive cycle. The second experiment concerned the delayed reproductive 
cycle and is reported below. During the third experiment (K36c) the young were being 
weaned but a highly significant result was obtained. The interval from copulation to 



221 



Normal and delayed cycles of reproduction in the Red Kangaroo 



13 



birth showed conclusively that a dormant phase had been induced and maintained in 
the embryo for about 14 days of the 47-day pregnancy. In the other female in which 
the cycle was prolonged (K4e) the embryo presumably had a dormant phase of about 
6 days. 

Effects of suckling on the delayed cycle of reproduction 

In ten non-lactating females thirteen intervals from RPY to the succeeding oestrus 
were 34.46 ± 1.92 days. In seven of these females the delayed gestation period was 
31.64 ± 0.65 days (Fig. 2A). There was no evidence that suckling one young-at-foot 
had any effect on the length of the delayed reproductive cycle (Fig. 2B). In one female 
(K12a) the interval from RPY to the following oestrus was 38 days but this falls short 
of the minimum interval accepted as significantly different. 

All six females suckling two young-at-foot (Fig. 2C) were carrying a dormant 
blastocyst in the uterus when the pouch young were removed. In five of these the 
Interval RPY to birth was significantly longer than in control females (Fig. 2C). The 
interval RPY to the next oestrus was longer than the mean for control non-lactating 
females in all six experimental females and in three of them (K4b, K30b, K36b) the 
difference from controls was highly significant. It must be concluded that the blasto- 
cysts of five of the above experimental females remained in the dormant phase for 
between 3 and 22 days longer afler RPY than did those of control non-lactating 
females and females suckling one young-at-foot. 



A 13 cycles 



B 



Kio 

K15 

K38b 

K12b 

K12a 

K38a 
K63b 
K32b 
K36b 
K30b 
K4b 



12 



16 20 



24 



28 



32 36 



40 



44 48 52 56 



Intervals between RPY and oestrus 



Fig. 2. Intervals between removal of pouch young (RPY) and the next oestrus in non-lactating 
(control) female Red Kangaroos (A), females suckling one young-at-foot (B) and females 
suckling two young-at-foot (C). Black lines — continuous embryonic development, broken 
lines — approximate periods of continued dormant phase of embryo maintained by suckling 
young-at-foot, bars inserted in A — standard deviations either side of mean. 



The amount suckling in relation to occurrence of parturition and return to oestrus 

Observations on the habits of the pouch young suggested that the stimulus causing 
withholding of the mother's reproductive cycles might be tactile and received via the 
teat. The young during the early stages of pouch life, when reproductive cycles were 
withheld, were suckled continuously and could not regain the teat if removed before 
the age of 6 weeks. Later young were able to take the teat back into their mouths but 
were seldom found free of the teat before the age of about 5 months. On the other 



222 



14 



G. B. Sharman 






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hand the pouch young 
present when the delayed 
reproductive cycle occur- 
red apparently frequently 
released the teat as they 
were seen protruding their 
heads from the pouch to 
feed from the ground or 
leaving the pouch entirely 
(Sharman and Calaby, 
1964). 

Theoretically it was to 
be expected that if repro- 
ductive cycles resumed in 
response to a lowered 
suckling stimulus, as they 
did during the terminal 
stages of pouch feeding, 
then the cycles which 
occurred as soon as the 
young left the pouch 
should have been of nor- 
mal length. Six of the eight 
cycles shown m Fig. 1 B 
were the first which oc- 
curred after termination 
of pouch feeding. Four 
were of normal length but 
two cycles in one female 
(K 31a, b) were lengthe- 
ned by a significant 
amount. Observations on 
the habits of the young, just 
after they left the pouch 
permanently, showed that 
they frequently attempted 
to regain the pouch but 
were restrained from 
doing so by their mothers 
(Sharman and Calaby, 
1964). In these cases they 
spent long periods with 
their heads in the pouch 
during which time they 
may have grasped the 
teat. It is also possible 
that the young, subjected 
permanently for the first 
time to the cooler environ- 
ment outside the pouch, 
fed more frequently than 
they did during the ter- 



223 



Normal and delayed cycles of reproduction in the Red Kangaroo 15 

minal stages of pouch life. This would result in a greater suckling stimulus being 
exerted: at least during the initial stages of life outside the pouch. 

A number of females suckling one or two young-at-foot were watdied continuously 
for varying periods and the amounts of time spent suckling were recorded (Table 1). 
It was at once apparent that females feeding two young-at-foot spent nearly twice as 
much time suckling as did females with a single young-at-foot. The relationship bet- 
ween amount of suckling and interruption or resumption of the reproductive cycle is, 
however, not so obvious. Thus, in female K31, 48 and 51 minutes of suckling per day 
were associated with lengthening of the interval between successive oestrous periods 
and 48 minutes per day with inducing and maintaining a short dormant phase in the 
embryo. In two other females (K60, K30c) a greater amount of suckling apparently 
had no effect on the length of the cycle or on pregnancy. However, although the 
watches were done during the relevant cycles, they were not necessarily done at the 
critical period of the cycle when the suckling stimulus exerted its effect. This period 
could not be ascertained since no evidence of its occurrence was available until the 
females gave birth or returned to oestrus. The figures in Table 1 are thus to be regar- 
ded as no more than a guide to the amount of suckling whidi occurred at the critical 
period. 

The most conclusive evidence about the effect of the suckling stimulus on the re- 
productive cycle came from the females from which pouch young were removed 
while they were suckling two young-at-foot (Fig. 2C). In one of these females (K38a) 
the suckling of two young-at-foot was without effect on the delayed reproductive 
cycle; in three (K32b, K36b, K63b) the delayed cycle began while two young were 
being sudcled but in two others (K4b, K30b) the delayed cycle was only initiated 
when one of the suckling young-at-foot was removed. The interval from removal of 
the young-at-foot to completion of the delayed cycle was approximately the same 
(31—32 days) as from RPY to the completion of the cycle in the control females. 

The two intervals between successive oestrous periods with intervening pregnan- 
cies which were observed in the same female (K36a, c) while suckling the same two 
young-at-foot call for some comment. Parturition and return to oestrus occurred 
when expected in the first cycle but were delayed significantly in a subsequent cycle 
when the young were much older and were being weaned (Fig. IC). During this, 
latter, cycle one of the young frequently grasped the teat for periods of 10 minutes 
or more but when the female's pouch was examined it was found that no milk could 
be expressed from the teat and that the mammary gland was regressing. This was in 
contrast to the condition in other females suckling young-at-foot in which milk could 
usually be readily expressed. No watdi was done to observe the amount of time the 
young spent sucking the dry teat as the significance of the observation was only 
realised after completion of the cycle. This cycle is, however, of particular significance 
because it appears likely that the suckling stimulus, in the absence of lactation, in- 
duced a quiescent phase in the uterus lasting some 14 days and a corresponding period 
of dormancy in the blastocyst. 

Discussion 

Delayed implantation in the Red Kangaroo is of the type usually referred to as lacta- 
tion controlled delayed implantation. This description is adequate in so far as the 
delayed cycle of reproduction is initiated following removal of the pouch young and 
cessation of lactation. However, the delayed cycle also occurs during the seventh and 
eighth months of the 12-month lactation period. It therefore follows that, in these 
cases, the delayed cycle does not begin in response to the cessation of lactation or 
to the imminent cessation of lactation. The quiescent phase of lactation with asso- 



224 



1^ G. B. Sharman 

ciated arrested development of the embryo is initiated during the early part of lac- 
tation while a sm.all young is suckled continuously in the pouch but the normal re- 
productive cycle may, as has been shown above, occur during the latter part of lac- 
tation. It is thus much more likely that the amount of suckling stimulus which the 
female receives at various phases of the lactation period is of paramount importance 
in determining whether the normal reproductive cycle shall be interrupted or whether 
the delayed cycle shall be initiated. The experiments reported above have shown that 
in some females the normal cycle is interrupted and a quiescent phase of lactation, 
with associated dormant phase of the embryo is induced by increasing the suckling 
stimulus. It has also been shown that the stimulus of suckling of young, outside the 
pouch, is capable of prolonging the quiescent phase of lactation and dormant phase 
of the embryo. 

Two other factors could be of importance in determining the time of onset of the 
delayed cycle of reproduction: 1. Temporary or permanent vacation of the poudi. 
2. Fall in milk yield. Temporary emergence from the pouch first occurs when the 
young are less than 190 days old and permanent emergence at the average age of 
235 days — that is a few days before the completion of the delayed cycle (Sharman 
and Calaby, 1964) but the delayed cycle apparently begins when the young are a 
little over 200 days old. Precise data on this point are difficult to obtain but assu- 
ming that the delayed cycle, once initiated, proceeds at the same rate in lactating 
females as it does in females from which the poudi young are removed then it must 
begin about 30 days before the young leaves the pouch. This is in agreement with the 
massive amount of data obtained from Red Kangaroos taken in the field. The onset 
of the delayed cycle can hardly occur in response to a fall in milk yield since it takes 
place when the young is actively growing and when it is increasing rapidly in weight. 
From the age of 200 days to the age of 220 days, during which period the delayed 
cycle is resumed, the pouch young increase from about 2.5 to 3.5 kg in weight which 
is not the expected result of a fall in milk yield. Furthermore removal of young from 
the pouches of females whidi were suckling two young-at-foot must have been ac- 
companied by a fall in milk yield yet under these circumstances the quiescent phase 
of lactation with associated dormant blastocyst continued in five of six females 
(Fig. 2C). 

The importance of the suckling stimulus in marsupial reproduction was demon- 
strated by Sharman (1962) and Sharman and Calaby (1964) who transferred new- 
born young Trichosurus vulpecula and Megaleia rufa to the pouches or teats of non- 
lactating, non-mated or virgin females of each of these species at the appropriate 
number of days after oestrus. The suckling stimulus exerted by the young induced 
the onset of lactation without the prior occurrence of pregnancy and oestrous cycles 
were withheld while the foster-young were suckled in the pouch. Sharman and Ca- 
laby (1964) were unable to demonstrate any behavioural differences between preg- 
nant and non-mated female Red Kangaroos at the same number of days after oestrus 
except that pregnant females repeatedly cleaned their pouches just before giving birth. 
Other authors (Hill and O'Donoghue, 1913; Hartman, 1923; Sharman, 1955; Pil- 
TON and Sharman, 1962) have drawn attention to the remarkable resemblances of 
post-oestrous dianges in pregnant females to those of non-mated females in various 
species of marsupials. It is apparent, that whereas in polyoestrous eutherian mammals 
hormones produced by the embryonic membranes modify the reproductive cycle and 
prevent the recurrence of oestrus during pregnancy, no such mechanism has yet been 
demonstrated in any marsupial. In those marsupials which do not have a seasonal 
anoestrous period, such as the Red Kangaroo, the reproductive cycle is continuous 
except when interrupted by the quiescent phase of lactation. 

Owen (1839—47) determined the gestation period (interval from mating to birth) 



225 



Normal and delayed cycles of reproduction in the Red Kangaroo 17 

of a lactating female Great Grey Kangaroo as 38—39 days. Hediger (1958) stated 
that K. H. WiNKELSTRATER and E. Cristen in Zurich Zoo found gestation periods 
of 30 and 46 days in the same species and later, in the same paper, stated that a 
young was born on the forty-sixth day after mating in a lactating female Great Grey 
Kangaroo. However the dates quoted by Hediger show that the „gestation period" 
was actually 57 days. In non-lactating Great Grey Kangaroos Miss Phyllis Pilton 
(pers. comm.) found the gestation period was about 30 days and in the C.S.I.R.O. 
Division of Wildlife Research four gestation periods in three non-lactating females 
were 33 days 6 hours to 34 days 6 hours, 33 days 18 hours to 34 days 10 hours, 
34 days to 34 days 17 hours and 34 days to 34 days 20 hours. It is apparent that, 
although the Great Grey Kangaroo does not have the same type of lactation con- 
trolled delayed implantation as occurs in the Red Kangaroo and other marsupials 
(Sharman, 1963), intervals between mating and birth in lactating females may be an 
unreliable guide to the gestation period. Hediger (1958) stated that exact gestation 
periods in kangaroos and other marsupials are difficult to determine because ovulation 
occurs several days after mating and spermatozoa can remain active in the oviduct 
for long periods. This may be true of the marsupial Dasyurus viverrinus, but Hill 
and O'Donoghue's (1913) work on this species has not been repeated and confirmed. 
Delayed ovulation and storage of spermatozoa do not occur in Didelphis (Hartman, 
1923), Setonix (Sharman, 1955) or Trichosurus (Pilton and Sharman, 1962) and 
gestation periods in non-lactating females of these species can be determined with 
considerable accuracy. In the Red Kangaroo the intervals between mating and birth 
in some lactating females (Table 2) are not true gestation periods since they include 



Table 2 

Intervals from mating to birth and intervals from removal of pouch young (RPY) to birth 
in seven female Red Kangaroos subjected to different levels of sudcling stimulus 



No. of female 


K4 


K30 K31 K32 K36 
Intervals from mating to birth 


K38 


K63 


Non-sudiling 


33 


— — 33 — 


— 


33 


Sudcling 1 young 


34 


33 40 33 — 


— 


33 


Suckling 2 young 


34,39 


33 — — 32,47 
Intervals from RPY to birth 






Non-suckling 


32 


2,2 — — — 


32 


— 


Suckling 1 young 


31 


— — — — 


31 


— 


Suckling 2 young 


54 


43 — 35 38 


32 


35 



a period of arrested development of the embryo. Plowever, in thirteen non-lactating 
female Red Kangaroos one gestation period was 32 days, one was 34 days and 
eighteen were 33 days in length (Sharman and Calaby, 1964). The true gestation 
period, as in the species above, can therefore be determined with precision. 

Perhaps failure to recognise the importance of the suckling stimulus accounts for 
the inaccuracy of some of the marsupial gestation periods given in International Zoo 
Year Book Vol. 1 (Jarvis and Morris, 1959). The list is incomplete and at least half 
of the figures given are wrong. 



226 



18 G. B. Sharman 

The occurrence of lactation controlled delayed implantation in marsupials was re- 
ported in 1954 (Sharman, 1954) and numerous papers have since appeared indicating 
that it is of widespread occurrence among kangaroo-like marsupials. Records of birth 
in captive female marsupials after long isolation from males, such as those reported by 
Carson (1912) in the Red Kangaroo and, recently, by Hediger (1958) in Bennett's 
Wallaby, are readily explained in terms of the occurrence of delayed implantation. 

I am indebted to Miss Pat Berger, Mr. John Libke and Mr. James Merchant 
who helped with animal maintenance, handling and watching. The interest, assistance 
and advice on the manuscript given by my colleague Mr. J. H. Calaby is gratefully 
adtnowledged. 

Summary 

In non-Iactating female Red Kangaroos the oestrous cycle lasted about 35 days and the 
gestation period was about 33 days. Gestation did not interrupt the oestrous cycle. Postpartum 
oestrus, at which copulation and fertilization took place if the female was with a male, 
occurred just after parturition. Recurring reproductive cycles were replaced by the quiescent 
phase of lactation for up to about 200 days while the young were suckled in the pouch. If 
fertilization occurred at postpartum oestrus a dormant blastocyst was carried in the uterus 
during the quiescent phase of lactation. The delayed cycle of reproduction during whidi the 
hitherto dormant blastocyst, if present, completed development occurred following removal 
of young less than 200 days old from the poudi. If the young were retained in the pouch 
until they emerged in the normal course of events the delayed cycle of reproduction occurred 
coincident with the last month of pouch life and was completed a day or two after the young 
permanently left the pouch. Suckling of the young occupied one year: they were suckled for 
about 235 days in the pouch and for a further 130 days after leaving the pouch. The delayed 
cycle of reproduction could thus occur during, and long before the cessation of, lactation. 
Normal cycles of reproduction occurred during lactation if the pouch was not occupied. 

The lengths of normal and delayed cycles of reproduction In females suckling one and two 
young-at-foot were compared with those In control, non-lactating, females. The results were 
as follows: 

Normal cycle of reproduction 

Females suckling one young-at-foot. Six cycles not significantly different from those of 
controls; two cycles significantly longer than in controls in one of which a dormant phase of 
about 7 days occurred In the embryo. Total: 8 cycles. 

Females suckling two young-at-foot. Three cycles not significantly different from those of 
control females: two cycles significantly longer than In control females which Included dor- 
mant periods of 6 and 14 days In the embryos. Total: 5 cycles. 

Delayed cycle of reproduction 

Females suckling one young-at-foot. No effect of suckling. Total: 5 cycles. 

Females suckling two young-at-foot. One cycle not significantly different from those of 
control females. Five cycles longer than those of control females In which the dormant periods 
of the blastocysts were extended by 3, 3, 6, 11 and 22 days. In the two latter cycles resumption 
of development of the dormant blastocysts did not occur until removal of one of the suckling 
young-at-foot. Total: 6 cycles. 

Observations showed that females with two young-at-foot suckled their young for about 
twice the length of time that females suckled a single young-at-foot. It was concluded that 
the suckling stimulus exerted by one or two young-at-foot could Induce and maintain the 
quiescent phase of lactation and the associated dormant phase in the embryo. Available 
evidence suggested that the stimulus causing onset of the quiescent phase was tactile and 
received via the teat and that the delayed cycle of reproduction occurred, or the Interrupted 
normal cycle was resumed, when the suckling stimulus was lessened. 

It is suggested that some published gestation periods of marsupials owe their error to the 
failure of observers to appreciate the significance of concurrent suckling. Reported cases of 
female marsupials giving birth after long isolation from males can readily be explained as 
due to the occurrence of the delayed cycle of reproduction. 



227 



Normal and delayed cycles of reproduction in the Red Kangaroo 19 

Zusammenfassung 

Bel nichtsaugenden 9$ ^^^ Roten RIesenkanguruhs dauert der Oestrus-Cyclus rund 
35 Tage, die Triichtigkeit rund 33 Tage. Trachtigkeit unterbricht den Cyclus nicht. Postpartum- 
Oestrus, bei dem Begattung und Befruchtung stattfanden, erfolgten unmittelbar nach der 
Geburt. Wiederkehr des Oestrus wurde durch eine Latenz wiihrend der Laktation bis zu 200 
Tagen verhlndert, wahrend welcher das Junge im Beutel gesaugt wurde. Wenn beim Postpar- 
tum-Oestrus Befruchtung erfolgt war, enthalt der Uterus wahrend dieser Latenzperiode eine 
ruhende Blastocyste. Der verzogerte Cyclus der Fortpflanzung, wahrend der die bisher ruhende 
Blastocyste (wenn sie vorhanden ist) ihre Entwicklung vollendet, tritt auf, wenn das Junge 
friiher als 200 Tage nach der Geburt aus dem Beutel entfernt wird. Wenn die Jungen jedoch 
so lange im Beutel bleiben, bis sie ihn normalerweise verlassen hatten, fallt der verzogerte 
Cyclus der Fortpflanzung mit dem letzten Monat des Beutellebens zusammen und ist vollendet 
ein oder zwei Tage nachdem die Jungen den Beutel endgiiltig verlassen haben. Das Saugen 
dauert ein voiles Jahr: die Jungen werden rund 235 Tage lang im Beutel und noch weitere 
130 Tage bei Ful^ gesaugt. 

Der verzogerte Cyclus der Fortpflanzung kann also wahrend und auch lange vor Beendi- 
gung der Laktation auftreten. Normaler Cyclus der Fortpflanzung tritt auf, wenn kein Junges 
im Beutel ist. Die Lange von normalen und verzogerten Cyclen der Fortpflanzung bei saugen- 
den $9 rn'*^ einem bzw. zwei Jungen bei Fuft wurde mit solchen bei nicht saugenden KontroU- 
5$ verglichen. Die Ergebnisse waren: 

Normaler Cyclus der Fortpflanzung 

bei 9?) ciis 1 Junges bei Fufi saugten: 6 Cyclen waren nicht besonders verschieden von den 
Kontroll-$9- Zwei Cyclen waren bedeutend langer; bei einem davon machte der Embryo eine 
Ruhepause von etwa 7 Tagen durch. Im ganzen 8 Cyclen. 

Bei 9$) die 2 Junge bei Fufi saugten: 3 Cyclen nicht besonders verschieden von den Kon- 
troll-99; 2 Cyclen bedeutend langer als bei den Kontroll-99 "^'^ Ruheperioden des Embryos 
von 6 und 14 Tagen. Im ganzen 5 Cyclen. 

Verzogerter Cyclus der Fortpflanzung 

bei99> die ein Junges bei Fufi saugten, ergab sich keinEinfluft des Saugens. Im ganzen 5 Cyclen. 

Bei 99> <ii^ 2 Junge bei Fufi saugten, war 1 Cyclus nicht sehr verschieden von den Kontroll- 
99- 5 Cyclen waren langer als bei den Kontroll-99> bei denen die Ruhezeit der Blastocyste 
resp. 3, 3, 6, 11 und 22 Tage betrug. In letzteren beiden setzte die Weiterentwicklung nicht ein, 
bevor nicht eines der Jungen weggenommen wurde. Im ganzen 6 Cyclen. 

Die Beobachtungen zeigten, dafi 9? ^^^ 2 Jungen bei Fufi ihre Jungen doppelt so lange 
saugen, wie sie ein einziges gesaugt haben wiirden. Daraus wurde geschlossen, dafi der Sauge- 
Stimulus, von einem oder zwei Jungen bei Fui5 ausgelost, sowohl die Ruhephase wahrend der 
Laktation, als auch die damit gleichlaufende Ruhephase des Embryos einleitet und erhalt. Die 
bisherige Erfahrung laEt annehmen, dafi der Stimulus, der den Beginn der Ruhephase bewirkt, 
tactil ist und iiber die Zitze empfangen wird, und dafi der verzogerte Cyclus der Fortpflanzung 
auftritt, oder der unterbrochene normale Cyclus wieder aufgenommen wird, wenn der Sauge- 
reiz sich vermindert. 

Einige von anderer Seite veroffentlichte Daten iiber Trachtigkeitsdauern von Beuteltieren 
enthalten offenbar Fehler, da die betreffenden Autoren die Bedeutung gleichlaufenden Saugens 
nicht beachteten. Mitgeteilte Falle, daf^ 9 Beuteltiere auch nach langer Isolierung vom S war- 
fen, kann ohne weiteres durch das Auftreten des verzogerten Fortpflanzungs-Cyclus erklart 
werden. 

Literature 

Carson, R. D. (1912): Retarded development in a red kangaroo; Proc. zool. Soc. Lond. 1912, 
234-235. — Hartman, C. G. (1923): The oestrous cycle in the opossum; Am. J. Anat. 32, 
353-421. — FiEDiGER, H. (1958): Verhalten der Beuteltiere (Marsupialia); Handbuch Zool. 8, 
18 Lief 10(9), 1-28. — FiiLL, J. P., and O'Donoghue, C. H. (1913): The reproductive cycle 
in the marsupial Dasyurus viverrinus. Quart. J. micr. Sci. 59, 133-174. — Hughes, R. L. 
(1962): Reproduction in the macropod marsupial Potorous tridactylus (Kerr); Aust. J. Zool. 
10, 193-224. — Morris, D., and Jarvis, C. (Eds.) (1959): The International Zoo Year Book, 
Vol. 1; London. — Owen, R. (1839-47): Marsupialia; In: The Cyclopaedia of Anatomy and 
Physiology, Vol. 3 (ed. R. B. Todd), London. — Pilton, P. E., and Sharman, G. B. (1962): 
Reproduction in the marsupial Trichosurus vulpecula. J. Endocrin. 25, 119-136. — Sharman, 
G. B. (1954): Reproduction in marsupials; Nature, Lond. 173, 302-303. — Sharman, 
G. B. (1955): Studies on marsupial reproduction. 3. Normal and delayed pregnancy in Setonix 
brachyurus; Aust. J. Zool. 3, 56-70. — Sharman, G. B. (1962): The initiation and maintenance 



228 



20 G. B. Sharman 

of lactation in the marsupial Trichosurus vulpecula; J. Endocrin. 25, 375-385. — Sharman, 
G. B. (1963): Delayed implantation in marsupials; In: Delayed implantation (ed. A. C. En- 
ders), Chicago. — Sharman, G. B., and Calaby, J. H. (1964): Reproductive behaviour in 
the red kangaroo in captivity; C. S. I. R. O. Wildl. Res. 9 (in press). — Sharman, G. B., and 
PiLTON, P. E. (1964): The life history and reproduction of the red kangaroo {Megaleia rufa). 
Proc. zool. Soc. Lond. 142 (in press). — Tyndale-Biscoe, C. H. (1963): The rule of the corpus 
luteum in the delayed implantation of marsupials; In: Delayed implantation (ed. A. C. Enders), 
Chicago. 

Author's address: Dr. G. B. Sharman, C. S. I. R. O. Division of Wildlife Research, Canberra, 
A. C. T., Australia 



229 



REPRODUCTION AND GROWTH IN AAAINE FISHERS' 

PHILIP L. WRIGHT, Montana Cooperafive Wildlife Research Unit and Departnnent of Zoology, University of Montana, 

Missoula 
MALCOLM W. COULTER, Maine Cooperative Wildlife Research Unit, University of Maine, Orono 

Abstract: New data concerning reproduction, aging techniques, and growth of fishers (Martes pennanti) 
were obtained from 204 specimens taken from October to April during 1950-64. All female fishers more 
than 1 year old were pregnant. The immature class consisted of juveniles in their first year. The period 
of delayed implantation lasted from early spring until mid- or late winter. Nine adult females taken in 
January, February, or March showed implanted embryos. Fishers in active pregnancy had corpora lutea 
7 times the volume of those in the period of delay. Most litters are bom in March, but some as early 
as late February and some in early April. Counts of corpora lutea of 54 animals taken during the period 
of delay and during active pregnancy averaged 3.35 per female. The number of embryos, either un- 
implanted or implanted, corresponded exactly with the number of corpora lutea in 18 of 21 animals. 
Two recently impregnated 1-year-old females, recognizable from cranial characters, had tubal morulae, 
confirming that females breed for the first time when 1 year old. Also confirmed are previous findings 
of Eadie and Hamilton that juvenile females can be distinguished from adults by open sutures in the 
skull throughout their first year. Juvenile males can be recognized in early fall by open sutures in the 
skull, absence of sagittal crest, immature appearance and lighter weight of bacula, unfused epiphyses 
in the long bones, and small body size. The sagittal crest begins to develop in December and often 
is well developed by March. The baculum grows slowly during the early winter, but by February there 
was some overlap with weights of adult bacula. Male fishers showed active spermatogenesis at 1 year. 
Open sutures were found in juvenile male skulls throughout the first year. Pelvic girdles of juveniles 
were distinguished by an open pubo-ischiac symphysis; adults of both sexes showed the two innominates 
fused into a single bone resulting from at least a partial obliteration of the symphysis. Mean body weights 
of animals weighed whole in the laboratory were as follows: adult males, 10 lb 12 oz; juvenile males, 8 
lb TV2 oz; adult females 5 lb 8 oz; juvenile females, 4 lb 11 oz. 



After reaching an all-time low during the 
early part of the century, the fisher has 
made a remarkable recovery during the 
past 25 or 30 years in Maine (Coulter 1960) 
and in New York State (Hamilton and Cook 
1955). The increase in abundance of this 



high quality furbearer in New York to the 
point that it could be legally trapped al- 
lowed Hamilton and Cook ( 1955 ) and later 
Eadie and Hamilton ( 1958 ) to discover sig- 
nificant facts from studying carcasses ob- 
tained from trappers. 



^ This study is a contribution from the Maine 
and the Montana Cooperative Wildlife Research 
Units, the University of Maine, the Maine De- 
partment of Inland Fisheries and Game, the Uni- 
versity of Montana, the Montana Fish and Game 



Department, the U. S. Bureau of Sport Fisheries 
and Wildlife, and the Wildlife Management In- 
stitute cooperating. The study was supported by 
Grant GB-3780 from the National Science Foun- 
dation. 



230 



Maine Fishers • Wright and Coulter 71 



In Maine, the season was reopened in 
1950, pennitting collection of data and ma- 
terial from fishers trapped there. The pur- 
pose of the present paper is to present new 
information about reproduction, age de- 
termination, and growth of fishers, derived 
from study of Maine animals obtained be- 
tween 1950 and 1964. 

More than a dozen biologists and many 
wardens of the Maine Department of In- 
land Fisheries and Game collected material 
from trappers. Special thanks are due to 
Myron Smart, Biology Aide, who assisted in 
numerous ways throughout the entire study, 
and to Maynard Marsh, Chief Warden, who 
made arrangements for confiscated speci- 
mens to be processed at the Maine Unit. 
Numerous graduate assistants at the Maine 
Unit helped with processing carcasses and 
the preparation of skulls and bacula. We 
are indebted to Howard L. Mendall for edi- 
torial assistance and to Virginia Vincent 
and Alden Wright who made the statistical 
calculations. Margaret H. Wright did the 
microtechnique work. Elsie H. Froeschner 
made the drawings. Some of these findings 
were summarized in an unpublished Ph.D. 
dissertation presented by Coulter at the 
State University College of Forestry at 
Syracuse University. 

FINDINGS OF PREVIOUS WORKERS 

Hall (1942:147) pubHshed data from fur 
farmers in British Columbia showing that 
the gestation period in captive fishers 
ranges from 338 to 358 days and that copu- 
lation normally takes place about a week 
after the young are born. Enders and Pear- 
son (1943) described the blastocyst of the 
fisher from sectioned uteri of trapper-caught 
animals and showed that the long gestation 
period is due to delayed implantation. It 
was assumed that the blastocysts remain in- 
active from spring until sometime during 
winter. De Vos ( 1952 ) studied fishers in 



Ontario and made preliminary attempts to 
establish an aging method based upon skulls 
of males and females and the bacula of 
males. Hamilton and Cook ( 1955 ) pub- 
lished information about the current status 
of fishers in New York State and described 
a technique for recovering the unimplanted 
blastocysts from fresh reproductive tracts 
by flushing them out with a syringe. Eadie 
and Hamilton (1958) provided additional 
data on the numbers of blastocysts in preg- 
nant tracts and described cranial differ- 
ences between adult and immature females. 

MATERIALS AND METHODS 

Coulter collected material in Maine from 
trapped fishers, starting in 1950 when the 
season was first reopened. The intensity of 
the collection varied over the years depend- 
ing upon the legal regulations in effect. 
Data are available from 204 animals. 

In addition to animals legally taken dur- 
ing the trapping season, Coulter obtained 
a number of animals both before and after 
the season, taken by trappers who were 
trapping other species, primarily bears and 
bobcats. Trappers who caught fishers ac- 
cidentally were required to turn them over 
to the Department of Inland Fisheries and 
Game which in turn brought or sent them 
to the Maine Unit at Orono where they 
were autopsied by Coulter. Unskinned fish- 
ers as well as skinned carcasses were sub- 
mitted to the laboratory. Whenever possi- 
ble, weights were taken immediately before 
and after skinning to obtain an index for 
converting the weights of carcasses re- 
ceived from trappers to whole weights. 
During the trapping season carcasses were 
collected at trappers' homes. Usually the 
material was submitted in fresh condition; 
often it was frozen or thoroughly chilled 
when received at the laboratory. Because 
of the interest of the cooperators, most of 
the material was accompanied by collection 



231 



72 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 



dates, method of capture, locality, and other 
notes. These data together with measure- 
ments, weights, observations about the con- 
dition and completeness of the specimens, 
and a record of material saved for future 
study were entered on individual cards for 
each animal. 

A special effort was made from the fall 
of 1955 to the spring of 1958 to obtain com- 
plete skeletons, and 59 such specimens were 
obtained. Coulter trapped a series of espe- 
cially needed animals in late March and 
early April, 1957. Because of excellent co- 
operation by State Game Wardens and Re- 
gional Biologists, a good sample of speci- 
mens was available for study over a 6- 
month period from October to April. 

This series of fishers is an unusually valu- 
able one for discerning important aspects 
of the growth and the reproductive cycle of 
this mustelid. For example, nine females in 
active pregnancy were obtained, as well as 
several adult males in full spermatogenesis. 
Furthermore, the juvenile fishers were grow- 
ing and maturing rapidly during the col- 
lecting period, and this fairly large collec- 
tion has allowed us to reach significant con- 
clusions concerning the onset of sexual ma- 
turity and the distinction between the age 
classes with more assurance than de Vos 
( 1952 ) was able to do with more limited 
material. 

The reproductive tracts of female fishers 
were removed in the laboratory and pre- 
served in 10-percent formalin, in AFA, or 
in special cases, Bouin's fluid. The bacula 
of all the males were air-dried, as were the 
skulls of both sexes. Testes from a few rep- 
resentative males were fixed in formalin 
also. Coulter solicited the cooperation of 
Wright in 1955 and all of the material then 
available was shipped to him for further 
analysis and for histological work. Most of 
the skeletal material was cleaned by der- 
mestid beetles in Montana. 



This study was carried out without the 
aid of known-age specimens. Since the 
study was completed, three known-age ani- 
mals have become available: an 18-month- 
old female in Maine which was in captivity 
for 1 year, and two females captured in 
central British Columbia, released in west- 
ern Montana, and recaptured 6 years later. 
Study of these three animals in no way af- 
fects the findings presented in this paper. 
Evidence is presented to indicate that 
young-of-the-year animals can be distin- 
guished from adults by studying either 
their skulls and skeletons or their reproduc- 
tive tracts. Animals judged by these criteria 
to be less than 1 year old are, for conve- 
nience, referred to as juveniles even though 
in a few cases they may be almost 1 year 
old. Except for one criterion for distinguish- 
ing yearUng females from older adult fe- 
males, described by Eadie and Hamilton 
(1958:79-81) and confirmed here, no method 
of determining the relative ages of adults 
was discovered. 

Wherever appropriate, standard devia- 
tions and standard errors have been calcu- 
lated, but generally such figures are not 
presented here. Wlien it is stated that a 
significant or highly significant difference 
exists, it is based upon the use of the t test. 

FINDINGS 

Female Reproductive Tracts 

The reproductive tract of the female fisher 
is similar to that of other mustelids. The 
ovaries are completely encapsulated with 
only a small ostium through which a small 
portion of the fimbria extends. The ovary 
must be cut free from the bursa under a 
dissecting scope with a pair of fine scissors. 
The oviduct encircles the ovary as in other 
mustelids. The oviducts were not highly 
enlarged in any animals studied, since no 
estrous stages were seen. The uterus has a 
common corpus uteri which allows embryos 



232 



Maine Fishers • Wright and Coulter 73 



developing in one horn to migrate to the 
other horn. The uterine horns are 40-60 mm 
long in adult females in inactive pregnancy, 
and 2y2-4 mm in diameter. Immature fish- 
ers show smaller uteri with horns about 30- 
40 mm long and IV2-2V2 mm in diameter. 
No search was made for an os clitoridis. 

The ovaries from each preserved tract 
were dissected from the fixed reproductive 
tract, blotted, and weighed. Each ovary 
from animals taken in fall or early winter 
was sliced macroscopically and the number 
of corpora lutea present determined by the 
use of a dissecting microscope. Of the 77 
tracts handled in this way, 44 animals 
showed corpora and were thus judged to be 
adults. Thirty-three animals were without 
corpora and were judged to be immature. 
The average combined weights of the 
ovaries was 134.4 mg for adults and 76.5 
mg for immatures. The average weight of 
the left ovaries ( I — 40.3 mg, A— 70.0 mg ) 
was greater than that of the right ovaries 
(1—36.2 mg, A— 64.4 mg) in both im- 
matures and adults, but no special signifi- 
cance is ascribed to this matter. The aver- 
age number of corpora lutea from this series 
of 44 adult females was 1.68 in the right 
ovaries and 1.60 in the left; the average was 
3.28 per adult female. Eadie and Hamilton 
(1958) reported that the mean number of 
corpora lutea in 23 adult New York fishers 
was 2.72. The difference in the average 
number of corpora lutea between the Maine 
and New York samples is highly significant. 
The distribution of the corpora lutea from 
all of the Maine, pregnant animals is shown 
in Table 1. 

To determine the relationship between 
the number of corpora lutea in the ovaries 
and the number of blastocysts in the uteri, 
11 tracts of adult females were studied in 
detail. After the ovaries were removed and 
sectioned by hand, uteri were selected that 
appeared to be the best preserved. These 



Table 1. Distribution of corpora lutea in ovaries of preg- 
nant Maine fishers. 







No. OF Cor- 




No. OF 




pora IN 




Corpora in 


No. OF 


Both Ova- 


No. of 


Single 


Cases 


ries of 


Females 


Ovaries 




Individual 
Females 





4 
3 
2 
1 




2 
14 

42 

43 

8 

Total 109* 



5 
4 
3 
2 



1 
21 
30 

2 

54 



* One case in which only one ovary available. 

entire uteri were dehydrated and cleared 
in wintergreen oil. Study of the entire 
cleared tract under a dissecting scope using 
transmitted light often revealed the loca- 
tion of blastocysts. Serial sections of each 
of these tracts were made to locate the 
blastocysts. As soon as all of the expected 
blastocysts were found, no further section- 
ing of that tract was done. In some cases 
the entire uterus was sectioned before all 
the blastocysts could be located, and in 2 
of the 11 tracts, 1 potential blastocyst was 
not found. This represents a loss of only 6 
percent, as there were 35 corpora in the 
ovaries of the 11 animals and 33 blastocysts 
were located. The technique of Hamilton 
and Cook (1955:30-31) of flushing the 
uteri for the blastocysts was not followed 
here since the tracts had been fixed in for- 
malin. 

The sectioned blastocysts were similar to 
those described by Enders and Pearson 
(1943:286). The extremely thick zona pel- 
lucida, 14.4 /a according to these authors, 
makes it possible to find the blastocysts in 
very poorly preserved material. None of 
the blastocysts studied was in better condi- 
tion than those seen by Enders and Pearson, 
and the relative numbers of nuclei in the 
trophoblast and the inner cell mass for this 
species is still not known. In order to ob- 



233 



January, 1965 
February 2, 1961 


118 


77 


3 


1 


February 7, 1956 
February 21, 1964 
Late February, 1959 
March 3, 1959 


182 

110 

98 

179 


98 

73 

108 

138 


3 

2 

1 
3 




1 
3 

1 


March 11, 1965 






2 


1 


March 13, 1956 
March 20, 1957 


92 
121 


92 
137 


2 
1 


1 

2 



74 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 



Table 2. Findings in nine reproductive tracts of female fishers in active pregnancy. 

Weight of Distribution of 

Date Ovaries (mg) Corpora Lutea State of 

Killed Uterus 

Right Left Right Left 

3 embryos, 18 mm CR (Crown-Rump) 

4 embryos, 2R, 2L, 17-mm swelhngs, em- 
bryo 8 mm CR 

3 embryos, IR, 2L, embryo 13 mm CR 

3 embryos, 2R, IL, embryo 18 mm CR 

4 embryos, 2R, 2L, embryo 8 mm CR 
4 fetuses, 2R, 2L, 2 males, 2 females, 

fetuses 53, 54, 55, 57 mm CR 
3 fetuses, 2R, IL, 3 males, fetuses 69, 71, 

74 mm CR 
3 early embryos, 2R, IL, 7-mm swellings 
3 fetuses, 2R, IL, 3 females, fetuses 74, 

80, 83 mm CR 

tain such material, adult tracts would have young before the end of February. Two re- 

to be preserved in a matter of minutes after cently captured females produced litters on 

the animal was killed. March 2 and on March 20 at the Maine 

Tracts of nine adult fishers in which Unit. The evidence indicates that the ma- 
there were implanted embryos were studied jority of Maine fishers produce their litters 
(Table 2). Studies of the marten and a during the month of March, but some do so 
weasel are of some value in estimating the as early as mid-February, and some as late 
times of parturition in these tracts. Jonkel as early April. 

and Weckwerth (1963:96-97) made a The ovaries of female fishers with im- 

series of laparotomies on late-winter adult planted embiyos were all serially sectioned, 

female marten ( Martes americana ) and de- The ovaries are much larger than those in 

termined that the interval between implan- inactive pregnancy, the average combined 

tation and parturition was less than 28 days, weight being 231.9 mg as compared with 

In the long-tailed weasel (Mustela frenata), 134.4 mg for the inactive group. The 

Wright (1948) showed that the postimplan- corpora lutea are markedly enlarged in 

tation period lasted about 23 or 24 days, active pregnancy as is generally known in 

In estimating the parturition dates from the mustelids with long periods of delayed im- 

pregnant fisher tracts it is assumed that the plantation (Wright 1963:87). The corpora 

period of active pregnancy is about 30 days, of three of these animals averaged 2,380, 

This seems reasonable on the basis of the 2,917, and 3,057 /x in diameter, whereas 

larger size of the fisher in comparison with corpora from two animals with unimplanted 

the marten and the weasel. blastocysts averaged 1,387 and 1,219 /x. Al- 

The female fisher with the largest fetuses, though these corpora in animals with im- 

taken on March 20, would probably have planted embryos are more than seven times 

borne young before April 1. The one with the volume of those with unimplanted em- 

the earliest stages was taken on March 13, bryos, the increased size of the ovaries is 

and it is estimated that her litter would not not due solely to the increase in corpus size, 

have been born until after April 1. The one In no case is the histological preservation 

with the 13-mm ( crown-rump ) embryos, of high quality, but the corpora lutea were 

taken on February 7, would have borne her readily seen and counted in all ovaries. 



234 



Maine Fishers • Wright and Coulter 75 



There is a great deal of interstitial tissue in 11 tracts which were preserved during in- 
all of these ovaries, and in this they differ active pregnancy and which were sectioned 
from weasel ovaries (Deanesly 1935:484) in to locate all of the blastocysts, 
which the interstitial tissue is most active On a few occasions at the time of au- 
in late summer but by implantation time topsy, Coulter observed darkened areas in 
shows considerable degeneration. There the uteri which were apparently placental 
are also numerous small and medium-sized scars. After being fixed and cleared, most 
follicles in these fisher ovaries. In all cases of these areas were no longer visible, 
the cells of the corpora lutea are highly Wright (1966:29) found that in the badger 
vacuolated. Vacuolated cells in corpora are ( Taxidea taxus ) placental scars can readily 
common in many mustelids during the be found in cleared tracts of parous fe- 
period of inactive pregnancy. Eadie and males, provided the uteri were preserved at 
Hamilton (1958:78) noted that their fisher once after death. Placental scars are diffi- 
corpora in ovaries in inactive pregnancy were cult to find, even in lactating badgers, in 
highly vacuolated. Wright and Rausch material that is not freshly preserved. It 
(1955:348-350) describe vacuolated corpora seems likely that the general level of preser- 
in the wolverine {Gido gulo) in inactive preg- vation in these fisher tracts was not good 
nancy, but during active pregnancy the enough to preserve placental scars, 
vacuolation had disappeared. It appears 
then that vacuolated corpora lutea during Breeding Season 

active pregnancy is a condition not com- Earlier workers, Hall (1942:147), for 
monly seen in this group. We suppose that example, indicate that the female fisher 
the corpora lutea of active pregnancy are breeds soon after her litter is born; thus 
secreting progesterone, whereas during the the gestation period may be as long as 51 
inactive period there may be no active weeks. Since no recently postparturient 
secretion of progesterone. This is suggested tracts were available for study, this particu 
by the urine analysis conducted in various lar point could not be confirmed from wild- 
stages of pregnancy by Ruffie et al. ( 1961 ) caught animals. However, among speci- 
on the European badger {Meles meles) mens collected in late March and early 
which has a similar reproductive cycle. April, 1957, two recently bred nulliparous 

The number of embryos or fetuses in females were obtained and the tracts pre- 

these eight animals averaged 3.38 and in served fresh. These two tracts are the bes*- 

each case the number of corpora lutea cor- preserved in the entire series, and tuba 

responded to the number of embryos; that embryos were found in each by serially sec- 

is, there was seen here no loss of potential tioning the oviducts. Each animal had 

embryos that may have occurred during three corpora lutea, 2 R, and 1 L, and 3 

either the preimplantation period or the morulae were found in one and 2 in the 

postimplantation period. other. In the one taken on March 28, one 

There was evidence of migration of em- morula had about 228 nuclei (Fig. lA); the 

bryos from one uterine horn to the other in other embr\'os were of comparable devel- 

five of the eight animals. Migration of em- opment, but it was not possible to count 

bryos is well known in other mustelids. It the nuclei. 

apparently occurs largely during the process The animal taken on April 4 showed 2 

of spacing just before implantation. Only morulae with 12 and 20 nuclei (Fig. IB). 

one example of migration was seen in all No evidence was found of the expected 



235 



76 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 




-^ 




m 



\h 



'■f 



:<V' 






Fig. 1. Photomicrographs of tubal morulae from recently impregnated female fishers. (Left) Embryo of about 225 nuclei, 
from 1 -year-old female taken on March 28. (Right) Embryo of about 12 nuclei from oviduct of 1 -year-old female taken 
on April 4. 



third embryo. The only musteUd possess- 
ing a long period of delay in implantation 
in which the rate of cleavage is known is 
the long-tailed weasel (Wright 1948). If 
the fisher has a comparable slow rate of 
cleavage, the March 28 animal was impreg- 
nated about March 18, and the April 4 
specimen was impregnated about March 
27. This is probably about the same time 
as recently parturient females would be im- 
pregnated. The young developing from 
these tubal embryos would normally have 
been bom about 1 year later. 

The ovaries of these nulliparous animals 
were largely masses of interstitial tissue, 
apparently of cortical origin. There were 
no graafian follicles of medium or large 
size. The small, almost fully formed corpora 
lutea with organized connective tissue cen- 
ters also suggested that ovulation had oc- 



curred some 8 or 10 days earlier. The luteal 
cells were not vacuolated. The medulla of 
these ovaries was discernible only as a 
small area adjacent to the mesovarium. 

Both of these recently bred females, even 
though nulliparous, showed slight mam- 
mary development. In weasels, Wright (Un- 
published data) has never seen mammary 
development associated with the summer 
breeding season. The nipples become con- 
spicuous for the first time about the time 
of implantation. 

Both of the fishers in question were 
judged to be 1 year old, on the basis of the 
development of both their skulls and skele- 
tons. Another nulliparous female taken at 
the same time, March 27, was also judged 
to be 1 year old, but showed no sign of 
reaching estrus. This animal might have 
attained estrus within 2 or 3 weeks. 



236 



Maine Fishers • Wright and Coulter 77 



Table 3. Findings in tracts of male fishers taken in late winter and early spring. 





Weight 




















OK Com- 




Paireu 




Status 












bined 


Paibed 


Epi- 


Status of 


OF 


Baculum 


Esti- 






Date 


Testes 


Testis 


didymis 


Sperm in 


Sperm 


Weight 


mated 


Body 




(1957) 


AND Epi- 


Weight 


Weight 


Testes 


IN Epi- 


(mg) 


Age of 


Weight 






didymides 

(G) 


(G) 


(G) 




didymides 




Animal 






January 5 


2.7 


1.8 


0.4 


None 


None 


1262 


Juv. 


7 lb 3 


oz 


February 26 


7.4 


5.6 


1.4 


Active 
spermato- 
genesis 


None 


? 


? 


? 




February or 




















early March 


6.3 


4.8 


1.1 


None 


None 


1725 


Juv. 


10 lb 7 


oz 


March 1 


6.3 


4.8 


1.0 


Active 

spermato- 
genesis 


Few 


1252 


Juv. 


8 lb 5 


oz 


March 1 


8.6 


6.9 


1.3 


Abundant 


Abundant 


1550 


Juv. 


9 lb 12 


oz 


March 1-15 


10.3 


7.6 


1.9 


Abundant 


Abundant 


1562 


Adult 






March 17 


11.3 


8.6 


1.9 


Abundant 


Abundant 


1522 


Adult 


11 lb 5 


oz 


March 27 


7.4 


5.8 


1.2 


Abundant 


Abundant 


1921 


Adult 


8 lb 3 


oz 


March 27 


13.0 


9.8 


2.2 


Abundant 


Abundant 


2053 


Adult 


14 lb 6 


oz 


April 4 


9.0 


7.0 


1.7 


Abundant 


Abundant 


1800 


Adult 


9 lb 5 


oz 



Coulter has often noticed a definite 
change in travel pattern beginning in March 
and suspects that it is associated with breed- 
ing activities. Earlier, the animals are fairly 
solitary and travel in long routes in more 
or less direct fashion. But during March 
there are numerous cases of animals travel- 
ing together. The incidence of scent posts 
is much higher than in early or midwinter. 
At this season, reports are received of 
"dozens of fisher" in a given locality. Closer 
study shows that only two or three animals 
may be responsible for an unbelievable 
maze of tracks in a small area. 

In the European badger, which may also 
have a gestation period of almost a full 
year, both Neal and Harrison (1958:115- 
116) and Canivenc and Bonnin-Laffargue 
(1963:121-122) present evidence for sterile 
matings occurring outside of the usual 
breeding season and ovulation in animals 
already in inactive pregnancy. Although no 
fishers were obtained during the period ex- 
tending from early April until October, it is 
clear from the material at hand that ovula- 
tion occurs only during the breeding sea- 



son, and there is no evidence of sterile 
matings. 

Male Tracts 

Since testes were generally inactive dur- 
ing the trapping season, they were not 
routinely saved from trapper-caught speci- 
mens. With a breeding season in March 
and April, it was obvious that late-winter 
animals would show transitional stages from 
the inactive early-winter condition to the 
active state in the breeding season. An ef- 
fort was made, therefore, in the late winter 
of 1957 to preserve testes from available 
males. The results of the observations are 
included in Table 3. 

The weights of the combined testes and 
epididymides were obtained after first 
stripping free the tunica vaginalis. Then 
the testes were further separated from the 
epididymides and both were weighed again. 
Thus, the total of the separated weights 
does not equal the combined weights be- 
cause additional connective tissue and fat 
had been removed. Representative sections 
of testes from each animal and from the 



237 



78 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 




Fig. 2. Dorsal and ventral views of adult and juvenile fisher pelvic girdles. (A) Dorsal view of adult $ showing complete 
disappearance of the symphysis in a portion of the anterior half of pubo-ischioc junction. (B) Ventral view of adult $ 
showing almost complete disappearance of pubo-ischiac symphysis. There are conspicuous rugosities projecting from each 
side of the symphyseal line. (C) Dorsal view of juvenile 9 showing complete separation of the innominates by symphyseal 
cartilage. (D) Ventral view of juvenile $ in which the two innominates are completely separated by a substantial symphys- 
eal cartilage. 



tail of the epididymis were prepared and 
stained. 

The juvenile male taken on January 5 
was aspermatic. By late February and early 
March three juveniles showed somewhat 
enlarged testes, but only one of these ani- 
mals was in breeding condition. All of the 
adults taken from early March into early 
April were fully developed with abundant 
sperm in the tails of the epididymides. It 
would have been desirable to have tracts 
from additional males taken earlier in the 
winter. The results indicate, however, that 
adult males are fully active sexually during 
the breeding season; and the young males, 
now just 1 year old, are also apparently in 
breeding condition. 

Skeletal Development 

The series of 59 skeletons was studied 
with respect to the fusion of the epiphyses 
in each of the long bones and representa- 
tive vertebrae. Sixteen specific sites were 



studied in addition to the status of fusion 
of the pubo-ischiac symphysis and certain 
sutures in the skulls. 

Examination of the November and De- 
cember skeletons showed striking differ- 
ences between two groups, apparently ju- 
veniles and adults, in both sexes. All of the 
sutures studied were open in November and 
December males judged to be juveniles; and 
most of the sutures were only partly closed 
in comparable females thought to be ju- 
veniles. The obviously juvenile animals 
were smaller and showed many open sutures 
in the skulls. The bacula of the males in 
this group were small and weighed less than 
1,000 mg, compared to an average of more 
than 2,000 mg for those with closed sutures. 
The ovaries of females regarded by skeletal 
criteria as juveniles were all without corpora 
lutea; the ovaries of all those classed as 
adults possessed corpora lutea. 

The pubo-ischiac symphysis clearly re- 
mains open longer than most of the sutures. 



238 



Maine Fishers • Wright and Coulter 79 



It was completely open in all animals that 
were regarded as less than 1 year old taken 
throughout the fall, winter, and early 
spring. It was at least partially obliterated, 
when \iewed either dorsallv or ventrallv, 
in all animals regarded as more than 1 year 
of age (Fig. 2). The findings of striking 
differences in the fusion of this symphysis 
parallel those of Taber (1956), who de- 
scribed differences in this symphysis ex- 
tending over several years in deer (Odo- 
coileus herniontis and O. virginianus) . The 
pubo-ischiac symphysis should be studied 
in other mammals in which aging criteria 
are needed. 

Baculum 

Weights of bacula are shown in Fig. 3, 
and drawings of representative types are 
shown in Fig. 4. The bacula of adults are 
more than 100 mm long, and they com- 
monly weigh 2,000 mg or more. The fully 
mature baculum shows an elevated ridge 
near the proximal end that completely en- 
circles the bone in a diagonal line when 
viewed from the side. The bacula of ju- 
veniles taken in the fall and early winter 
are much smaller. Although they show the 
typical splayed tip at the distal end, which 
is universally perforated by a small, round, 
or oval foramen, they do not show the en- 
larged proximal end typical of the adults. 
The series of bacula in Fig. 3 shows that 
those of the juveniles are growing rapidly 
during the winter months. By February 
some of them weigh as much as 1,600 mg 
(one 2,099 mg) and thus overlap the weight 
of those of adults. Two such bacula are 
shown in Fig. 4, F and G. Since the testes 
of juveniles in February were becoming 
active, it seems reasonable to assume that 
such animals were secreting androgen at 
high levels. 

The fully adult baculum undoubtedly 
develops under the influence of androgen. 



3000 



2800 



2600- 



2400- 



e> 2200- 



■ 2000- 



UJ 

1600- 



1400 



1200- 



1000- 



800 



600- 



400 



• • 



• • t 

o* 



o 



•• ^- 






• • 



o 
o 
o 

o o 
o 



OCT 



NOV 



T 



DEC 



JAN 



TT^rr 



MAR 



T 



APR 



Fig. 3. Baculum weights. Adults are shown in solid dots, 
juveniles with open circles. The continued growth of the 
juvenile baculum during the winter months is clearly shown 
as is the overlap in weights of February, March, and April 
juveniles and adults. 

as it probably does in all mustelids. This 
was demonstrated (Wright 1950) to be the 
case in the long-tailed weasel. Probably the 
fully adult type of baculum would develop 
by late spring in these year-old males, since 
Deanesly (1935:469) concluded that the 
adult baculum of the European stoat 
{Mustela erminea) develops to adult type 
within 1 month after the testes become 
active for the first time. Although Elder 
(1951:44) showed that bacula may continue 
to develop in succeeding years in sexually 
mature mink (Mustela vison), the lack of 
known-age fishers in this series does not 
make such conclusions possible here. The 
tentative conclusion reached by de Vos 
(1952), that bacula were not of value in 
distinguishing adult from juvenile fishers, 
resulted from failure to recognize changes 



239 



80 Journal of Wildlife Managemeni, Vol. 31, No. 1, January 1967 




240 



Maine Fishers • Wright and Coulter 81 



in the rapidly maturing skulls of juvenile 
male fishers during the late winter. This 
will be discussed further in a later section. 

Skulls 

The specimens were placed in four 
groups (adult males, juvenile males, adult 
females, and juvenile females) on the basis 
of reproductive condition and skeletal 
analysis, and 12 measurements were taken 
of each skull (see Wright 1953:78-79). 
Means, standard errors, and coefficients of 
variation were calculated for each group. 
It is clear from study of these statistics that 
the skulls of tlie juvenile animals in both 
sexes have not reached maximum growth. 
In many cases the differences between the 
means is statistically significant, but, be- 
cause of overlap between the measure- 
ments in adults and juveniles, it is not pos- 
sible to develop aging criteria based on 
measurement of a single skull parameter, 
with one exception to be discussed later. 

The differences between the means of 
these measurements was generally much 
greater among males than among females. 
For example, the mean weight of adult 
male skulls was 70.6 g, whereas in juvenile 
males it was 53.9 g, a difference of some 
20 percent. In female skulls, however, the 
adults average 32.1 g and the juveniles 31.1 
g, a difference of only 3 percent. 

The postorbital constriction becomes 
somewhat smaller with increased age in 
both sexes of fishers, as it does in other 
mustehds. Another striking difference be- 



tween adult and juvenile skulls was seen in 
males where the zygomatic breadth averages 
77.4 mm in adults and only 64.8 mm in 
juveniles. In spite of this 18 percent smaller 
measurement in juveniles, there is overlap. 
It is not possible to classify a male fisher as 
juvenile or adult solely on the basis of this 
measurement. Tire difference in zygomatic 
breadth would, in most cases, produce a 
broader appearing face on adult males than 
on juvenile males. 

The sutures in the skulls of fishers, like 
those of all other mustelids, tend to dis- 
appear at a relatively young age (Marshall 
1951:278, Greer 1957:322^23) as com- 
pared to the Ursidae, for example, where 
they persist for many years (Rausch 1961: 
86, Marks and Erickson 1966:398). Juvenile 
male fishers taken in early fall (Fig. 5A) 
show almost all of the sutures unfused, but 
on specimens during March or April (Fig. 
5C) almost all have completely disappeared. 
Eadie and Hamilton (1958:77) showed, in 
New York fishers from which they had re- 
productive tracts, that "All breeding fe- 
males showed at least partial fusion of the 
temporal ridges ... to form a sagittal crest, 
and [that] the maxillary-palatine sutures 
were completely fused. Non-breeding fe- 
males showed the temporal ridges in various 
degrees of separation and had the maxillary- 
palatine sutures at least partly open. It is 
concluded that female fisher normally 
breed at the age of one year in the wild, 
and that these criteria will separate young- 
of-the-year from adults." 



Fig. 4. (A) Lateral view of skull of winter juvenile male, February, showing well developed sagittal crest and open zygo- 
matic-maxillary suture. (B) Lateral view of skull of fully adult male showing typical tremendously developed sagittal crest 
and disappearance of zygomatic-temporal suture. The heavily worn teeth shown ore not necessorily characteristic of adult 
fishers. (C to J) Bacula of male fishers showing progressive changes with age, distal end to the top, the youngest to the 
left and oldest to the right. C, D, and E ore from juveniles, C taken October 12, D taken December 3, E taken January 5. 
F and G are from late winter juveniles showing progressive changes toward the adult type with increased deposition of bone 
at the basal end. Both F and G were taken in February or early March. H, I, and J ore selected adult bacula showing the 
characteristic oblique ridge near the basal end and generally more massive appearance. H is from a smaller-than-average 
male (body weight, 9 lb, 5 oz), I and J from iarger-than-overoge males (I, carcass weight 10 lb; J, body weight, 14 lb 
6 oz). 



241 



82 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 




242 



Maine Fishers • Wright and Coulter 83 



Our findings from study of 66 female 
fishers from Maine, from which comparable 
data were available, confirm in detail the 
findings of Eadie and Hamilton ( 1958 ) . It 
is also clear that the maxillary-palatine su- 
ture is among the last, if not the last, to 
disappear. 

These authors also describe a frequency 
distribution in the length of the sagittal 
crests in adult females, and reference to 
their Fig. 3 shows that there are two peaks 
of sagittal crest lengths which they tenta- 
tively regarded as representing a group of 
iy2-year-old females and another group of 
older females. When we plotted our data 
in comparable fashion, the line exactly 
paralleled theirs; and there is thus further 
evidence that such separation into young 
adults and older adults is possible. The 
distribution of the lengths of the sagittal 
crests of the adult Maine female fishers, 
plotted in the same fashion as did Eadie 
and Hamilton, is as follows: 0-10, 1; 11-20, 
11; 21-30, 3; 31-40, 8; 41-50, 19; 51-60, 1. 

The findings in the skulls and skeletons 
of the two recently bred nulliparous fe- 
males, whose reproductive tracts were des- 
cribed in an earlier section, also provide 
significant evidence that the onset of breed- 
ing in female fishers occurs when they are 
1 year old. In each case there was no 
sagittal crest, and the maxillary-palatine 
suture was partially open. Eadie and Ham- 
ilton (1958:79) found this suture closed 
in all New York fishers judged to be adults. 
In their collection, adult fishers, taken en- 



tirely in fall and winter, would have been 
at least 20 months old, whereas our two 
animals were almost exactly 1 year of age. 
One of these animals shows the pubo- 
ischiac symphysis still open; the other 
shows it partly closed. Further, the fact 
that during the fall and winter there is only 
one type of skull to be found in fishers that 
have not bred makes it virtually certain 
that wild Maine fishers are regularly im- 
pregnated at the age of 1 year and thus 
produce their first litters at the age of 2 
years. 

The sagittal crests of adult male fishers 
are extremely well developed as was men- 
tioned by Coues (1877:65), and the degree 
of sexual dimorphism in skulls of fishers is 
greater than in any other American muste- 
lid. All adult females develop sagittal 
crests, but even the most highly developed 
crests in females are almost vestigial com- 
pared with those of adult males. It is natu- 
ral to suspect that with this tremendous 
development in mature males the crest 
might begin to develop earlier in juvenile 
males than in females. This is exactly the 
case, and sagittal crests were first seen in 
one of two juvenile males taken in Decem- 
ber (Fig. 5B). By February, March, and 
April the crests of the juvenile class, now 
almost 1 year old, are well developed ( Fig. 
5C), as much so as they ever become in 
adult females. 

In the female fishers it is clear that the 
sagittal crest develops first at the posterior 
end of the skull and grows progressively 



Fig. 5. Dorsal view of male fisher skulls showing characteristic changes associated with development. (A) Juvenile mole, 
October 12, showing narrow zygomatic breadth, all sutures in nasal region clearly open; the frontoparietal sutures are 
partly fused. The poorly developed temporal lines are wide apart and thus there is no sagittal crest. (B) Juvenile male, 
December 3, showing disappearance of fronto-parietal suture, less conspicuous sutures in nasal region, and characteristic early 
development of sagittal crest running throughout the middle and posterior portions of the cranium. (C) Juvenile male in late 
winter, February, in which these naso-maxillary and maxillary-frontal sutures are barely visible, but the zygomatic-temporal 
sutures are still very distinct and the sagittal crest is better developed. (Same skull as shown in Fig. 4A). (D) Skull of adult 
male in which the entire dorsal skull is ankylosed into a single unit; no suture visible except for faint remains of posterior 
internasal suture. The characteristic highly developed keel-like sagittal crest of all adult males is clearly shown. (Same 
skull as shown in Fig. 4B). 



243 



84 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 



forward over a period of months or prob- as well as his "juvenile" class, and that only 

ably years. In the male fisher the temporal the animals he called "old adults" were 

lines move rapidly together during the win- adult males over 1 year of age. 

ter months; and as soon as the crest is It is concluded, therefore, that during 

formed, it mns essentially the entire length the early winter, adult males can be sepa- 

of the dorsal region from the postorbital rated from juvenile males by the occur- 

constriction to the inion, a distance of 50- rence of a well developed sagittal crest on 

60 mm. The sagittal crest continues to adults; but by mid- or late winter only those 

develop in adult males, and they have the males with all of the skull sutures closed 

crest developed to the extent of forming a are adults, 
"thin, laminar ridge" (Coues 1877:65). It 

is difficult to measure the extent of this Body Weights 

ridge objectively; but since it extends Both de Vos (1952) and Hamilton and 

posteriorly in fully adult males, one can use Cook ( 1955 ) have provided body weights 

the method employed by Wright and Rausch of wild-caught fishers, and both studies 

( 1955 ) on wolverines to subtract the con- show that males often weigh twice as much 

dylobasal length from the greatest length as females. The latter indicate an average 

of the sk-ull. This is one accurate method weight for males of 3,707 g (8 lb 3 oz) and 

of showing the posterior extension of this 2,057 g (4 lb 9 oz) for females. De Vos's 

crest. This indirect measurement shows no figures are roughly comparable. In both 

overlap whatever between males classed studies many of the body weights were esti- 

as adults and those classed as juveniles, mated from carcass weights by applying a 

The mean for the former group is 11.9 mm correction factor to skinned carcasses. (Most 

and for the latter, 3.9 mm (see Fig. 4, A fisher specimens coming to biologists are 

and B). Thus in male skulls if the differ- likely to be carcasses skinned by trappers.) 

ence between the greatest length of the Hamilton and Cook (1955:21-22) state 

skull and the condylobasal length is 6 or that the fresh carcasses average 80 percent 

more mm (may be as much as 15 mm), of the unskinned weight. In the present 

the animal is an adult; if it is less than 6 study many fishers were confiscated and 

mm, the animal is a juvenile. were available intact. Thus, it was pos- 

Another reason for assuming that skulls sible to obtain a sample of weights taken 

of males with immature bacula, but with directly from the entire unskinned carcasses, 

sagittal crests, are still in their first year of allowing consideration of differences be- 

life is provided by data on the closure of tween adult and juvenile classes in both 

sutures in the skull. The last sutures to sexes. 

close in males are the zygomatic-temporal, Data obtained from those fishers which 

the naso-maxillary, the internasal, and the were weighed entire in the laboratory are 

naso-frontal. In all of the skulls classed as shown in Table 4. The differences between 

adult, all of these sutures were closed, but the juveniles and adults in both sexes is 

in every male skull classed as juvenile, all highly significant although there is some 

four of these sutures were still open ( Figs, overlap in each case. Furthermore, juvenile 

4 and 5 ) . males are significantly heavier than the 

On the basis of this evidence, it seems adult females. The available mean weights 

clear to us that males classed by de Vos of adults are probably more satisfactory 

(1952) as "adults" were in effect juveniles than those of the juveniles. Presumably, 



244 



Maine Fishers • Wright and Coulter 85 



tlie adults were no longer growing, but 
the ]u\eniles were growing throughout the 
collection period from October to April. 
The sample is not large enough to allow a 
breakdown \\ithin the juvenile classes b\" 
month, but the smallest juveniles were 
taken in the fall. 

The fact that weights of the juvenile 
males are 21 percent less than those of the 
adult males, while the weights of juvenile 
females are onh" 15 percent less than those 
of the adult females, further indicates that 
juvenile female fishers are more nearly full 
grown during the first winter of life than 
are the juvenile males. 

In man\- cases, the fishers that were 
weighed whole were also weighed after 
skinning. This allowed detennination of 
a correction factor. Thirty-nine animals 
were weighed both before and after skin- 
ning: 14 adult males, 5 juvenile males, 
8 adult females, and 12 juvenile females. 
The carcasses averaged 81.9 percent of 
the whole weight; or, stated conversely, 
one could multiply the carcass weight by 
1.22 to obtain an estimate of the entire 
adult weight. This latter conversion factor 
was applied to those animals that were 
weighed only after being skinned. Esti- 
mated entire body weights obtained in 
this fashion were comparable for both adult 
and juvenile males, but weights of females 
were significantly below the weights of 
those females weighed entire. For this 
reason, it was obvious that in the interval 
between skinning and weighing, many of 
the female carcasses had lost significant 
weight. It was therefore necessary to aban- 
don any attempt to use the more numerous 
carcass weights for interpretation of pos- 
sible growth rates in the juveniles or other 
weight changes that might exist between 
months. 



Table 4. Body weights of Maine fishers weighed whole. 



-No. Mean Body sf. 

Class ok Weight in Max. Min. 

Ani- (0UNt:ES) oz 

MALS 



Adult S 23 172.1 ±6.30 14- 6 7-4 

(10 lb 12 oz) 
Juv. 6 10 135.5 ±7.08 10- 8 6-8 

(8-71/2) 
Adult 9 13 88.2 ±3.61 7-11 4- 8 

(5-8) 
Juv. 9 17 75.0 ±2.35 6- 8 3-13 

(4-11) 

DISCUSSION 

Tliis study indicates that in the fisher the 
adult class consists of all animals more than 
1 year of age and that all animals of both 
sexes less than 1 year are sexually imma- 
ture. Females older than 1 year normally are 
carrying unimplanted blastocysts through- 
out the year except during active preg- 
nancy in late winter. The fisher, then, 
differs from all other American mustelids 
studied in this regard except the wolverine. 
The weasels, Mustela erminea and M. 
frenata, are similar in that the males reach 
sexual maturity in 1 year; but the females 
breed during their first summer and thus 
produce young at the age of 1 year 
(Wright 1963:83-84). In the marten, males 
also apparently reach sexual maturity in 1 
year, but females may not breed until they 
are 2 years old, and thus two year-classes 
of immature females may be found in wild 
populations (Jonkel and Weckwerth 1963: 
95-96). This has made further refinement 
of Marshall's ( 1951 ) original study of 
marten quite difficult. 

In the female otter it appears that sexual 
maturity is delayed another year beyond 
that in the fisher and that there are two 
age-classes of immature otters (Hamilton 
and Eadie 1964:245). In the badger the 
same type of situation prevails as in the 
fisher except that some females breed pre- 
cociously during their first summer and 



245 



86 Journal of Wildlife Management, Vol. 31, No. 1, January 1967 



such females would produce litters at the 
age of 1 year, whereas most badgers pro- 
duce their first litters at the age of 2 years 
(Wright 1966:42). Only in the wolverine 
{Gulo gulo) does it appear that a repro- 
ductive cycle like that of the fisher is 
found; but owing to a small sample of ani- 
mals of the former species, the matter of 
age at sexual maturity is somewhat in 
doubt. 

The recovery of the marten in Maine has 
been much slower than in the fisher 
(Coulter 1959) although both species orig- 
inally occurred sympatrically in much the 
same habitat. The present study indicates 
that the potential rate of reproduction in 
the fisher is higher than in the marten. A 
large sample of winter-caught marten is not 
available from Maine, but such material 
was obtained from Montana. Wright ( 1963: 
79) indicates that corpora lutea counts 
averaged 3.02 in a sample of 44 trapper- 
caught marten. The present study showed 
3.28 for the fisher. Perhaps of greater sig- 
nificance, though, is the fact that some 
female martens (in Glacier National Park) 
(Jonkel and Weckwerth 1963) do not 
produce litters for the first time until they 
are 3 years old. 

LITERATURE CITED 

Canivenc, R., and M. Bonnin-Laffargue. 1963. 
Inventory of problems raised by the delayed 
ova implantation in the European badger 
{Meles meles L.). Pp. 115-125. In A. C. 
Enders (Editor), Delayed implantation. Uni- 
versity of Chicago Press, Chicago, Illinois. 
309pp. 

CouES, E. 1877. Fur-bearing animals: a mono- 
graph of North American mustelidae. Dept. 
Interior, Misc. Pub. 8, Washington, D. C. 
348pp. 

Coulter, M. W. 1959. Some recent records of 
martens in Maine. Maine Field Naturahst 
15(2):50-53. 

. 1960. The status and distribution of 

fisher in Maine. J. Mammal. 41(l):l-9. 

Deanesly, Ruth. 1935. The reproductive proc- 
esses of certain mammals. Part IX: Growth 



and reproduction in the stoat {Mustela 
erminea). Philos. Trans. Roy. Soc. London 

225 (528): 459-492. 

de Vos, a. 1952. Ecology and management of 
fisher and marten in Ontario. Ontario Dept. 
Lands and Forests Tech. Bull. 90pp. 

Eadie, W. R., and W. J. Hamilton, Jr. 1958. 
Reproduction in the fisher in New York. New 
York Fish and Game J. 5(l):77-83. 

Elder, W. H. 1951. The baculum as an age 
criterion in mink. J. Mammal. 32(l):43-50. 

Enders, R. K., and O. P. Pearson. 1943. The 
blastocyst of the fisher. Anat. Rec. 85(3): 
285-287. 

Greer, K. R. 1957. Some osteological charac- 
ters of known-age ranch minks. J. Mammal. 
38(3):319-330. 

Hall, E. R. 1942. Gestation period in the fisher 
with recommendations for the animal's pro- 
tection in California. California Fish and 
Game 28(3) :143-147. 

Hamilton, W. J., Jr., and A. H. Cook. 1955. 
The biology and management of the fisher in 
New York. New York Fish and Game J. 
2(l):13-35. 
-, and W. R. Eadie. 1964. Reproduction 



in the otter {Lutra canadensis). J. Mammal. 
45(2):242-252. 

Jonkel, C. J., and R. P. Weckwerth. 1963. 
Sexual maturity and implantation of blasto- 
cysts in the wild pine marten. J. Wildl. Mgmt. 
27(l):93-98. 

Marks, S. A., and A. W. Erickson. 1966. Age 
determination in the black bear. J. Wildl. 
Mgmt. 30(2):389-410. 

Marshall, W. H. 1951. An age determination 
method for the pine marten. J. Wildl. Mgmt. 
15(3):276-283. 

Neal, E. G., and R. J. Harrison. 1958. Re- 
production in the European badger {Meles 
meles L.). Trans. Zool. Soc. London 29(2): 
67-130. 

Rausch, R. L. 1961. Notes on the black bear, 
Ursus americanus Pallas, in Alaska, with par- 
ticular reference to dentition and growth, 
Z. Saugetier. 26(2):77-107. 

RuFFiE, A., M. Bonnin-Laffargue, and R. 
Canivenc. 1961. Les taux du pregnandiol 
urinaire au cours de la grossesse chez le 
Blaireau europeen. Meles meles L. Comptes 
rendus des seances de la Societe de Biologie 
155(4):759-761. 

Taber, R. D. 1956. Characteristics of the pelvic 
girdle in relation to sex in black-tailed and 
white-tailed deer. California Fish and Game 
42(1):15-21. 



246 



Maine Fishers • Wright and Coulter 87 



Wright, P. L. 1948. Preimplantation stages in 
the long-tailed weasel ( Mustela frenata ) . 
Anat. Rec. 100(4):593-607. 

— . 1950. Development of the baculum of 

the long-tailed weasel. Proc. Soc. Expt. Biol, 
and Med. 75:820-822. 

. 1953. Intergradation between Martes 

americana and Martes caurina in western 
Montana. J. Mammal. 34(l):74-86. 

. 1963. Variations in reproductive cycles 

in North American mustelids. Pp. 77-97. In 
A. C. Enders (Editor), Delayed implantation. 



University of Chicago Press, Chicago, Illinois. 
309pp. 

. 1966. Observations on the reproductive 

cycle of the American badger {Taxidea taxus). 
Pp. 27^5. In I. W. Rowlands, Editor, Com- 
parative biology of reproduction in mammals. 
Symposia Zool. Soc. London, No. 15. Aca- 
demic Press, London. 527pp. 

, AND R. Rausch. 1955. Reproduction in 

the wolverine, Gulo gulo. J. Mammal. 36(3): 
346-355. 

Received for publication August 22, 1966. 



247 



GROWTH, DEVELOPMENT, AND WING LOADING 
IN THE EVENING BAT, NYCTICEIUS HUMERALIS (RAFINESQUE) 

Clyde Jones 

Abstract. — Selected aspects of growth and development of young evening bats 
are presented and summarized. In addition, information on wing loading and de- 
velopment of flight in known-age animals is given. Data regarding growth, de- 
velopment, and wing loading of Nycticeius humeralis and information that is 
available for some other species of bats are compared and discussed. 

Few observations have been made previously on growth and development 
of bats, and such information has been frequently incidental to other studies 
of natural history or reproduction. Ryberg (1947), while presenting data on 
parasites and natural history of bats, made some mention of growth and de- 
velopment of young. Considerable information on growth and development 
of two North American bats has been contributed by Pearson et al. ( 1952 ) 
and Orr ( 1954 ) . Some observations of young and early growth and develop- 
ment of Nycticeius humeralis were noted by Gates (1941). In general, re- 
production of bats has been summarized by Cockrum ( 1955 ) and Asdell 
(1964). 

To my knowledge, no information has been made available with regard to 
wing loading of Nycticeius humeralis. Vaughan ( 1959 ) , while presenting data 
on aerodynamic considerations of three species of bats, provided a survey of 
important earlier works. More recently, limited information on flight of some 
North American bats has been contributed by Struh&aker (1961), Davis and 
Cockrum (1964), Hayward and Davis (1964), Vaughan (1966), and others. 

The purpose of this report is to present information on growth and develop- 
ment and to discuss briefly some aspects of wing loading of Nycticeius 
humeralis. 

Materials and Methods 

This report is based upon observations of 28 young of 14 litters born in captivity to 
females netted at Clear Springs, Homochitta State Park, Franklin County, Mississippi. 
The adults were captured between 11:30 pm and 4:30 am on 9 and 10 May 1965. 

Pregnant bats were weighed periodically prior to parturition; following birth of the 
young, weights and measurements of all bats were taken regularly. The growth and 
development of three litters were followed in detail and the animals were measured daily. 
The remaining animals were measured each 3- or 5-day period. Because the bats were 
not anesthetized, it was not always possible to obtain relaxed individuals for measuring. 

1 



248 



2 JOURNAL OF MAMMALOGY Vol. 48, No. 1 

As a result of these methods, some discrepancies in the measurements of individuals from 
one date to another are evident in the data. Measurements that were taken include total 
length, length of tail, length of foot, length of ear from notch, length of forearm, and 
length of fifth finger. All measurements were taken with a Vernier caliper. 

At regular intervals of age of the animals, wings were outlined for the analysis of surface 
areas utilized in flight. For the purposes of measuring wing loading, I have followed 
the assumption of Vaughan (1959) that the wings extend through the body and I 
have computed the wing loadings in lb per sq ft. 

Pregnant females and females with young were housed in one-quart cardboard cans 
with screen tops. Following the weaning of the young, each female and her offspring 
were housed in one-half gallon cardboard cans with screen tops. Cardboard cans containing 
bats were stored on the sides. The animals were maintained at room temperatures and 
provided a daily diet of larvae of Tenebrio molitor and water with Theragran (Squibb 
Therapeutic Formula Vitamin) added. Feeding, watering, and handling of the bats were 
started at about the same time every day, usually between 3:30 and 5:30 pm. 

For purposes of identification, adult bats were banded. Young animals were toe clipped 
soon after birth, but were banded when adult size was attained. 

Some animals were sacrificed at various stages of development and then cleared and 
stained or were preserved either in fluid or as dried specimens. 

Results 

Birth of young. — The females gave birth to the young within 15 to 26 days 
after capture. The births recorded herein occurred on 25 May (two Htters), 
26 May (one Htter), 29 May (two Htters), 30 May (five htters), 31 May (two 
htters), 2 June (one Htter), and 4 June (one Htter). Fourteen adult females 
gave birth to 12 females and 16 males. This ratio of sexes (0.75 to 1.00) was 
similar to the ratio (0.736 to 1.00) reported by Hooper (1939). AsdeH (1964) 
reported two young as the usual number per litter and stated that birth oc- 
curred in late May. 

All births observed were by breech presentation and the times recorded 
for births were from 3 to 114 minutes. With the exception of two litters that 
were bom at about 9:00 and 10:45 am, all litters were dropped between 1:00 
and 4:00 pm. 

During parturition all females moved to the bottoms of the containers. 
Females ate the placentae and umbiHcal cords and licked the young very 
soon after birth. Placentae were eaten first, then umbilical cords were eaten 
to within 2 or 3 mm of the naval area. Some of the females hung head up 
on the screening of the containers while eating the placental materials, but 
then turned head down and licked the young thoroughly. Placentae and 
umbilical cords were eaten and the young were licked usually within 35 to 
70 minutes after delivery. 

In every case observed, the young found and grasped the nipples of the 
adult within a short time, usually 5 to 8 min following birth. The young were 
aided often by the adult in climbing to the mammary glands. The young 
were oriented in the same direction as the adult. The plagiopatagium and 
uropatagium of the female enveloped the young. The young bats held firmly 
to the nipples of the females and had to be removed forcibly for measuring. 



249 



February 1967 

100 -1 



E 
E 



c 
o 



o 



90 



80 



70 - 



60 



■S 50 



40 - 



30 



20 



JONES— EVENING BAT 



(' 



\\. 



1 1 1 1 1 1 1 1 1 1 

10 20 30 40 50 60 70 80 90 100 

Days 

Fig. 1. — Total lengths of young Nycticeius humeralis. Dots represent the arithmetic 
means and lines represent the ranges of measurements. 



250 



JOURNAL OF MAMMALOGY 



Vol. 48. No. 1 



E 
E 



o 
o 



-I 



42 



38 



34 



30 



o 26 



22 



18 - 



14 



10 



( ■ 
■ . 

lip 

1 





— I 1 1 1 1 1 \ \ 1 1 

10 20 30 40 50 60 70 80 90 100 

Days 

Fig. 2. — Tail lengths of young evening bats. Dots represent the arithmetic means and 
lines represent the ranges of measurements. 



251 



February 1967 



JONES— EVENING BAT 



Table 1. — Correlation of age and various aspects of growth and development 

of young evening bats. 















<U u. 








_>, 




Cfl 


*J 


1 




g 


5 -o 

O >" 

.S E 




c 
o 


0; 


a! 

"a 




_4; 


"H '^ 


"a 


"gs 


1 •« 


c 1 




c 




5 




.5* 
'c 

S 


1^ 


o 

o 

1 


« S 
II 

^ a 


1° 


1^ 


E ii 






C 


Age in 




a * 
.So 


>> 

"0 


C 

2 2 




-1 

C3 O 


2 S 


4~> ^ 





weeks 


< 


£ o 


o 
n 




ol 


it' "- 


^ % 


« 




1 


X 


X 


















2 


X 


X 


X 


X 














3 




X 


X 


X 


X 


X 


X 


X 






4 












X 


X 


X 






5 


















X 




6 


















X 


X 


7 


















X 


X 


8 




















X 


9 




















X 



In addition, the feet and first fingers were utilized for clinging to the fur of 
the adults. 

'^kin and pelage. — Young bats examined within 1 hr after birth were pink 
with smooth, soft skin. Vicera were seen through the skin of the abdomen. 
There was slight dark pigmentation on the feet, membranes, tips of the pinnae, 
and lips. Only a few hairs were present on the feet and on the dorsum of the 
head and shoulders. Some vibrissae were evident on the swollen glandular 
areas of the lips. 

When about 6 hr old, the young had more pigmentation on the dorsal 
sides of the back and head than at birth. Pigmentation became evident on the 
venter at approximately 18 hr of age. Within 24 hr the dorsum was pigmented 
heavily and the venter was pigmented except for a small abdominal area 
that appeared rather opaque. The skin was very wrinkled and had the 
appearance of being hard and dry, but was soft and pliable to the touch. 

In the 2-day-old young, a few hairs appeared on the dorsum at the 
base of the uropatagium. The hairs and vibrissae on the feet and lips were 
noticeably stiffened. 

At 3 days of age a small patch of hair became noticeable on the dorsum over 
the scapulae. 

By the 4th day, pelage was seen on the dorsum over the scapulae, on the 
rump, and along the flanks. At this age, fur was first apparent on the venter 
at the base of the uropatagium and in the pectoral region. 

At 5 days of age, fur was present on the dorsum across the scapular region 
to the flanks and extended onto the rump. At this time the fur was short, 
soft, and gray in color. 



252 



6 



JOURNAL OF MAMMALOGY 



Vol. 48, No. 1 



E 

o 



a» 



42 1 



38 - 



34 - 



E 

E 30 



26 - 



^ 22 



18 - 



14 - 



10 



_ 1 



"T- 

10 



— T" 
20 



30 



T 



40 
Days 



50 



— 1 1 1 1 1 

60 70 80 90 100 



Fig. 3. — Forearm lengths of young Nycticeius humeralis. Dots represent the arithmetic 
means and Hnes represent the ranges of measurements. 



253 



February 1967 JONES— EVENING BAT 7 

On the 6th day, soft gray hairs covered most of the dorsum, and, except 
for a bare abdominal region, much of the venter. The feet were well furred. 

At 7 days of age, the hairs on the dorsum, in the scapular region, appeared 
longer and darker than the rest of the general pelage. 

At 8 to 9 days of age, the young were furred completely with grayish black 
hairs on the dorsum with long, dark fur over the scapulae. In contrast to the 
dorsum, the venter was grayish white in color. 

The aforementioned general appearance of the pelage remained until the 
young were approximately 30 days of age. At this time the hair became 
burnished slightly with brown at the tips, perhaps due to wearing of the ends 
of the hairs. Young bats were not observed to undergo molt during the course 
of this study. At the time the young bats reached about 80 to 95 days of age, 
the parent females molted; the pelages of young and adults were similar in 
appearance. 

Eyes, ears, and vocalization. — At birth the lids of the eyes were sealed, but 
the line of fusion was very evident. At 18 to 24 hr following birth, the eyes 
opened. At this age, the young would jump and scamper about in response 
to the flash of light from a photographic strobe. 

Young examined soon after birth had pinnae that were folded over. When 
the young were 24 to 36 hr old, the pinnae were unfolded and held erect. 

The young bats were vocal almost immediately after birth. The utterances 
of weak "squeaks" or "chirps" seemingly were continuous for about 10 days. 
After this time, bats made vocal sounds only when disturbed or handled. 

Dentition. — The complete number of deciduous teeth in young Nijcticeiiis 
humeralis is expressed by the formula i 2/3, c 1/1, p 2/2 = 22. Examination of 
newly-born young revealed that all of the deciduous teeth were erupted at 
birth. The deciduous teeth have two accessory cusps, one on either side of the 
main central cusp. In general, each cusp is in the shape of a hook and is 
curved backward and inward toward the mouth. The highest degree of 
development of curved, hook-shaped cusps is on the incisors. The cusps 
of the canines are hooked noticeably, but some premolars have relatively 
poorly developed accessory cusps that appear as small bumps rather than 
hooks. Hooked cusps are more highly developed in 2- and 7-day old young 
than in young 1 day of age. 

The complete number of permanent teeth is expressed by the formula 
i 1/3, c 1/1, p 1/2, m 3/3 = 30. In specimens of young 2 days old that were 
cleared and stained, the crowns of the permanent teeth are clearly visible in 
a position internal to the deciduous teeth. In specimens of young 7 days old, 
the permanent canines have penetrated through the gums and crowns of the 
other teeth are seen at the gum line just beneath the surface. In the order 
of appearance of permanent dentition, the canines become apparent first, fol- 
lowed in eruption by the incisors, premolars, and molars. At 4 weeks of age, 
the permanent teeth are generally in place; the third molars may not be in 
place fully, but the crowns are apparent well above the gum lines. 



254 



8 



JOURNAL OF MAMMALOGY 



Vol. 48, No. 1 



42 -1 



38 



34 - 



30 - 



S 26 



^ 22 

c 

-I 



8 - 



4 - 



O O 00 o 



o 

°o OcPo° 



o ° o o oo o 

o ° o 

o o 



o o • * • _*' 

o o ° .•• •.•^* •••^ 

o • , • • 

o • • • 

• • 

o -• •• 



• «•*•• . •• ^ 



o o^ 



1 1 1 1 1 1 1 1 1 f 

10 20 30 40 50 60 70 80 90 100 



Days 

Fig. 4. — Forearm lengths of known-age evening bats. The open circles represent the 
arithmetic means of measurements for females; the dots represent the arithmetic means of 
measurements for males. 



255 



February 1967 JONES— EVENING BAT 9 

Digits. — The digits of the hind limb were separated at birth and the claws 
were well developed and pigmented. Young bats at birth had feet nearly 
equal in size to the feet of adults. 

The first finger of the forelimb was developed very well at birth and thumbs 
of young were similar in size to thumbs of adults. Measurements of the length 
of the first finger of young and adults were 5.5 to 6.2 mm. 

The remaining digits of the forelimb were developed to a lesser degree 
in young than in adults. In the young less than 15 days of age, the distal 
portion of the forelimb was less developed than the proximal part of the 
wing; digits two to five were shorter in length than the forearm. In adults, 
the lengths of digits two to five were 18 to 61% greater than the length of 
the forearm. 

Flight of young. — In an attempt to determine the exact age when the young 
bats could fly, four young were thrown into the air each day when the adults 
were fed; four young and adults were housed in containers placed on a shelf 
4.6 ft from the floor and the tops of the containers were taken off at feeding 
time; the remaining young and adults were cared for in the manner mentioned 
previously. When the young bats 10 to 14 days of age were thrown into the 
air, the wings were extended and fluttered, but the animals simply fell to 
the floor, sometimes without righting themselves. When the bats were 15 
days of age, the fifth fingers were flexed and the bats would right themselves 
and then glide or "parachute" to the floor. At 18 days of age, bats thrown into 
the air flew 10 to 12 ft, but would hit a wall or the ceiling and flutter down 
to a flat surface such as the floor or a desk or would hang head up on a wall. 
At 19 days of age, one young bat housed on the aforementioned shelf emerged 
and flew across the room. When the young were 20 to 21 days old, they were 
observed to negotiate turns, land, and hang head down from walls and ceilings 
of the room. All of the young animals, including those with no practice 
previously, could fly short distances ( 10 to 12 ft) at 21 days of age, and all could 
fly well, turn, and land head down on the walls or ceilings at 23 days of age. 

All observations of flight were made in a room that measured 18 by 15 ft 
with a partial comer partition separating an area about 8 by 8 ft. The young 
bats could fly and avoid obstacles well in these spaces. 

Behavior of young and adults. — The young evening bats seemed weak and 
uncoordinated at birth. Although the babies attached themselves firmly to 
the parent, young 1 day of age seemed rather helpless when separated from 
the adult. At 1 day of age, the young could crawl about only feebly and 
were unable to right themselves when placed on the dorsum on a flat surface. 

By 3 days of age the young could crawl about very well and could right 
themselves quickly. In part, these abilities may be a reflection of the afore- 
mentioned unfolding of the pinnae at this time. 

For nearly the first 2 weeks of age the young were attached to the nipples 
of the adults almost constantly and remained enveloped by the membranes of 
the adults. With the exception of a few occasions when a young bat was 



256 



10 



JOURNAL OF MAMMALOGY 



Vol. 48, No. 1 



E 
E 






c 



42 n 



38 - 



34 - 



30 



26 



H- 22 - 



18 - 



14 - 



10 



\ 1 1 1 1 1 1 1 1 1 

10 20 30 40 50 60 70 80 90 100 

Days 

Fig. 5. — Fifth-finger lengths of young Nycticeius humeralis. Dots represent the arith- 
metic means and hnes represent the ranges of measurements. 



257 



February 1967 
42 



E 
E 



E 
E 



c 



o» 


o» 


c 


c 


0> 


a> 


_l 


-I 


II 


II 


o 


X 



38 



34 



E ;;: 

k. 

a 

o .ti 

^ ^ 26 



14 



JONES— EVENING BAT 



11 



E 30 - 



XX 



^x"** X X 



X X 

XX X 



,X X 



xx 



v» X X 



X 

X X 
X X 



« "X ^° 0, 00 

X ° ° <: 

X . 00 



Cb%cPo%°<?o°%.o„° 

5 nr. ^ O r> _ O 0-, 

00 ^0 



00 



X 



22 - 



8 - 



o°o°o 

O^x 




X 





o 



x\ 



,t 



X 

ox 

IX 



1 1 1 1 1 1 1 1 1 1 

10 20 30 40 50 60 70 80 90 100 

Days 

Fig. 6. — Relationships of forearm lengths and fifth-finger lengths of Nycticeius humeralis. 
Open circles represent arithmetic means of measurements of forearm lengths; crosses 
represent arithmetic means of measurements of fifth-finger lengths. 

observed uncovered, the young did not leave the close association with the 
parent and move about in the containers until about 3 weeks of age. After 
this time, young scampered frequently about the cages, but hung adjacent 
to the female when at rest. 



258 



12 



JOURNAL OF MAMMALOGY 



Vol. 48, No. 1 



10 n 



9 - 



8 - 



6 - 



E 

o 

o> 
c 5 



4 - 



3 - 



2 - 



— I 1 1 1 1 \ 1 1 1 r 

10 20 30 40 50 60 70 80 90 100 

Days 

Fig. 7. — Weights of young bats. Dots represent the arithmetic means and lines represent 
the ranges of weights. 



259 



February 1967 JONES— EVENING BAT 13 

Table 2. — The relationships of wing loading, proportions of the forearm and fifth finger, 
and total body weight of known-age Nycticeius humeralis. 



Age in 


Weight 


Wing loading 


Length of forearm/ 


Size of 


days 


in g 


in Ib/sq ft 


length of fifth finger 


sample 


1 


2.0 


0.5365 


1.00 


11 


2 


2.2 


0.4067 


0.99 


11 


4 


2.6 


0.4523 


1.02 


7 


5 


2.8 


0.3765 


1.02 


8 


8 


3.0 


0.3300 


1.04 


11 


12 


3.4 


0.2500 


1.02 


19 


15 


3.8 


0.2500 


0.99 


23 


18 


4.2 


0.2433 


0.97 


23 


35 


5.2 


0.2375 


0.93 


23 


43 


5.6 


0.2220 


0.85 


22 


60 


6.2 


0.2079 


0.85 


19 


73 


7.1 


0.1921 


0.85 


19 


97 


8.4 


0.2261 


0.83 


5 



As mentioned previously, the young were highly vocal for the first 10 days 
following birth, but then made vocal sounds only when disturbed or handled. 
During these observations, the adults emitted sounds only when disturbed, 
handled, or sometimes when offered food. 

Some definite specificities of adults for their young were noted. As long 
as the young bats were returned to the same nipples from which they were 
taken, no female refused to accept the young after they had been removed 
from the mother and measured or handled otherwise. On several occasions 
attempts were made to get adult females to accept nursing young from other 
females; all such efforts failed. The adults would bite and move away from 
the strange young. One young bat that was allowed to become attached to 
the nipple of a restrained female was attacked and thrown from her when 
the adult was released. This same adult accepted her own young a few 
minutes later. Litters and females could not be mixed successfully until nursing 
ceased. The refusal of adult females to accept other young may be a reflection 
of the manner in which the animals were maintained in relative isolation 
from other young and adults. Gates ( 1941 ) reported that he detected no 
specificity with regard to nursing young and adult females when the young 
and adults no longer remained together during periods of feeding. 

The young first showed an interest in food and water at approximately 
3 weeks of age, when they appeared to smell and lick items of food ( portions 
of mealworm larvae) held before them. Early interests of young in water 
included considerable licking of the end of a water-filled dropper. At the 
age of 4 weeks, young bats were taking water from a dropper and eating 
small mealworms that were presented with forceps. 

Throughout the course of this study, the adults were given mealworms 
from forceps and water was administered from a dropper. In only two cases 



260 



14 



JOURNAL OF MAMMALOGY 



Vol. 48, No. 1 



14 -, 



12 - 



10 - 



i 8 



• 



6 - 



4 - 



2 - 



•• V*^* 






• •• 



•v.\\.. 



•Art-^" 



• % 



-• 







>v 



/ 



T 



T 



T 



T 



T 



T 



T 



— \ r 1 n 

20 10 10 20 30 40 50 60 70 80 90 100 

Days 

Fig. 8. — Weights of Nycticeius humeralis. Open circles represent arithmetic means of 
weights of adults and dots represent the arithmetic means of weights of young. 

did individuals become accustomed to picking up and eating mealworms 
that were not presented by hand. In general, the bats made little effort to fly 
or move about while being fed and it was possible to feed four to six animals 
at one time. One adult crawled about almost continually while being fed. 
The young reared by this female behaved in similar fashion during the periods 
of feeding. 

Some animals began eating immediately when food was offered; others 
simply held a food item in the mouth for a short time. During this time the 



261 



February 1967 



JONES— EVENING BAT 



15 



Flight 




Fig. 9. — Actual outlines of a wing of a young Nycticeius htimeralis of known age. Wing 
outlines were made when the bat was 1, 2, 4, 5, 8, 12, 15, 18, 35, 43, 60, 73, and 97 
days of age. 



animals exhibited considerable shivering, presumably while the body tem- 
perature was increased. 

Growth. — Information relating to growth and development of young Nyc- 
ticeius humeralis given herein is based upon bats bom and reared in captivity. 
No malformations of any kind were noted and all animals seemed normal, 
but it is possible that under laboratory conditions the rate of growth and 
development may not have been normal. 

Data regarding growth and development of young bats are presented in 
Tables 1 and 2 and Figs. 1-9. Because the length of the first finger and 
length of foot of newborn bats were noted to increase little between birth 
and adulthood, those measurements are not depicted graphically. 

At 45 to 50 days of age, total length, length of tail, and length of fifth 
finger of young bats were of adult proportions and little growth occurred 
thereafter (Figs. 1, 2, and 5). Length of forearm, on the other hand, was 
of adult proportions when the bats were about 30 days of age (Figs. 3 and 4) 
and little growth occurred at later ages. Some sexual dimorphism of the 
length of the forearm was noted (Fig. 4). The smaller size of the forearm 



262 



16 JOURNAL OF MAMMALOGY Vol. 48, No. 1 

of males became apparent when the animals were about 20 days of age. 
Pearson, Koford, and Pearson ( 1952 ) found a similar situation in their studies 
of growth of Plecofus townsendii. In young bats, the proportional relation- 
ships of the length of the forearm and the length of the fifth finger (Table 2 
and Fig. 6) are correlated with flight and are discussed later with regard to 
flight. 

\\'eights of young bats were noted to increase rather constantly throughout 
the period of study (Figs. 7 and 8). Some activities of the bats, such as the 
development of the ability for flight and the acceptance of mealworms and 
water are reflected in the weights of the young. The gradual cessation of 
nursing and lactation seemingly is reflected more vividly in the weights of 
the adults ( Fig. 8 ) than in the weights of young during the same period of time. 

Growth, de\elopment, and relative surface area of the wings of bats of 
known ages are depicted in Fig. 9. The data presented indicate a gradual 
increase in surface area of the wing with the development of a wing of adult 
proportions at the age of 60 to 97 days; surface area is stabilized with the 
cessation of growth. 

At the age when young bats first began to fly, several changes in the wings 
were apparent for the first time. The length of the fifth finger was greater 
than the length of the forearm (Table 2 and Fig. 6) and the distal portion 
of the wing, that area from the apex of the wing to the first and fifth fingers, 
was nearly equal in surface area to the proximal portion of the wing, that region 
between the body and the first and fifth fingers (Fig. 9). In addition, there 
was a change in the ratio of body weight to surface area of the wing ( Table 2 ) . 

Discussion 

Data on various aspects of growth and development of some species of 
North American vespertilionids have been presented by Pearson et al. ( 1952 ) , 
Orr (1954), and others. The availibility of these data permits a general com- 
parison of the rates of growth and development of Nycticeius humeralis with 
those of Flecotus townsendii and Antrozous pallidus. 

The development of fur over the entire body of young evening bats was 
completed by 8 to 9 days of age. Short gray hair covered the bodies of Plecotus 
4 days old and scanty fur was evident on the bodies of Antrozous at 10 days 
of age. 

The eyes of young Nycticeius were opened at the age of 18 to 24 hr, but 
eyes of young Plecotus and Antrozous were not opened until the age of 7 to 
10 days. Pinnae of young Nycticeius were erected after 2 to 3 days of age; 
pinnae of the two other species were erected after 7 days of age. Vocalization 
was noted almost immediately following birth of Nycticeius and was evident 
within a few hours after birth of Plecotus. 

The complete set of deciduous teeth of Nycticeius was present at birth 
and these teeth were grown out fully by 7 days of age. Orr ( 1954 ) found 
the deciduous premolars lacking in newborn Antrozous, but noted that the 



263 



February 1967 JONES— EVENING BAT 17 

deciduous teeth were grown out fully by the second week of age. In Nycticeius, 
all of the permanent teeth were erupted at an age of 4 weeks, and in Antrozous, 
permanent teeth were erupted at an age of 5 weeks. 

The forearm in young Nycticeius was of adult proportions at 30 days of 
age, but the forearm in young Plecotus reached adult size at 21 days of age. 

Comparisons of the rates of growth and development of the young of 
Nycticeius humeralis, Plecotus townsendii, and Antrozous pallidus, indicate 
that young Nycticeius exhibit more rapid growth and development and are 
perhaps more precocious than young of the other species. 

On the basis of the data presented in this report, it seems that young Nyc- 
ticeius humeralis, prior to 18 days of age, simply lack adequate surface areas 
of wing membranes to support the weight of the body in flight. For informa- 
tion with regard to surface areas of flight membranes and body weights of 
bats, see Vaughan (1959 and 1966) and Struhsaker (1961). In addition to 
the relationships of surface areas and weights, other factors of growth and 
development must have considerable bearing on the abilities of young bats 
to fly. For example, both lift and power for flight of young bats must be 
highly dependent upon the development of the ventral thoracic flight muscles 
as well as development of the musculature of the entire forehmb. For a 
discussion of surface areas of flight membranes and volumes of fhght muscles 
in relation to total volumes of the body, see Struhsaker (1961), and for 
descriptions and discussions of flight muscles, see Vaughan (1959 and 1966). 
It was noted that after the forearm of the bats observed during this study 
reached maximum length ( at about 30 days ) there was an increase in diameter 
of this portion of the forelimb. This increase in diameter of the forearm 
was noticed especially at the proximal portion and was due apparently to 
growth and development of the muscles that are located in this region. 

Sexual dimorphism in the surface area of wings was not detected, but some 
dimorphism in the length of the forearm was noted (Fig. 4). The slightly 
greater length of the forearm in females implies that perhaps females may 
be capable of supporting a slightly greater load in flight than males. 

At 18 to 21 days of age when young bats were capable of flight for the 
first time, the relationships of the surface areas of the wings to the total 
weights of the animals ( Table 2 ) perhaps were indicative of the optimal wing 
loading for flight in the species of bat considered herein. If this were true, 
an indication of maximum weight-carrying capacity of these bats could be 
obtained by comparing the wing loadings of bats capable of first flight 
with wing loadings of mature animals. It is of interest that none of the young 
bats were capable of flight unless the wing loading was less than 0.250 lb 
per sq ft (Table 2). Young bats may be capable of flight with the optimal 
wing loading for the species, but probably would lack the coordinations 
and skills of flight that were developed in the adults, thus more mature 
bats probably have the ability to carry extra weight at least for brief periods 
of time. The achievement of the relationship of surface area versus weight 



264 



18 JOURNAL OF MAMMALOGY Vol. 48, No. 1 

was correlated closely with the relative growth rate of the forearm and fifth 
finger (Table 2 and Fig. 6). Wing loading of adult animals (73 and 97 days 
of age) varied from 0.1921 to 0.2261 lb per sq ft. On the basis of these afore- 
mentioned data, it can be suggested that, allowing for reasonable amounts 
of variation, adult animals with a weight of 9 to 11 g would have a wing 
loading not far removed from the postulated maximum of about 0.2500 lb per 
sq ft. 

According to Gates (1941), weight of two females prior to parturition was 
11.6 g each. Some of the females observed in this study weighed as much 
as 14 g (the average was slightly more than 12 g) prior to parturition, but 
these animals were kept in confined situations. At the time of capture, 20 
days before parturition, average weight of females was slightly more than 10 g 
(Fig. 8). Because weights of newborn bats recorded during this study 
were greater than weights of young bats given by Gates (1941), it is suggested 
that the young and females kept in captivity may have weighed more, due 
to overfeeding, than animals living in natural conditions. 

Bats have been reported to carry various weight loads in addition to the 
normal weight of the body (Davis and Cockrum, 1964). The weight carrying 
capacity of individuals of any given species of bats undoubtedly is important 
with regard to the relationships between adult females and the young, and 
may be reflected in the behavior of adults prior to and following parturition. 
As noted earlier in this report ( Table 1 ) , young Nycticeius humeralis remained 
associated closely with the parents for nearly 3 weeks. This relationship may 
be a reflection of the methods of housing the animals during these observa- 
tions. Gates ( 1941 ) suggested that the young remained with the adult for less 
than 10 days and he implied that this is a reflection of the weight carrying 
capacity of the adults. Hamilton (1943) mentioned that nursing female 
Nycticeius probably do not carry the young while foraging for food. The re- 
lationships of weights, surface areas of flight membranes, and related abilities 
of flight of the animals may be reflected in the selection of sites for roosting 
by adults both prior to and following birth of the young. 

Acknowledgments 

Sincere thanks are clue Dan Walton and Dr. Francis Rose for help in collecting the 
original material, Dr. Clyde Barbour for the preparation of photographs, and Glenn 
Clemmer for help in caring for the animals. This study could not have been conducted 
without the countless hours of help in feeding and caring for the animals that were con- 
tributed by Dr. Francis Rose and Charlene Jones. Dr. Andrew Arata photographed bats 
and made many helpful suggestions throughout this study. The study was supported in 
part by an American Cancer Society Grant to Tulane University (IN-24-G). 

Literature Cited 

AsDELL, S. 1964. Patterns of mammalian reproduction. Comstock Publishing Associates, 

New York, 2nd ed., 670 pp. 
Cockrum, E. 1955. Reproduction in North American bats. Trans. Kansas Acad. Sci., 

58: 487-511. 



265 



February 1967 JONES— EVENING BAT 19 

Davis, R., and E. Cockrum. 1964. Experimentally determined weight lifting capacity 

in individuals of five species of western bats. J. Mamm., 45: 643-644. 
Gates, W. 1941. A few notes on the evening bat, Nycticeius humeralis ( Raf inesque ) . 

J. Mamm., 22: 53-56. 
Hamilton, W. 1943. The mammals of eastern United States. Comstock Publishing 

Company, Inc., Ithaca, New York, 432 pp. 
Hayward, B., and R. Davis. 1964. Flight speeds in western bats. J. Mamm., 45: 

236-242. 
Hooper, E. 1939. Notes on the sex ratio in Nycticeius humeralis. J. Mamm., 20: 369- 

370. 
Orr, R. 1954. Natural history of the pallid bat, Antrozous pallidus (LeConte). Proc. 

California Acad. Sci., 28: 165-246. 
Pearson, O., M. Koford, and A. Pearson. 1952. Reproduction of the lump-nosed bat 

(Corynorhinus rafinesquei) in California. J. Mamm., 33: 273-320. 
Ryberg, O. 1947. Studies on bats and bat parasites. Svensk Natur, Stockholm, 319 pp. 
Struhsaker, T. 1961. Morphological factors regulating flight in bats. J. Mamm., 42: 

152-159. 
Vaughan, T. 1959. Functional morphology of three bats: Eumops, Myotis, Macrotus. 

Univ. Kansas Publ, Mus. Nat. Hist., 12: 1-153. 
. 1966. Morphology and flight characteristics of molossid bats. J. Mamm., 

47: 249-260. 

Department of Biology, Tulane University, New Orleans, Louisiana. Accepted 28 No- 
vember 1966. 



266 



Growth, 1961, 25, 127-139. 

A COMPARATIVE STUDY OF GROWTH AND DEVELOPMENT 
OF THE KANGAROO RATS, DIPODOMYS DESERTI 
STEPHENS AND DIPODOMYS MERRIAMI MEARNS 



Bernard B. Butterworth 



Department of Biology, University of Wichita, Wichita 8, Kansas 



During a recent study of sexual behavior and reproduction of the 
kangaroo rats, Dipodomys deserti and Dipodomys merriami, a com- 
parison of growth and development of closely related sympatric species 
reared under identical laboratory conditions was possible. Litters 
born in the laboratory were carefully examined and measured from 
birth to maturity. 

Although growth in other genera of mammals has been carefully 
studied, few instances of breeding in the genus Dipodomys have been 
recorded and limited growth data are available. The solitary nature of 
the animals prevents laboratory breeding under ordinary conditions. 
Animals confined in restricted space engage in fighting which usually 
results in the death of one or both of them. Chew and Butterworth (3) 
published an analysis of growth and development of Merriam's kanga- 
roo rat, D. merriami in which the senior author was successful in 
laboratory breedings of this species. The scattered literature on growth 
and development in the genus Dipodomys is summarized in their paper. 

Materials and Methods 

A total of 32 laboratory animals representing 8 D. deserti litters and 
4 D. merriami litters that were the direct progeny of wild parents were 
used in this study. Seven of the 8 litters of D. deserti were the products 
of laboratory breedings, the first recorded instances for this particular 
species. The other litters were from pregnant females captured in the 
field and brought back to the laboratory for observation and which 
subsequently produced young. 

The parent animals were all obtained from one locality at the 
western edge of the Mojave Desert near the base of Alpine Butte 
located approximately 16 miles northeast of Palmdale in Los Angeles 

127 



267 



128 GROWTH AND DEVELOPMENT OF KANGAROO RATS 

County, California. The altitude of the collecting area was approxi- 
mately 1000 meters (3261 feet). 

The captive animals were placed in two large breeding cages 
measuring 3 by 4 meters at the University of Southern California. A 
partition separated the two cages and sand and desert soil up to several 
inches in depth was spread on the floor. Animals were allowed to 
run in these cages without restriction. Nesting sites consisting of glass 
bottles, empty cardboard mailing tubes and cardboard boxes were pro- 
vided. One pair of each species was placed in each cage. Instances 
of breeding in D. dcscrti occurred in these cages. Animals were fed 
rolled oats and sunflower seeds. Lettuce was provided and water was 
also made available. An excess amount of food material was always 
available. 

All animals were measured from birth and the measurements were 
continued daily or at frequent intervals until adult sizes were attained. 
Standard measurements of total length, tail length, hind foot length, 
ear (from the notch) length, and body weight were taken. Measure- 
ments were analyzed as in Brody ( 2 ) and values were plotted on a 
semilogarithmic scale against age on the arithmetic scale. Linear seg- 
ments of such a plot indicate periods when growth increments are 
constant percentages of previous sizes. From these linear sections 
instantaneous growth rates were calculated as: 

T^ In m_> — In mi 
K = 

The value of K is the instantaneous percentage rate of growth for the 
unit of time in which tj and ti are expressed. Ln m^ and In mi are 
natural logarithms of the measurements made at ti and t2. 

Observations and Discussion 

General Development. The general pattern of development in D. 
deserti is similar to that described by Chew and Butterworth (3) for 
D. merriami. The desert kangaroo rat is born hairless and has a thin, 
pink, wrinkled, transparent integument. Viscera are apparent through 
the skin of the venter and sutures and blood vessels on the skull are 
visible. The snout area containing the vibrissa sheaths appear to be 
swollen and are richly vascular. The yellowish-brown vibrissae are 
about 6 millimeters long at birth, but lengthen to 13 mm. in 5 days and 



268 



BERNARD B. BUTTERWORTH 129 

23 mm. by 15 days. The adult length of 72 mm. is attained by 90 
days. 

Black pigmentation appears about 5 days after birth. The pigmenta- 
tion begins on the dorsum and top of the head. A faint dorsal tail 
stripe is present. The end of the tail is unpigmented for 10 mm. and 
then a black ring circles the entire tail for about 7 mm. The black 
area extends on the dorsal side of the tail for about 30 mm. and shades 
out to a pale gray color. The entire ventral surface of the tail is white 
except for the small black area near the tip. The feet and venter are 
white. The site of the dermal gland shows as a light depression just 
posterior to the scapulae. It darkens by 15 days, begins to lighten by 
19 days and is covered with hair by 21 days. The head is sufficiently 
pigmented by 7 days so that the dorsal cranial sutures and blood 
vessels are no longer visible. By 21 days the mammae have become 
very distinct. The insides of the thighs and the venter, in general, are 
sparsely haired until about 15 days. By 21 days the animal is fully 
furred and the color pattern of the young is now similar to that of the 
adult. The young appear darker than the parents, however. 

The pelage of D. merriami is a darker yellowish-buff than that of 
D. deserti, the white tail stripe is wider than the dark tail stripe, and 
the terminal tuft is brown. Dark whisker patches are distinct in D. 
merriami but are absent in D. deserti. Juvenile D. merriami are com- 
pletely furred by 15 days. Developmental stages are shown in Figures 
1 to 6. 

The pinnae of the ears, closed at birth, and only two mm. in length 
gradually open from 9 to 15 days. The length of time until opening 
varies with different litters. The ears are fully opened by 15 days in 
D. deserti and by 10 days in D. merriami. 

The nails are soft at birth and gradually become hard by 15 days in 
both species. 

The incisor teeth appear later in D. deserti than in D. merriami. 
They break through the gums at about 2 days in the latter ( Chew and 
Butterworth, 3 ) while they do not appear until about 9 days in the 
former. Teeth are white at first but gradually darken to yellow. By 
25 days the teeth of D. deserti are strong enough to pierce the skin of 
man. 

Eye development is summarized in Figure 7 for various species of 
kangaroo rats. In my laboratory, individuals of D. deserti had their 
eyes open as follows: 3 on the 15th day; 3 on the 16th day and 6 on 



269 



130 



GROWTH AND DEVELOPMENT OF KANGAROO RATS 




FIGURE 1 

Dipodomys deserti, 3 days old. Note absence of hair and the relative sizes of the 
feet. Both eves and ears are tightly closed. 

FIGURE 2 
Dipodoiuvs uien-iaini, a mother nursins her voung. 
FIGURE 3 
Dipodomys deserti, 10 days old. A litter of 5. Note the white tail tip, one of the 
distinguishing features of this species. 

FIGURE 4 

Dipodonivs uierriami, 11 davs old. A litter of 3. 

FIGURE 5 

Dipodomvs deserti, 16 davs old. From the same litter as pictured in Figure 3. 

FIGURE 6 
Dipodomys merriami, 16 days old 



270 



BERNARD B. BUTTERWORTH 



131 



the 17th day. D. merriami had their eyes open between the 11th and 
15th days. 





Davs after birth 




Species 


that e\es open 


Reference 


Dipodomvs deserti 


15-17 


Butterworth 


D. deserti 


16 


Rush (8) 


D. merriami 


11 


Butterworth 


D. merriami 


11-15 


Chew and Butterworth (3) 


D. merriami 


21 


Do ran (5) 


D. merriami 


by third week 


Reynolds (7) 


D. heermanni 


12-15 


Fitch (6) 


D heermanni 


14-16 


Tappe (9) 


D. nit rat aides 


13-14 


Culbertson (4) 


D. spectabilis 


14 


Bailey (1) 



FIGURE 7 
Eye development in various species of kangaroo rats. 

A comparison of general development in the two species in this 
study is shown in Figure 8. 



Eyes open 

Ears open 

Incisor teeth erupt 

Solid food eaten 

Solid feces first noted 

Nails harden 

Sand used for cleaning pelage 

Well haired 

Weaned 

Mammae first visible 

Drumming with feet first noted 





Days 


after 


birth 




D. deserti 


[ 




D. 


merriarni 


11-17 








11-15 


9-15 








8-10 


7-10 








2-8 


15 








13 


15 








17 


12-15 








12-15 


17 








13-15 


11-15 








14 


15-25 








17-22 


21 








11 


35 












FIGURE 8 
Comparison of sequences of general development of Dipodomys deserti and Dipodomys 
merriami. Selected features based on 8 Utters of D. deserti and 4 litters of D. merriami. 

Growth Analyses: A comparison of weight increases in D. deserti and 
D. merriami is shown in Figures 9 and 10. Weights become constant 
at adult levels of approximately 145 grams in D. deserti and 40 grams 
in D. merriami. An analysis indicates that early growth is rapid in 
D. merriami and continues more slowly toward the maximum weight. 
At 10 days D. deserti had reached 16 per cent of its total adult weight 
while D. merriami had attained 26 per cent of its adult weight. At 30 
days the two species had reached approximately half their maximum 
weight, 47 per cent in D. deserti and 53 per cent in D. merriami. At 



271 



132 GROWTH AND DEVELOPMENT OF KANGAROO RATS 





15 


days 


20 


days 


30 days 


50 


days 


90 


days 




D.d. 


D.m. 


D.d. 


D.m. 


D.d. D.m. 


D.d. 


D.m. 


D.d. 


D.m. 


Total length 


47 


54 


55 


70 


72 80 


83 


95 


97 


99 


Tail length 


39 


47 


50 


61 


73 81 


91 


97 


93 


99 


Foot length 


70 


82 


80 


87 


82 95 


96 


99 


100 


100 


Ear length 


63 


63 


67 


82 


78 90 


81 


95 


88 


99 


Weight 


27 


35 


33 


43 


47 53 


75 


64 


91 


78 



FIGURE 9 

Percentages of growth toward maturity completed at indicated intervals in D. deserti 
nd D. merriami. 



50 days D. deserti had reached 75 per cent of its adult weight while 
D. merriami had only attained 64 per cent. At this point D. merriami 
lagged behind and then very slowly approached the maximum weight. 
At 90 days D. deserti had attained 91 per cent of its weight while in 
D. merriami only 78 per cent had been reached. In the later phases 
of growth D. merriami gained weight more slowly than D. deserti. 
Both attained full adult average weights by 150 to 180 days. 

In total length ( Figures 9 and 1 1 ) Z>. merriami grew more rapidly 
than D. deserti throughout the growth period. Maximum adult lengths 
are difficult to measure but approximate adult dimensions are attained 
by 90 days. 

The tail of D. merriami (Figures 9 and 11) grew faster than that 
of D. deserti during the developmental period. After 90 days D. 
merriami had little tail growth while D. deserti continued to increase 
its tail length by 7 per cent. 

The foot (Figures 9 and 12), which was already well developed at 
birth, grew fastest of all. At 15 days D. deserti had a foot 70 per cent 
of adult size while D. merriami had attained 82 per cent of the adult 
foot size. Both species attained maximum foot size between 50 and 
90 days. 

The ear (Figures 9 and 12) grew rapidly in both species, that of 
D. merriami faster than that of D. deserti. The ear was approximately 
fully grown by 90 days in D. merriami but continued to grow slowly 
in D. deserti. 

Size of the litter (Figure 13) made little difference on increases 
in weight of D. deserti. Litters containing 2, 3, 4, and 5 individuals 
were compared and showed very little variation in weight changes. 
Apparently all individuals in the respective litters received sufficient 
food both by nursing and individually after weaning. Litters of 
D. merriami were not numerous enough to permit these observations. 



272 




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134 



GROWTH AND DEVELOPMENT OF KANGAROO RATS 



80-1 



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SO 



20 — 



O 



z 


10 
9 




R 


I 




1- 


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o 


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INCREASE IN LINEAR DIMENSIONS 

X P. DESERTI 
D. MERRIAMI 



J I I L 



1_J L_± 



6 12 18 24 30 36 42 48 54 60 66 72 78 84 

AGE IN DAYS 

FIGURE 11 
A composite graph showing increase in linear dimensions of total length and tail 
length in D. deserli and D. merriami, semilogarithmic plot. 



274 



BERNARD B. BUTTERWORTH 



135 



80-1 



50 



30- 



20- 



X 10- 
I- 9 

LiJ 7- 
_l 6. 

5- 
4- 



3- 



2- 



FOOT - 




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INCREASE IN LINEAR 
DIMENSIONS 

y p. DESERTI 
o D. MERRIAMI 



J_ 



_L 



_L 



_L 



_L 



_L 



6 12 18 24 30 36 42 48 54 60 66 72 78 84 

AGE IN DAYS 

FIGURE 12 
A composite graph showing increase in linear dimensions of foot length and ear length 
of D. deserti and D. merriami, semilogarithmic plot. 



275 



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276 



BERNARD B. BUTTERWORTH 137 

The differential rates of growth during development in the two 
species of kangaroo rats is significant. The smaller D. merriami 
matures more rapidly than the larger D. deserti. The development of 
various body parts in growing juveniles of D. merriami demonstrates 
more rapid growth and an earlier maturity than D. deserti. The 
precocious growth, especially during early development, brings D. 
merriami to an earlier seasonal reproductive potential than D. deserti 
and may allow for an earlier dispersion. Rapid development may be 
one contributing factor for the larger geographical range of Merriam's 
kangaroo rat. 

Summary and Conclusions 

The growth and development of two sympatric species of kangaroo 
rats is discussed, utilizing data from 8 litters of D. deserti and 4 litters 
of D. merriami reared under identical laboratory conditions. General 
development and sequences of hair acquisition are described. Animals 
of both species were completely furred by 15 days. Their pelages were 
darker than those of their parents. 

The ears, which were closed at birth, opened in 15 days in D. deserti 
and in 10 days in D. merriami. The nails hardened by 15 days in both 
species and the teeth erupted after 5 days in D. merriami and in 8 days 
in D. deserti. The teeth were white at first but gradually darkened to 
a shade of yellow. Eyes opened at about 16 days in D. deserti and 
from 11 to 15 days in D. merriami. 

Instantaneous growth rates were calculated for various measure- 
ments, such as weight, total length, tail length, foot length, and ear 
length. Both species of kangaroo rats attained average adult weights 
from 150 to 180 days. Each species reached approximately one-half 
of its adult weight by 30 days. Early growth was rapid in D. merriami 
but continued more slowly toward maximum weight. D. deserti at- 
tained maximum adult weight at a slightly earlier age than D. merriami. 
In total length, D. merriami grew more rapidly than D. deserti through- 
out the growth period. Both grew to approximately adult lengths by 
90 days. The tail of D. merriami grew faster than that of D. deserti 
during development. After 90 days D. merriami had little tail growth 
while the tail of D. deserti continued to increase slowly in length. The 
foot showed the fastest development. By 15 days D. deserti had 70 
per cent of its adult size while D. merriami had attained 82 per cent 
of its adult size. Both species attained maximum size between 50 and 



277 



138 GROWTH AND DEVELOPMENT OF KANGAROO RATS 

90 days. The ear of D. merriami grew slightly faster than that of 
D. deserti. Ears were almost completely grown to adult size in D. 
merriami by 90 days. They continued to grow slowly in D. deserti. 
Size of litter made no appreciable difference in growth rates. 

The precocious early development of D. merriami may partly explain 
its larger geographical range. 

Acknowledgments 

Special appreciation is extended to the University of Southern 
California Graduate School which readily furnished equipment and 
facilities for carrying on the necessary laboratory work connected 
with this research and to the Committee for Research in Problems of 
Sex, National Academy of Sciences — National Research Council, 
which provided, in part, the financial help needed to complete the 
study. 

References 

1. Bailey, V. 1931. Mammals of New Mexico. North American Fauna, 53, 412 pp. 

2. Brody, S. 1945. Time relations of growth of individuals and populations. Chapter 

16:487-574 in Bioenergetics and growth. New York: Reinhold. 1023 pp. 

3. Chew, R. M., & Butterworth, B. B. 1959. Growth and development of 

Merriam's kangaroo rat, Dipodomys merriami. Growth, 23, 75-95. 

4. CuLBERTSON, A. E. 1946. Observations on the natural history of the Fresno 

kangaroo rat. Jour. Mamm., 27, 189-203. 

5. DoRAN, D. J. 1952, Observations on the young of the Merriam kangaroo rat. 

Jour. Mamm., 33, 494-495. 

6. Fitch, H. S. 1948. Habits and economic relationships of the Tulare kangaroo 

rat. Jour. Mamm., 29, 5-35. 

7. Reynolds, H. G. 1956. The ecology of the Merriam kangaroo rat {Dipodomys 

merriami Mearns) on the grazing lands of Southern Arizona. Ecol. Monographs, 
28, 111-127. 

8. Rush, W. M. 1945. Beau Brummel of the wild. Nat. Hist., New York, 54, 40-41. 

9. Tappe, D. T. 1941. Natural history of the Tulare kangaroo rat. Jour. Mamm., 

22, 117-148. 



278 



Article IX.— CRANIAL VARIATIONS IN NEOTOMA 
MICROPUS DUE TO GROWTH AND INDIVIDUAL 
DIFFERENTIATION. 

By J. A. Allen. 
Plate IV. 

In view of the stress naturally, and very properly, laid upon 
the importance of cranial characters in the discrimination of 
species in groups of closely-allied forms, it seems desirable to 
ascertain the character and amount of change in not only the 
general form of the skull but in the form of its separate bones 
due to growth, and also to determine the amount and kind of 
individual variation that may be expected to occur in skulls 
unquestionably of the same species. Having of late had occasion 
to examine a large amount of material relating to the genus 
Neotoma^ the subject has been forcibly brought to my attention, 
and some of the results of a careful examination of a large series 
of skulls pertaining to several species of this genus are here 
presented. No attempt is made to treat the subject exhaustively, 
only a few special points being here presented. 

As is well known to all experienced workers in mammalogy, 
tlie general contour of the brain-case, the relative size and form 
of individual bones, notably the interparietal, and the condition 
of the sujjraorbital and other ridges for muscular attachment, 
alter materially after the animal reaches sexual maturity ; the 
deposition of osseus matter, the closing of sutures, the building 
out of crests and rugosities continuing throughout life, so that a 
skull (){ a very old animal may differ notably from that of an indi- 
vidual of the same species in middle life, and this latter from one 
just reaching sexual maturity. 

The Museum has at present a large series of specimens of 
Neoionia niicropus Baird, including ages ranging from nursling 
young to very old adults. They are mainly from three localities 
in the eastern coast district of Texas, namely, Brownsville, Cor[)us 
Christi, and Rockport. In order to avoid any complications that 

[233] 



279 



2,34 Bulletin American Museum of Natural History. [Vol. VI, 

might arise through geographic variation, only the specimens from 
Rockjjort and Corpus Christi — localities less than twenty-five 
miles apart, and similar in physical conditions — are here consid- 
ered. There is not the slightest reason for questioning their con- 
specific relationshi|). The series selected to illustrate variations 
due to age are, with one exception, from Rockport ; those figured 
to show individual variation are all from Corpus Christi. 

Variations due to Age. 

General Contour. — The variation in the general form of the 
skull resulting from growth is due mainly to the lengthening of 
the several skull segments without a corresponding relative in- 
crease in the breadth of the skull. Hence in the young skull, in 
comparison with an adult skull of the same species, the brain- 
case is disproportionately large in comparison with the anteor- 
bital and basal portions of the skull. This is well shown in 
Plate IV, and in the subjoined table of measurements of three 

Measurements and Ratios showing Cranial Variations due to Age 

IN Neotoma tnicropus. 



Occipito-nasal length 

Length of nasals 

Length of frontais 

Length of parietals on median line. . . . 

(Ireatest length of parietals 

Length of interparietal 

Length of brain-case 

(Ireatest rostral breadth 

Least interorbital breadth . . , 

Breadth of brain-case 

Breadth of interparietal 

Greatest zygomatic breadth 

Depth of skull at middle of palate 

Depth of skull at front of basisphenoid. 
Length of tooth-row (crown surface). . . . 

Length of incisive foramina 

Width of incisive foramina 

Length of palatal floor 



No. 

5834, 
9 JUV. 

1 


Ratioi 


No. 
4480, 
.', juv. 


31 


100 


41 


10 


32.3 


14.5 


13 


42 


15 


5 


19.4 


6 


12 


39 


15 


4.5 


14.5 


5.5 


14 


45.2 


17 


5.5 


17.7 


6.3 


6 


1 ;» . 4 


6 


16 


51. H 


19.5 


11 


35.5 


10 


20? 


ti4.B 


23 


8 


2rt 


11 


11 


35.5 


12 


8- 


26.8 


8 


6 


19.3 


8.5 


3 


9.7 


3 


5 


16.1 


7 





No. 


Ratio" 


4478, 

,' very 

old. 


100 


53 


35.4 


22 


36.6 


18 


14.6 


8 


36.6 


16 


13.4 


7 


41.5 


21 


15.4 


6.5 


14.6 


6 


45 


20 


24.4 


7.5 


56.1 


30 



26 
29 . 3 
19.5 

20.7 
7.3 
17 



15 

14 

9 
11. 

3. 

7 



Ratioi 



100 
41.5 
34 
15 

30.2 
13.2 
39. 
12. 
11 
38 

14.2 
56.6 
28.5 
26.4 
17 

21.7 

6.6 

13.2 



.6 
.3 
.3 



' Ratio to occipito-nasal length. 

2 From No. 448?, 9 juv., in which the last molar has Just come into use. 



280 



1 894-] Allen, Cranial Variations in JVeo/oma micropus. 235 



specimens of A', micropus from Rockport, Texas. No. 5834, 
$ juv., is a nursling so young that the last molar is still wholly 
enclosed in the jaw ;' No. 4480, ^, jnv., though not (]uite full- 
grown, would pass as a 'young adult'; No. 4478, r? ad., is a very 
old male, with the teeth well worn down, and the fangs visible 
at the alveolar border. Other specimens in the series furnish a 
complete series of gradations between the two extremes (Nos. 
5834 and 447^)- 

In general contour (Figs, i-ii, PI. IV), the young skull, in 
comparison with adults, is much more convex in dorsal outline,' 
very broad posteriorly, and very narrow anteriorly. In compar- 
ing the relative length of the several skull segments the occipito- 
nasal length is taken as the basis, and the skulls will be referred 
to as A ( = No. 5834), B ( = No. 4480), and C( = No. 4478). 

Rostral Segment. — In A the ratio of the rostral segment to the 
total length is 32.3 per cent. ; in B, 35.4; in C, 41.5 — giving a 
rapid increase in the ratio with age. 

Frontal Segment. — In A the ratio of the frontal segment — /. e., 
the distance between the naso-frontal and fronto-parietal sutures 
— to the total length is 42 per cent. ; in B, 36.6 ; in C, 34 — a 
considerable decrease in the ratio with age. 

Parietal Segment. — In A the ratio of the parietal segment — 
/. (?., the distance from the latero-anteri<jr angle of the parietal 
bone on either side to the occipito-parietal suture — to the total 
length is 39 per cent.; in ^, 36.6; in C\ 30.2 — again a rapid 
decrease in the ratio. 

Brain-case. — The length of the brain-case in A is 5 1.6 per cent, 
of the total length of the skull ; in B, 45 ; in C, t,?>. 

In each case the change in ratio is due to the disproportionate 
growth of the rostral portion of the skull. Thus in A the nasals 
have a length of only 10 mm. ; in B they have increased to 14.5 
mm., and in C to 22 mm., while the total occipito-nasal length of 

' The length of the tooth-row given in the table is taken from an older specimen (No. 4482, 
^ juv.), in which the last molar has reached the level of the others and is just beginning to 
show traces of wear. 

'•^ In Figs. 10 and 11 it should be noted that the greater flatness of the skull interorbitally, 
as compared with Fig. 6, is masked by the raised supraorbital borders in the older skulls wiien 
viewed in profile. 



281 



236 Bulletin American Museum of Natural History. [Vol. VI, 

the skull has increased only from 31 mm. in A to 53 mm. in C. 
In other words, the nasal bones have increased in length 120 per 
cent., while the total length has increased only 77 per cent. 

Transverse Breadth. — In respect to the breadth of the skull 
the variations with growth are much less than in its length. 
Thus tlie greatest diameter of the rostrum varies only from 5.5 
mm. in A to 6.5 in C — an increase of about 20 per cent, in the 
breadth of the rostrum, against an increase of 120 per cent, in 
its length. The interorbital breadth remains nearly constant, 
being 6 mm. in all three of the skulls here compared. The width 
of the brain-case shows an increase of 25 per cent, against an 
increase in the total length of the skull of 77 per cent. The 
zygomatic breadth shows an increase of about 50 per cent., due 
almost wholly to the thickening and increased convexity of the 
zygomatic arches. 

Vertical Depth. — In respect to the depth of the skull, the vari- 
ations with age prove especially interesting, although only such 
as would be expected from the facts already given. For present 
purposes the depth of the skull is taken at two points, namely, 
{a) at the middle of the palatal region, and {b) at the posterior 
border of the basisphenoid (basisphenoid-basioccipital suture). 
The palatal depth increases markedly with age, correlalively with 
the growth of the rostrum ; the basisphenoidal depth changes but 
slightly after the molars have attained to functional development. 
Thus in A the basisphenoidal depth is 11 mm. ; in /^, 12 mm. ; 
in C, 14 mm. — an increase of about 28 per cent. The palatal 
depth in ^4 is 8 mm. ; in B, 11 mm. ; in C\ 15 mm. — an increase 
of nearly 88 per cent. 

Tooth-row. — The length of the upper tooth-row varies about 12 
per cent., due almost wholly to the wearing down of the teeth, 
the length of the crown surface being much less, in slightly 
worn teeth, than the length taken at the alveolar border. 

Interparietal. — The interparietal shows sur[jrising modilication 
with age, both as to size and form, but especially in respect to 
the latter. At early stages, as in ^, this bone is more or less 
crescentic in shape, with the transverse diameter more than twice 



282 



1894-] Allen, Cranial Variations in Neoto7na micropus. 237 



the antero-posterior diameter. Thus in A the two diameters are 
respectively 11 and 4.5 mm. ; in B, 10 and 5.5 mm. ; in 6\ 7.5 
and 7 mm. In other words, the short, broad, convex sub-cres- 
centic interparietal in A becomes transformed in C into a 
squarish, flat bone in which the two diameters are nearly equal, 
instead of the transverse being twice as great as the antero- 
posterior, as in A. This would be almost incredible were not 
the proof so abundantly furnished by the material in hand, where 
every stage of transition is shown. (Figs. i-S, PI. IV.) This 
change is coincident with the development of the raised supra- 
orbital borders and their prolongation backward as ridges to the 
parieto-occipital suture, and the flattening of the whole dorsal 
aspect of the post-rostral portion of the skull. In old age these 
ridges become confluent with the lateral edges of the interparietal 
which has now lost its postero-lateral moieties, partly apparently 
by absorption and partly by their being overgrown by the mediad 
posterior angle of the parietals. A sharp thin ridge for muscular 
attachment also extends back from the posterior base of the 
zygomatic arch. The interparietal at the same time develops a 
more or less prominent median angular projection at its posterior 
border, confluent with the median ridge of the supraoccipital. 
The contrast between these conditions, obtaining only in very 
old skulls, and their almost entire absence in skulls which have 
iust reached sexual maturity, is strikingly great. 

Supraoccipital. — The supraoccipital changes from a posteriorly 
convex, thin lamina of bone, in early life, to a thick, nearly ver- 
tical plate, with a strongly-developed median ridge produced into 
an angular spine at its superior border, and with a lateral ridge 
on either side about midway between the median line and its 
lateral borders ; these lateral ridges also each develop an angular 
rugosity or process about midway their length. The superior 
border is also produced into an incipient occipital crest. 

Basioccipital. — The basioccipital becomes greatly altered by 
growth, as in fact is the case with the whole postpalatal region. 
In comparing stages A and C it is found that the distance across 
the occipital condyles increases only about 15 per cent., while 
the breadth of the anterior border increases 100 per cent, and 
the length about 50 per cent. (Figs. 12-14, P^- ^^ ■) 



283 



230 Bulletin American Museum of Natural History. [Vol. VI, 

Basisphenoid. — The basisphenoid doubles in length, and its 
anterior third becomes differentiated into a narrow projecting 
neck. The presphenoid at stage A is nearly hidden by the 
palatal floor. (Figs. 12-14, PI. IV.) 

Postpalatal Region as a whole. — This doubles its length with an 
increase in breadth of only about 50 per cent. At stage A the 
postpalatal border terminates slightly behind the posterior edge 
of M.2 ; in stage 3 it holds very nearly the same position. The 
distance between the postpalatal border and the front border of 
the auditory bullae, compared with the total length of the skull, 
is as I to 9 in ^, and as i to 5 in C. In A the pterygoid hamuli 
reach the second fourth of the bullae ; in C they terminate 
slightly in advance of the bullae. The bullae themselves in A are 
more obliquely placed than in C, in relation to the axis of the 
skull, and are quite differently shaped. Also the form of the 
foramen magnum has undergone much change. These points 
are all well shown in Figs. 12-14 of ^l^e accompanying plate. 

Incisive Foramina. — Consequent upon the growth of the 
rostral portion of the skull, the incisive foramina undergo marked 
change in form, and somewhat in position, as regards both their 
anterior and posterior borders. In the stage designated as A 
they are short and broad, and extend relatively further both 
anteriorly and posteriorly than in stage B or C, their anterior 
border being nearer the base of the incisors, and their posterior 
border being carried back to or slightly behind the front border 
of the first molar. Thus in A the length of the incisive foramina 
is 6 mm., with a maximum breadth of 3 mm., while in C the 
dimensions are respectively 11.5 and 3.5 mm. — a great increase 
in length with only slight increase in breadth. At the same 
time the anterior border is considerably further from the base of 
the incisors, and the posterior border is slightly in advance, 
instead of slightly behind, the front border of the molars. 

Sphe7io-palatine Vacuities. — Va adults of N'eotoma micropus^ as in 
other species of the ' round-tailed ' section of the genus, there is 
a long, broad vacuity on each side of the presphenoid and ante- 
rior third of the basisphenoid, which Dr. Merriam has recently 



284 



1 894-] Allen, Cranial Vai'iations in Neotoma micropus. 239 



named' the ^ spheno-palatine vacuilies,' and he has also called atten- 
tion to the fact that they are not present in some forms of the 
* bushy-tailed ' section of the genus. It is therefore of interest 
in the present connection to note that these vacuities are absent 
at stage A, and are only partially developed at later stages (Figs. 
12-14, PI. IV). My attention was called to the matter by finding 
several nearly fully-grown skulls from Texas and northeastern 
Mexico with these vacuities either quite absent or represented by 
an exceedingly narrow slit, while I could find no differences in 
the skins or in other cranial characters that gave the slightest 
hint that the animals were not referable to JV. micropus. Further 
examination of young skulls of undoubted JV. micropus from 
Rockport and Corpus Christi, Texas, showed that the closed 
condition was in this species a feature of juvenility. It is thus of 
interest to find that a feature which proves to be merely a char- 
acter of immaturity (and quite inconstant as well) in IV. micropus 
is a permanent condition in N. cinerea occidentalis: 

In the development of these vacuities it appears that as the 
presphenoid increases in length it becomes reduced in width ; 
at the same time, as the skull broadens, the edges of the ascend- 
ing wings of the palatine bones become slightly incised. There 
is, however, much individual variation in this respect, as will be 
shown later. 

Molars. — When the molars first cut the gum they have nearly 
the entire crown-surface capped with enamel. Very soon, even 
before the tooth has attained its full height, the enamel begins to 
disappear from the centers of the enamel loops, the capping re- 
maining longer over the narrower loops than over the broader 
ones ; it quickly disappears from all as soon as the crown-surface 
becomes subject to wear. In stage ^, in which only M.i and 
M.2 have appeared, and are less than one-third grown, the 
enamel walls of the loops nearly meet over the dentinal areas — 
quite meeting over the narrower portions, especially in the case of 
the middle transverse loop of each tooth. Some time before the 
age represented by B is reached, the crown-surface is worn to an 

1 Proc. Biol. Soc. Wash., VII I, p. 112, July, 1893. 

2 Unfortunately the outline figures here given (Figs. 12-15, PI- IV, ) fail to show clearly the 
points at issue. 



285 



240 Bulletin American Museum of Natural History. [Vol. VI, 



even plane ; the tooth has reached its normal length, but the 
fluting of the sides still extends to the alveolar border. As 
attrition goes on, with the advance of the animal in age, the 
crown-surface wears down, and the neck of the tooth appears 
above the alveolar border, till, especially in the upper molars, the 
fluted terminal and the smooth basal portions are of nearly equal 
extent ; but in old age (as in C) the smooth basal portion is the 
longer and the division of the root into fangs is clearly shown. 
With this wearing down the tooth increases somewhat in both 
width and length, but the pattern of the enamel folds undergoes 
but slight change until nearly the whole crown is worn away, 
exce|:)t that the angles become gradually more rounded. 

Resume. — As already stated the change with age in the general 
form of the skull is due to the relatively disproportionate increase 
in length of the pre- over the post-orbital region, and the same 
disproportionate increase of the basal region as compared with 
the frontoparietal elements. In the first case the rostrum be- 
comes relatively greatly produced ; in the second the basiocci- 
pital and adjoining parts become so greatly enlarged as to change 
the entire aspect of the basal region of the skull. Thus the 
occipital condyles, which in A terminate slightly in advance of 
the most convex portion of the supraoccipital, and are crowded 
u]) very close to the bullae, form in C the most posterior part of 
the skull, with a considerable interval between them and the 
bulla;. (Figs. 12-14, PI- IV.) 

Individual Variation. 

In comparing a large series of skulls of the same species it 
quickly becomes apparent that no element of even the adult 
skull is constant, either as to form or relative size. There is also 
much variation in the size of skulls of the same sex and approxi- 
mately the same age. 

Variation in .5'/sr.— Thus in Neotoma micropiis, from the same 
locality, there are dwarfs and giants. While the females average 
smaller than the males, size is by no means a safe criterion of 
sex. Thus two old females, not appreciably different in age, 
from Corpus Christi, Texas, vary as follows : No. 2948, total 



286 



1 894-] Alleti, Crania/ Variations in Ncotoma micropus. 24 1 



length 51 mm., zygomatic breadth 26 mm. ; the corresponding 
dimensions in No. 2955 are 45 mm. and 24 mm. These are 
merely the extremes of a series of six specimens ; with a much 
larger series doubtless the difference would be considerably 
increased. A series of six old males, from the same locality and 
indistinguishable as to age, vary as follows: No. 2952, total 
length 50.5 mm., zygomatic breadth 27 mm. ; the corresponding 
dimensions in No. 2956 are 45 mm. and 25 mm. 

Nasals and ascending branches of the Premaxillce. — Ordinarily 
in N. micropus the nasals terminate in a gradually narrowed 
evenly rounded point, a little less than 2 mm. in front of the 
posterior termination of the ascending branches of the premaxills. 
The distance between the points of termination of the nasals and 
premaxillse, however, frequently varies between 1.5 and 2.5 mm. ; 
more rarely from i to 3 mm. These extremes each occur in the 
ratio of about 10 per cent, of the whole, while probably 60 per 
cent, would not vary much from the normal average of about 
2 mm. (See Figs. 1-8 and t6, 17, PI. IV.) 

The nasals, as already said, usually terminate in an evenly 
rounded point, but in several of the 50 skulls of N. micropus 
before me their posterior border forms a double point, each nasal 
terminating in a distinctly rounded point ; in one or two the 
posterior border is squarely truncate ; in others it is irregularly 
uneven. The ascending branches of the premaxillae usually 
terminate in an obtusely V-shaped point, with a uniformly even 
outline, their breadth, however, being subject to variation ; in 
some specimens they terminate in a brush of irregular spiculae. 
(Figs. 1-8 and 16, 17, PI. IV.) 

Frontals. — The posterior border of the frontals is subject to 
great irregularity, varying from a nearly transverse line (rounded 
slightly at the outer corners) to a gentle, rather even convexity, 
and thence to an acute angle, involving the whole posterior 
border. It is difficult to decide what outline is the most frequent, 
though the tendency seems to be greatest toward a well-pro- 
nounced rather even convexity. Figures 1-8 and 18, 19, Plate V, 
well show the variation in the position and direction of the 
fronto-parietal suture. 

\_Scptenibcr , /Sq/.] 



287 



242 Bulletin American Museum of Natural History. [Vol. Vl, 

Parietals. — The anterior outline of the parietals of course con- 
forms to the posterior outline of the frontals, and must be equally 
variable. It hence follows that their length on the median line 
is also variable. Their posterior border is also subject to much 
variation in consequence of the great diversity in the form of the 
interparietal. 

Intej'parietal. — In middle-aged specimens the interparietal tends 
strongly to a quadrate form, varying from quadrate to diamond 
shape, through a more or less marked median angular extension 
of both its anterior and posterior borders, and occasionally of its 
lateral borders as well. Often it forms a quadrate figure, in which 
each of its four sides is slightly convex ; again the corners are so 
much rounded, and the lateral breadth so much in excess of the 
antero-posterior, as to give a lozenge-shaped figure. In other 
cases it is distinctly shield-shaped ; in others it is hexagonal. In 
size the variation is fully 50 per cent, of what may be regarded 
as the average dimensions. These remarks have strict reference 
to fully adult specimens, and as nearly as can be judged these 
variations are not at all due to differences of age, which, as 
already shown, has so great an influence upon the size and form 
of this exceedingly variable element of the skull.' (Figs. 20-23, 
PI. IV. Compare also the interparietal, as shown in Figs. 1-8.) 

Ventral aspect. — The ventral aspect of the skull presents 
numerous points of variability, only a few of which will be here 
mentioned. The palate varies more or less in breadth, and 
especially in the development of the anterior palatal spine, which 
is sometimes slight, and sometimes so strongly produced anteri- 
orly as to touch the vomer. The postpalatal border may be 
evenly concave, or present a slight median process. The pre- 
sphenoid is very variable in size, being often an exceedingly 
slender rod of bone, and at other times very stout, the variation 
in thickness being nearly or quite 100 per cent. The anterior 
third of the basisphenoid shares in the same variability. As the 

' As regards variation with age in the form of the interparietal, Neotoma jnicropus is only 
an example of what doubtless prevails throughout the genus, and even in many other genera as 
well. Yet in adult animals the form of this bone seems, as a rule, to be sufficiently constant to 
be of more or less taxonomic value. Thus in the A'^. cinerea group it may be said to be nor- 
mally quadrate ; in the N .fuscipes group it is quite constantly shield-shaped. In N. floridana., 
however, and in the N. mexicana group, it seems to be nearly or quite as variable as in N. 
jiiicropus, both as to size and shape. 



288 



1 894-] Allen, Cranial Variations in Neotoma ?nicropus. 243 

ascending borders of the palatals are also variable in respect to 
the extent of their development, it follows that there is, even 
among adults, a wide range of variation in the size of the spheno- 
palatine vacuities. 

Teeth. — Aside from differences due to age and attrition, the 
teeth vary in size to a considerable extent among individuals 
strictly comparable as to sex and age, some having a much 
heavier dental armature than others. But more particularly note- 
worthy in this connection is the variation in the color of the 
teeth, which seems strongly a matter of individuality. Although 
Dr. Merriam has recently placed JV. micropus in his " Neotoma 
leucodon group,'" which has, among other alleged characters, 
" color of teeth white or nearly white," the teeth in N. micropus 
average blacker than in any other species of the genus known to 
me. Were this all it might be considered that N. micropus was 
erroneously referred to X^^t' leucodon group'; but unfortunately 
the range of individual variation in the color of the teeth in the 
large series at hand covers also the whole range of variation for 
the genus. Thus in some instances the molar teeth are intensely 
black from base to crown, while the crown-surface itself is 
strongly blackish, even the enamel loops, as well as the enclosed 
dentine being tinged with blackish ; in other cases the teeth 
are merely slightly tinged with brownish near the base and at the 
bottom of the sulci. These extremes are connected by a series 
of very gradual intergradations. In other words, among hun- 
dreds of skulls of Neotoma, those with the blackest teeth occur 
in N. micropus, as well as those in which the teeth are practically 
white. 

In the suckling young the teeth are pure white ; before M.3 
has come to wear, M.i and M.2 have become more or less 
blackened ; in young adults, and in middle aged specimens, the 
teeth are often intensely black ; in old specimens, with the teeth 
much worn, the teeth average lighter than in the younger indi- 
viduals. There is, however, a wide range of variation in the 
color of the teeth in specimens of corresponding age, whether 
old or young. The black coloring consists to a large extent of a 



» Proc. Biol. Soc. Wash., IX, p. ii8, July 2, 1894. 



289 



244 Bulletin American Museum of Natural History. [Vol. VI, 

superficial incrustation which tends to scale off in flakes in the 
prepared skull, and its absence apparently may be due sometimes 
to removal in the process of cleaning the skull for the cabinet. 
In other words, the blackness is to some extent an accidental or 
pathological condition, due probably more or less to the particu- 
lar character of the food or to the health of the animal. 

General Remarks. 

The bearing of what has been stated above respecting varia- 
tions in the form of the skull and of its principal elements due 
to age is of course obvious, the inference being that in animals 
which have reached sexual maturity variations due wholly to 
growth, in passing through adolescence to senility, may readily 
be mistaken, when working with very small series or with single 
specimens, for differences of subspecific or even specific import- 
ance. Not only do the individual bones vary in their outlines 
and proportions and in relative size, but the skull varies as a 
whole in its relative dimensions, including depth as well as length 
and breadth. There is beside this a wide range of purely indi- 
vidual variation, affecting every character that can be used in a 
diagnostic sense. Thus in a series of fifty skulls of Neotoma 
micropus it would be easy to select extremes, of even individual 
variation, that depart so widely from the average, in one or more 
characters, as to deceive even an expert, on considering these 
alone, into the belief that they must represent very distinct 
species ; yet in the present instance the proof that such is not 
the case is overwhelming. In N. micropus the coloration is re- 
markably constant, for a member of this genus, at all seasons 
and ages, so that the case is less complicated than it would be in 
many other species of the group, where the color of the pelage 
varies radically with season and age. 

Personal criticism is not the purpose of the present paper, and 
it was not my intention at the outset to refer specifically to the 
work of any of my confreres. Since its preparation was begun, 
however, its raison d'etre has perhaps been emphasized by the pub- 
lication of two brochures of ' preliminary descriptions ' of species 
and subspecies of the genus Neotoma.^ numbering altogether lo 
species and 8 subspecies, which added to the 22 species and sub- 



290 



1 894-] Allen, Cranial Variations in Neotonia nilcropus. 245 



species previously standing practically unchallenged, makes, at the 
present writing, a total of 40 forms of the genus Neotoma. Of 
these no less than 26 have been described within the last nine 
months.' Without the material before me used by the original 
describers of these forms it would be presumptive to give an 
opinion respecting the merits of many of them. While the greater 
part may have some real basis, it is evident that others are almost 
unquestionably synonyms of previously-described forms, judging 
by ' topotypes ' in this Museum, the brief diagnoses accompanying 
the names affording in these cases no characters that are in the 
least degree distinctive. 

The genus Neotoma was chosen for treatment in this connec- 
tion in preference to some other almost solely by chance, as the 
facts of variation above presented are not at all exceptional. In 
fact the common muskrat {Fiber zlbethlcus) would have shown a 
still more striking case of variability, as would also various species 
of many other genera. Yet describers of new species are con- 
stantly laying stress upon cranial differences that have not neces- 
sarily the slightest s])ecific or even subspecific importance ; and, 
so far as can be judged from their descriptions, they are entirely 
unconscious that such can be the case. 

On the other hand, it is equally certain that such alleged 
characters may have the value assigned them ; since it is now a 
well known fact that the extremes of purely individual variation 
in any character, external or internal, may exceed in amount the 
average difTerences that serve to satisfactorily distinguish not 
only well-marked subspecies, but even forms that are unques- 
tionably specifically distinct. Hence it must often happen that 
the determination of the status of a species or subspecies origin- 
ally described from one or two specimens, in groups especially 
susceptible to variation, must depend upon the subsequent exam- 
ination of a large amount of material bearing upon this and its 
closely-related forms. 



' For a list of the species and subspecies of Neotovta described prior to July 6, 1894, see 
Abstr. Free. Linn. Soc. New York, No. 6, pp. 34, 35, July, 1894. 



291 



246 Bulletin American Museum of Natural History. [Vol. VI,] 



EXPLANATION OF PLATE IV. 

Figures all Natural size. 

Neotoma micropus Baird. Showing cranial variations due to age and 
individualism. (Unless otherwise stated, the specimens are from Rockport, 
Texas.) 

Figs. 1-8. Dorsal aspect of skull, showing gradual change in form with age, 
and especially in the form and relative size of the interparietal. Fig. i. No. 
5834, S juv. (suckling). Fig. 2, No. 2975, $ juv. (nearly sexually adult). 
Corpus Christi, Texas. Fig. 3, No. 5841, ? ad. Fig. 4, No. 4480, f, ad. 
Fig. 5, No. 2958, c? ad^., Corpus Christi. Fig. 6, No. 4479, c5 ad. Fig. 7, 
No. 4477, ? ad. Fig. 8, No. 4478, 6 ad. 

Figs. 9-1 1. vSkuU in profile, to show change of form with growth. Fig. 9, 
No. 5834, S juv. (nursling). Fig. 10, No. 44S0, _<; ad. (rather young). 
Fig. II, No. 4478, (5 ad. (very old). 

Figs. 12-15. Ventral aspect, showing variations in postpalatal region due 
to age. Fig. 12, No. 5834, ? juv. (nursling). Fig. 13, No. 5841, ? ad. (young- 
adult). Y\g. 14, No. 2958, Corpus Christi, (5 ad. (very old). Fig. 15, No. 
1456, Neotoma cinerea occidentalis, (?ad.. Ducks, B. C. (for comparison with 
N. iincroptis). 

Figs. 16, 17. To show extremes of individual variation in relative posterior 
extension of nasals and ascending branches of premaxillie. Locality, Corpus 
Christi. Texas. Fig. 16, No. 2958, ,^ ad. Fig. 17, No. 2948, $ ad. 

Figs. 18, 19. To show extremes of individual variation in posterior border 
of frontals. Locality, Corpus Christi, Texas. Fig. 18, No. 2949, ,5 ad. Fig. 
19, No. 2951, .^ ad. 

Figs. 20-23. To show individual variation in the size and form of the inter- 
parietal. Specimens all from Corpus Christi, Texas. Fig. 20, No. 2949, f, ad. 
Fig. 21, No. 2948, $ ad. Fig. 22, No. 2952, .5 ad. Fig. 23, No. 2945, S ad. 

Note. — If the Brownsville, Texas, series of specimens had also been included, 
the range of individual variation would have been considerably increased. 



292 



HiLi.. A. M. X. H. 



Vol.. VI., Pl. IV. 




Neotoma micropus. 

Fiarures nat. size. 



293 



MATURATIONAL AND SEASONAL MOLTS IN THE 
GOLDEN MOUSE, OCHROTOMYS NUTTALLI 

Donald W. Linzey and Alicia V. Linzey 

Abstract. — The adult pelage of the golden mouse {Ochrotomys mittalli) is 
attained by a single maturational molt. Data on the post-juvenile molt were 
obtained from 96 young golden mice. This molt began on the ventral surface and 
spread dorsally, meeting in the dorsal midline. It then proceeded anteriorly and 
posteriorly. The average age at which male golden mice began molting was 36 
days, whereas that of females was 38 days. The average duration of molt for the 
sexes was 29 days and 25 days, respectively. Golden mice undergo two seasonal 
molts — spring and fall. Data were obtained from 36 mice. Tlie winter pelage 
was generally much darker than the summer pelage. Both spring and fall molts 
were more irregular than the post-juvenile molt, and the spring molt tended to be 
more irregular than the fall molt. Young golden mice born after 1 October and 
8 April appeared to combine the post-juvenile and seasonal molt. Hair replace- 
ment was more irregular than during the normal post-juvenile molt. 

During the course of a study on the ecology and Hfe history of the golden 
mouse, Ochrotomys mittalli nuttaUi, in the Great Smoky Mountains National 
Park (Linzey, 1966), considerable data were obtained on pelage changes. 
The limited data presented by Layne (1960) have been the only published 
infomiation concerning molt in this species. 

Maturational Molt 

The adult pelage of the golden mouse is attained after a single matura- 
tional molt. Data on the post-juvenile molt were obtained from 96 young 
golden mice. Eighty-four of these mice were raised in captivity. Data from 
the remaining 12 individuals were obtained from field observations. 

The molt from the golden-brown juvenile pelage to the golden-orange adult 
pelage, although varying in details, followed a definite pattern ( Fig. 1 ) . The 
first indication of the beginning of the dorsal molt was the appearance of 
new golden fur along the line separating the golden-brown dorsal fur from 
the white fur of the ventral surface. The replacement of the juvenile pelage 
progressed dorsally on both sides and met on the dorsal midline forming a 
continuous band of new fur. The molt then proceeded anteriorly between the 
ears and onto the head, while posteriorly, it joined the molt proceeding 
dorsally near the thighs. By this time, new fur had appeared on the sides 
of the face and just anterior to the ears. The molt along the sides of the body 
had nearly been completed by this time. The last two areas in which the fur 
was replaced were the top of the head and the base of the tail. In some 
individuals, the new fur first appeared just in back of the front leg. It pro- 
ceeded both posteriorly and dorsally and formed a band of new fur just 
behind the ears. The molt proceeding posteriorly then covered the remainder 
of the body. 

This pattern of molt generally agrees with that described for Peromyscus 

236 



294 



May 1967 LINZEY AND LINZEY— MOLT OF GOLDEN MOUSE 



237 



^^^^.iirf^J^ 
















Fig. L — Sequence of post-juvenile molt on the dorsum in Ochrotomys nuttalli. Shaded 
portions represent areas of active hair replacement. Stippled areas represent adult pelage. 



295 



238 JOURNAL OF MAMMALOCiY Vol. 48, No. 2 

Taule 1. — Duration of post-juvenile molt and average age at beginning and ending of 
molt in 34 captive golden mice (Range of values in parentheses). 

Males (15) Females (19) 

Duration 29 days (14-45) 25 days (12-49) 

Beginning 36 days (33-42) 38 days (31-47) 

Ending 64 days (51-87) 63 days (51-84) 

tmei ( Hoffmeister, 1944), Feromyscus gossypinus (Pournelle, 1952) and 
Peromysctis boy lei (Brown, 1963). It differs from that reported for Pero- 
myscus leucopiis noveboracensis (Gottschang, 1956). 

Data on the begmning, ending, and duration of the post-juvenile molt on 
the dorsum in male and female golden mice are compared in Table 1. The 
average duration of molt for males was slightly longer than for females. The 
shortest time recorded was between 12 and 14 days, whereas the maximum 
time required was about 49 days. Approximately 3.5 weeks are required for 
most Peromysciis leucopus noveboracensis to attain their full adult coat 
according to Gottschang ( 1956 ) . He recorded a minimum duration of 12 days 
for captive individuals and 10 days for one wild mouse to undergo the com- 
plete molt; the maximum number of days required was about 36. 

In the field, animals undergoing various stages of maturational molt were 
recorded in June (1), July (1), August (2), and December (8). These mice 
were between 150 mm and 164 mm in total length (mean, 156 mm). In the 
captive population, male golden mice began molting when their total length 
was 149 mm, whereas females averaged 146 mm. At the completion of molt, 
their measurements averaged 163 mm and 160 mm, respectively. From these 
data, it appears that both wild and captive individuals molted at approxi- 
mately the same body size, although it is not known whether they were the 
same age. 

The youngest individuals in captivity to begin molting during the current 
study were 31 days of age. Layne (1960) recorded one young Ochrotomys 
molting at 31 days of age with the molt apparently being complete 10 days 
later. Molting was in progress in one four week old mouse, while in another 
of the same age, it had not yet begun (Layne, 1960). Collins (1918) reported 
that the transition from juvenile to post-juvenile pelage in Peromyscus usually 
began at 6 weeks and was completed about 8 weeks later. The earliest age 
at which Peromyscus leucopus noveboracensis began molting was 38 days 
(Gottschang, 1956). These were all males. The youngest female to begin 
molting was 40 days of age. Ninety-five per cent of his mice of both sexes 
started the pelage change between the ages of 40 and 50 days. Young Pero- 
myscus gossypinus began molting when they were between 34 and 40 days 
of age (Pournelle, 1952). 

Gottschang ( 1956 ) found that, in general, mice of the same sex in a single 
litter started molting simultaneously. However, in every case where a dif- 
ference did occur, he found that the males started to molt first. In the current 



296 



May 1967 LINZEY AND LINZEV— MOLT OF C;OLDE.\ MOUSE 239 

study, the males in 13 out of 21 litters containing mice of both sexes began 
molting before the females, whereas the females began molting first in three 
litters. The initiation of molt was simultaneous in the remaining five litters. 
The progression of the ventral molt was studied in seven individuals (four 
males, three females). The white belly fur was dyed purple by the stain 
Nyanzol A (20 g per liter of water-hydrogen peroxide mixture in ratio of 
two to one) and replacement by new hairs was followed. The ventral molt 
began approximately 2-4 days before the dorsal molt. Hair replacement 
occurred first in the center of the belly and continued laterally, and then 
dorsally into the golden fur. Simultaneously, new hair appeared over the 
entire chest and abdomen. The last areas to acquire new pelage were the 
throat and the ventral bases of the hind limbs. The ventral molt was complete 
at about the time that the dorsal molt covered the entire back ( Fig. 1 ) , 

Seasonal Molt 

Mice of the genus Peromyscus are generally considered to undergo one 
annul adult molt in autumn (Collins, 1923). However, Osgood (1909) and 
Brown ( 1963 ) recorded two annual molts in Peromyscus melanotis and Pero- 
myscus boylei, respectively. 

Golden mice in the Great Smoky Mountains National Park apparently un- 
dergo two annual molts. These take place during the spring (April-June) and 
fall ( October-December ) . The difference between summer and winter pelage 
was clearly distinguishable with the unaided eye. The winter pelage was 
much darker than the usual summer pelage, especially on the mid-dorsum. 
Osgood (1909) noted that winter specimens of Peromyscus melanotis pos- 
sessed a paler colored pelage, whereas summer specimens were in a dark 
pelage. The fall molt of P. boylei was characterized by the replacement of a 
bright cinnamon-brown pelage by a more drab, brown winter pelage (Brown, 
1963). 

Nineteen of 21 adult golden mice in captivity underwent a fall molt 
between October 20 and December 24. A total of 10 adult golden mice were 
observed in the wild between December 12-17. Six of these were molting; 
four already had the winter pelage. The fall molt appeared to be more 
irregular than the post-juvenile molt. In several animals, it began near the 
hind leg, covered the rump and then progressed anteriorly to the head. 
Replacement of the hair was completed first over the posterior half of the 
body. This separated the two remaining areas of molt — the base of the tail 
and the head. The replacement of fur at the base of the tail was completed 
shortly thereafter. The final area of molt was on the head between the ears, 
and this sometimes required several weeks for completion. This is in contrast 
to the post-juvenile molt, where the last area of molt in all of the animals 
was at the base of the tail. 

The spring molt must have occurred between 1 April and 15 June. All wild 
individuals observed between 26 March and 1 April 1964 still retained their 



297 



240 JOURNAL OF MAMMALOGY Vol. 48, No. 2 

winter pelage. By 15 June, all adult golden mice had either already com- 
pleted their spring molt or were very near completion. Seventy-four per cent 
(23) of the adult individuals in the captive population molted during the 
spring. Of those molting, 83% (19) did so between 15 May and 30 June. 
As in the fall molt, the pattern was irregular. Hair replacement occurred in 
patches along the sides and across the shoulders, and a simultaneous molt 
of the entire dorsum took place in only five of 31 individuals ( 16% ) . In the 
cases where this molt was complete, it followed a more regular pattern, with 
hair replacement occurring last on the nape of the neck. 

Gottschang ( 1956 ) noted no difference in the onset, progress or length of 
time required for the pelage change between spring-, summer-, or fall-born 
litters of Pcromyscus leiicopus. During the current study, however, golden 
mice born after 1 October and 8 April appeared to combine the post-juvenile 
molt and seasonal molt. The process of hair replacement was more irregular 
than during the normal post-juvenile molt. The molt began at a point just 
behind the front legs, as in the regular post-juvenile molt. It then proceeded 
dorsally and posteriorly at approximately equal rates. During the combined 
fall molt (post- juvenile plus fall molt), the replacement of hair at the base of 
the tail was completed prior to the completion of molt on the head in all cases. 
In this respect, this combined molt was more similar to the regular seasonal 
molt than to the regular post-juvenile molt. Upon completion of this molt, 
the mice had acquired the typical dark winter pelage. However, during the 
combined spring molt (post-juvenile plus spring molt), hair replacement was 
completed last at either the tail or head regions. 

On the average, those animals born after 1 October began molt at a later 
age than did those animals bom earlier in the breeding season. Males in this 
group began molting at an average age of 37 days, whereas spring and 
summer-born males began at 35 days of age. Females born after 1 October 
began molting at an average age of 43 days, while females bom earlier in 
the season began molting at an average age of 37 days. 

Acknowledgments 

We thank Dr. W. Robert Eadie of Cornell University for his advice and criticism of the 
manuscript. We gratefully acknowledge the financial assistance provided by The Society 
of the Sigma Xi and the cooperation of the National Park Service. 

Literature Cited 

Brown, L. N. 1963. NLaturational and seasonal molts in Peromyscus boylei. Amer. 

Midland Nat., 70: 466-469. 
Collins, H. H. 1918. Studies of normal molt and of artificially induced regeneration 

of pelage in Peromyscus. J. Exp. Zool., 27: 73-99. 
. 1923. Studies of the pelage phases and nature of color variations in mice of 

the genus Peromyscus. J. Exp. Zool., 38: 45-107. 
Gottschang, J. L. 1956. Juvenile molt in Peromyscus leucopus noveboracensis. J. 

Mamm., 37: 516-520. 
HoFFMEiSTER, D. F. 1944. Phylogeny of the Nearctic cricetine rodents, with especial 



298 



May 1967 LINZEY AND LINZEY— MOLT OF GOLDEN MOUSE 241 

attention to variation in Peromtjscus truei. Ph.D. thesis, Univ. Cahfornia, 

406 pp. 
Layne, J. N. 1960. Tlu> growth and development of younp golden mice, Ochrotomijs 

mittalU. Quart. J. Fla. Acad. Sci., 23: 36-58. 
LI^fZEY, D. W. 1966. The life history, ecology and behavior of the golden mouse, 

Ochrotomijs n. nuttalli, in the Great Smoky Mountains National Park. Ph.D. 

thesis, Cornell Univ., 170 pp. 
Osgood, W. H. 1909. Revision of the mice of the American genus Peromyscus. N. Amer. 

Fauna, 28: 1-285. 
PouRNELLE, G. H. 1952. Reproduction and early post-natal development of the cotton 

mouse, Peromyscus gossypinus gossypinus. J. Mamm., 33: 1-20. 

Division of Biological Sciences, Cornell University, Ithaca, New York. Accepted 16 
January 1967. 



299 



SECTION 4— ECOLOGY AND BEHAVIOR 

Ecology and behavior comprise amazingly varied, active, and expanding 
fields. Probably most current mammalogical publications relate to one or both 
of these disciplines. Ecology particularly is of special importance to man owing 
to his increasing awareness of, and concern for, his own environment and such 
problems as the need to regulate human populations and to reduce pollution of 
air and water. The papers selected here can suggest to the perspective reader 
some basic ecological principles that apply to man himself. 

A host of topics other than those we were able to include in our selection 
come to mind when the ecological literature is contemplated — topics such as 
food habits as learned from stomach contents or droppings, or small mammal 
populations as censused by various methods (one such method is the study of 
bones in pellets regurgitated by owls, which are very eflBcient "mouse traps" ) . 
Long term cycles in populations and daily cycles in activity have had their 
share of ecological work also, but lack of space precludes further discussion 
of these topics. 

A large and well-documented textbook on animal ecology is that by Allee 
et al. ( 1949 ) . Three books relating to animal populations and factors that may 
regulate them are by Lack (1954), Andrewartha and Birch (1954), and 
Wynne-Edwards (1962). Their views differ and are interesting; their exam- 
ples, however, are largely non-mammalian. 

The older term "natural history" is perhaps a broader concept than ecology, 
but the older naturalists were deeply committed to the types of studies that 
have come to be called ecological, as well as ethological (a word currently 
used for studies of behavior ) . In the latter context, Ewer's ( 1968 ) recent book 
entitled Ethology of Mammals is of note to the student interested in a general 
coverage of the field, and Maternal Behavior in Mammals (Rheingold, 1963) 
also is useful. 

Papers reproduced here illustrate concepts such as territoriality and home 
range (applied to mammals in the paper by Burt), relatively larger studies 
( note the numbers of specimens mentioned in Frank's paper for example ) that 
provided a firm statistical base and sound quantitative results, and the applica- 
tion of experimental procedures (as in the manipulation of rats in city blocks 
reported by Davis and Christian or the tests run by McCarley in compart- 
mented cages). The application of newer techniques such as Pearson's traflBc 
counter for mouse runways, the squirrel radio described by Beal, and auto- 
matic recording equipment of various types, all have contributed to advances 
in ecology and ethology. The recent study by Estes and Goddard of the 
African wild dog will serve to remind the reader that careful observational 
methods such as were used so effectively by older field naturalists certainly 
have not been supplanted, but only expanded and supplemented. 

Recent field studies dealing with primates have relied heavily on good 
observational techniques. Schaller's (1963) book on the gorilla is a good 
example. Other recent workers have studied baboons, chimpanzees, langurs, 
and other primates in similar ways. A report by Struhsaker (1967), not here 



301 



reproduced, on vervet monkeys is a good example of a shorter paper on primate 
behavior in the field. 

The short paper, here included, by Miller, written more than 60 years ago, 
was based on limited data, but reflects a thoughtful and somehow modern way 
of looking at the problem of bat migration, about which, incidentally, little is 
known even today. 

Ecological problems may be approached at different levels of inclusiveness. 
For example, the relationships of all species of plants and animals in an entire 
community may be studied. Such a broad approach to entire ecosystems 
merges imperceptibly with problems concerning factors that limit distribu- 
tions, hence to ranges of species and faunal and zoogeographic problems. A 
short paper by L. R. Dice (1931), not included here, on the relation of mam- 
mahan distribution to vegetation types is a classic, for here he adopted the 
term "Biotic Province" for a major concept that he and others expanded in 
later American zoogeographic studies. Even an analysis of a few species such 
as Brown's study of six species of shrews has obvious zoogeographic relevance. 
At a less inclusive level the ecological relationships of a single species may be 
studied. This approach is called autecology as opposed to community or syn- 
ecological studies. If we restrict ourselves further to the environmental rela- 
tionships of individual animals, we find our studies, again by gradual stages, 
merge with those that are primarily physiological and behavioral. Physiologi- 
cal techniques also enter directly into the study of ecosystems when energy 
flow is considered, as often is the case in recent studies. Lyman's paper, repro- 
duced here, on hibernators relates to energy, its sources, and its dissipation. 
Two noteworthy contributions to the study of hibernation are by Lyman and 
Dawe (1960) and Kayser (1961); these and other studies are summarized and 
cited in the textbook by Davis and Golley ( 1963 ) . 

Some of the more important journals that regularly publish contributions 
relating to ecology and behavior, and of which the serious student should be 
aware, are Animal Behavior, Behavior, Ecological Monographs, Ecology, 
Journal of Animal Ecology, and Zeitschrift fur Tierpsychologie. 



302 



MORTALITY PATTERNS IN MAMMALS 

Graeme Caugiiley 

Forest Research Instilute, New Zealand Forest Service, Rotorua, and Zoology Department, 

Canterbury University, New Zealand 

(Accepted for publication December 8, 1965) 

Abstract. Methods of obtaining life table data are outlined and the assumptions implicit 
in such treatment are defined. Most treatments assume a stationary age distribution, but 
published methods of testing the stationary nature of a single distribution are invalid. Samples 
from natural populations tend to be biased in the young age classes and therefore, because 
it is least affected by bias, the mortality rate curve (q^) is the most efficient life table series 
for comparing the pattern of mortality with age in different populations. 

A life table and fecundity table are presented for females of the ungulate Heniitragiis 
jcmlahiens, based on a population sample that was first tested for bias. They give estimates 
of mean generation length as S.4 yr, annual mortality rate as 0.25, and mean life expectancy 
at birth as 3.5 yr. 

The life table for Hemitragus is compared with those of Ovis aries, O. dalli, man, Rattus 
norvegiciis, Microtns agrestis, and M. orcadensis to show that despite taxonomic and ecological 
differences the life tables have common characteristics. This suggests the hypotheses that 
most mammalian species have life tables of a common form, and that the pattern of age- 
specific mortality within species assumes an approximately constant form irrespective of the 
proximate causes of mortality. 



Introduction 

Most studies in population ecology include an 
attemin to determine mortality rates, and in many 
cases rates are given for each age class. This is 
no accident. Age-specific mortality rates are 
usually necessary for calculating reproductive 
values for each age class, the ages most susceptible 
to natural selection, the population's rate of in- 
crease, mean life expectancy at birth, mean gen- 
eration length, and the percentage of the popula- 
tion that dies each year. The importance of these 



statistics in the fields of game management, basic 
and applied ecology, and population genetics re- 
quires no elaboration. 

The pattern of changing mortality rates with 
age is best expressed in the form of a life table. 
These tables usually present the same information 
in a variety of ways : 

1 ) Survivorship (/x) : this series gives the prob- 
ability at birth of an individual surviving to any 
age, X (/x as used here is identical with P^ of 
Leslie, Venables and Venables 1952). The ages 



303 



Autumn 1966 



MORTALITY PATTERNS IN MAMMALS 



907 



are most conveniently spaced at regular intervals 
such that the values refer to survivorship at ages 
0, 1, 2 etc. yr, months, or some other convenient 
interval. The probability at birth of living to birth 
is obviously unity, but this initial value in the 
series need not necessarily be set at 1 ; it is often 
convenient to multiply it by 1,000 and to increase 
proportionately the other values in the series. If 
this is done, survivorship can be redefined as the 
number of animals in a cohort of 1,000 (or any 
other number to which the initial value is raised ) 
that survived to each age x. In this way a ^/^ 
series is produced, where k is the constant by which 
all h values in the series are multiplied. 

2) Mortality (c/x) : the fraction of a cohort that 
dies during the age interval x, x + 1 is designated 
dx- It can be defined in terms of the individual as 
the probability at birth of dying during the interval 
X, X + 1. As a means of eliminating decimal 
points the values are sometimes multiplied by a 
constant such that the sum of the d^ values equals 
1,000. The values can be calculated from the h 
series by 

c'x = 'x — 'x + l 

3) Mortality rate {q-s.) '■ the mortality rate q 
for the age interval x, x + 1 is termed ^x- It is 
calculated as the number of animals in the cohort 
that died during the interval x, x -f 1. divided by 
the number of animals alive at age x. This value 
is usually expressed as l,000(7x, the number of 
animals out of 1,000 alive at age x which died 
before x -f- 1- 

These are three ways of presenting age-specific 
mortality. Several other methods are available — 
e.g. survival rate {px), life expectancy (tx) and 
probability of death (Qx) — but these devices only 
present in a different way the information already 
contained in each of the three series previously 
defined. In this paper only the Ix, dx and qx series 
will be considered. 

Methods of Obtaining Mortality Data 

Life tables may be constructed from data col- 
lected in several ways. Direct methods : 

1 ) Recording the ages at death of a large num- 
ber of animals born at the same time. The fre- 
quencies of ages at death form a kdx series. 

2) Recording the number of animals in the 
original cohort still alive at various ages. The 
frequencies from a klx series. 



Approximate methods : 

3) Recording the ages at death of animals 
marked at birth but whose births were not coeval. 
The frequencies form a kdx series. 



4) Recording ages at death of a representative 
sample by ageing carcasses from a population that 
has assumed a stationary age distribution. Small 
fluctuations in density will not greatly affect the 
results if these fluctuations have an average wave 
length considerably shorter than the period over 
which the carcasses accumulated. The frequencies 
form a kdx series. 

5 ) Recording a sample of ages at death from 
a population with a stationary age distribution, 
where the specimens were killed by a catastrophic 
event (avalanche, flood, etc.) that removed and 
fixed an unbiased sample of ages in a living popu- 
lation. In some circumstances (outlined later) the 
age frequencies can be treated as a klx series. 

6) The census of ages in a living population, 
or a sample of it, where the population has assumed 
a stationary age distribution. Whether the speci- 
mens are obtained alive by trapping or are killed 
by unselective shooting, the resultant frequencies 
are a sample of ages in a living population and 
form a klx series in certain circumstances. 

Methods 1 to 3 are generally used in studies of 
small mammals while methods 4 to 6 are more 
commonly used for large mammals. 

Tests for Stationary Age Distribution 

Five methods have been suggested for deter- 
mining whether the age structure of a sample is 
consistent with its having been drawn from a 
stationary age distribution : 

a) Comparison of the "mean mortality rate," 
calculated from the age distribution of the sample, 
with the proportion represented by the first age 
class (Kurten 1953, p. 51). 

b) Comparison of the annual female fecundity 
of a female sample with the sample number multi- 
plied by the life expectancy at birth, the latter 
statistic being estimated from the age structure 
(Quick 1963, p. 210). 

c) Calculation of instantaneous birth rates and 
death rates, respectively, from a sample of the 
population's age distribution and a sample of ages 
at death (Hughes 1965). 

d ) Comparison of the age distribution with a 
prejudged notion of what a stationary age distri- 
bution should be like (Breakey 1963). 

e) Examination of the "/x" and "dx" series, 
calculated from the sampled age distribution, for 
evidence of a common trend (Quick 1963, p. 204). 

Methods a to c are tautological because they 
assume the sampled age distribution is either a klx 
or kdx series ; method d assumes the form of the 
life table, and e makes use of both assumptions. 

These ways of judging the stationary nature of 



304 



908 

a population are invalid. But I intend something 
more general than the simple statement that these 
five methods do not test what they are supposed 
to test. Given no information other than a single 
age distribution, it is theoretically impossible to 
prove that the distribution is from a stationary 
population unless one begins from the assumption 
that the population's survival curve is of a par- 
ticular form. If such an assumption is made, the 
life table constructed from the age frequencies 
provides no more information than was contained 
in the original premise. 

Mortality Samples and Age Structure 
Samples 

Methods 4 to 6 for compiling life tables are 
valid only when the data are drawn from a sta- 
tionary age distribution. This distribution results 
when a population does not change in size and 
where the age structure of the population is con- 
stant with time. The concept has developed from 
demographic research on man and is useful for 
species which, like man, have no seasonally re- 
stricted period of births. 

Populations that have a restricted season of 
births present difficulties of treatment, some of 
which have been discussed by Leslie and Ranson 
(1940). Very few mammals breed at the same 
rate throughout the year, and the stationary age 
distribution must be redefined if it is to include 
seasonal breeders. For species with one restricted 
breeding season each year, a stationary population 
can be defined as one that does not vary either in 
numbers or age structure at successive points in 
time spaced at intervals of 1 yr. The stationary 
age distribution can then be defined for such popu- 
lations as the distribution of ages at a given time 
of the year. Thus there will be an infinite num- 
ber of different age distributions according to the 
time of census, other than in the exceptional case 
of a population having a constant rate of mor- 
tality throughout life. 

The distribution of ages in a stationary popula- 
tion forms a kl^; series only when all births for the 
year occur at an instant of time and the sample is 
taken at that instant. This is obviously impossible, 
but the situation is approximated when births 
occur over a small fraction of the year. If a popu- 
lation has a restricted season of births, the age 
structure can be sampled over this period and at 
the same time the number of live births produced 
by a hypothetical cohort can be calculated from 
the number of females either pregnant or suckling 
young. In this way a set of data closely approxi- 
mating a kl^ series can be obtained. 



GRAEME CAUGHLEY 



Ecology, Vol. 47, No. 6 



If an age distribution is sampled halfway be- 
tween breeding seasons, it cannot be presented as 
a A;/x series with x represented as integral ages in 
years. With such a sample (making the usual 
assumptions of stability and lack of bias) neither 
/x nor dx can be established, but Qx values can be 
calculated for each age interval x -(- 3^, x + l^^. 
The age frequencies from a population with a con- 
tinuous rate of breeding are exactly analogous ; 
they do not form a kl^ series but can be treated as 
a series of the form 

^(/x + /x + l)/2 

This series does not allow calculation of l^ values 
from birth unless the mortality rate between birth 
and the midpoint of the first age interval is known. 

Because a sample consists of dead animals, its 
age frequencies do not necessarily form a mor- 
tality series. The kdx series is obtained only when 
the sample represents the frequencies of ages at 
death in a stationary population. Many published 
samples treated as if they formed a kdx series are 
not appropriate to this form of analysis. For 
instance, if the animals were obtained by shooting 
which was unselective with respect to age, the 
sample gives the age striicture of the living popu- 
lation at that time ; that the animals were killed to 
get these data is irrelevant. Hence unbiased 
shooting samples survivorship, not mortality, and 
an age structure so obtained can be treated as a 
klx series if all other necessary assumptions obtain. 
Similarly, groups of animals killed by avalanches, 
fires, or floods — catastrophic events that preserve 
a sample of the age frequencies of animals during 
life — do not provide information amenable to kdx 
treatment. 

A sample may include both Ix and dx compo- 
nents. For instance, it could consist of a number 
of dead animals, some of which have been unselec- 
tively shot, whereas the deaths of others are at- 
tributable to "natural" mortality. Or it could be 
formed by a herd of animals killed by an avalanche 
in an area where carcasses of animals that died 
"naturally" were also present. In both these cases 
dx and /x data are confounded and these hetero- 
geneous samples of ages at death can be treated 
neither as kdx nor klx series. 

Even if a sample of ages at death wc/e not 
heterogeneous in this sense, it might still give mis- 
leading information. If, for instance, carcasses 
attributable to "natural" mortality were collected 
only on the winter range of a population, the age 
frequencies of this sample would provide ages at 
death which reflected the mortality pattern during 
only part of the year. But the dx series gives the 
proportion of deaths over contiguous periods of 



305 



Autumn 1966 



MORTALITY PATTERNS IN MAMMALS 



909 



the life span and must reflect all mortality during 
each of these periods. 

It has been stressed that the frequencies of ages 
in life or of ages at death provide Ufe-table in- 
formation only when they are drawn from a popu- 
lation with a stationary age distribution. This age 
distribution should not be confused with the stable 
distribution. When a population increases at a 
constant rate and where survivorship and fecun- 
dity rates are constant, the age distribution even- 
tually assumes a stable form (Lotka 1907 a, b; 
Sharpe and Lotka 1911 ). Slobodkin (1962, p. 49) 
gives a simple explanation as to why this is so. A 
stable age distribution does not form a kl^, series 
except when the rate of increase is zero, the season 
of births is restricted, and the sample is taken at 
this time. Hence the stationary age distribution 
is a special case of the stable age distribution. 

The Relative Usefulness of the 
/x, dx and gx series 

Most published life tables for wild mammals 
have been constructed either from age frequencies 
obtained by shooting to give a ^/x series, or by de- 
termining the ages at death of animals found dead, 
thereby producing a kd^ series. Unfortunately, 
both these methods are almost invariably subject 
to bias in that the frequency of the first-year class 
is not representative. Dead immature animals, 
especially those dying soon after birth, tend to 
decay faster than the adults, so that they are under- 
represented in the count of carcasses. The ratio 
of juveniles to adults in a shot sample is usually 
biased because the two age classes have different 
susceptibilities to hunting. With such a bias estab- 
lished or suspected, the life table is best presented 
in a form that minimizes this bias. An error in 
the frequency of the first age class results in dis- 
tortions of each Ix and dx value below it in the 
series, but q^ values are independent of frequencies 
in younger age classes. By definition, q is the ratio 
of those dying during an age interval to those 
alive at the beginning of the interval. At age y the 
value of q is given by 

Qy = dy/ly 



but 



dy ty I- 



y + 1 



therefore 

Qy ^ (^y — ^y + i)/^y • 

Thus the value of ^y is not directly dependent on 
absolute values of /^ but on the differences between 
successive values. If the Ix series is calculated 
from age frequencies in which the initial frequency 



is inaccurate, each Ix value will be distorted. How- 
ever, the difference between any two, divided by 
the first, will remain constant irrespective of the 
magnitude of error above them in the series. Thus 
a qx value is independent of all but two survivor- 
ship age frequencies and can be calculated directly 
from these frequencies (fx) by 

qx = {fx — fx + i)/ix 

if the previously discussed conditions are met. 

The calculation of q from frequencies of ages 
at death is slightly more complex : 

by definition qy = dy/U- 



but 



therefore 



00 y-i 
ly = 2dx — SOx 

x=o x=o 

00 y-1 
qy = dy/{i:dx — Zdx) 

x=o x=o 



= dy/Xdx: 

x=y 

but the frequencies of ages at death (fx) are them- 

00 

selves a kdx series and so Q'y=/'y/2/ x ■ 

x = y 

Thus the value of q at any age is independent of 
frequencies of the younger age classes. Although 
the calculated value of q for the first age class may 
be wrong, this error does not affect the qx values 
for the older age classes. 

The qx series has other advantages over the Ix 
and dx series for presenting the pattern of mor- 
tality with age. It shows rates of mortality di- 
rectly, whereas this rate is illustrated in a graph 
of the Ix series (the series most often used when 
comparing species) only by the slope of the curve. 

A Life Table for the Thar, 

Hemitragus jemlahicus 
The Himalayan thar is a hollow-horned ungu- 
late introduced into New Zealand in 1904 (Donne 
1924) and which now occupies 2,000 miles^ of 
mountainous country in the South Island. Thar 
were liberated at Mount Cook and have since 
spread mostly north and south along the Southern 
Alps. They are still spreading at a rate of about 
1.1 miles a year (Caughley 1%3) and so the popu- 
lations farthest from the point of liberation have 
been established only recently and have not yet 
had time to increase greatly in numbers. Closer 
to the site of liberation the density is higher (cor- 
related with the greater length of time that animals 
have been established ther^), and around the point 
of liberation itself there is evidence that the popu- 
lation has decreased (Anderson and Henderson 
1961). 



306 



910 



GRAEME CAUGHLEY 



Ecology, Vol. 47, No. 6 



The growth rings on its horns are laid down 
in each winter of life other than the first (Caugh- 
ley 1965), thereby allowing the accurate ageing of 
specimens. An age structure was calculated from 
a sample of 623 females older than 1 yr shot in 
the Godley and Macaulay Valleys between Novem- 
ber 1963 and February 1964. Preliminary work 
on behavior indicates that there is very little dis- 
persal of females into or out of this region, both 
because the females have distinct home ranges and 
because there are few ice-free passes linking the 
valley heads. 

As these data illustrate problems presented by 
most mammals, and because the life table has not 
been published previously, the methods of treat- 
ment will be outlined in some detail. 

Is the population stationary f 

Although it is impossible to determine the sta- 
tionary nature of a population by examining the 
age structure of a single sample, even when rates 
of fecundity are known, in some circumstances a 
series of age structures will give the required in- 
formation. This fact is here utilized to investigate 
the stability of this population. 

The sample was taken about halfway between 
the point of liberation and the edge of the range. 
It is this region between increasing and decreasing 
populations where one would expect to find a 
stationary' population. The animals came into the 
Godley Valley from the southwest and presumably 
colonized this side of the valley before crossing the 
2 miles of river bed to the northeast side. This 
pattern of establishment is deduced from that in 
the Rakaia Valley, at the present edge of the 
breeding range, where thar bred for at least 5 yr 
on the south side of the valley before colonizing 
the north side. Having colonized the northeast 
side of the Godley Valley, the thar would then 
cross the Sibald Range to enter the Macaulay 
Valley, which is a further 6 miles northeast. The 
sample can therefore be divided into three sub- 
samples corresponding to the different periods of 
time that the animals have been present in the 
three areas. A 10 X 3 contingency test for differ- 
ences between the three age distributions of fe- 
males 1 yr of age or older gave no indication 'that 
the three subpopulations differed in age structure 
(X=^ = 22.34; P = 0.2). 

This information can be interpreted in two 
ways : either the three subpopulations are neither 
increasing nor decreasing and hence are likely to 
have stationary age distributions, or the subpopu- 
lations could be increasing at the same rate, in 
which case they could have identical stable age 
distributions. The second alternative carries a 



Table I. Relative densities of thar 


in three 


zones 


Zone 


Number 

females 

autopsied 


Mean 
density 
inde.x" 


Standard 
error 


Godley Valley south 

Godley Valley north 

Macaulay Valley. 


258 
240 
115 


2.19 
1.67 
2.66 


0.56 
0.53 
69 







F2.56 for densities between valleys == 1.74, not significant 

'Density indices were calculated as the number of females other than kids 

recorded a,s autopsied in a zone each day. divided by the number of shooters 

hunting in the zone on that day. 

corollary that the subpopulations would have dif- 
ferent densities because they have been increasing 
for differing periods of time. But an analysis of 
the three densities gives no indication that they 
differ (Table I). This result necessitates the 
rejection of the second alternative. 

The above evidence suggesting that the sample 
was drawn from a stationary age distribution is 
supported to some extent by observation. When 
I first passed through the area in 1957, I saw 
about as many thar per day as in 1963-64. J. A. 
Anderson, a man who has taken an interest in the 
thar of this region, writes that the numbers of 
thar in 1956 were about the same as in 1%4 
(Anderson, pers. comm.). These are subjective 
evaluations and for that reason cannot by them- 
selves be given much weight, but they support in- 
dependent evidence that the population is station- 
ary or nearly so. 

Is the sample biased? 

A sample of the age structure of a population 
can be biased in several ways. The most obvious 
source of bias is behavioral or range differences 
between males and females. For instance, should 
males tend to occupy terrain which is more diffi- 
cult to hunt over than that used by females, they 
would be underrepresented in a sample obtained 
by hunting. During the summer thar range in 
three main kinds of groups : one consists of fe- 
males, juveniles and kids, a second consists of 
young males and the third of mature males. The 
task of sampling these three groupings in the same 
proportions as they occur throughout the area is 
complicated by their preferences for terrain that 
differs in slope, altitude and exposure. Conse- 
quently the attempt to take an unbiased sample 
of both males and females was abandoned and the 
hunting was directed towards sampling only the 
nanny-kid herds in an attempt to take a repre- 
sentative sample of females. The following analy- 
sis is restricted to females. 

Although bias attributable to differences in be- 
havior between sexes can be eliminated by the 
simple contrivance of ignoring one sex, some age 



307 



Autumn 1966 



MORTALITY PATTERNS IN MAMMALS 



911 



classes of females may be more susceptible than no bias could be detected from a sample of this 
others to shooting. To test for such a difference, size, 
females other than kids were divided into two 
groups : those from herds in which some mem- 
bers were aware of the presence of the shooter 
before he fired, and those from herds which were 
undisturbed before shooting commenced. If any 
age group is particularly wary its members should 
occur more often in the "disturbed" category than 
is the case for other age groups. But a x" test 
(X^ = 7.28, df = 9, P = 0.6) revealed no signifi- 
cant difference between the age structures of the 
two categories. 

The sample was next divided into those females 
shot at ranges less than 200 yards and those shot 
out of this range. If animals in a given age class 
are more easily stalked than the others, they will 
tend to be shot at closer ranges. Alternatively, 
animals which present small targets may be under- 
represented in the sample of those shot at ranges 
over 200 yards. This is certainly true of kids, 
which are difficult to see, let alone to shoot, at 
ranges in excess of 200 yards. The kids have 
therefore not been included in the analysis be- 
cause their underrepresentation in the sample is 
an acknowledged fact, but for older females there 
is no difference between the age structures of the 
two groups divided by range which is not ex- 
plainable as sampling variation (x" = 9.68, df := 9. 
P^O.4). This is not to imply that no bias 
exists — the yearling class for instance could well 
be underrepresented beyond 200 yards — but that 



The taking of a completely representative sam- 
ple from a natural population of mammals is prob- 
ably a practical impossibility, and I make no claim 
that this sample of thar is free of bias, but as bias 
cannot be detected from the data, I assume it is 
slight. 

Construction of the life table 

The shooting yielded 623 females 1 yr old or 
older, aged by growth rings on the horns. As 
the sampling period spanned the season of births, 
a frequency for age cannot be calculated directly 
from the number of kids shot because early in the 
period the majority had not been born. In any 
case, the percentage of kids in the sample is biased. 

The numbers of females at each age are shown 
in Table II, column 2. Although the ages are 
given only to integral years each class contains 
animals between ages x yr — "/^ month and x yr 
4" 2j^ months. Variance owing to the spread of 
the kidding season is not included in this range, 
but the season has a standard deviation of only 15 
days (Caughley 1965). 

Up to an age of 12 yr (beyond this age the 
values dropped below 5 and were not treated) 
the frequencies were smoothed according to the 
formula 

log y = 1.9673 -f 0.0246x — 0.01036 x^, 

where y is the frequency and x the age. The 
linear and quadratic terms significantly reduced 



Table II. Life table and fecundity table for the thar Hemitragus jemlahicus (females only) 



1 

Age in years 

X 


2 

Frequency 
in sample 


3 

Adjusted 
frequency 


4 

No. female 

live births 

per female 

at age x 

nil 


5 
1,000?. 


6 
1,000 d. 


7 
l,000gi 




1 


94 
97 
107 
68 
70 
47 
37 
35 
24 
16 

11 
6 

3 
4 
3 


1 


205" 
95.83 
94.43 
88.69 
79.41 
67.81 
55.20 
42.85 
31.71 
22.37 
15,04 

9.64 
5.90 


0.000 
0.005 
0.135 
0.440 
0.420 
0.465 
0.425 
0.460 
0.485 
0.500 
0.500 

1 

^0.470 

J 

0.350 


1,000 
467 
461 
433 
387 
331 
269 
209 
155 
109 
73 

47 
29 


533 
6 
28 
46 
56 
62 
60 
54 
46 
36 
26 

18 


533 
13 


2 


61 


3 


106 


4 


145 


5 


187 


6 


223 


7 


258 


8 


297 


9 


330 


10 


356 


11 


382 


12 




13 




14 




15 




16 




17 









■Calculated from adjusted frequencies of females other than kids (column 3) and mx values (column 4). 



308 



Q12 



GRAEME CAUGHLEY 



Ecology, Vol. 47, No. 6 




AGE IN YEARS 



Fig. 1. Age frequencies, plotted on a logarithmic scale, 
of a sample of female thar, with a curve fitted to the values 
from ages 1 to 12 yr, and the mortality rate per 1,000 for 
each age interval of 1 yr (IfiOOq^^) plotted against the 
start of the interval. 

variance around the regression, but reduction by 
the addition of a cubic term was not significant 
at the 0.05 level. There are biological reasons 
for suspecting that the cubic term would have 
given a significant reduction of variance had the 
sample been larger, but for the purposes of this 
study its inclusion in the equation would add very 
little. The improved fit brought about by the 
quadratic term indicates that the rate of mortality 
increases with age. Whether the rate of this rate 
also increases, is left open. The computed curve 
closely fitted the observed data ( Fig. 1 ) and should 
greatly reduce the noise resulting from sampling 
variation, the differential effect on mortality of 
different seasons, and the minor heterogeneities 
which, although not detectable, are almost certain 
to be present. The equation is used to give ad- 
justed frequencies in Table II, column 3. 

The frequency of births can now be estimated 
from the observed mean number of female kids 
produced per female at each age. These are shown 
in column 4. They were calculated as the number 
of females at each age either carrying a foetus" or 
lactating, divided by the number of females of that 
age which were shot. These values were then 
halved because the sex ratio of late foetuses and 
kids did not differ significantly from 1:1 (93 S S : 
97 9 9 ) . The method is open to a number of 
objections : it assumes that all kids were born 
alive, that all females neither pregnant nor lac- 
tating were barren for that season, and that twin- 
ning did not occur. The first assumption, if false, 
would give rise to a positive bias, and the second 



and third to a negative bias. However, the ratio 
of females older than 2 yr that were either preg- 
nant or lactating to those neither pregnant nor 
lactating did not differ significantly between the 
periods November to December and January to 
February (x' = 0.79, P = OA), suggesting that 
still births and mortality immediately after birth 
were not common enough to bias the calculation 
seriously. Errors are unlikely to be introduced 
by temporarily barren females suckling yearlings, 
because no female shot in November that was 
either barren (as judged by the state of the uterus) 
or pregnant was lactating. Errors resulting from 
the production of twins will be very small ; we 
found no evidence of twinning in this area. 

The products of each pair of values in columns 
3 and 4 (Table II) were summed to give an esti- 
mate of the potential number of female kids pro- 
duced by the females in the sample. This value 
of 205 is entered at the head of column 3. The 
adjusted age frequencies in column 3 were each 
multiplied by 4.878 to give the 1,000/x survivor- 
ship values in column 5. The mortality series 
(column 6) and mortality-rate series (column 7) 
were calculated from these. 

Conclusions 

Figure 1 shows the mortality rate of females in 
this thar population up to an age of 12 yr. Had 
the sample been larger the graph could have been 
extended to an age of 17 yr or more, but this 
would have little practical value for the calcula- 
tion of population statistics because less than 3% 
of females in the population were older than 12 yr. 

The pattern of mortality with age can be di- 
vided into two parts — a juvenile phase charac- 
terized by a high rate of mortality, followed by a 
postjuvenile phase in which the rate of mortality 
is initially low but rises at an approximately con- 
stant rate with age. 

Table II gives both the k and m^ series, and 
these two sets of values provide most of the in- 
formation needed to describe the dynamics of the 
population. Assuming that these two series are 
accurate, the following statistics can be derived : 
generation length (i.e. mean lapse of time between 
a female's date of birth and the mean date of birth 
of her offspring), T: 

^'^'"^^-^5.4yr; 



r = 



S/xWs 



mean rate of mortality for all age groups, g^: 

'q^ — l/S/x = 0.25 per female per annum; 

life expectancy at birth, eo : 

^0 = 2 /x — >^ = 3.5 yr. 



309 



Autumn 1966 



MORTALITY PATTERNS IN MAMMALS 



913 



The last two statistics can also be expressed 
conveniently in terms of the mortality series by 

^,= l/S(x+l)(f. 



and 



eo 



S (2x+l) d. 



The relationship of the two is given by 

^, = 2/(2^0+1). 

Life Tables for Other Mammals 

The difficulty of comparing the mortality pat- 
terns of animals that differ greatly in life span can 
be readily appreciated. To solve this problem, 
Deevey (1947) proposed the percentage deviation 
from mean length of life as an appropriate scale, 
thereby allowing direct comparison of the life tables 
of, say, a mammal and an invertebrate. For such 
comparisons this scale is obviously useful, but for 
mammals where the greatest difference in mor- 
tality rates may be at the juvenile stage the scale 
often obscures similarities. 

By way of illustration, Figure 2 shows l.OOOgx 
curves for two model populations which differ 
only in the mortality rate of the first age class. 
When the values are graphed on a scale of per- 
centage deviation from mean length of life the 
close similarity of the two sets of data is no longer 
apparent. Thus the use of Deevey's scale for 

•/. DEVIATION FROM MEAN LENGTH OF LIFE 



eoo - 



X 
O 



100 


-50 


.50 


•100 


♦15 




T ■ 1 


» 

1 
1 


^ 


P 


- 


/ 
/ 


1 

1 


/ / 
1 / 


- 


} 




/ 


p 


- 


\ 


\'. *' P 


p 




- 


s. 


1 1 1 


1 


f 


1 



AGE IN ^'-A^'; 

Fig. 2. The mortality rate per 1,000 for each year of 
life for two model populations that differ only in the de- 
gree of first-year mortality. These l.OOOq^ values are 
each graphed on two time scales : absolute age in years 
(continuous lines) and percentage deviation from mean 
life expectancy (broken lines). 



comparing mortality patterns in mammals might 
result in a loss rather than a gain of information. 
In this paper, absolute age has been retained as 
a scale in comparing life tables of different species, 
although this scale has its own limitations. 

Domestic sheep, Ovis aries. — Between 1954 and 
1959, Hickey (19(30) recorded the ages at death 
of 83,113 females on selected farms in the North 
Island of New Zealand. He constructed a ^x 
table from age IJ^ yr by "dividing the number of 
deaths which have occurred in each year of age 
by the number 'exposed to risk' [of death] at the 
same age." An age interval of 1 yr was chosen 
and the age series V/z, 2]^, 3>4 etc. was used in 
preference to integral ages. 

The qx series conformed very closely to the 
regression : log g^ ^ 0.1 56x -f 0.24, enabling him 
in a subsequent paper (Hickey 1963) to present 
the interpolated q^ values at integral ages. He 
also calculated q for the first year of life from a 
knowledge of the number of lambs dying before 1 
yr of age out of 85,309 (sexes pooled) born alive. 

These data probably provide the most accurate 
life table for any mammal. The 1,000^^ curve 
is graphed in Figure 3. 



800 


- 


I 


1 


T ■ 


I 


■ y ■ ■ 


? 


600 


- 










/ 


■ 


400 


- 










^ 


■ 


200 


\ 








1 




- 








2 


4 


6 


8 


10 


12 



AGE IN YEARS 

Fig. 3. Domestic sheep : mortaHty rate per 1,000 for 
each age interval of 1 yr (l,000qj, plotted against the 
start of the interval. Data from Hickey (1963). 

Dall sheep, Ovis dalli. — During his study on the 
wolves of Mount McKinley National Park, Murie 
(1944) aged carcasses of dall sheep he found 
dead, their ages at death being established from 
the growth rings on the horns. This sample can 
be divided into those that died before 1937 and 
those that died between 1937 and 1941. The 
former sample was used by Deevey (1947) to 
construct the life table presented in his classic 
paper on mortality in natural populations. Kur- 
ten (1953) constructed a life table from the same 



310 



914 



GRAEME CAUGHLEY 



Ecology, Vol. 47, Mo. 6 



data, but corrected the iinderrepresentation of 
first-year animals resulting from the relatively 
greater perishability of their skulls by assuming 
that adult females produce 1 lamb per annum from 
about their second birthday. Taber and Dasmann 
(1957) constructed life tables for both males and 
females from the sample of animals dying between 
1937 and 1941, and adjusted both the to 1- and 
1 to 2-year age frequencies on the assumption that 
a female produces her first lamb at about her third 
birthday and another lamb each year thereafter, 
that the sex ratio at birth is unity and that the 
loss of yearlings is not more than 10%. 



1000 


1 ■ ■ I I I 


1 


■ 


aoo 


-■ 


/ 


/ 


eoo 


- 


// 


/. 


400 


A ?? - 


/ / 


- 


200 


^="=5=^=0- — "^ , 1 


i<S 


- 



AGE IN YEARS 

Fig. 4. Dall sheep : mortality rate per 1,000 for each 
age interval of 1 yr (1,000(7,^), plotted against the start 
of the interval. Data from Murie (1944). 

Figure 4 shows a version of this table con- 
structed from the pre- 1937 sample. The mortality 
of the first year class has been adjusted by assum- 
ing that the sex ratio at birth is unity, that 50% 
of females produce their first kids at their second 
birthday and that thereafter 90% produce kids 
each year. The figure of 50% fecundity at age 
2 is borrowed from \\'oodgerd's (1964) study on 
the closely related Ov'xs canadensis, and the sub- 
sequent 90% fecundity is based on Murie's (1944) 
statement that twins are extremely rare. To 
allow for temporarily or permanently barren ani- 
mals, 10% is subtracted from the potential fecun- 
dity. 

This life table must be taken as an approxima- 
tion. As Deevey (1947) has pointed out, the 
pre-1937 and 1937^1 samples dififer significantly 
in age structure. The obvious conclusion is that 
the mortality rate by age was changing before and 
during the period of study. Consequently the age 
structure of the sample is likely to be only an 
approximation of the kdj, series. Furthermore, 



the qx values for age 1 yr are likely to have been 
biased by differential perishability of skulls, but 
no arbitrary adjustment has been made. 

Man. — Most of the life tables available for man 
show that males have a higher rate of mortality 
than females. However, Macdonell's (1913) 
tables for ancient Rome, Hispania and Lusitania 
suggest that this might not always have been so 
and that in some circumstance the reverse can be 
true. 

A l,OOO^x curve for Caucasian males and fe- 
males in the United States between 1939 and 
1941 is shown in Figure 5. The values are taken 
from Dublin, Lotka, and Spiegelman (1949). 

Rat, Rattus norvegicus. — Wiesner and Sheard 
(1935) gave the ages at death of 1,456 females of 
the albino rat (Wistar strain) in a laboratory 
population. Their table begins at an age of 31 
days, but Leslie et al. (1952) calculate from Wies- 
ner and Sheard's data that the probability of 
dying between birth and 31 days was 0.316. Fig- 
ure 6 gives a ^x curve constructed from these data. 

Short-tailed vole, Microtus agrestis. — The ages 
at death of 85 males and 34 females were reported 
by Leslie and Ranson (1940) from a laboratory 
population of voles kept -at the Bureau of Animal 
Population, Oxford. Frequencies for both sexes 
were pooled and the data were smoothed by the 
formula fx = fo e"'"'" where / is the frequency of 
animals alive age x, and ^ is a constant. The com- 
puted curve closely fitted the data (P = 0.5 to 
0.7). Figure 6 shows the 1,000^^ curve derived 
from the authors' sixth table. 



250 



200 



150 - 



o 
o 
o 




100 - 



AGE IN YEARS 

Fig. 5. Man in U.S. : mortality rate per 1,000 per 
year of age (1,000^^). Data from Dublin et al. (1949). 



311 



Autumn 1966 



MORTALITY PATTERNS IN MAMMALS 



915 




VOLE 



RAT 



16 



20 



AGE UNITS 

Fig. 6. Short-tailed voles and rats : mortality rate per 
1,000 for each age interval (1,000(7^), plotted against the 
start of the interval. Age interval is 56 days for voles 
and 50 days for rats. Rat data from Wiesner and Sheard 
(1935) ; vole data from Leslie and Ranson (1940). 

The pooling of mortality data from both sexes 
is strictly valid only when the two qx series are 
not significantly different. Studies on differential 
mortality between sexes are few, but those avail- 
able for man (Dublin et al. 1949, and other au- 
thors), dall sheep (Taber and Dasmann 1957, and 
this paper), the pocket gopher (Howard and 
Childs 1959) and Orkney vole (Leslie et al. 1955) 
suggest that although mortality rates certainly 
■differ between sexes, the trends of these age- 
specific rates tend to be parallel. Consequently, 
this life table for voles, although based on pre- 
sumably heterogeneous data, is probably quite 
adequate for revealing the gross pattern of mor- 
tality with age. 

Orkney vole, Microtus orcadensis. — Leslie et al. 
(1955) gave a life table for both males and females 
in captivity from a base age of 9 weeks. In addi- 
tion they gave the probability at birth of surviving 
to ages 3, 6, and 9 weeks, but did not differentiate 
sexes over this period. The (/x curve given here 
(Fig. 7) was constructed by calculating survivor- 
ship series for both males and females from these 
data, drawing trend lines through the points, and 
interpolating values at intervals of 8 weeks. 

Proposed life tables not accepted 
In the Discussion section of this paper the life 
tables discussed previously are examined in an 




ACE UNITS 

Fig. 7. Orkney vole: mortality rate per 1,000 for each 
age interval of 56 days (l,000g^), plotted against the 
start of the interval. Data from Leslie et al. (1955). 

attempt to generalize their form. Only a small 
proportion of published life tables are dealt with, 
and any generalization from these could be inter- 
preted as an artefact resulting from selection of 
evidence. 

To provide the reader with the information 
necessary for reaching an independent conclusion, 
the published life tables not selected for compari- 
son are listed below with the reason for their 
rejection. Only those including all juvenile age 
classes are cited. These tables are rejected only 
for present purposes because comparison of mor- 
tality patterns between species demands a fairly 
high level of accuracy for individual tables. The 
inclusion of a table in this section does not neces- 
sarily imply that it is completely inaccurate and of 
no practical value. 

Tables based on inadequate data (i.e. less 

than 50 ages at death or 150 ages of living 

animals) : Odocoileus hemionus (Taber and 

Dasmann 1957), OzHs canadensis (Wood- 

gerd 1964) ; 

Probable sampling bias : Lepus americanus 

(Green and Evans 1940), Rupicapra rupi- 

capra (Kurten 1953), fossil accumulations 

(Kurten 1953, 1958; Van Valen 1964), 

Balaenoptera physalus (Laws 1962) ; 

Age structure analyzed as a kdx series : Syl- 

vilagus floridanus (Lord 1961), Odocoileus 

virginianus and Capreolus capreolus (Quick 

1963); 

Death and emigration confounded : Peromys- 

cus maniculatus (Howard 1949), Capreolus 

capreolus (Taber and Dasmann 1957, Quick 

1963); 



312 



916 



GRAEME CAUGHLEY 



Ecology, Vol. 47, No. 6 



Sample taken between breeding seasons : 
Odocoileus znrginianns (Quick 1963) ; 
Form of life table, or significant portion of it, 
based largely on assumption : Callorhinus 
iirsinus (Kenyon and Scheffer 1954), M\otis 
mysta^inus (Sluiter, van Heerdt, and Bezem 
1956), Cennis elaphus (Taber and Dasmann 
1957), Rhinolophus hipposideros, Myotis 
emarginatus, and Myotis daubentonii (Bezem, 
Sluiter, and van Heerdt 1960), Halichoerus 
grypiis (Hewer 1963, 1964) ; 
Sample from a nonstationary population : 
Syhnlagus floridaniis (Lord 1961); 
Inadequate aging: Gorgon tanrinns (Talbot 
and Talbot 1963) ; 

Confounding of /^ and d-s, data : Rangifer arc- 
ticus (Banfield 1955). 

Discussion 

The most striking feature of the g^ curves of 
species accepted for comparison is their similarity. 
Each curve can be divided into two components : 
a juvenile phase where the rate of mortality is 
initially high but rapidly decreases, followed by 
a post juvenile phase characterized by an initially 
low but steadily increasing rate of mortality. The 
seven species compared in this paper all produced 
9x curves of this "U" or fish-hook shape, suggest- 
ing that most mammals share a relationship of this 
form between mortality rate and age. This con- 
clusion, if false, can be invalidated by a few more 
life tables from other species. It can be tested 
most critically by reexamining some of the species 
for which life tables, although published, were not 
accepted in this paper. Those most suitable are 
species that can be adequately sampled, and accu- 
rately aged by growth rings on the horns or growth 
layers in the teeth (chamois. Rocky Mountain 
sheep, and several species of deer), or those small 
mammals that can be marked at birth and subse- 
quently recaptured. 

High juvenile mortality, characterizing the first 
phase of the g.^ curve, has been reported also for 
several mammals for which complete life tables 
have not yet been calculated (e.g. for Oryctolagus 
cuniculus (Tyndale-Biscoe and Williams 1955, 
Stodart and Myers 1964), Gorgon taurinns (Tal- 
bot and Talbot 1963), Cervus elaphus (Riney 
1956) and Oreamnos americanns (Brandborg 
1955). Kurten (1953, p. 88) generalized this 
phenomenon by stating that "the initial dip [in the 
survivorship curve] is a constitutional character 
in sexually reproducing forms at least . . .". This 
phase of mortality is highly variable in degree but 
not in form. Taber and Dasmann (1957) and 
Bourliere (1959) have emphasized the danger of 



considering a life table of a population in given 
circumstances as a typical of all populations of 
that species. Different conditions of life tend to 
affect life tables, and the greatest differences be- 
tween populations of a species are likely to be 
found at the juvenile stage. For example, the rate 
of juvenile mortality in red deer (Riney 1956) 
and in man differ greatly between populations of 
the same species. 

The second phase — the increase in the rate of 
mortality throughout life — is common also to the 
seven species compared in this paper. However, 
although the increase itself is common to them, 
the pattern of this increase is not. Mortality rates 
have a logarithmic relationship to age in domestic 
sheep and to a less marked extent in the rat, the 
Orkney vole, and the dall sheep, whereas the re- 
lationship for the thar and the short-tailed vole 
appears to be approximately arithmetic. How- 
ever, this difference may prove to be only an arte- 
fact resulting from the smoothing carried out on 
the data from these two species. 

Despite these differences, the characteristics 
common to the various q^ curves dominate any 
comparison made between them. The similarities 
are all the more striking when measured against 
the ecological and taxonomic differences between 
species. Taxonomically, the seven species repre- 
sent three separate orders (Primates, Rodentia, 
and Artiodactyla), and ecologically they comprise 
laboratory populations (rats and voles), natural 
populations (thar, dall sheep and man) and an 
artificial population (domestic sheep). The agents 
of mortality which acted on these populations must 
have been quite diverse. Murie (1944) reported 
that most of the dall sheep in the sample had been 
killed by wolves ; most mortality in the thar popu- 
lation is considered to result from starvation and 
exposure in the winter ; mortality of domestic 
sheep seems to be largely a result of disease, physi- 
ological degeneration, and possibly iodine defi- 
ciency in the lambs (Hickey 1963) ; whereas the 
deaths in the laboratory populations of voles and 
rats may be due to inadequate parental care and 
cannibalism of the juveniles, and perhaps disease 
and physiological degeneration in the adults. 
These differences suggest that the ^x curve of a 
population may assume the same form under the 
influence of various mortality agents, even though 
the absolute rate of mortality of a given age class 
is not the same in all circumstances. This hy- 
pothesis is worth testing because it implies that 
the susceptibility to mortality of an age class, rela- 
tive to that of other age classes, is not strongly 
specific to any particular agent of mortality. A 
critical test would be to compare the life tables of 



313 



Autumn 1966 



MORTALITY PATTERNS IN MAMMALS 



917 



two stationary populations of the same species, 
wliere only one population is subjected to preda- 
tion. 

Although no attempt is made here to explain the 
observed mortality pattern in terms of evolutionary 
processes, an investigation of this sort could be 
informative. A promising line of attack, for in- 
stance, would be an investigation of what appears 
to be a high inverse correlation between the mor- 
tality rate at a given age and the contribution of 
an animal of this age to the gene pool of the next 
generation. Fisher (1930) gives a formula for 
the latter statistic. 

Bodenheimer (1958) divided expectation of life 
into "physiological longevity" ("that life duration 
which a healthy individual may expect to live 
under optimum environment conditions until dying 
of senescence") and "ecological longevity" (the 
duration of life under natural conditions). This 
study suggests that such a division is inexpedient 
because no clear distinction can be made between 
the effect on mortality rates of physiological de- 
generation and of ecological influences. 

It is customary to classify life tables according 
to the three hypothetical patterns of mortality given 
by Pearl and Miner (1935). These patterns can 
be characterized as : 1 ) a constant rate of mor- 
tality throughout life, 2) low mortality through- 
out most of the life span, the rate rising abruptly 
at old age. and 3 ) initial high mortality followed 
by a low rate of mortality. Pearl (1940) empha- 
sizes that the three patterns are conceptual models 
having no necessary empirical reality, but a few 
subsequent writers have treated them as laws 
which all populations must obey. None of these 
models fit the mortality patterns of the seven spe- 
cies discussed in this paper although Pearl's 
(1940) later modification of the system provides 
two additional models (high-low-high mortality 
rate and low-high-low mortality rate), the first 
of which is an adequate approximation to these 
data. For mammals at least, the simple three- 
fold classification of mortality patterns is both con- 
fusing and misleading. The five-fold classification 
allows greater scope ; but do we yet know enough 
about mortality patterns in mammals to justify 
the construction of any system of classification? 

Acknowledgments 

This pajier has greatly benefited from criticism of pre- 
vious drafts by M. A. Bateman, CSIRO ; P. H. Leslie, 
Bureau of Animal Population ; M. Marsh, School of 
Biological Sciences, University of Sydney ; J. Monro, 
Joint FAO/IAEA Div. of Atomic Energy; G. R. Wil- 
liams, Lincoln College, and B. Stonehouse, Canterbury 
University, New Zealand ; and B. B. Jones and W. G. 
Warren of this Institute. The equation for smoothing 
age frequencies of thar was kindly calculated by W. G. 



Warren. For assisting in the shooting and autopsy of 
specimens, I am grateful to Chris Challies, Gary Chis- 
hojm. Lin Hamilton, Ian Rogers and Bill Risk. 

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918 



C. DAVID MCINTIRE 



Ecology, \'ol. 47, No. 6 



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381-391. 



315 



THE CAUSALITY OF MICROTINE CYCLES IN GERMANY 

(Second Preliminary Research Report) 



Fritz Frank 

Institut fiir Griinlandfragen der Biologischen Bundesanstalt fiir Land- 

Philosophenweg 16, Oldenburg (Oldb), Germany 



und Forstwirtschaft, 



Hitherto the phenomenon of cycles has not 
been a subject of detailed research in central 
Europe, so one could have the impression 
that cycles of extreme degree do not exist in 
the temperate zones of this continent ( and 
this is often asserted, indeed); but this is not 
the case. The central European rodents not 
only exhibit irregular population fluctua- 
tions, but some of them also show regular 
cycles of an intensity and a strict periodicity 
not inferior to those of the cyclic animals in 
the arctic zone. Primarily, there are large 
plague districts of Microtus arvalis Pallas 
in Germany and her neighbouring countries 
which can be followed back at least to the 
fifteenth century. Recently, these plague 
districts have increased because of cultiva- 
tion measures, especially the drainage of 
moist lowlands and fens, which create opti- 
mal biotopes for the voles (Frank, 1953c, 
1955, 1956b ) . Besides, particularly since the 
end of the last war, Microtus agrestis L. 
caused heavy damage in the forest planta- 
tions, as it did in Great Britain, and it did 
so in a decidedly cyclic manner (Frank, 
1952 ) . Systematic research on the causality 
of these cycles was started by the author in 
1951 at first with main emphasis on M. ar- 
valis. Besides detailed publications, a first 
preliminary report was given in 1954 (Frank, 
1954b ) . In the meantime, many new results 
have been collected — in laboratory popula- 
tions of more than 10,000 animals and in 
outdoor-cage populations, as well as in wild 
populations involving 1,150 individually 
marked animals. This paper summarizes the 
present state of the work, including as-yet- 
unpubhshed material. I am much indebted 
to Frances Hamerstrom, Plainfield (Wis.), 
and to Robert Rausch, Anchorage ( Alaska ) 
for critically revising my English rough copy, 
and also for inducing me to adjust my eco- 



logical terms to American usage and to 
formulate some passages more precisely. 

The main emphasis on cyclic work for- 
merly was mostly placed on the attempt to 
get to the bottom of the causality of cycles 
by analysing and explaining the periodicity 
from phenological data, often with specula- 
tion on cosmic causalities before having ex- 
plored all terrestrial events and influences. 
In contrast, the German researches were 
concentrated on the observation and analysis 
of the internal events occurring in cyclic 
populations and on the environmental fac- 
tors influencing them. Naturally, we are 
not able to solve all problems connected 
with microtine cycles in so short a time, 
but I dare say many partial solutions have 
now been attained. When assembled, they 
already show a rough picture of the cyclic 
structure established on a foundation of 
facts containing few elements of a specula- 
tive or hypothetical nature. In this way the 
cyclic phenomenon presents itself — as do 
other biological problems — as an interaction 
between biological events and environmen- 
tal factors of a particularly complicated 
structure, depending on several factor- 
groups and many individual factors. 

Population Increase 

First, population increase results from 
three factor-groups — the "reproductive po- 
tential" of the cyclic species, the "carrying 
capacity" of the environment, and that which 
I call in German "Verdichtungspotential" 
(Frank, 1954b), in English "condensation 
potential" of the cyclic species. 

Reproductive Potential 

This first factor-group is based on age at 
maturity, litter size, litter succession, and 
length of the reproductive season. Working 



113 



316 



114 



Journal of Wildlife Management, Vol. 21, No. 2, April 1957 



with a captive population of more than 
10,000 laboratory-reared animals (Frank, 
1956a ) and individually marked wild popu- 
lations of M. arvaJis (yet unpublished), my 
findings concerning this point had most re- 
markable results. M. arvalis distinguishes 
itself by having a pronounced suckling-ma- 
turity. The young females, which suckle un- 
til the seventeenth day, already show a per- 
forated vagina from the eleventh day on 
and are mated by old males from the thir- 
teenth day on. Correspondingly, the earliest 
litters were dropped by a wild female 33 
days old and by a captive female 34 days old 
(pregnancy lasts 19-21 days, on an average 
20 days ) . Indeed under natural conditions, 
a high proportion of the young females 
mate in the maternal home range before 
being weaned or immediately after being 
weaned.^ But this happens only in the spring 
and summer; the females born during and 
after September for the most part do not 
reach sexual maturity in the same year. In 
the autumn the young generally show a slow- 
er growth rate than in the spring and sum- 
mer, when an astonishing growth rate is evi- 
dent. At the age of about 40 days a pregnant 
female can weigh up to 34g., and the males 
of this age also may be as heavy as very old 
animals. Every analysis of vole populations 
for age classification based on weight classi- 
fication, therefore, must lead to serious 
errors, and conclusions based on them are 
subject to question ( Frank and Zimmerman, 
1957). 

Besides age at maturity, reproductive po- 
tential is based on litter size and litter suc- 
cession. Litter size depends upon inherit- 
ance, upon age and size of the female, and 
upon season ( Frank, 1956a ) , and is modified 
by several environmental influences; in par- 
ticular, quality and quantity of food are of 
decisive importance. In M. arvalis maximum 
litter size is 12; in one case Reichstein (1957) 
found 13 embryos. Under optimal condi- 
tions postpartum mating is usual, so that one 
litter follows another every 20 days. The 
maximum number of litters produced by 



'Early maturity of females seems to be a general 
feature of the genus Microtus because I found 
mating females 20 days old also in M. oeconomus 
(Frank and Zimmermann, 1956). As far as I know 
suckling-maturity among other mammals has hither- 
to been established only for Mustela erminea L. 
(Miiller, 1954). 



one female in my laboratory-reared popula- 
tion of more than 10,000 animals has been 
33, with 127 young and an average litter 
size of 3.85. Under optimal food and cli- 
matic conditions in spring and summer, the 
average litter size in wild populations can 
amount to 7 young. Concerning reproduc- 
tive efficiency, M. arvalis represents a maxi- 
mum among all mammals hitherto investi- 
gated. In captive females the Htter weight 
amounts to 53.2 per cent of the mother's 
weight (both measured immediately after 
birth ), while in other mammals, for instance 
some other rodents and pygmy dogs, it is 
only one-third (Frank, 1956a). 

Length of the reproductive season, a fur- 
ther factor influencing reproductive poten- 
tial, continues from February or March to 
October or November, but under favourable 
conditions, for example in cornricks, repro- 
duction goes on through the winter ( Stein, 
1953a; Frank, 1954b). On the whole, 
M. arvalis, and probably M. agrestis, both 
showing pronounced cycles, possess an un- 
common reproductive potential attainable 
under the optimal environmental conditions 
presented in the plague districts. 

Carrying Capacity of Environment 

Whether or not this high reproductive po- 
tential causes a violent population increase 
depends on the second factor-group, the 
carrying capacity of the environment. In 
other words, it depends on whether or not 
the environment can support a high popula- 
tion. The individual factors influencing this 
are especially food, cover, sunlight, good 
overwintering places, and ground-water 
level (but in the case of M. arvalis not the 
nature and humidity of the soil ) . Also it is 
striking that all plague districts of M . arvalis, 
although they lie in very different geological 
formations (lowlands, marshes, fens, loam 
steppes, lower mountain regions, etc. ), show 
very similar characteristics in the structure 
of their landscape. They always represent 
large, open, monotonous, and uniform bio- 
topes with extremely scant cover of trees 
and bushes, which we call "cultivation 
steppes" caused by human activity in the 
once-wooded or marshy central European 
country. Extremely severe and regular 
plagues of M. arvalis occur only in such 
biotopes, evidently representing the eco- 
logical optimum for this species; in districts 
miscellaneously covered by varied biotopes 



317 



Causality of Microtine Cycles in Germany — Frank 



115 



and higher proportions of woods, trees, and 
bushes, only moderate fluctuations are visi- 
ble. Doubtless these circumstances repre- 
sent certain parallels to the opinion of 
Dymond (1947), that the uniformity of the 
arctic biotopes favours the amplitude of 
cycles. This further shows that not only 
the climate but also the structure of environ- 
ment is important for the origin of regular 
cycles, which indeed are observable in the 
temperate zones where there are correspond- 
ing environmental conditions. The abun- 
dance and the cycles of M. arvalis are also 
influenced by the economic use of the coun- 
try. Extensive agricultural use favours 
plagues, intensive use prevents plagues. On 
grazing land a low stock of cattle and an 
extensive pasturing favours plagues, while 
high stocks of cattle and intensive pasturing 
prevent plagues ( Frank, 1956b ) . 

Thus, in central Europe, the cycles of 
M. arvalis are "released" by human cultiva- 
tion. This enables us to stop the develop- 
ment of plagues by an ecological and eco- 
nomic reorganisation of the plague districts. 
Based on this example the author has postu- 
lated the introduction of the more effective 
"ecological plague control" for crop protec- 
tion, rather than the usual chemical pest 
control by poisons and biological control by 
encouragement of enemies and parasites 
(Frank, 1956b). In principle, the same is 
valid for M. agrestis, which shows regular 
fluctuations only in former woodland where 
the trees have been felled or new plantations 
of trees are laid out, and tlie bare plains are 
covered with large grass jungles, evidently 
representing the ecological optimum for this 
species (Frank, 1952, 1954b). In any case 
true cycles appear only under optimal en- 
vironmental conditions permitting both the 
realization of the high reproductive potential 
and the establishment of the descendants 
produced by this potential: in other words, 
where a high carrying capacity is present. 
On this point our conclusions probably come 
near to some of the ideas expressed by Paul 
Errington. 

Condensation Potential 

The degree of the population increase 
depends decisively on the third factor-group: 
the condensation potential, which consists 
of certain behaviour mechanisms that en- 
able many cyclic species to live at an un- 
commonly high population density. Before 



describing these behaviour mechanisms I 
must explain the new term "condensation 
potential" (Frank, 1954b). It is based on 
all intraspecific and especially social be- 
haviour that favours the increase of density. 
Normally the condensation potential is 
limited by intrinsic behaviour, especially by 
territoriality, to a "saturation point" which 
is approximately adapted to the carrying 
capacity of the environment. It seems to 
be a feature of many cyclic species that they 
show particular social behaviour that abol- 
ishes the normal limits, and enables them, 
under optimal environmental conditions, to 
exceed the saturation point so far that the 
carrying capacity of the environment is 
greatly exceeded, and simultaneously popu- 
lation regulation by crash, mass emigration, 
or other drastic mechanisms becomes neces- 
sary and inevitable. In M. arvalis the con- 
densation potential concerns: reduction of 
the home ranges, social communities of the 
females, and diminution or elimination of 
males. These points seem worth stressing 
as aspects of cycle research that further the 
understanding of this phenomenon and of 
population dynamics in general (Frank, 
1954b, 1956a). 

Fundamentally the European microtines 
are territorial animals; this we have demon- 
strated in the laboratory (Frank, 1953a, 
1956a) as well as in individually marked 
wild populations. Females occupy a range 
around their burrows where they tolerate no 
stranger of their species. Females tolerate 
a strange male in their home ranges only 
when they are in heat and even then the male 
must fight to approach. With the exception 
of the short period of heat, all strangers of 
either sex are driven away. This home range 
has a diameter of 10-20 meters during the 
reproductive season. Males inhabit an ir- 
regular larger range, wandering from female 
to female to mate those that are in heat. 
They are only intolerant of strange males of 
mature age. Recently we found that in 
spring and summer the young males with- 
out exception disappear from their mother's 
territory and its surroundings after becoming 
mature, and the old males mating the resi- 
dent females are all strangers, having im- 
migrated from other places. This would 
tend to prevent inbreeding. In contrast, the 
young females settle in the immediate vicin- 
ity of their mother's home range, or some- 
times within it. When space becomes scarce, 



318 



116 



Journal of Wildlife Management, Vol. 21, No. 2, April 1957 



the size of the home ranges can be reduced. 
This also gives the voles a considerable con- 
densation potential (Frank, 1953a). 

In contrast to the territorial behaviour 
that causes intraspecific demarcation and 
guarantees the individual space and food 
needed for life and reproduction, the follow- 
ing mechanisms favour life in social com- 
munities and also high density. In the first 
place we have die "mother-family," con- 
sisting of the female and her suckling young, 
sometimes also her unmated subadult off- 
spring. But this is not typical of spring and 
summer when, for the most part, the weaned 
young, particularly the males, leave the 
maternal home range. "Great families" arise 
every autumn, for the last two to three litters 
of the year remain in the maternal home 
range (because the female does not drive 
them out ) , and constitute the overwintering 
community (Frank, 1954a). This lightens 
existence in the cold season when stress is 
great; all live together in a single, thickly 
lined nest, the many small individuals form 
a greater thermal unit, and the loss of heat 
and energy is significantly reduced. Freez- 
ing weather and heavy precipitation reduce 
the activity of the voles, which remain in 
their nests and eat the food stores they 
have brought in during autumn. Neverthe- 
less, the size of the home ranges and the 
radius of activity of the voles is importantly 
enlarged during winter (about four or five 
times larger than the summer home range ) , 
probably because of both the greater 
number of the inhabitants (overwintering 
community instead of the female and her 
last litter in summer), and because of the 
shortage of available food requiring a larger 
feeding area for these herbivorous animals. 
In the peak years the impossibility of such 
an enlargement of activity radius, caused 
by population density, might contribute 
much to intensify competition for food and 
to bring on a crash situation. In spring the 
overwintering communities dissolve by 
scattering. 

Furthermore, a behaviour mechanism of 
highest importance is involved in the nest 
communities of the females ( Frank, 1953a ) , 
Increasingly with population condensation, 
the young females remain together, occupy 
a common territory, and bring up their 
litters in a single nest by means of social 
breeding care. Generally they remain to- 
gether for the rest of their lives, and if they 



change their home range because of distur- 
bance, etc., they move as a community, often 
with their young also. The nest community 
can consist of 2-4 (perhaps 5) sisters, and 
sometimes of their mother too. The decisive 
influence of this behaviour upon the popu- 
lation dynamic is that it enables these pri- 
marily territorial animals to Hve in an ab- 
normally high density. In this way not only 
more females can live in the same space, 
but also a correspondingly greater number 
of young can be produced and brought up. 
Doubtless this particular social behaviour of 
M. arvolis explains the uncommon popula- 
tion density and the outright explosive popu- 
lation increase in plague centres, i.e., those 
parts of the plague districts ecologically most 
favourable and first occupied by the voles. 

In contrast to the females, the mature 
males cannot draw so near to one another 
because they generally display rivalry (ex- 
cept as members of a family or of an over- 
wintering community). During population 
increase in a given space, the number of 
old males remains the same, while that of 
the mature females rapidly increases. Pro- 
gressing with population condensation, a 
considerable elimination of mature males 
occurs (Frank, 1953a, 1954a, 1954b; Stein, 
1953b). This reduction is also evident from 
the pellets of owls ( Becker, 1954 ) , and thus 
not caused by selective predation (on the 
males), but by intraspecific competition 
( among the males ) . In spring and summer 
the weaned young males, without exception, 
leave their birthplaces, probably because of 
an innate drive after maturing. They must 
look for a new home range and come up 
against all other males they meet. Whether 
their number diminishes by killing each 
other or merely by driving each other away 
requires further observations. A large num- 
ber of the wild males show injuries, espe- 
cially bites in the region of the hindquarters, 
and lost tails, caused by intraspecific fight- 
ing; however, these injuries might have been 
acquired from resident females as well as 
from other males. 

Thus we see that the intraspecific, es- 
pecially social, behaviour of the animals is 
of great importance to all population-dy- 
namic events. Further research is needed 
on this point, especially in other cyclic 
species, to find out whether similar or other 
condensation mechanisms are prevalent. 



319 



Causality of Microtine Cycles in Germany — Frank 117 

Population Decline curs among them during spring. They do 

not mount in weight and can hardly bring 
What causes the population decline of up their young, which therefore show heavy 
M. arvalis? The life span of the little micro- mortality. This has already been pointed out 
tines is naturally short. Periods of crises and by Chitty ( 1952, 1955 ) and in every way 
losses seem to be: ( 1 ) becoming acquainted confirmed also by my own researches in 
with the maternal home range first, in which outdoor cages ( Frank, 1954a ) as well as by 
there is danger if strange neighbours are research on wild populations of M. arvalis 
encountered; (2) the period of spreading and M. agres^is (as yet unpublished). There- 
after weaning, which involves heavier losses fore, vole populations always have a diffi- 
in the males than in the females; and (3) cult and slow start toward recovery after 
the winter season, which normally dimin- severe winters and after crashes. Predation 
ishes the population up to 50 per cent or plays only a very small part, because preda- 
more (Frank, 1954b). The animals of my tors are not at all numerous in the plague 
marked wild populations never survived districts, having been kept down both by 
two winters, and the markedly old individ- the unfavourable, monotonous and coverless 
uals almost all succumb to the stresses of the biotope and by human persecution ( Frank, 
first winter months. Not only those individ- 1954b, 1955, 1956b). 

uals that have survived a winter die, but In the peak years characterized by over- 
also those born in spring and summer that crowding, the regulation of microtine popu- 
had reproduced suffer mortality. Their body lation density by no means shows itself as 
weight gradually diminishes throughout the mass emigration as with the lemmings 
autumn, and their body reserves are nearly (Lemmus lemmus L. ), for we observed 
consumed by then. In contrast, the young movement of individuals only, more com- 
animals born in the autumn increase in monly in the males than in the females. As 
weight and lose only a little in the begin- previously stated, the latter are generally in- 
ning of winter; then their weight is main- dined to settle in the neighbourhood of their 
tained during the winter months (mostly birthplaces as long as they are able to find 
about 12- 18g.) and mounts again quickly in places unoccupied by other females. But 
early spring. While the period of spreading space finally becomes scarce ( in spite of and 
causes heavier losses among males, winter after reduction of the size of the home 
mortality strikes more females because they ranges ) and competition among females in- 
are mostly somewhat smaller and weaker creases. Reproduction is then gradually re- 
( Frank, i954b). Nevertheless, mortality stricted (Frank, 1953a, 1954a). The degree 
effects a real selection by eliminating the of embryonal resorptions, infertility, and 
less fit individuals. After the winter period, mortality of young all mount quickly, but 
the surviving population consists nearly ex- population density can no longer be regu- 
clusively of autumn-born animals that had lated by these; the carrying capacity of the 
remained sexually immature until spring, environment has already been greatly ex- 
The older voles, already having participated ceeded. For this reason regulation must be 
in reproduction during the last year, have performed by a more effective mechanism: 
vanished with only few exceptions. the crash. Our investigations could not pro- 
Winter mortality can be so great, partic- d^ce any evidence for the hypothesis that 
ularly in extremely severe winters, that the epizootic diseases or parasites cause the 
population declines to a minimum level by crash, although our material was examined 
a gradual die-off of most individuals; but by many specialists (Frank, 1953b). An ex- 
this happens only when population density planation was only possible on the basis of 
is not high enough to produce a regular Christian's (1950) important idea that the 
crash. However, the physiological mechan- "shock disease" of the varying hare ( Lepus 
ism of this gradual die-off seems to be similar americanus Erx. ) , discovered by Green and 
to that of the regular crash, and to be based Larson ( 1938 ), seems to be an appearance of 
on the endocrine system also (see below), the general adaptation syndrome of Selye 
In this way, the stress of such a severe winter ( 1946 ) . 

can injure the survivors of the gradual die- First I must say that the crash symptoms 

off (and also of a regular crash) so much in M. arvalis are the same as in L. amer- 

that a remarkable subsequent mortality oc- icanus: lethargy, convulsions, liver degen- 



320 



118 



Journal of Wildlife Management, Vol. 21, No. 2, April 1957 



oration, enlargement of the adrenals and 
hypoglycemia, and moreover (not mentioned 
by Green and Larson) marked decline in 
body temperature long before death, and 
behavioural changes such as crowding and 
cannibalism. The last represents an impor- 
tant chance for survival of the fitter individ- 
uals by making use of the carcasses of their 
dead companions as food reserves during the 
period of general deficiency or shortage of 
vegetable food already used up by the over- 
crowded population (Frank, 1953b). Not 
only have we found these symptoms experi- 
mentally in outdoor cages where vole popu- 
lations were kept overcrowded and showed 
drastic crashes, but we were also able to 
produce crash symptoms by artificial hypo- 
glycemia induced by insulin injections; con- 
versely, the symptoms could be suspended, 
temporarily at least, by injection of grape 
sugar (Frank, 1953b). 

We get the impression that condensation 
and crowding favour competition and cause 
a state of psychological excitement being 
transformed by the pituitary-adrenocortical 
system into a physical stress. This, acutely 
combined with the stress of food shortage, 
produces a "readiness" for crash, whether 
the real releasing of the crash is caused by 
an increase in the force of these stresses, or, 
in nature, largely by additional meteorologi- 
cal stresses, such as periods of cold or pre- 
cipitation. On the whole, a situation with 
several stress-producing components ulti- 
mately produces the resulting "crash" either 
when all stress factors jointly reach a critical 
point or value, or when a new stress is super- 
imposed on the already stressed adreno- 
pituitary system. 

In my opinion, our results confirm the 
basic trends of ideas presented by Christian's 
( op. cit. ) important working hypothesis, but 
my results differ in one essential point. 
Christian supposes that the crash, the readi- 
ness for which is brought about by several 
stresses, is ultimately caused and released 
by the additional stress of the activation of 
gonads happening in the early spring. But 
I never found any enlargement of testes and 
uteri in crashing wild populations. Also in 
my experimentally induced crashes of out- 
door-cage populations, activation of gonads 
was certainly not in play. I am therefore 
convinced that gonadotrophic demands are 
not involved in the crash phenomenon, in 
Microtus at least. In my conception the 



ultimate trigger, producing the crash of vole 
populations, is an additional stress of mete- 
orological events, particularly frost periods. 
I believe that this conception explains better 
than Christian's the sudden advent of a 
crash within a few days. The stress of 
gonadotrophic demands would be extended 
over longer time and would operate in very 
different moments upon the single animal. 
In contrast, the meteorological stress caused 
by the intrusion of frost periods acts equally 
and suddenly upon all individuals and makes 
more easily understandable the suddenness 
of the crash. 

Nevertheless, gonadotrophic activation 
might play an essential role, indeed, in the 
subsequent mortality occurring in spring 
among the survivors from crashes and grad- 
ual winter die-offs, which was discovered by 
Chitty ( op. cit. ) and also found in the vole 
populations investigated by the author ( see 
above). In this case, gonadotrophic activa- 
tion presents a true additional stress upon 
the endocrinological system, as Christian has 
supposed. 

I must emphasize that this conception is 
based on investigations in vole populations 
only. In any event, it now seems to be cer- 
tain that the adreno-pituitary system has de- 
cisive importance in intraspecific regulatory 
events occurring in vertebrate populations. 
Further research is needed to complete and 
deepen our knowledge of this important 
point, and to find out in what manner and 
with which different effects this psycho- 
physiological mechanism is operating and 
which environmental factors are acting up- 
on them, in voles as well as in other rodents 
and vertebrates generally. 

The Periodicity of Cycles 

Many workers on the periodicity of cycles 
(recently again Siivonen and Koskimies, 
1955 ) attempt to connect this problem with 
cosmic factors before having explored all 
terrestrial environmental factors possibly 
influencing it. But nearly all such work on 
this subject generally seems to suffer from 
the fact that the phenological data, particu- 
larly the meteorological conditions, are not 
brought into relationship as the most im- 
portant environmental factors acting upon 
cyclic populations. Favoured by the ex- 
tremely equalized temperate climate in the 
Gulf Stream neighbourhood of northwestern 
Germany, Maercks ( 1954 ) has been able to 



321 



Causality of Microtine Cycles in Germany — Frank 



119 



evaluate the interaction between the cycles 
of M. arvalis and meteorological events over 
a period of 39 years, based on the five-day 
median values of temperature, quantity and 
frequency of precipitation, and duration of 
sunshine. Therefore the cyclic events take 
place in a rather "pure culture" generally 
little influenced by extreme changes in 
weather conditions, which — if they occurred 
— could easily be analysed regarding their 
effects on the cyclic events. Maercks found 
a clear and strict microtine-cycle periodicity 
of three years from peak to peak, obviously 
caused by the reproductive and condensa- 
tion potential of the species and the carrying 
capacity of its environment. Under optimal 
environmental conditions M. arvalis is able 
to replenish a plague district within three 
years so completely that the carrying capa- 
city is exceeded and natural regulation by 
crash must occur. Every population has its 
own autonomous periodicity, and in other 
spheres ( other species or other environment, 
or both) there will be other frequencies of 
the periodicity (Frank, 1954b). Dymond 
( 1947 ) has already suggested that animals 
with a high and constant reproductive po- 
tential may be able to populate deficiently 
buffered^ biotopes of optimal and constant 
ecological conditions at regularly occurring 
intervals to an unbearable density. 

As to the influence of meteorological con- 
ditions, Maercks (ibid.) found frequent 
quantitative oscillations in the degree of the 
peak population density and plague damage, 
but few temporal mutations of the periodi- 
city itself. The former are caused by changes 
of rainfall and duration of sunshine, for ex- 
ample, while the latter are all reducible 
to uncommon and extreme deviations in 
weather conditions, especially in winter. In 
the 39 years investigated by Maercks, the 
three-year periodicity has undergone three 
mutations, which led to the following con- 
clusions: (1) A particularly mild winter 
prolongs the plague over a two-year period, 
and therefore the cyclic interval extends to 
four years, because the expected crash does 
not happen but comes a year later; ( 2 ) an 
extremely long and severe winter cuts off 
the population increase by causing a gradual 



*These are biotopes with a scarcity of natural 
counterpowers to the species in question, as enemies, 
competition by other species, limit of food and habi- 
tats, or other unfavourable ecological conditions. 



die-off or a precocious crash and forcing a 
new start of population increase. 

In both cases the cycle periodicity suffers 
a shifting of phase by one year (or more 
perhaps in other cases). This shiJFting, in- 
deed, is a point in the cycle phenomenon 
that has caused considerable difficulty to 
cycle workers, who have almost established 
a periodicity of 3 1/3 years. But this was 
unsatisfactory because the cyclic periodicity 
is based ( in my opinion at least ) on the re- 
productive season's being fixed by the astro- 
nomical year. Every biological periodicity 
extended over several years might also pre- 
sent whole numbers corresponding to the 
whole numbers of years. This difficulty is 
removed by the shifting of phase caused by 
meteorological deviations that occur in every 
climate; the phase shift easily explains the 
fact that animal cycles never show a sym- 
metrical periodicity over a long period of 
time but always show a few exceptions or 
deviations from the prevailing equal pe- 
riodicity ( three years in the case of Microtus 
arvalis ) . 

Also the striking conformity in the peri- 
odicity of different cyclic populations and 
plague districts, independent of and isolated 
from each other, is produced by meteoro- 
logical conditions prevailing equally over a 
large region ( Frank, 1954b ) . For example, 
an uncommon and extremely severe winter 
will simultaneously throw back all popula- 
tions influenced by it ( each having its own 
autonomous periodicity previously), to a 
new (and common) starting point. Never- 
theless, some populations exposed to special 
environmental conditions can show a dif- 
ferent periodicity, most commonly because 
favourable overwintering conditions have 
counterbalanced unfavourable meteorologi- 
cal conditions. 

Summary 

The results of recent work on microtine 
cycles occurring in Germany enable us to 
understand this phenomenon as an inter- 
action between biotic and environmental 
factors only, and without aid of any hypo- 
thetical explanation by extraterrestrial "cos- 
mic" factors. It may be supposed that the 
causality of other animal cycles will find 
a similarly "natural" explanation after being 
explored as intensively as the cycles of Mi- 
crotus arvalis in Germany. Although these 



322 



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Journal of Wildlife Management, Vol. 21, No. 2, April 1957 



are indeed "released" by human cultivation 
measures, which have produced optimal bio- 
topes and thus the ecological base of cycles, 
the biotic causalities and laws of these cycles 
must be the same as those prevailing in 
cycles occurring in natural districts not in- 
fluenced by man. 

Concerning M. arvalis the population in- 
crease is based on: ( 1 ) a high reproductive 
potential based on ( a ) extremely early ma- 
turity and mating (in females often before 
being weaned), (b) high reproductive ef- 
ficiency (litter weights to 53.2 per cent of 
the mother's weight), (c) large litter size 
(maximum 12-13, average in wild popula- 
tions about 7 young), (d) rapid litter suc- 
cession (pregnancy about 20 days, post- 
partum mating normal), and (e) extended 
season of reproduction ( sometimes through- 
out winter); (2) a high carrying capacity 
of the environment under the optimal eco- 
logical conditions of the plague districts, 
based on food, cover, ground-water level, 
sunlight, overwintering places, and last but 
not least on the uniform structure of the 
landscape; and (3) a high "condensation 
potential" based on behaviour, particularly 
social mechanisms concerning ( a ) reducible 
home-range size during population increase, 
formation of (b) "great families" and (c) 
overwintering communities, (d) communal 
nesting of females, and (e) elimination of 
males. On the whole, these factors suffi- 
ciently explain the outright explosive in- 
crease and the uncommon density of micro- 
tine populations in German plague districts. 

Because this rapid population increase 
cannot be regulated by normal mortality 
and dispersal, more efficient regulatory 
mechanisms are called into play. When the 
supportable density of population is ap- 
proached, restriction of reproduction and 
accelerated individual emigration take 
place, but these are not enough to keep the 
population within the limits set by the car- 
rying capacity of the environment. When 
supportable density is exceeded, crash, 
caused by shock disease, occurs in the fol- 
lowing winter. Psychological stresses ( such 
as crowding and competition ) and physical 
stresses (such as food shortage) produce a 
"readiness" for crash, but the real trigger 
is largely the additional meteorological stress 
of winter. Three years are ordinarily re- 
quired to reach this point, hence an auto- 
nomous and strict 3-year periodicity exists. 



The seldom-occurring deviations ("shifting 
of phase") are caused only by uncommon 
meteorological conditions. Unusually severe 
winters synchronize the periodicity of iso- 
lated populations over large districts. 

On the whole, cycles take place where the 
high biotic potential of the species is fully 
realizable in the optimal biotopes of plague 
or other cyclic districts. It seems remarka- 
ble that this disproportion is not balanced 
by selection. Cycles have undoubtedly gone 
on from time immemorial, and the quick 
succession of generations of voles should 
have favoured such an adaption in a rela- 
tively short time. 

Literature Cited 

Becker, K. 1954. Beitrage zur Geschlechtsbestim- 
mung von Mausen (Muridae) nach Skelettresten 
aiis Eulengewollen. Zool. Jahrb. ( Systematik ) , 
82:463-472. 

Chitty, D. 1952. Mortality among voles ( Microf us 
agrestis) at Lake Vyrnwy, Montgomeryshire, 
in 1936-39. Phil. Trans. Roy. Soc. London, 
Ser. B, 236:505-552. 

. 1955. Adverse effects of population den- 
sity upon the viability of later generations. 
Pp. 57-67 in: "The numbers of man and ani- 
mals," edited by J. B. Cragg and N. W. Pirie. 
Oliver and Boyd, Edinburgh. 152pp. 

Christian, J. J. 1950. The adreno-pituitary system 
and population cycles in mammals. J. Mamm., 
31:247-259. 

Dymond, J. R. 1947. Fluctuations in animal popu- 
lations with special reference to those of 
Canada. Trans. Roy. Soc. Canada, Ser. Ill, 
16:1-34. 

Frank, F. 1952. Umfang, Ursachen und Bekampf- 
ungsmoglichkeiten der Mausefrassschaden in 
Forstkulturen. Nachrichtenbl. Deutsch. Pflan- 
zenschutzdienst (Braunschweig), 4:183-189. 

. 1953a. Zur Entstehung iibemormaler Pop- 

ulationsdichten im Massenwechsel der Feld- 
maus, Microtus arvalis ( Pallas ) . Zool. Jahrb. 
(Systematik), 81:610-624. 

. 1953b. Untersuchungen iiber den Zusam- 

menbruch von Feldmausplagen (Microtus ar- 
valis Pallas). Zool. Jahrb. (Systematik), 
82:95-136. 

. 1953c. Zur Entstehung neuer Feldmaus- 

plagegebiete durch Moorkultivierung und 
Melioration. Wasser und Boden (Hannover), 
5:342-345. 

. 1954a. Beitrage zur Biologic der Feld- 

maus, Microtus arvalis (Pallas). Teil I: 
Gehegeversuche. Zool. Jahrb. (Systematik), 
82:354-404. 

. 1954b. Die KausaUtat der Nagetier-Zyklen 

im Lichte neuer populationsdynamischer Un- 



323 



Causality of Microtine Cycles in Germany — Frank 



121 



tersuchungen an deutschen Microtinen. Zeit- 
schr. f. Morphol. u. Oekol., 43:321-356. 

— . 1955. Naturschutz und Mauseplagen. 
Natur und Landschaft (Liineburg), 30:109- 
112. 

— . 1956a. Beitrage zur Biologic der Feld- 
maus, Microtus arvalis (Pallas). Teil II: 
Laboratoriumsergebnisse. Zool. Jahrb. (Sys- 
tematik), 84:32-74. 

— . 1956b. Grundlagen, Moglichkeiten und 
Methoden der Sanierung von Feldmausplage- 
gebieten. Nachrichtenbl. Deutsch. Pflanzen- 
schutzdienst (Braunschweig), 8:147-158. 

— AND K. ZiMMERMANN. 1956. Zur Biologic 
der Nordischcn Wiihlmaus (Microtus oecono- 
mus stimmingi Nehring). Zeitschr. f. Sau- 
getierkundc, 21:58-83. 

1957. Die Verwendbarkeit morphologis- 



cher Merkmale als Alterskritericn bei der 
Fcldmaus, Microtus arvalis (Pallas). Zool. 
Jahrb. (Systcmatik), 85: in press. 

Green, R. G. and C. L. Larson. 1938. A descrip- 
tion of shock disease in the snowshoe hare. 
Amer. J. Hyg., 28:190-212. 

Maercks, H. 1954. Uber den Einfluss der Witter- 



ung auf den Massenwechsel der Feldmaus 
( Microtus arvalis Pallas ) in der Wesermarsch. 
Nachrichtenbl. Deutsch. Pflanzenschutzdienst 
(Braunschweig), 6:101-108. 

MiJLLER, H. 1954. Zur Fortpflanzungsbiologie des 
Hermelins (Mustela erminea L. ). Rev. Suisse 
Zool., 61:451-453. 

Reichstein, H. 1957. Feldmaus, Microtus arvalis 
(Pallas 1779), mit 13 Embryonen. Saugetier- 
kundliche Mitt., 5: in press. 

Selye, H. 1946. The general adaptation syndrome 
and the diseases of adaptation. J. Clin. Endo- 
crinol., 6:117-230. 

SiivoNEN, L. AND J. KosKiMiES. 1955. Population 
fluctuations and the lunar cycle. Papers on 
Game Research (Helsinki), 14:1-22. 

Stein, G. H. W. 1953a. Uber Umweltabhangig- 
keiten bei der Vermehrung der Feldmaus, 
Microtus arvalis. Zool. Jahrb. ( Systematik ) , 
81:527-547. 

. 1953b. tJber das Zahlenverhaltnis der 

Geschlechter bei der Feldmaus, Microtus ar- 
valis. Zool. Jahrb. (Systematik), 82:137-156. 

Received for publication October 9, 1956. 



324 



TERRITORIALITY AND HOME RANGE CONCEPTS AS APPLIED 

TO MAMMALS 

By William Henry Burt 

territoriality 

The behavioristic trait manifested by a display of property ownership — a 
defense of certain positions or things — reaches its highest development in the 
human species. Man considers it his inherent right to own property either as 
an individual or as a member of a society or both. Further, he is ever ready 
to protect that property against aggressors, even to the extent at times of 
sacrificing his own life if necessary. That this behavioristic pattern is not 
peculiar to man, but is a fundamental characteristic of animals in general, has 
been shown for diverse animal groups. (For an excellent historical account 
and summary on territoriality, with fairly complete bibliography, the reader is 
referred to a paper by Mrs. Nice, 1941). It does not necessarily follow that 
this trait is found in all animals, nor that it is developed to the same degree in 
those that are known to possess it, but its wide distribution among the verte- 
brates (see Evans, L. T., 1938, for reptiles), and even in some of the invertebrates, 
lends support to the theory that it is a basic characteristic of animals and that 
the potentialities are there whether the particular animal in question displays 
the characteristic. Heape (1931, p. 74) went so far as to say: 

"Thus, although the matter is often an intricate one, and the rights of terri- 
tory somewhat involved, there can, I think; be no question that territorial 
rights are established rights amongst the majority of species of animals. There 
can be no doubt that the desire for acquisition of a definite territorial area, the 
determination to hold it by fighting if necessary, and the recognition of individual 
as well as tribal territorial rights by others, are dominant characteristics in 
all animals. In fact, it may be held that the recognition of territorial rights, 
one of the most significant attributes of civilization, was not evolved by man, 
but has ever been an inherent factor in the life history of all animals." 

Undoubtedly significant is the fact that the more we study the detailed be- 
havior of animals, the larger is the list of kinds knowoi to display some sort of 
territoriality. There have been many definitions to describe the territory of 
different animals under varying circumstances. The best and simplest of these, 
in my mind, is by Noble (1939); "territory is any defended area." Noble's 
definition may be modified to fit any special case, yet it is all-inclusive and to 
the point. Territory should not be confused with "home range" — an entirely 
different concept that will be treated more fully later. 

The territoriality concept is not a new one (see Nice, 1941). It has been only 
in the last twenty years, however, that it has been developed and brought 
to the front as an important biological phenomenon in the lower animals. 
Howard's book "Territory in Bird Life" (1920) stimulated a large group of 
W'Orkers, chiefly in the field of ornithology, and there has hardly been a bird 
life-history study since that has not touched on this phase of their behavior. 



325 



BURT — TERRITORIALITY AND HOME RANGE 



347 



In the field of mammals, much less critical work has been done, but many of the 
older naturalists certainly were aware of this behavior pattern even though 
they did not speak of it in modern terms. Hearne (1795) apparently was 
thinking of property rights (territoriality) when he wrote about the beaver as 





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HOME RANGE BOUNDARY 1^^:^^ NEUTRAL AREA 

TERRITORIAL BOUNDARY • NESTING SITE 

BLANK— UNOCCUPIED SPACE O REFUGE SITE 

Fig. 1. Theoretical quadrat with six occupants of the same species and sex, showing 
territory and home range concepts as presented in text. 

follows: "I have seen a large beaver house built in a small island, that had near 
a dozen houses under one roof; and, two or three of these only excepted, none 
of them had any communication with each other but by water. As there were 
beavers enough to inhabit each apartment, it is more than probable that each 
famOy knew its own, and always entered at their own door without having any 



326 



348 JOURNAL OF 1VL\MMAL0GY 

further connection with their neighbors than a friendly intercourse" (in Morgan, 
1868, pp. 308-309). Morgan (op. cit., pp. 134-135), also writing of the beaver, 
made the following observation; "a beaver family consists of a male and female, 
and their offspring of the first and second years, or, more properly, under two 
years old. . . . When the first litter attains the age of two years, and in the 
third summer after their birth, they are sent out from the parent lodge." Mor- 
gan's observation was later confirmed by Bradt (1938). The works of Seton 
are replete wath instances in the lives of different animals that indicate territorial 
behavior. In the introduction to his "Lives" Seton (1909) states "In the idea 
of a home region is the germ of territorial rights." Heape (1931) devotes an 
entire chapter to "territory." Although he uses the term more loosely than 
I propose to, (he includes home ranges of individuals and feeding ranges of 
tribes or colonies of animals), he carries through his work the idea of defense of 
an area either by an individual or a group of individuals. Not only this, but 
he draws heavily on the literature in various fields to support his thesis. Al- 
though the evidence set forth by Seton, Heape, and other early naturalists is 
of a general nature, mostly garnered from reports by others, it cannot be brushed 
aside in a casual manner. The old time naturalists were good observers, and, 
even though their techniques were not as refined as those of present day biolo- 
gists, there is much truth in what they wrote. 

A few fairly recent published observations on specific mammals serve to 
strengthen many of the general statements made by earlier workers. In speak- 
ing of the red squirrel (Tamiasciurus), Klugh (1927, p. 28) writes; "The sense 
of ownership seems to be well developed. Both of the squirrels which have 
made the maple in my garden their headquarters apparently regarded this tree 
as their private property, and drove away other squirrels which came into it. 
It is quite likely that in this case it was not the tree, but the stores that were 
arranged about it, which they were defending." Clarke (1939) made similar 
observations on the same species. In raising wild mice of the genus Peromyscus 
in the laboratory, Dice (1929, p. 124) found that "when mice are placed together 
for mating or to conserve cage space it sometimes happens that fighting takes 
place, especially at first, and sometimes a mouse is killed. . . . Nearly always 
the mouse at home in the cage will attack the presumed intruder." Further 
on he states, "However, when the young are first born, the male, or any other 
female in the same cage, is driven out of the nest by the mother, who fiercely 
protects her young." Similarly, Grange (1932, pp. 4-5) noted that snowshoe 
hares (Lepus americanus)- in captivity "showed a definite partiality for certain 
spots and corners to which they became accustomed" and that "the female 
would not allow the male in her territory (cage) during late pregnancy and the 
males themselves were quarrelsome during the breeding season." 

Errington (1939) has found what he terms "intraspecific strife" in wild musk- 
rats (Ondatra). Much fighting takes place when marshes become overcrowded, 
especially in fall and winter during readjustment of populations. "But when 
invader meets resident in the tunnel system of one of [the] last lodges to be used 
in a dry marsh, confhct may be indeed savage." Gordon (1936) observed def- 



327 



BURT TERRITORIALITY AND HOME RANGE 349 

inite territories in the western red squirrels (Tamiasciurus fremonti and T. 
douglasii) during their food gathering activities. He also performed a neat 
experiment with marked golden mantled squirrels {Citellus lateralis chysodeirus) 
by placing an abundance of food at the home of a female. This food supply- 
attracted others of the same species. To quote Gordon: "she did her best to 
drive away the others. Some of her sallies were only short, but others were 
long and tortuous. There were rather definite limits, usually not more than 
100 feet from the pile, beyond which she would not extend her pursuit. In 
spite of the vigor and the number of her chases (one day she made nearly 60 
in about 6 hours) she never succeeded in keeping the other animals away." 
This individual was overpowered by numbers, but, nevertheless, she was 
using all her strength to defend her own log pile. To my knowledge, this 
is the best observation to have been published on territorial behavior in 
mammals. I have observed a similar situation (Burt, 1940, p. 45) in the east- 
ern chipmunk (Tamias). An old female was watched fairly closely during 
two summers. Having marked her, I was certain of her identity. "Although 
other chipmunks often invaded her territory, she invariably drove them away 
[if she happened to be present at the time]. Her protected area was about 
fifty yards in radius ; beyond this fifty-yard limit around her nesting site she 
was not concerned. Her foraging range (i.e., home range) was considerably 
greater than the protected area (territory) and occasionally extended 100 or 
more yards from her nest site." From live trapping experiments, plotting 
the positions of capture of individuals on a map of the area covered, I in- 
terpreted (op. cit., p. 28) the results to mean that there was territorial be- 
havior in the white-footed mouse (Peromyscus leucopus), a nocturnal form. 
When the ranges of the various individuals were plotted on a map, I found 
that "the area of each of the breeding females is separate — that although 
areas sometimes adjoin one another, they seldom overlap." Carpenter (1942) 
writes thus: "The organized groups of every type of monkey or ape which has 
been adequately observed in its native habitat, have been found to possess 
territories and to defend these ranges from all other groups of the same species." 
In reporting on his work on the meadow vole {Microtus pennsylvanicus) , Blair 
(1940, pp. 154-155) made the statement "It seems evident that there is some 
factor that tends to make the females occupy ranges that are in part exclusive ; 
.... Possibly there is an antagonism between the females, particularly during 
the breeding season, but the available evidence does not indicate to me that 
they have definite territories which they defend against all trespassers. It 
seems highly probable that most mammalian females attempt to drive away 
intruders from the close vicinity of their nests containing young, hut this does 
not constitute territoriality in the sense that the term has been used by Howard 
(1920), Nice (1937), and others m reference to the breeding territories of birds." 
(Ital. mme.) To quote Howard (1920, pp. 192-193): "But the Guillemot is 
generally surrounded by other Guillemots, and the birds are often so densely 
packed along the ledges that there is scarcely standing room, so it seems, for 
all of them. Nevertheless the isolation of the individual is, in a sense, just as 



328 



350 JOURNAL OF MAMMALOGY 

complete as that of the individual Bunting, for each one is just as vigilant in 
resisting intrusion upon its few square feet as the Bunting is in guarding its 
many square yards, so that the evidence seems to show that that part of the 
inherited nature which is the basis of the territory is much the same in both 
species." Blair, in a later paper (1942, p. 31), writing of Peromyscus manicu- 
latus gracilis, states: "The calculated home ranges of all sex and age classes 
broadly overlapped one another. Thus there was no occupation of exclusive 
home ranges by breeding females. . . . That individual woodland deer-mice 
are highly tolerant of one another is indicated by the foregoing discussion of 
overlapping home ranges of all sex and age classes." Reporting on an extensive 
field study of the opossum, Lay (1942, p. 149) states that "The ranges of indi- 
vidual opossums overlapped so frequently that no discernible tendency towards 
establishment of individual territories could be detected. On the contrary, 
tracks rarely showed that two or more opossums traveled together." It seems 
quite evident that both Blair and Lay are considering the home range as syno- 
nymous with the territory when in fact they are two quite distinct concepts. 
Further, there is no concrete evidence in either of the above papers for or against 
territoriality in the species they studied. It is to be expected that the territory 
of each and every individual will be trespassed sooner or later regardless of how 
vigilant the occupant of that territory might be. 

It is not intended here to give a complete list of works on territorial behavior. 
The bibliographies in the works cited above lead to a great mass of literature 
on the subject. The point I wish to emphasice is that nearly all who have 
critically studied the behavior of w^ild mammals have found this behavioristic 
trait inherent in the species with which they worked. Also, it should be stressed, 
there are two fundamental types of territoriality hi mammals — one concerns 
breeding and rearing of young, the other food and shelter. These tw^o may be 
further subdivided to fit special cases. Mrs. Nice (1941) gives six major types 
of territories for birds. Our knowledge of territoriality in mammals is yet too 
limited, it seems to me, to build an elaborate classification of types. Some day 
we may catch up with the ornithologists. 

HOME RANGE 

The home range concept is, in my opinion, entirely different from, although 
associated with, the territoriality concept. The two terms have been used so 
loosely, as synonyms in many instances, that I propose to dwell briefly on them 
here. My latest Webster's dictionary (published in 1938), although satisfac- 
tory in most respects, does not list "home range," so I find no help there. Seton 
(1909) used the term extensively in his "Lives" where he explains it as follows: 
"No wild animal roams at random over the country: each has a home region, 
even if it has not an actual home. The size of this home region corresponds 
somewhat with the size of the animal. Flesh-eaters as a class have a larger 
home region than herb-eaters." I believe Seton was thinking of the adult 
animal when he wrote the above. We know that young adolescent animals 
often do a bit of wandering in search of a home region. During this time they 
do not have a home, nor, as I consider it, a home range. It is only after they 



329 



BURT TERRITORIALITY AND HOME RANGE 351 

establish themselves, normally for the remainder of their lives, unless disturbed,, 
that one can rightfully speak of the home range. Even then I would restrict 
the home range to that area traversed by the individual in its normal activities 
of food gathering, mating, and caring for young. Occasional sallies outside the 
area, perhaps exploratory in nature, should not be considered as in part of the 
home range. The home range need not cover the same area during the life 
of the individual. Often animals will move from one area to another, thereby 
abandoning the old home range and setting up a new one. Migratory animals 
have different home ranges in summer and winter — the migratory route is not 
considered part of the home range of the animal. The size of the home range 
may vary with sex, possibly age, and season. Population density also may 
influence the size of the home range and cause it to coincide more closely with 
the size of the territory. Home ranges of different individuals may, and do, 
overlap. This area of overlap is neutral range and does not constitute part of 
the more restricted territory of animals possessing this attribute. Home ranges 
are rarely, if ever, in convenient geometric designs. Many home ranges prob- 
ably are somewhat ameboid in outline, and to connect the outlying points gives 
a false impression of the actual area covered. Not only that, it may indicate a 
larger range than really exists. A calculated home range based on trapping 
records, therefore, is no more than a convenient index to size. Overlapping of 
home ranges, based on these calculated areas, thus may at times be exaggerated. 
From trapping records alone, territory may be indicated, if concentrations of 
points of capture segregate out, but it cannot be demonstrated without question. 
If the occupant of an area is in a trap, it is not in a position to defend that area. 
It is only by direct observation that one can be absolutely certain of terri- 
toriality. 

Home range then is the area, usually around a home site, over which the 
animal normally travels in search of food. Territory is the protected part of 
the home range, be it the entire home range or only the nest. Every kind of 
mammal may be said to have a home range, stationary or shifting. Only those 
that protect some part of the home range, by fighting or agressive gestures, from 
others of their kind, during some phase of their lives, may be said to have 
territories. 

SIGNIFICANCE OF BEHAVIORISTIC STUDIES 

I think it will be evident that more critical studies in the behavior of wild ani- 
mals are needed. We are now spending thousands of dollars each year in an 
attempt to manage some of our wild creatures, especially game species. How 
can we manage any species until we know its fundamental behavior pattern? 
What good is there in releasing a thousand animals in an area large enough to 
support but fifty? Each animal must have so much living room in addition to 
other essentials of life. The amount of living room may vary somewhat, but 
for a given species it probably is within certain definable limits. This has all 
been said before by eminent students of wildlife, but many of us learn only by 
repetition. May this serve to drive the point home once more. 



330 



352 JOURNAL OF MAMMALOGY 

LITERATURE CITED 

Blair, W. F. 1940. Home ranges and populations of the meadow vole in southern Michi- 
gan. Jour. Wildlife Management, vol. 4, pp. 149-161, 1 fig. 

1942. Size of home range and notes on the life history of the woodland deer- 
mouse and eastern chipmunk in northern Michigan. Jour. Mamm., vol. 23, 
pp. 27-36, 1 fig. 

Bradt, G. W. 1938. A study of beaver colonies in Michigan. Jour. Mamm., vol. 19, 

pp. 139-162. 
Burt, W. H. 1940. Territorial behavior and populations of some small mammals in 

southern Michigan. Miscl. Publ. Mus. Zool. Univ. Michigan, no. 45, pp. 1-58, 

2 pis., 8 figs., 2 maps. 
Carpenter, C. R. 1942. Societies of monkeys and apes. Biological Symposia, Lan- 
caster: The Jaques Cattell Press, vol. 8, pp. 177-204. 
Clarke, C. H. D. 1939. Some notes on hoarding and territorial behavior of the red 

squirrel Sciurus hudsonicus (Erxleben). Canadian Field Nat., vol. 53, no. 3, 

pp. 42-43. 
Dice, L. R. 1929. A new laboratory cage for small mammals, with notes on methods of 

rearing Peromyscus. Jour. Mamm., vol. 10, pp. 116-124, 2 figs. 
Errington, p. L. 1939. Reactions of muskrat populations to drought. Ecology, vol. 

20, pp. 168-186. 
Evans, L. T. 1938. Cuban field studies on territoriality of the lizard, Anolis sagrei. 

Jour. Comp. Psych., vol. 25, pp. 97-125, 10 figs. 
Gordon, K. 1936. Territorial behavior and social dominance among Sciuridae. Jour. 

Mamm., vol. 17, pp. 171-172. 
Grange, W. B. 1932. Observations on the snowshoe hare, Lepus americanus phaeonotus 

Allen. Jour. Mamm., vol. 13, pp. 1-19, 2 pis. 
Heape, W. 1931. Emigration, migration and nomadism. Cambridge: W. Heffer and 

Son Ltd., pp. xii + 369. 
Hearne, S. 1795. A journey from Prince of Wale's fort in Hudson's Bay, to the Northern 

Ocean. London: A. Strahan and T. Cadell, pp. xliv + 458, illustr. 
Howard, H.E. 1920. Territory in bird life. London: John Murray, pp. xii + 308, illustr. 
Klugh, a. B. 1927. Ecology of the red squirrel. Jour. Mamm., vol. 8, pp. 1-32, 5 pis. 
Lay, D. W. 1942. Ecology of the opossum in eastern Texas. Jour. Mamm., vol. 23, pp. 

147-159, 3 figs. 
Morgan, L. H. 1868. The American beaver and his works. Philadelphia: J. B. Lippin- 

cott and Co., pp. xv + 330, illustr. 
Nice, M. M. 1941. The role of territory in bird life. Amer. Midi. Nat., vol. 26, pp. 

441-487. 
Noble, G. K. 1939. The role of dominance in the life of birds. Auk, vol. 56, pp. 263-273. 
Seton, E. T. 1909. Life-histories of northern animals. An account of the mammals of 

Manitoba. New York City: Charles Scribner's Sons, vol. 1, pp. xxx + 673, 

illustr., vol. 2, pp. xii + 677-1267, illustr. 

1929. Lives of game animals, Doubleday, Doran and Co., Inc., 4 vols., illustr. 

Museum of Zoology, Ann Arbor, Michigan. 



331 



[Rejninted from SCIENCE, N. S., Vol. V., No. 118, 
Pages 541-543, April 2, i597.] 



MIGRATION OF BATS ON CAPE COD, MASSA- 
CHUSETTS. 

Bat migration has received little atten- 
tion. Various writers have made vague 
reference to the fact that certain bats are 
found in winter at localities where they are 
not known to breed, but no detailed ac- 
count of the migratory movements of any 
species has yet been published. The only 
special paper on the subject that I have 
seen is by Dr. C. Hart Merriam,* who 
clearly establishes the fact that two North 
American bats migrate. The data on 
which this conclusion, rests are as follows : 
The hoary bat, one of the migratory species, 
is not known to breed south of the Cana- 
dian fauna. In the Adirondack region it 
appears about the middle of M'ay and dis- 
appears early in October. During the 
autumn and winter it has been taken in South 
Carolina (Georgetown, January 19th), 
Georgia (Savannah, February 6th), and on 
the Bermudasf (' autumn '). As the writer 
remarks, these facts may be fairly regarded 
as conclusive evidence of migration. The 
evidence of the migratory habits of the 
silver-haired bat rests chiefly on the ani- 
mal's periodical appearance in spring aud 
fall at the lighthouse on Mount Desert 
Rock, thirty miles off the coast of Maine. 
This species has also been observed on the 
Bermudas. 

In August and September, 1890 ajid 1891, 
I had the opportunity to watch the appear- 

*Trans. Royal Soc. Canada V (1887), Section V, p. 
85, 1888. 

1 1 may add that I have a bat of this species, killed 
at Brownsville, Texas, on October 22d. 



ance aud disappearance of three species of 
bats at a locality where none could be found 
during the breeding season. Highland 
Light, the place where my observations 
were made, is situated near the edge of one 
of the highest points in the series of steep 
blufts of glacial deposit which form the 
outer side of Cape Cod, Massachusetts. The 
lidit, which is less than ten miles from the 
northern extremity of the cape, is separated 
from the mainland toward the east and 
northeast by from twenty- five to fifty miles 
of water. The bluff on which it stands 
rises abruptly from the beach to a height of 
one hundred and fifty feet. I found the 
bats for the most part flying along the face 
of this bluff, where they fed on the myriads 
of insects blown there by the prevailing 
southwest winds. They chiefly frequented 
the middle and upper heights and seldom 
flew over the beach at the foot of the bluff 
or over the level ground about the light- 
house. I do not know where the animals 
spent the day, as careful search in old 
buildings, under the overhanging edge of 
the bluff, and in deserted bank swallow 
holes, failed to reveal their hiding places. 
It is possible that they found shelter in the 
dense, stunted, oak scrub with which the 
bluff is in many places crowned, but of this 
I have no evidence. I hope that the ob- 
servations given below may again call the 
attention of field naturalists to a subject 
which presents many difficult and interest- 
ing problems. 

Atalapha noveboracensis* (red bat) . 
Augtist 21, 1890. The first bats of the sea- 
son were seen this evening. There were 

*With bat nomenclature in its present unsettled 
state it is well to use the names adopted by Dr. 



332 



only two, and I could not positively identify 
them, but the}'^ were probablj- red bats. 

August 25, 1890. An adult male taken. 

August 28, 1890. Two seen. 

August 29, 1890. The evening was too 
chilly for many bats to be on the wing. A 
few A. noveboracends seen and two taken. 

Aiigust SO, 1890. Six or eight A. novehora- 
censis seen and three taken. The evening 
was warm and bats flew much more freely 
than on the 29th. 

Aiigust 31, 1890. A chill}' evening again, 
and onl}' two bats seen , both A. noveboracen- 

September 2, 1800. A few red bats seen 
and two taken. 

September 5, 1890. I was not at Highland 
Light this evening, but Mr. W. M. Small re- 
ported a heavy flight of bats. He shot five, 
all A. noveboracensis. 

September 8, 1890. Heavy fog, so that no 
bats could be seen, if any were moving along 
the face of the bluff. Three or four red 
bats flew about the light house tower dur- 
ing the first half of the night, feeding 
on insects attracted by the light. They 
flew mostly below the level of the deck 
which encircles the tower about six feet be- 
low the lantern and never approached the 
light itself. 

September 12, 1890. A single red bat shot 
this evening. 

After this date I watched for bats on sev- 
eral consecutive evenings. As I saw no 
more I concluded that the migration had 
ended. 

August 25, 1891. Fourteen Atalapha nove- 
boracensis, the first bats of the season, seen 

Harrison Allen in his latest Monograph of the Bats 
of North America (1893), although many of these 
will require revision. 



this evening. They were flying both north 
and south. 

Augiist 26, 1891. Evening very foggy. A 
red bat which flew about the lighthouse 
was the only one seen. 

August 27, 1891. Half a dozen red bats 
seen and one taken. 

August 28, 1891. Four red bats seen. All 
flew toward the south. 

August SO, 1891. A red bat caught in a 
house near the edge of the bluff. 

September 2, 1891. Eight or ten seen and 
three taken. The movement this evening 
was mostly, though not wholly, from north 
to south. 

September S, 1891. Six seen and three 
tak^n. 

September 5, 1891. Evening cold and 
misty. No bats moving. 

September 7 and 8, 1891. A few bats seen 
each evening, but none taken. All ap- 
peared to be this species. 

September 10, 1891. One red bat shot. 

September 11, 1891. One seen. 

September 12, 1891. One killed. About a 
dozen bats seen, but how many were of this 
species, and how manj^ Lasionycteris nodiva- 
gans T could not determine. 

September IS, 1891. About a dozen bats 
seen. Two of these were certainly red 
bats. 

After this date I watched for bats on con- 
secutive evenings for more than a week. As 
I saw none I finally gave up the search. 

ATALAPHA CINEREA (HOARYBAT). 

August 26, 1890. One Atalapha cinerea, 
the only bat seen, shot this evening. 

August 28, 1890. Two hoary bats taken, 
and at least two, and probably four, others 
seen. 



333 



August 30, 1890. Two taken and two 
others seen. 

September 2, 1890. Only two seen. Both 
taken. 

No more hoary bats seen during 1890. 

Augttst 25, 1891. A single Atalapha cinerea 
seen fljnng south along the face of the bluff 
this evening. 

September 2, 1891. One seen flying north. 

September 12, 1891. An adult male shot — 
the last of the season. 

At Highland Light I found the hoary bat 
less active and irregular in its movements 
than the red bat. Its large and compara- 
tively stead}^ flight made it easier to shoot 
than either of the two smaller species with 
which it was associated. It began to fly 
immediately after sunset. In the Adiron- 
dacks Dr. C. Hart Merriam found the hoary 
bat a late flyer, and an exceeding difficult 
animal to kill on account of its swift, ir- 
regular motions.* It is possible that while 
on Cape Cod the animal modifies its habits 
on account of the unusual surroundings in 
which it finds itself. The fatigue of a long 

* Trans. Linn. Soc New York, II, p. 78-83. 1884. 



migration might also have an appreciable 
effect on a bat's activity. 



lasionycteris noctivagans (silver-haired 

bat). 

September 1, 1890. One silver-haired bat 
taken. 

September 2, 1890. Four taken and per- 
haps a dozen others seen. 

The silver-haired bat was not seen again 
during 1890. 

September 10, 1891. Three shot and prob- 
ably half a dozen others seen. They were 
mostly flying north. 

September 11, 1891. Two shot and four or 
five more seen. 

September 12, 1891. About a dozen bats 
seen. Some were without doubt this species, 
but just what proportion I could not tell. 

While September 12th is' the latest date 

at which I have seen Lasionycteris nodivagans 

at Highland Light, I have a specimen killed 

there by Mr. W. M. Small on October 28, 

1889. 

Gerrit S. Miller, Jr. 



334 



ECOLOGICAL DISTRIBUTION OF SIX SPECIES OF SHREWS AND 
COMPARISON OF SAMPLING METHODS IN THE CENTRAL 

ROCKY MOUNTAINS 

Larry N. Brown 

Abstract. — The ecological distribution of six species of shrews was studied 
using sunken cans in 14 montane and intermontane habitats in southern Wyoming. 
The vagrant shrew ( Sorex vagrans ) and masked shrew ( Sorex cinereiis ) were cos- 
mopolitan in distribution. Sorex cinereus was slightly more abundant in moist plant 
communities, whereas Sorex vagrans predominated in slightly drier communities. 
Merriam's shrew ( Sore.t merriami) occurred only in arid portions of the plains and 
foothills, and in short-grass prairie was the only shrew taken. The water shrew 
(Sorex palustris) occurred only along or near cold mountain streams and ponds. 
The dwarf shrew (Sorex iwmis) and pigmy shrew (Microsorex hotji) occupied re- 
stricted mountain habitats. The dwarf shrew was abundant in rocky locations in 
both alpine and subalpine plant communities; the pigmy shrew was taken only in 
peat-moss bogs in the spruce-fir zone. A comparison of snap traps and sunken 
cans as methods of collecting shrews revealed that snap traps failed to demonstrate 
the presence of Sorex nanus and Microsorex hoyi in areas where they were abun- 
dant. Also, densities of Sorex vagrans and Sorex cinereus indicated by snap traps 
were considerably below those indicated by sunken cans. 

The habitat preferences and ecological distribution of the six species of 
shrews found in the Central Rocky Mountains have not been extensively stud- 
ied. Only scattered references to the ecological distribution of shrews in the 
Rocky Mountains occur in the literature (Gary, 1911; Warren, 1942; Negas and 
Findley, 1959; and Spencer and Pettus, 1966). No thorough study dealing with 
Wyoming shrews has been reported. 

The species studied were the masked shrew (Sorex cinereus), the vagrant 
shrew (Sorex vagrans), the dwarf shrew (Sorex nanus), the Merriam's shrew 
(Sorex merriami), the water shrew (Sorex palustris), and the pigmy shrew 
(Microsorex hoyi). Information was collected on the ecological distribution 
of these species in southern Wyoming in terms of type of plant cover and prox- 
imity of water. Data on the indicated abundance of shrews using two different 
trapping methods were also compiled. 

Materials and Methods 

The Medicine Bow Mountains and Laramie Basin area of southern Wyoming have a wide 
range of plant communities, which occur at altitudes of from 7000 to 12,000 ft. The eight 
montane and intermontane plant communities selected for sampling were cottonwood-wil- 
low, short-grass prairie, sagebrush, mountain mahogany, aspen, lodgepole pine, spruce-fir 
and alpine tundra. Brief descriptions of the sampled areas in Albany County, Wyoming, 
are as follows: 

1. Cottonwood-willotc. — 7160 ft; 10 miles SW Laramie, along Big Laramie River. Dom- 
inants: Populus angustifolia, Salix sp. Several grasses (Poa, Agropijron, Carex) present in 
understory. 

617 



335 



618 JOURNAL OF MAMMALOGY Vol. 48, No. 4 

2. Short-firass prairie. — 7180 ft; V2 mile E Laramie. Dominants: Boiiteloiia gracilis, 
Buchloe dactijloides. Numerous forbs {Eriogoniim, Gaitra, Phlox) also represented. 

3. Sagebrush. — 7220 ft; 20 miles N Laramie. Dominants: Artemisia Iridentata, Purshia 
tridentaia. Several grasses ( Poa, Koeleria, and Agropijrorx ) abundant in open spaces be- 
tween shrubs. 

4. Mountain mahogany. — 7250 ft; 1 mile E Laramie. Dominant: Cercocarpus montanus. 
Present: Symphoricarpos, Artemisia, Amelanchier, as well as several grasses and forbs. 

5. Aspen. — 8205 ft; % mile NW Centennial. Dominant: Populus tremuloides. A dense 
understory of grasses (Poa, Agropyron) and scattered shrubs {Acer, Rosa, and Berberis). 

6. Lodgepole pine. — 9300 ft; 5 miles VV Centennial. Dominant: Pinus contorta. Under- 
story of scattered forbs (Lupinus, Antennaria, etc.) and small trees (Abies, Juniperus, and 
Picea ) . 

7. Spruce-fir. — 9630 ft; 7 miles W Centennial. Dominants: Picea engelmanni, Abies 
lasiocarpa. Several shrubs (Ribes, Rosa, Vaccinium, Berberis) common in understory. 

8. Alpine tundra. — 10,470 ft; 5 miles W University of Wyoming Science Camp. Domi- 
nants: Artemisia scopulorum, Silene acaulis, Poa alpina, Trifolium sp., Salix sp. 

A more detailed description of most communities in the Front Range of the Rocky Moun- 
tains is found in Marr (1961). 

Moist bogs or marshes interrupted the uniformity of four of the above plant communities, 
specifically the aspen, lodgepole pine, spruce-fir, and alpine tundra. Therefore, to compare 
shrew populations in adjacent wet and dry situations, a bog or marsh near each original 
sampling station was trapped (sampling sites were 500-1000 ft apart). Brief descriptions 
of these wet plant communities are as follows: 

1. Bog in alpine tundra. — 10,460 ft; 5 miles W University of Wyoming Summer Science 
Camp. Dominants: sedges (Carex .sp.), dwarfed willows (Salix sp.) around small, shallow 
pond. 

2. Bog in spruce-fir. — 9620 ft; 7 miles W Centennial. Dominants: sedges (Carex sp.), 
horsetails (Equisetum sp.), willows (Salix sp.), sphagnum moss (Sphagnum sp. ). 

3. Bog in lodgepole pine. — 9295 ft; 5 miles W Centennial. Dominants: willow (Salix 
sp.), alder (Alnus tenuifolia), sedges (Carex sp. ). Small pond of open water at edge of bog. 

4. Bog in aspen. — 8200 ft; % mile W Centennial. Dominants: willow (Salix sp. ), alder 
(Alnus tenuifolia), aspen (Populus tremuloides) , sedges (Carex sp.), horsetails (Equisetum 
sp.). Two beaver ponds adjacent to the area. 

To check the preference of certain shrews for rocky areas, two e.xtensive rockslides were 
sampled at different elevations. One of these was a subalpine rockslide at 8480 ft elevation 
(3 miles NW Centennial) in an ecotone area of lodgepole pine, aspen, and sagebrush. The 
other trapping station was in a vast alpine rockslide above tree line at 10,600 ft elevation. 
Thus, 14 locations were sampled. 

Shrews were trapped in pit-fall traps made of one-gallon tin cans. These were buried in 
the ground with the mouth of each can just below the ground's surface. A grid with an 
interval of 30 ft was used in placing these traps. Each sampling plot consisted of 25 cans 
arranged in five rows having five cans each. 

In areas with a high water table, it was necessary to punch holes in the bottom or sides 
of each can. This allowed water to enter the can to equalize pressure and prevent the can 
from lieing forced up out of the ground. To catch shrews in such localities, it was desirable 
that the top of the water table ])e at least' an inch or so below ground surface. High water 
tables in several bogs required that cans be placed on a slight elevation or hummock nearest 
each grid intersect. 

The sinking of cans in rockslides was accomplished by removing rocks by hand until a 
pit into the interior of the slide was created. Wedged rocks and large lioulders usually 
limited the depth of each excavation to three to five feet. Each can was then placed at the 
deepest point and fist-sized rocks were used to rebuild the sulistrate almost up to the lip of 



336 



November 1967 BROWN— ECOLOGICAL DISTRIBUTION OF SHREWS 



619 




Fig. 1. — Diagrammatic representation of placement of pitfall traps (gallon cans) in study 
of rockslide habitats in mountain locations. 

the can. Then gravel was used to build a pavement to the lip of the can (Fig. 1). If only 
larger, fist-sized rocks were placed around each can, sufficient spaces remained adjacent to 
the mouth to constitute a barrier for access by the shrews. 

Between .30 May and .3 June 1966, 350 can traps were set out at the 14 locations. Cans 
were checked on alternate days for slightly more than 3 months. The total number of shrews 
by .species taken per habitat was determined for the total sampling period. 

In September 1966, a direct comparison of two methods of collecting shrews was made 
involving standard mouse-sized snap traps and the sunken cans. A snap trap was baited 
and set adjacent to each can in the sampling grid of the subalpine rockslide and the spruce- 
fir bog. Both sets of traps were checked once daily for 12 days. The bait for the snap traps 
consisted of a mi.xture of peanut butter, bacon grease, rolled oats, and chopped raisins. 

Results and Discussion 

Following the placement of cans in various plant communities no shrews 
were captured in any plot for a period of 10 to 14 days. After this period, 
shrews appeared in the cans with regularity throughout the remainder of the 
summer; this suggested that all shrews avoided the areas where cans were 
placed until they became accustomed to the change. 

Table 1 summarizes the relative abundance of five species of shrews at the 
various sampling stations. The masked shrew (Sorex cinereus) and vagrant 
shrew (Sorex va^rans) were the most cosmopolitan in distribution, being rep- 
resented in all the habitats sampled except short-grass prairie. These species 
were always taken together, but in varying densities that appeared to correlate 
with moisture conditions. Sorex cinereus was generally more abundant than S. 
va^rans in the moist bog localities regardless of altitude. Sorex va^ran.s had 



337 



620 



JOURNAL OF MAMMALOGY 



Vol. 4H, No. 4 



Tahle L — Ecological cllstrihuiion and relative abundance of five species of shrews in rela- 
tion to varions habitats in the Medicine Bow Mountains and Laramie Basin of Wyoming, 

summer 1966. 















Micro- 








Sorcx 


Sorcx 


Sorcx 


Sorcx 


sorex 


Total 


Habitat and ele\ 


ition 


cincrciis 


vagrans 


nanus 


mcrriami 


hoyi 


collected 


Cottoiiwood-willow 


(7160) 


2 


14 











16 


Short-grass prairie 


(7180) 











3 





3 


Sagel:)nish 


( 7220 ) 


4 


11 





3 





18 


Mountain mahogany 


( 7250 ) 


2 


6 





2 





10 


Aspen 


( 8205 ) 


5 


16 











21 


Bog in aspen 


( 8200 ) 


28 


12 











40 


Snbalpine rockshde 


(8480) 


11 


20 


25 








56 


Lodgepole pine 


( 9300 ) 


6 


16 











22 


Bog in lodgepole 


( 9295 ) 


29 


11 











40 


Spruce-fir 


( 9630 ) 


8 


18 











26 


Bog in spruce-fir 


( 9620 ) 


32 


15 








6 


53 


Alpine tundra 


(10,470) 


4 


8 


2 








14 


Alpine willow bog 


(10,460) 


9 


5 











14 


Alpine rockslide 


(10,600) 


3 


9 


21 








33 



higher population densities in the mesic communities that were paired with 
the bogs (aspen, lodgepole pine, spruce-fir, and alpine tundra). The vagrant 
shrew was likewise slightly more abundant than S. cinereus in the other mesic 
situations sampled such as rockslides, sagebrush, mountain mahogany, and cot- 
tonwood-willow communities. These findings are in disagreement with those 
of Clothier (1955), who reported that S. vafirans was always more numerous 
in Montana than S. cinereus regardless of habitat. My results confirm the find- 
ings of Getz (1961) that S. cinereus is abundant in moist or standing-water 
situations, and the findings of Hoffmann and Taber (1960) that S. vagrans is 
present at high altitudes as well as low. 

The dwarf shrew, which is generally considered by mammalogists to be rare, 
was abundant in two restricted habitats and was present at a third. It was 
more numerous than S. vagrans by a slight margin (25 S. nanus as compared 
to 20 S. vagrans) in the subalpine rockslide and was by far the predominant 
shrew in the alpine rockslide (21 animals out of 33). Sorcx nanus was also rep- 
resented in the alpine tundra plot by two animals taken near a rock outcrop. 
This represents an altitudinal range extending from 8480 to 10,600 ft and in- 
cluding several types of montane plant communities. Since rockslides extend 
continuously from 10,600 to 12,000 ft in the Medicine Bow Range, there is little 
doubt the species reaches that altitude in this habitat. All dwarf shrews were 
captured at considerable distances from water, suggesting they may be some- 
what adapted to dry situations. 

The preference of S. nanus for rocky areas in the mountains was first sug- 
gested by Hoffmann and Taber (1960), who collected several in polygonal rock 
fields on the Beartooth Plateau. They have been recorded in a variety of other 



338 



Novetnber 1967 BROWN— ECOLOCIICAL DISTRIBUTION OF SHREWS 621 

montane habitats by Schellbach (1948), Clothier (1957), and Bradshaw (1961). 
Spencer and Pettus (1966) reported S. nanus was abundant in an open clear- 
cut area of spruce-fir forest. They did not mention the presence or absence of 
rocks. 

Sorcx merriami was trapped in three plant communities that were repre- 
sented only at lower elevations in southern Wyoming. These habitats were 
short-grass prairie, sagebrush, and mountain mahogany. None of these habi- 
tats occurred higher than the mountain foothills ( 7500 ft ) . These three plots 
produced onl\ eight Merriam's shrews for the whole summer, indicating that 
population levels in the areas sampled were not high. In the short-grass prairie 
plot, S. merriami was the only species of shrew present; in the low foothills, 
where sagebrush and mountain mahogany communities were sampled, they 
were present in low numbers with S. vagrans and S. cinercus. The only Mer- 
riam's shrew previously taken in southeastern Wyoming was reported by 
Mickey and Steele (1947), from short-grass prairie near Laramie. In W^ash- 
ington, Johnson and Clanton ( 1954 ) found that this species preferred the sage- 
brush-bunch grass community, where individuals were taken in the tunnels of 
the sagebrush vole (Laounis curtatus). Hoffmann (1955) likewise collected 
S. merriami in sagebrush in California. One of the few records of occurrence 
of the species in mountain mahogany was that of Hoffmeister ( 1956 ) in Owl 
Creek Canyon in northeastern Colorado, about 40 miles south of the present 
study area. 

In southeastern Wyoming, S. merriami occurred in the driest habitats and 
generally at lower elevations than did other species. Merriam's shrew was 
taken with Lagurus curtatus in the sagebrush and short-grass prairie area, but 
this vole was absent from the mountain mahogany community. 

The pigmy shrew (Microsorex hoiji) was not known to occur in Wyoming 
until it was taken in 1963 in the Medicine Bow Range ( Brown, 1966 ) . A dis- 
junct population occurs in southern Wyoming and adjacent northern Colorado 
and is more than 500 miles south of the nearest locality in Montana where the 
species has been reported (Hall and Kelson, 1959). In the course of the pres- 
ent study, pigmy shrews were captured at one sampling station, in the spruce- 
fir bog at 9620 ft elevation. Here Microsorex was encountered only around the 
periphery of the bog in an area dominated by a deep, spongy mat of sphagnum 
moss. In the strip of sphagnum, they were taken in equal numbers with S. 
cinereiis and in greater numbers than S. vagrans. Spencer and Pettus (1966), 
in their study of a single bog area west of Fort Collins, Colorado, reported that 
the pigmy shrew was most abundant in the transition area between the bog 
and the surrounding spruce-fir forest. This is in agreement with my findings. 

The habitat preferences of Microsorex in the other parts of its range seem to 
be rather broad, including heavy woods, clearings, and pastures in both wet 
and dry situations (Burt, 1957). However, Jackson (1961) and Buchner (1966) 
noted that in Wisconsin and Canada the species occasionally is found in cold 
sphagnum or tamarack bogs. In the MacDonald Range of northwestern Mon- 



339 



(y22 journal of MAMMALOGY Vol. 48, No. 4 

Taisle 2. — Comparison of trap])ii\<^ results for .shrews ii.sinfi .snap traps and .sunken cans for 
12 days at two location.s in the Medicine Bow Mountains, Wtjoniin^. 

Subalpine rockslide Spruce-fir bog 



Species 


Snap tr 


aps 


Sunken 


cans 


Snap traps 


Sunken cans 


Horex vapran.s 


2 




4 




2 


3 


Sorex cinereu.s 


1 




2 




4 


9 


Sorcx nanus 







6 










Microsorex hoiji 















2 


Totals 


3 




12 




6 


14 



tana, Conaway (personal communication) captured Microsorex in dry areas of 
clearcut forest having a dense ground cover. The relict population located in 
the central Rockies may have a broader habitat specificity than indicated by 
the present study. 

The water shrew {Sorcx palustris) is too large to be retained in gallon cans 
unless there is some water present. Water shrews were taken in partially 
flooded cans in habitats ranging from the alpine willow bog at 10,470 ft eleva- 
tion down to the willow-alder bog in the aspen community at 8200 ft elevation. 
The species was never trapped at a distance greater than 100 ft from a moun- 
tain stream or pond. 

The total samples of shrews at each location were compared, and two types 
of habitats were found to support especially high densities of shrews. The most 
productive habitats were rockslide areas and marshy or boggy areas, both of 
which have high invertebrate populations that can serve as a readily available 
food supply. The least productive trapping plot for shrews was located in short- 
grass prairie. This may have been due to the scarcity of suitable cover or to 
a relative scarcity of invertebrates. 

A comparison of the number and species of shrews collected utilizing equal 
numbers of snap traps and cans is presented in Table 2. In 300 trap-nights us- 
ing snap traps, three shrews of two species were collected at the subalpine rock 
slide. The sunken cans produced four times as many shrews during the same 
period and three species were represented. Six S. tmnus were taken in cans 
while none appeared in adjacent snap traps, suggesting that the species readily 
avoids traps and therefore gives the appearance of being rare. 

Twenty-five sunken cans produced slightly more than twice as many shrews 
( 14 animals) than did 25 snap traps (six animals) in the bog in the spruce-fir 
community during the 12-day period. Again, S. vagrans and S. cinereus were 
taken in both snap traps and cans, but Microsorex was captured only in cans. 
Even for the two "common" species, higher numbers were recorded for the 
can traps. 

These and other trapping results indicate that S. nanus, S. merriami, and 
Microsorex hoiji are seldom captured in snap traps even when all are abun- 
dant. Sorex vagrans, S. cinereus, and S. palustris were readily captured in snap 
traps, but data provided by pitfall traps suggest that densities calculated for 



340 



Xoinnhcr /.967 BHOWN— ECOI .OCICAL DISTRIBl'TION OK SUKEWS 62:3 

tlit'se species on the basis ot snap-trap catches ma\ l)e consistently too low. 
MacLeod and Lethiecq (1963) presented similar data when comparing these 
trapping methods for S. cinereus in Newfoundland. 

ACKNOWLEDCMENTS 

I wisli to thank tlie following students who helped with colleetiiiK the shrews: James 
Bradley, Robert CiiKj-Mars, Ronald Lynde, Paul Lussow, Mar\in Maxell, and Richard Mc- 
(luire. 

Literature Cited 

Bradshaw, C. \. R. 1961. New Arizona localit\ for the dwarf shrew. J. Manini., 42: 96. 

Rhown. L. X. 1966. First record of the pigmy shrew in Wyoming and description of a 
new subspecies (Mammalia: InsectiNora ). Proc. Biol. Soc. Washington, 79: 
49-51. 

BucKNEH, C. H. 1966. Populations and ecological relationship.s of shrews in tamarack 
Iiogs of southeastern Manitoba. J. Mamm., 47: 181-194. 

BiHi, W. 11. 1957. Mammals of the Clreat Lakes Region. Uni\. Michigan Press, .Ann 
.Arbor, \\ + 246 pp. 

Gary, .M. 1911. A biological surve\ of Colorado. \. Amer. P'auna, 33: 1-256. 

Clothieh, R. R. 1955. Contribution to the life history of So/c.r vagrans in Montana. J. 
Mamm., 36: 214-221. 

. 1957. .\ second dwarf shrew from \ew Mexico. J. Mamm., 38: 256. 

C.ETZ, L. L. 1961. Factors influencing the local distribution of shrews. Amer. Midland 
Nat., 65: 67-88. 

Hall, E. R., and K. R. Kelson. 1959. The mammals of North America. The Ronald 
Press, New York, 1: xxx + 546 + 79. 

Hoffmann, R. S. 1955. Merriam shrew in California, j. Mamm., 36: 561. 

Hoffmann, R. S., and R. D. Taueh. 1960. Notes on Suicx in the Northern RocIcn Moun- 
tain alpine zone. J. Mamm., 41: 230-234. 

HoFFMEisTER, D. F. 1956. A record of ^orex merriami from northeastern Colorado. J. 
Mamm., 37: 276. 

Jackson, H. H. T. 1961. Mammals of Wisconsin. Uni\-. Wisconsin Press, Madison, xii 
+ 504 pp. 

Johnson, M. L., and C. W. Clanton. 1954. Natural history of Sorex merriami in Wash- 
ington State. Murrelet, 35: 1—1. 

MacLeod, C. F., and J. L. Lethiecq. 1963. A comparison of two trapping procedures 
for Sorex cinereus. J. Mamm., 44: 277-278. 

NLahk, J. 1961. Ecosystems of the east slope of the Front Range in Colorado. L'niv. Colo- 
rado Stud. Biol., 8: 1-134. 

Mickey, A. B., and C. N. Steele, Jh. 1947. A record of Sorex merriami merriami for 
.southeastern Wyoming. J. Mamm., 28: 293. 

Negus, iX. C, and J. S. Flndley. 1959. Mammals of Jackson Hole, Wyoming. J. Mamm., 
40: .371-381. 

ScHELLB.\CH, L., HI. 1948. A record of the shrew Sorex luiiius for Arizona. J. Mamm., 
29: 295. 

Spenceh, A. W., AND D. Pettus. 1966. Habitat preferences of fi\e sympatric species of 
long-tailed shrews. Ecology, 47: 677-683. 

Warhen, E. R. 1942. The mammals of Colorado. . . . l'ni\ . Oklahoma Press, x\ iii + 
330 pp. 

Department of Zoology and Physiology, University of Wyoming, Laramie {present ad- 
dress: Department of Zoology, University of Sonthern Florida. Tampa). Accepted 1 Sep- 
tember 1967. 



341 



378 



Journal of Wildlife Management, Vol. 20, No. 4, October 1956 



CHANGES IN NORWAY RAT POPULATIONS INDUCED 
BY INTRODUCTION OF RATS 

David E. Davis and John J. Christian 

Division of Vertebrate Ecology, Johns Hopkins School of Hygiene and Pubhc Health, Baltimore 5; Naval 

Medical Research Institute, Bethesda, Maryland 



The introduction of aliens into an existing 
population of mammals may be followed 
by unexpected effects that relate to social 
structure and population composition. These 
effects were studied by introducing alien 
rats into stationary and increasing popula- 
tions of rats in city blocks. This work is part 
of a continuing study of the mechanisms of 
change in vertebrate populations using Nor- 
way rats ( Rattus norvegicus ) in residential 
areas in Baltimore as experimental animals 
(Davis, 1953). These rats inhabit back yards, 
basements, and garages and feed on garbage. 
The human sanitary conditions in general 
are poor and remain unchanged for months 
at a time, so that the food supply of the rats 
has only slight seasonal variations. Other 
environmental conditions are similarly sub- 
ject to little change for many months at a 
time. The constancy of these factors permits 



Methods and Procedures 

The procedures followed to study the ef- 
fects of introducing strange rats into a popu- 
lation consisted of taking some rats from a 
stationary or increasing population in one 
block and introducing them into a compara- 
ble population in another block and observ- 
ing the resulting changes in the second pop- 
ulation. The status (stationary or increasing) 
of the population was determined by esti- 
mates at bimonthly intervals for more than 
a year. Blocks that appeared to be either 
stationary or increasing were selected in 
October and monthly estimates made. From 
this group 4 stationary and 4 increasing pop- 
ulations were chosen. To get a base line for 
adrenal weights, six rats of one sex, weighing 
over 200 grams each, were removed from 
each block during the first experimental 
week ( week 1 ) . Alien rats were then intro- 



experiments on populations in a relatively duced into each block during the third week, 

stable environment. Finally, the population and at the same time native rats were re- 

of rats in each block is essentially discrete moved from the increasing populations. The 

and isolated, as rats rarely travel from one details of these removals and introductions 

block to another ( see Davis, 1953, for refer- are contained in tables 2 and 3. Estimates 

ences). were made during the sixth and eighth 

342 



' 



Changes in Rat Populations — Davis and Christian 



379 



weeks, each followed by the removal of a 
small sample of rats for adrenal weights. 
The adrenal weights were expressed for each 
sample as the mean per cent of standard 
reference values (Christian and Davis, 1955). 
The rats to be introduced into a population 
were indi\'idually marked by toe-clipping 
prior to introduction, whereas the native rats 
were not marked. The details of the history 
of each population were complicated by the 
impossibility of introducing exactly the same 
number of rats into each block on exactly 
the same days, and the numerical popula- 
tion size also differed in each block. 

A discussion of the likelihood of error is 
desirable when it is claimed that two popu- 
lations differ in number, since the detection 
of changes is fundamental to the conclusions 
derived from these introductions. Some as- 
pects of the census method were discussed 
by Brown, et al. ( 1955 ) . However, the basic 
problem is that, even witli trapping, the true 
number of rats in a block is not known. 
Nevertheless, a check on the validity of esti- 
mation can be made by comparing estimates 
before and after a trapping program. Sup- 
pose that an estimate of Nj rats is first ob- 
tained, subsequently T rats are removed 
and a second estimate of No rats is made. 
Obviously N^ should equal T + No. A 
figure for percentage of error can be given as 
Ni-(T + N,). 



Table 1. - 


- Distribution 


OF Differences Among 






Estimates 








r" 


Blocks 






Per cent Erro 


Positive 




Negative 


Total 


0-9 




13 




6 


19 


10-19 




6 




11 


17 


20-29 




4 




4 


8 


30-39 




2 




3 


5 


40-49 




1 







1 


Totals 




26 




24 


50 


» Ni - 


(T + 


No) 









N, 



For example, if the estimate 



for a block is 151 rats and then 81 are re- 
moved by trapping and an estimate of 63 

is made, then ^ti — 4.6 per 

cent. Other procedures could be used such as 

^-(^j-N') or N- -^y_-/- The first 

procedure is preferred because it bases the 
calculations on N^, which is the estimate that 
was used to determine the status of the 
block. A total of 50 populations was avail- 
able to determine the extent of error. Each 
had been trapped during the past 6 years, 
and an estimate had been made before trap- 
ping and another within a month after ces- 
sation of trapping. Naturally, some changes 
can occur during the intervening month, but 
for practical reasons it is usually not possible 
to make an estimate promptly after the ces- 
sation of trapping. These blocks contained 
3,707 rats by the estimates (NJ and 1,502 
were trapped. The number of rats per block 



Ni 



varied from 15 to 182. The distribution of 
errors is given in Table 1. The percentage 
of error was independent of the number of 
rats in the population. From these differ- 
ences the standard error of the difference 
can be calculated to be 10.7 per cent. This 
value can be used as an indication of the 
errors to be expected in estimates of popula- 
tion changes in blocks. For example, from 
Table 2 it is seen that the estimate (block 
150128) before introduction was 116 and 
after was 89. The percentage difference is 
23.3 which when divided by 10.7 gives a 
ratio of 2.2. This difference appears to be 
statistically significant. 

Results and Discussion 

The histories of the populations are given 
by blocks in tables 2 and 3 and figures 1, 2, 
and 3. The terms "replacement" and "sup- 
plement" require clarification for this dis- 
cussion. We mean by replacement that ap- 
proximately the same number of rats was 
introduced as was removed. Supplement 
means that many more alien rats were intro- 
duced than were removed. A quantitative 
percentage might have been used to dis- 
tinguish these two terms, but it would have 
been rather meaningless because ( 1 ) the 
size of the individual rats varies consider- 
ably, and (2) immediate mortality is prob- 
ably high. Therefore, we really do not know 
the actual number of rats that produced the 
results. Another factor is that births and 
deaths are normally high in any population 
of rats. The average monthly death rate is 
about 20 per cent for stationary rat popula- 
tions; therefore, their birth rate is also about 
20 per cent. Comparable mortality and birth 
rates for increasing populations are prob- 



343 



380 Journal of Wildlife Management, Vol. 20, No. 4, October 1956 

Table 2. — Results of Introduction of Rats into Stationary Populations 



Block number 

Zero week is 


140338 
Dec. 16 


140344 
Dec. 16 


140118 
Feb. 9 


150128 
Feb. 9 











Week 


Rats 


w 


R 


w 


R 


w 


R 


Population 


-20 


62 


-20 


30 


-19 


105 


-18 


122 


Population 


-13 


42 


-13 


32 


-11 


98 


-10 


118 


Population 


- 5 


40 


- 5 


38 


- 6 


87 


- 6 


120 


Population 





49 





35 





100 





116 


Rats removed 


1 


6M 


1 


6F 


1 


6F 


1 


6M 


Rats introduced 


3 


lOM 


3 


8F 


2-6 


23F 


2-6 


27M 


Rats removed 


— 


— 


— 


— 


— 


— 


— 


— 


Population 


6 


45 


6 


44 


6 


76 


7 


89 


Rats removed 


6 


6M 


6 


6F 


6 


6F 


7 


6M 


Population 


8 


56 


8 


23 


11 


63 


10 


86 


Rats removed 


8 


22 


8 


12 


11 


27 


10 


36 




Week 


Indexi 


w 


I 


w 


1 


w 


1 




1 


83.0 


1 


91.8 


1 


93.4 


1 


79.2 


Adrenal size 


6 


84.1 


6 


85.3 


6 


90.4 


7 


71.4 




8 


88.0 


8 


102.4 


11 


68.4 


10 


73.6 


1 Mean of the individual 


per cent of appropriate reference value for the sex 


and size 


of the rat. 






ablv about 15 per c 


ent and 25 


per cent ] 


Der 






STATIONARY 







month respectively. It is unwise, under these 
circumstances, to attempt a precise measure- 
ment of numerical differences in the num- 
bers of rats used. 

The population estimates (Table 2) in 
the two replacement blocks 6 weeks after 
the introduction of rats showed ( Fig. 1 ) that 
block 140338 was not significantly different 
from the previous estimate, while block 
140344 had apparently increased ( P is about 
.04). While the apparent difference in re- 
sults in these 2 blocks might be due to sex 
( the females less disturbing ) or to numbers 
(fewer introduced into 140344), no inter- 
pretation will be attempted for the reasons 
cited above. The two supplemented blocks 
declined significantly (P is about .04 for 
each) (Fig. 1). 

We recognize that the replacement pair of 
populations was done in December 1953, 
and the supplemented pair in February 1954, 
and that differences might be due to some 
seasonal aspect. However, the only known 
seasonal change, an increase in breeding 
from December to February, would produce 
the opposite result. 

Population growth ceased in all four in- 
creasing populations following the replace- 
ment of native with alien rats (figs. 2, 3,). 
In no block was the difference statistically 
significant. It apparently made no differ- 
ence whether the sex of the introduced rats 




Fig. 1. The changes in four stationary populations 
for 20 weeks before introduction of rats ( at time ) 
and about 10 weeks after. The number added is 
indicated by a plus sign, the number removed by 
a minus sign. 



344 



Changes in Rat Populations — Davis and Christian 
Table 3. — Results of Introduction of Rats into Increasing Populations 



381 



1 Block number 


140111 


140134 


140201 


140222 


Zero week is 


. . Dec 


16 


Dec 


. 16 


Feb 


9 


Feb 


9 








Week 


Rats 


W 


R 


W 


R 


w 


R 


Population 


-20 


110 


-20 


80 


-25 


86 


-20 


57 


Population 


-13 


118 


-13 


88 


-16 


100 


-14 


62 


Population 


- 5 


133 


- 4 


115 


- 8 


105 


- 5 


95 


Population 





150 





140 





135 





90 


Rats removed 


1 


6F 


1 


6F 


1 


6M 


1 


6M 


Rats introduced 


3 


22F 


3 


28F 


3 


18M 


3 


20M 


Rats removed 


3 


28F 


3 


22F 


3 


20M 


3 


ISM 


Population 


6 


167 


6 


130 


6 


130 


6 


85 


Rats removed 


7 


6F 


7 


6F 


7 


6M 


7 


6M 


Population 


10 


152 


10 


130 


10 


130 


10 


70 


Rats removed 


10 


48 


10 


73 


10 


57 


10 


24 




Week 


Indexi 


W 


I 


w 


I 


w 


I 




1 


92.1 


1 


91.5 


1 


104.4 


1 


93.8 


Adrenal size 


7 


93.8 




102.8 


7 


85.3 


7 


99.1 




10 


101.5 


10 


90.4 


10 


91.1 


10 


84.6 



1 Mean of the individual per cent of appropriate reference value for the sex and size of the rat. 



was male or female. The population from 
block 140222 (Fig. 2) may have become 
stationary just prior to the introduction of 
aliens, but the high rate of reproduction ( 4/6 
mature females were pregnant) suggests that 
the population was increasing. The popula- 
tion in block 140111 increased numerically 
after the introduction, but the difference be- 
tween the two estimates is within the error 
of estimate and does not indicate a change 
in population. It appears that introducing a 
number of alien rats may halt the growth of 
increasing populations. 

The reader may have noticed that the total 
number of rats removed from the four in- 
creasing blocks was about 5 per cent greater 
than the number introduced, so that the rats 
in these populations were not replaced in the 
strict arithmetic sense of the word. However, 
considering the previously mentioned birth 
and mortality factors, it is not desirable to 
be more precise. All aspects considered, it 
is likely that the four increasing populations 
were somewhat reduced following replace- 
ment procedures. The four blocks (taken 
together) increased by 173 rats in the 20 
weeks preceding replacement, so that they 
might have been expected to have had 600 
rats 10 weeks after replacement instead of 
the observed 482, although the rate of in- 
crease would decline as the population in- 
creased. 

On several occasions episodes have been 
noted that appear to be explainable on the 



Q. 
O 
Q. 



< 

tr. 



150 



125 



100- 



75 



50 



25 







MALES 



_L 



-30 



•20 




-t — • 



-10 
WEEKS 



10 



Fig. 2. The changes in two increasing blocks before 

and after the introduction of males (symbols as in 

Fig. 1.) 

basis of introduction or actual immigration. 
In January 1946, about 60 rats were released 
in a block in one night as part of an experi- 



345 



382 



Journal of Wildlife Management, Vol. 20, No. 4, October 1956 



I75r 



150 



125 



100 

z 
o 

!5 

^75 

Q. 

o 

Ql 



< 

DC 



50 



25 



-6 




+22 

-28 / \ 
/ \ 

/ \ 



+ 28 
22 



FEMALES 



^x ^X 



-30 



-20 



-10 
WEEKS 



10 



Fig. 3. The changes in two increasing blocks before 

and after the introduction of females ( symbols as in 

Fig. 1.) 

ment on "homing" ability in rats. The block 
originally contained about 100 rats but with- 
in 3 weeks there were so few rats left in the 
block that the project was stopped. Calhoun 
( 1948 ) noticed the same result when he in- 
troduced rats into blocks. These episodes, 
as well as miscellaneous observations, stim- 
ulated a test in 1947 of the idea that the in- 
troduction of rats into a population would 
result in its decline. Accordingly, rats were 
introduced over a period of 4 months into 
two populations that had just reached a level 
judged to be stationary (Davis, 1949). The 
introduction of 90 rats in one block and 101 
in the other was accompanied by declines of 
about 25 per cent and of 40 per cent respec- 
tively. The populations increased after the 
introductions ended. 

The present experiments suggest that the 
introduction of large numbers of rats into 
a population disrupts the population mech- 



anisms in some way that causes the popula- 
tions either to decline in numbers or stop 
growing. 

The decrease is due in part to a decline in 
reproduction. Data are not available for the 
period immediately after introduction, as it is 
not feasible to follow the population changes 
and simultaneously to collect a number of 
rats for reproductive data. However, the 
large sample of rats collected from the blocks 
8 to 11 weeks after introduction had a high 
reproductive rate ( Table 4 ) and a low lacta- 
tion rate. One would conclude from these 
data that the number of pregnancies was 
low immediately after the introduction. Only 
about 25 per cent of the females were lacta- 
ting at 10 weeks, whereas normally about 
40 per cent of the females of these rats are 
lactating (Davis, 1953). The high preva- 
lence of pregnancy presumably resulted 
from their more or less simultaneous re- 
covery from the effects of introduction. The 
decreases in rat populations obviously may 
have been due largely to mortality and move- 
ment, but data on this aspect are impossible 
to obtain under these conditions. 

Table 4. — Reproductive Records of Local Rats 
Captured 8-11 Weeks after Artificial Immi- 
gration of Rats into Blocks 



Number Mean 

Population Mature Per cent Number Per cent 

status Females Pregnant Embryos Lactating 



Increasing 
Stationary 



85 
66 



33.0 

31.8 



10.38 
9.63 



20.0 
28.8 



Previous experiments have shown that the 
weight of the adrenal glands in rats responds 
to changes in population. An increase in 
adrenal weight parallels increases in popu- 
lation; the artificial reduction of a popula- 
tion also results in a decrease in adrenal 
weight (Christian, 1954; Christian and Davis, 
1955). The adrenal responses of the two 
sexes are parallel ( ibid. ) . Experiments have 
indicated that changes in adrenal weight in 
response to changes in population result 
primarily from changes in cortical mass 
( Christian, 1955a, 1955b, 1956 ) . To examine 
these problems, the adrenals of the rats from 
each block were removed and weighed. The 
observed adrenal weight for each rat was 
compared with a standard reference weight 
for the appropriate sex and size (length of 
head and body ) of rat ( Christian and Davis, 



346 



Changes in Rat Populations — Davis and Christian 



383 



1955), and expressed as a per cent of the 
reference value. These percentages for the 
rats from each sample were averaged and 
the means are recorded at the bottom of 
tables 2 and 3. We have used the mean value 
of a given sample as the unit of measurement 
for comparing adrenal weight with popula- 
tion size (Christian, 1954; Christian and 
Davis, 1955). 

The results indicate that, in the replace- 
ment stationary blocks (140338 and 140344), 
there was a small increase in adrenal weight 
after 8 weeks, while the populations appar- 
ently remained practically unchanged (ta- 
bles 2 and 3, Fig. 1 ) . 

A mean decline in population size, par- 
alleled by a decrease in adrenal weight in 
at least one of the two blocks, followed the 
addition of a large number of alien rats to 
stationary populations (blocks 140118 and 
150128 ) . The adrenal weights probably re- 
flect largely the final results of population 
manipulation rather than the immediate ef- 
fects, as the adrenal samples were obtained 
several weeks after the introductions or esti- 
mates. Therefore, the changes in adrenal 
weight probably reflect overall population 
changes rather than any immediate social 
strife resulting from the introductions. An 
experiment to collect samples a few days 
after the introductions is in progress and 
may show an increase in adrenal weight. 

The adrenal glands of rats from the in- 
creasing blocks showed no consistent change, 
although population growth terminated ( Ta- 
ble 3, figures 2 and 3 ) . The replacement of 
rats in increasing populations had little ef- 
fect on the adrenal weights of rats examined 
10 weeks later. 

The results reported here may be applica- 
ble to certain stocking programs. A routine 
part of many game-management programs 
has been the introduction of a number of 
animals into an area with the expressed hope 
of increasing the population either directly 
or eventually by reproduction. Indeed, such 
stocking has often been considered a pana- 
cea for all hunting problems. The present 
results, using rats as experimental animals, 
show that the disruption of a population 
following an introduction may actually pro- 
duce a decline under certain conditions. Evi- 
dently the introduction of a number of ani- 
mals may have disastrous results when a 
population is above the halfway point on a 
growth curve. 



Summary 

Wild Norway rats {Rattus norvegicus) 
were introduced from one city block to an- 
other to simulate immigration. The pop- 
ulation changes were determined by fre- 
quent estimates for about 20 weeks before 
introduction and 8 to 11 weeks thereafter. 
From two blocks with stationary rat popula- 
tions, some rats were removed and then 
replaced by aliens. The populations re- 
mained stationary. In two blocks about four 
times as many rats were introduced as were 
removed. The populations declined about 
25 per cent. In four blocks with increasing 
populations about one-fourth of each pop- 
ulation was removed and replaced by alien 
rats from other blocks. The increase halted. 

The reproductive rate 8 to 11 weeks after 
the introduction was normal for an increas- 
ing population, but the lactation rate was 
low, indicating that the decline in popula- 
tion growth was due in part to a decreased 
reproductive rate, and that the population 
was back to normal pregnancy rate in two 
months. The adrenal weights were also es- 
sentially normal for the population level 
two months after introduction. 

References 

Brown, R. Z., W. Sallow, David E. Davis, and 
W. G. Cochran. 1955. The rat population of 
Baltimore 1952. Amer. J. Hyg., 61( 1 ) : 89-102. 

Calhoun, J. B. 1948. Mortality and movement of 
brown rats {Rattus norvegicus) in artificially 
super-saturated populations. J. Wildl. Mgmt., 
12(2):167-172. 

Christl^n, J. J. 1954. The relation of adrenal size 
to population numbers of house mice. Sc. D. 
dissertation, Johns Hopkins Univ., Baltimore. 

. 1955a. Effect of population size on the adre- 
nal glands and reproduction organs of male 
mice in populations of fixed size. Amer. J. 
Physiol., 182(2):292-300. 

. 1955b. Effect of population size on the 

weights of the reproductive organs of white 
mice. Amer. J. Physiol., 181(3) :477-480. 

. 1956. Adrenal and reproductive responses to 

population size in mice from freely growing 
populations. Ecology, 37(2):258-273. 

AND D. E. Davis, 1955. Reduction of adrenal 

weight in rodents by reducing population size. 
Trans. N. Amer. Wildl. Conf., 20:177-189. 

Davis, D. E. 1949. The role of intraspecific compe- 
tition in game management. Trans. N. Amer. 
Wildl. Conf., 14:225-231. 

. 1953. The characteristics of rat populations. 

Quart. Rev. Biol, 28(4):373-401. 

Received for publication October 24, 1955. 



347 



A TRAFFIC SURVEY OF MICROTUS-REITHRODONTOMYS RUNWAYS 

By Oliver P. Pearson 

Patient observation of the comings and goings of individual birds has long 
been one of the most rewarding activities of ornithologists. The development 
in recent years of inexpensive electronic flash photographic equipment has 
made it possible and practical for mammalogists to make similar studies 
on this aspect of the natural history of secretive small mammals. The report 
that follows is based on photographic recordings of the vertebrate traffic in 
mouse runways over a period of 19 months. Species, direction of travel, time, 
temperature and relative humidity were recorded for each passage. In addi- 
tion, many animals in the area were live-trapped and marked to make it possible 
to recognize individuals using the runways. 

THE APPARATUS 

Two recorders were used. Each consisted of an instrument shelter and a 
camera shelter. Each instrument shelter was a glass-fronted, white box con- 
taining an electric clock with a sweep second hand, a ruler for measuring the 
size of photographed individuals, a dial thermometer and a Serdex membrane 
hygrometer. The ends of the box were louvered to provide circulation of air 
as in a standard weather station. This box was placed along one side of the 
runway, across from the camera shelter, so that the instruments were visible 
in each photograph ( Plate I ) . The camera shelter was a glass-fronted, weather- 
proof box containing a 16-mm. motion picture camera synchronized to an 
electronic flash unit. In one of the recorders the camera was actuated by a 
counterweighted treadle placed in the mouse runway immediately in front 
of the instrument shelter (Plate I, bottom). An animal passing along the 
runway depressed the treadle, thereby closing an electrical circuit through a 
mercury-dip switch. This activated a solenoid that pulled a shutter-release 
pin so arranged that the camera made a single exposure. The electronic 
flash fired while the shutter was open. This synchronization was easily ac- 
complished by having the film-advance claw close the flash contact. The 
camera would repeat exposures as rapidly as the treadle could be depressed, 
but at night about three seconds were required for the flash unit to recharge 
sufficiently to give adequate light for the next exposure. 

169 



348 



170 JOURNAL OF MAMMALOGY Vol.40,No.2 

The other recorder was actuated by a photoelectric cell instead of by a 
treadle. A beam of deep red light shone from the camera shelter across the 
runway and was reflected back from a small mirror in the instrument shelter 
to a photoelectric unit in the camera shelter. When an animal interrupted the 
light beam, the photoelectric unit activated a solenoid that caused the camera 
to make a single exposure, as in the other recorder. 

To avoid the possibility of frightening the animals it would be desirable 
to use infra-red-sensitive film and infra-red light, but standard electronic flash 
tubes emit so little energy in the infra-red that this is not practical. Instead, 
I used 18 layers of red cellophane over the flash tube and reflector to give 
a deep red flash of light. Wild mice, like many laboratory rodents, are probably 
insensitive to deep red light. I found no evidence that the flash, which lasts 
for only 1/lOOOth of a second, frightened the mice. A muffled clunk made by 
the mechanism also seemed not to alarm the mice unduly. 

When the camera diaphragm was set to give the proper exposure at night, 
daytime pictures were overexposed, since the shutter speed was considerably 
slower than l/30th of a second. To reduce the daytime exposure, a red filter 
was put on the camera lens. The filter did not affect night exposures because 
red light from the flash passed the red filter with little loss. In addition, on 
one of the cameras the opening in the rotary shutter was reduced to give a 
shorter exposure. 

Both recorders function on 110- volt alternating current. The treadle-actuated 
one could be adapted to operate from batteries. The units continue to record 
until the motion picture camera runs down or runs out of film. One winding 
serves for several hundred pictures. The film record can be studied directly 
by projecting the film strip without making prints. 

The camera shelter and instrument shelter had overhanging eaves to prevent 
condensation of frost and dew on the windows. A small blackened light bulb 
was also kept burning in the camera shelter to raise the temperature enough 
to retard fogging on the glass. Animals were encouraged to stay in their usual 
runway by a picket fence made of twigs or slender wires. No bait was used. 

A few individual animals could be recognized in the pictures by scars or 
molt patterns, but most had to be live-trapped and marked. Using eartags and 
fur-clipping I was able to mark distinctively (Plate I, bottom) all of the mice 
captured at any one station. The clipping remained visible for days or months 
depending upon the time of the next molt. 

The apparatus produces photographic records such as those shown in the 
lower pictures in Plate I. These can be transposed into some form as Fig. 2. 

THE STUDY AREA 

The study centered around a grassy-weedy patch surrounding a brush pile 
in Orinda, Contra Costa County, California (Plate I). The runways wound 
through a 20 X 20-foot patch of tall weeds ( Artemisia vulgaris, Hemizonia sp. 
and Rumex crispus) and under the brush pile. The weeds were surrounded 



349 



May, 1959 PEARSON— TRAFFIC SURVEY 171 

by and somewhat intermixed with annual grasses. Oaks and other trees, as 
well as a house and planting, were 50 feet away. 

Summer climate in this region is warm and sunny with official mean daily 
maximum temperatures rising above 80 °F. in late summer. Official temper- 
atures occasionally reach 100°, and temperatures in the small instrument shelters 
used in this study sometimes exceeded this. Nights in summer are usually clear 
and with the mean daily minimum temperature below 52° in each month. 
About 27 inches of rain fall in the winter and there is frost on most clear 
nights. The mean daily maximum temperature in January, the coldest month, 
is 54°, and the mean daily minimum 31°. 

PROCEDURE 

I placed the first recorder in operation on January 29, 1956, and the second 
on October 19, 1956. Except for occasional periods of malfunction and a few 
periods when I was away they continued to record until the end of the study 
on September 10, 1957. Approximately 778 recorder-days or 111 recorder- 
weeks of information were thus obtained. The monthly distribution of records 
was as follows: January, 54 days; February, 70; March, 90; April, 80; May, 84; 
June, 67; July, 52; August, 88; September, 48; October, 33; November, 52; and 
December, 60. 

The recorders were placed at what appeared to be frequently used Microtus 
runways, usually situated on opposite sides of the weedy patch 20 to 30 feet 
apart. For one period of four months one of the recorders was placed at a 
similar weedy patch 70 yards away. Early in the study it was discovered that 
a neighbor's Siamese cat sometimes crouched on the camera shelter waiting 
for mice to pass along the exposed runway in front of the instrument shelter. 
Consequently, a 2iA-foot fence of 2-inch-mesh wire netting was set up enclosing 
most of the weedy patch. This prevented further predation by cats at the center 
of the study area, although cats continued to hunt outside of the fence a few 
yards away from the recorders. The only other tampering with predation was 
the removal of two garter snakes on April 11, 1957. 

RESULTS 

Traffic in individual runways. — The recorders were operated at eighteen 
different stations. At seven of these apparently busy runways a traffic volume 
higher than a few passages per day never developed, and so the recorders 
were moved within two weeks. Perhaps the mice originally using these runways 
had abandoned them or had been killed shortly before a recorder was moved 
to their runway, or perhaps the disturbance of placing a recorder caused the 
mice to divert their activities to other runways. At the other eleven stations 
a satisfactory volume of traffic was maintained for three to more than twenty 
weeks. A station was abandoned and the recorder moved when the traffic 
had decreased to a few passages per day. Subsequently, I found that even this 
little activity does not indicate that the mice are going to abandon the runway, 



350 



172 



JOURNAL OF MAMMALOGY 



Vol. 40, No. 2 



for on several occasions traffic in a runway dropped this low and then climbed 
again to high levels. At one recorder the total number of passages in consecutive 
weeks was 183, 84, 26, 75 and 203. The runway represented in Fig. 1 was one 
of those used most consistently, but even it shows marked daily and weekly 
fluctuations. It is probable that after a few weeks of disuse during the season 
when grass and weeds are growing rapidly, a runway would not be reopened, 
but during the rest of the year an abandoned runway remains more or less 
passable and probably more attractive to mice than the surrounding terrain. 

Figure 1 summarizes the traffic in one of the busiest runways. On the first 
night there were an unusual number of records of harvest mice whose curiosity 
may have been aroused by the apparatus. Obviously they were not frightened 
away. After a short time traffic increased to a high level and remained high 
until the middle of November, when passages by Microtus decreased sharply. 
During the week before the decrease, seven marked individuals provided most 
of the Microtus traffic. One of these individuals, an infrequent passerby, dis- 
appeared at the time of the decrease, but the other six remained nearby for 
at least another week and continued to pass occasionally. Those Microtus that 
disappeared later were replaced by others so that even the infrequent passages 
in late November and early December were being provided by seven marked 
individuals. The decrease of Microtus traffic was caused, therefore, not by 
deaths but by a change in runway preference. Several of these same individuals 
were using another runway 20 feet away in mid-January, February and March. 

Three to six marked Reithrodontomys, depending upon the date, were pro- 
viding most of the harvest-mouse traffic in the runway represented in Fig. 1. 
The average number of passages per day of animals of all kinds was eighteen. 
In the ten other most successful runways, the average number of passages 
per day ranged from two to nineteen. 

Figure 2 gives a detailed accounting of the traffic at a single recording station 
for six days. One can judge from this figure the kind of information (excluding 



n 'OTHER 

^ = MEADOW MICE 

f{ ■HARVEST MICE 




OCTOBER 



NOVEMBER 



DECEMBER 



Fig. 1. — Traffic volume along one runway for 16 weeks. Meaning of symbols under 
the base line: T= live-trapping carried out for part of this day; 0= full moon; £= total 
eclipse of the moon; R= rain. Columns surmounted by a vertical line represent days for 
which the recording was incomplete; the heights of the various segments of these columns 
should be considered minimum values. 



351 



May, 1959 



PEARSON— TRAFFIC SURVEY 



173 



temperatures and humidities) obtained with the recorders and can at the 
same time catch a reveahng ghmpse of an aspect of the biology of small 
mammals that has heretofore been revealed inadequately by trapping and other 
techniques. It may be seen that the mouse traffic was provided by one female 
and two male harvest mice and by three male, three female, and one or more 
unidentified meadow mice; together they gave between 15 and 24 passages 
each day. No individual passed more than eight times in one day. One hai-vest 
mouse ( R2 ) seemed to spend the day to the left and to make a single excursion 




^:^:M^k^- 




PLATE I 
Top: Camera shelter (foreground) and instrument shelter in position at a mouse runway 
on the study area. Bottom: The kind of records obtained with the recorder; left — a meadow 
mouse marked by cHpping two strips of fur on the hips; riglit — a marked harvest mouse 
crossing the treadle. 



352 



174 JOURNAL OF MAMMALOGY Vol. 40, No. 2 

to the light each night. Harvest mice first appeared in the evening between 
6:37 and 7:22 and none passed after 6:26 in the morning. Five or six Microtus 
passed within a few hours (February 24), and there was nightly near-coinci- 
dence of Reithrodontomijs and Microtus. 

Traffic in all runways combined. — During the 111 recorder-weeks, the follow- 
ing passages of animals were photographed: 

Meadow mouse, Microtus calif ornicus 6,077 

Harvest mouse, Rcithrodontomys megalotis 1,753 

Bird (see following account) 382 

Brush rabbit, Sylvilagus hachmani 94 

Shrew, Sorex ornatus 56 

Peromyscus (see following account) 39 

Fence lizard, Sceloporus occidentalis 33 

Garter snake, Thamnophis sp. 17 

Salamander (see following account) 11 

Alligator lizard, Gerrhonotus sp. 10 

House cat, Felis domesticus 6 

Newt, Taricha sp. 5 

Pocket gopher, Thomomys hottae 3 

Gopher snake, Pituophis catenifer 3 

Mole cricket, Stenopelniatus sp. 2 

Ground squirrel, Citellus beecheyi 1 

Weasel, Mustela frenata 1 

King snake, Lampropeltis getulus 1 

Racer, Coluber constrictor 1 



Total 8,495 

On the basis of trapping results in this and in similar habitat nearby, large 
numbers of meadow mice and harvest mice were expected. The recording of 
at least 26 other species in the runways came as a pleasant surprise. Whereas 
all of these species would be expected to record their presence eventually, 
some of them are rarely seen or trapped near this location. After living five 
years on the study area, after doing considerable field work nearby, and after 
checking the recorders twice each day during the study, I have not yet seen 
a weasel or a ground squirrel within at least a mile of the study area. Weasels 
could easily escape detection, but large, diurnal ground squirrels must be 
very rare. The single individual recorded on August 31 may have been a 
young squirrel emigrating from some distant colony. Noteworthy absences 
were those of wood rats (Neotoma fuscipes), moles {Scapanus latimanus), 
and probably California mice (Peromyscus calif ornicus) , all of which were 
common within 100 feet of the recorders. An opossum (Didelphis marsupicilis) 
was seen a few feet from one of the recorders but did not appear on the films. 
No house mice [Mtis musculus) were detected in the photographs, although 



353 



May, 1959 PEARSON— TRAFFIC SURVEY 175 

it is possible that some passages of Mtis were listed as of Reithrodontomys. 
House mice were caught occasionally in houses nearby and in a field near 
a poultry house 200 yards away, but none was caught during frequent live- 
trapping near the recorders. 

The total of 8,495 passages of animals gives an average of 11 passages per 
day in each runway. A patient, non-selective predator waiting for a single 
catch at runways such as these could expect, theoretically, a reward each 2.2 
hours. The mean weight of animal per passage was about 31 grams, which 
would yield approximately 40 calories of food. This much each 2.2 hours 
would be more than enough to support an active mammal the size of a fox. 

Meadow mouse. — The 6,077 Microtus passages were distributed throughout 
the day and night as shown in Fig. 3 (above). The hours of above-ground 
activity, however, were quite different in winter than in summer, so Fig. 3 
is only a year-around average somewhat biased by the fact that more Microtus 
were recorded in the spring than in the other seasons. A more detailed analysis 
of the Microtus data will be given in a later report. By marking as many of 
the mice as possible, it was found that usually four or more individual Microtus 
were using each runway but rarely more than ten. On some occasions more 
than 60 Microtus passages were recorded at a single point in 24 hours. 

Harvest mouse. — Harvest mice were almost entirely nocturnal (Fig. 3, 
center). They not only used the Microtus runways, but their passages were 
frequently intermixed with those of Microtus ( Fig. 2 ) . On fourteen occasions 
the two species passed within 60 seconds of each other, and on one occasion 



-■ r-i ' 1 ' — I • — ^1 — 1 ■ r— 1 1 ni- 

o MB M M MM M MM MM R M M MM MM MM RMRR 

2 566 55 765BJ59 '' ^ %l ^ K IIV, 

9 a i a (J(J 9cJc;9(J<J<J 9<J(J9 9iJ Jddcf 



FEB. , , . *J „ 1 1_] , 1 1 1 

25 - 26 I I 



■n — ' ■— ' — I ' ' ' — 1—; —I — I 

RMR MMR MMMMMRRM M RM H 

373 57 4 8 6 6 5. ^ . 5 7 3 5 

(39(J <J9(f 9 <J(J(J(J(J(J 9 iJ d 



FES. JJ , ,_IJ 1_,_^ _LJ ,J-rl_ 

^^ ^' RM B RRM R RMM of M MMMM 

36 2274388 7 57 

dcJ 999 (5(599 9*9 



FEB. 
27-28 



-H 1 1—1 1 1 '-'-' ' I "" I I 'I 

e M M M M R RRM RMM MRMMM M MM 

6 5 8 5 2 345 3 5 6 7258 5 6 

(J(J9 (f 9tf(JiJ 6 i <S 99i39 i (f 



FEB 28- 



, M^ /—' rV r-^-V ' ■ ■ I ' I " V- 

"*'''^" ' B BBS RM M MRMM M M MMM M M MMMMMR MM 

2577 35 5 57118 5 857752 7 5 

9(J 9 9(S(J(J (J 9 999 tf 9 (59 9(J9 9(5 



MARCH 



-r'-' H IT-' 1 '-'— 1 rn- 



'-2 MR BB B M RRM MM MR R M MM M MMM MRH R 

73 5 335577347 77 8 5772 52 

9^ cr (5(5(5 i59 9(5(5 9 9 9 9^9 99(5 9 

6 7 8 9 10 II NOON I 23456789 10 II NIOHT 1 2 3 4 5 6 

Fig. 2. — A sample record of the total traffic in a single runway over a period of six days. 
Marks above the base Hnes indicate passages from right to left, and marks below the base 
line passages from left to right. R represents Reithrodontomtjs; M, Microtus; B, bird ( includes 
brown towhee, wren-tit, and song sparrow); and RAB, brush rabbit. Most of the mice are 
further identified by number and sex. 



354 



176 



JOURNAL OF MAMMALOGY 



Vol. 40, No. 2 



a 4-month-old male Microtus and a 5-month-old male Reithrodontomys ap- 
peared in the same photograph. 

The history of one runway indicates that traffic by Reithrodontomys alone 
does not keep a Microtus runway open. One or more Microtus passed almost 
daily along this runway during February. At the end of the month the 
Microtus disappeared and two Reithrodontomys became active in the same 
runway. Despite an average of 3.3 passages per day by Reithrodontomys 
throughout March and up to mid-April, grass and weed seedlings grew up 



3,0 

>- 
O 

z 

UJ 

§5 


- 








MEADOW MICE 
ALL MONTHS 
N = 6077 
























- 


UJ 


















U. 













6 7 8 9 10 II 12 I 
NOON 



234567 89 lO II 12 I 23456 

NIGHT 



Sic 

>- 
o 

z 

UJ 

cr 

u. 



HARVEST MICE 

ALL MONTHS 

N = 1753 



6 7 8 9 10 II 12 I 2 3 4 5 6 7 8 9 10 II 12 I 
NOON NIGHT 



2 3 4 5 6 



20 



> 
o 

I 10 
o 

or 



BRUSH RABBIT 
N= 94 



m 



6 7 8 9 10 II 12 I 2 3 4 5 6 7 8 9 10 II 12 I 
NOON NIGHT 



2 3 4 5 6 



Fig. 3. — Distribution by hours of 6,077 passages of meadow mice (above); 1,753 passages 
of harvest mice (center); and 94 passages of brush rabbits (below). 



355 



May, 1959 



PEARSON— TRAFFIC SURVEY 



177 



in the runway and it began to look unused. By the end of April almost all 
traffic had ceased. 

The Reithrodontomys data will be analyzed in a later report. 

Birds. — Of the 382 bird records, at least 255 were of sparrows ( at least 122 
song sparrow; the remainder mostly fox sparrow, white-crowned sparrow and 
■golden-crowned sparrow ) . Other birds recognized were wren-tit, wren, brown 
towhee and thrush. On several occasions birds, especially song sparrows, battled 
their reflections in the window of the instrument shelter. This caused long 
series of exposures. Each series was counted as a single passage. If the bird 
stopped for a minute or more and then returned to the battle, this was counted 
as another passage. All bird records were during daylight hours. 

On three occasions a sparrow and an adult Microtus appeared in the same 
photograph. On one of these occurrences a song sparrow was battling its 
reflection when an adult, lactating Microtus came along the runway. The 
sparrow retreated about 12 inches toward the camera shelter and, as soon 
as the mouse had passed, returned to the runway. 

Brush rabbit. — All except four of the records of brush rabbits were in June 
and July of 1957, a season when these animals, especially young ones, were 
abundant. Figure 3 (below) shows that they were most active in the early 
morning. 



-^20- 



o 

^ 10 

■=> 
a 
tu 



CL 



jh 



30 



>20 
o 

z 

UJ 

3 

S 10 
cr 



6 8 10 12 2 4 6 
NOON 



8 10 12 2 4 

NIGHT 



JFMAMJJASOND 



Fig. 4. — Distribution by hours of 56 passages of shrews (left) and distribution by months 
of 56 passages of shrews (right). 

Shrew. — The dry, weedy habitat chosen was not favorable for shrews, and 
they were near the minimum weight necessary to depress the treadle of one of 
the recorders, so that some may have passed along the runway without making 
a record. The shrews were highly nocturnal (Fig. 4, left) and avoided the 
surface runways during the dry summer months (Fig. 4, right). Since captive 
specimens of Sorex are rarely inactive for more than one hour ( Morrison, Amer. 
Midi. Nat., 57: 493, 1957), the scarcity of records in the daytime probably 
means only that the shrews were not moving above ground at this time. They 
may have been foraging along gopher, mole and Microtus tunnels during the 
daytime. 



356 



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JOURNAL OF MAMMALOGY 



Vol. 40, No. 2 



A shrew was marked on March 4, a few inches from one of the recorders. 
It was captured 15 feet away on May 30 and 5 feet farther away on June 23. 
It passed along the study runway five times in the 16-week interval between 
first and last capture: on March 13, 27, 31, and April 17, and possibly on 
April 10 (markings obscured). Another shrew was recorded on March 27. 
Unless baited traps attract shrews from a considerable distance, or the recorder 
repels them, a trapper setting traps in this runway for a few nights would have 
had small chance of recording the presence of this individual which apparently 
was nearby for at least 16 weeks. 

Not a single shrew was recorded during the dry summer months of June, 
July and August. Nevertheless, on July 8 when I was checking the photo- 
electric recorder at 5:55 am, a shrew emerged completely from a small hole in 



100 



90 



80 



70 



60 



1 50 

Q 

i 

X 



UJ 40 
> 



UJ 

a: 



30 



20 



10 




• : SHREWS 
O = LIZARDS 



50 60 

TEMPERATURE 



CF) 



Fig. 5. — A comparison of the temperatures and humidities encountered by shrews and 
fence Hzards in tlie runways. The larger circles show the position of the mean for each 
species. The large polygon encloses the range of temperatures and humidities available 
to the animals during the study. 



357 



May, 1959 PEARSON— TRAFFIC SURVEY 179 

the ground a few inches from the instrument shelter, twitched his nose rapidly 
for a few seconds, and retreated down the same hole. The air temperature was 
54° and the relative humidity 78 per cent — normal for this season. Obviously 
shrews were present on the study area during some or all of the summer months 
but were not frequenting the surface runways. 

Figure 5 shows the temperatures and relative humidities encountered above 
ground by the shrews on the study area compared with the total range of 
temperatures and humidities recorded throughout the study. By their nocturnal, 
winter-time activity shrews encountered the coldest, most humid conditions 
available in the region. In contrast, the similarly small, insectivorous fence 
lizards existing in the same habitat managed by their own behavioral patterns 
to encounter a totally different climate (Fig. 5). The mean of the temperatures 
recorded at the times of lizard passages was 39° warmer than that recorded 
for shrew passages, and relative humidity was 36 per cent lower. 

This activity pattern of shrews differs from that reported by Clothier (Jour. 
Mamm., 36: 214-226, 1955) for Sorex vagrans in Montana. He found shrews 
there to be active "both day and night and throughout the year, even during 
extremely bad weather." It is important to understand, however, that he 
collected in damp areas near water, where the shrews may not have had to 
modify their activity to avoid desiccation. Extremely bad weather, for a 
shrew, is hot dry weather. 

Peromyscus. — Peromyscus truei was abundant in brushy places and in houses 
nearby; P. maniculatus was scarce. Some of the Peromyscus records were 
clearly of truei and some may have been of maniculatus, but many could not 
be identified with certainty. No adult P. californicus was recognized although 
a few young ones may have passed and been listed as truei. All passages of 
Peromyscus were at night. 

Salamander. — The record includes passages by both Etisatirui escholtzii and 
Aneides luguhris. They were recorded in October, November, March and April. 
By being nocturnal and by avoiding the dry season, they encountered in these 
autumn and spring months about the same microclimate as shrews, but were 
recorded neither in the winter months nor at temperatures below 39°. A third 
species, Batrachoccps attenuatus, was common in the study area but is so small 
that it could not be expected to actuate either of the recorders. One 
Batrachoccps electrocuted itself underneath the treadle but has not been 
included in the records. 

Comparison of traps and recorders. — The combination of live-trapping and 
photographing revealed a failure of small mammals to move between runways 
only a few feet apart. On several occasions meadow mice and harvest mice 
were live-trapped a few feet from one of the recorders, were released at the 
same place, and were recaptured a week or more later not more than a few 
feet away, yet during the intervening time they failed to pass the recorder. 
Conversely, some individual mice repeatedly recorded themselves on the films 
yet could never be induced to enter any of a large number of live traps placed 



358 



180 JOURNAL OF MAMMALOGY Vol. 40, No. 2 

in the same runway and in nearby runways. It is obvious that all mice present 
do not use all of the active runways close to their home, and it is also obvious 
that neither the recorders nor traps give a complete accounting of the mice 
present. 

SUMMARY 

A motion-picture camera synchronized to an electronic flash unit was used to record the 
passage of animals along meadow-mouse runways and to record the temperature, relative 
humidity and time at which they passed. More than 26 species used the runways during 
111 weeks of recording. Meadow mice, harvest mice, sparrows, brush rabbits and shrews 
passed most frequently. The average traffic per day in each runway was 11 passages; on 
some days there were more than 60 passages. Rarely more than ten meadow mice or 
six harvest mice used a runway in any one period. Meadow mice and harvest mice used 
the same runways simultaneously. Traffic by harvest mice alone did not keep the run- 
ways open. 

Meadow mice were active during the day and night; harvest mice were strongly nocturnal. 
Brush rabbits were active primarily early in the morning. Almost all shrews were recorded 
at night and in the winter months. Consequently, they encountered the coldest, most 
humid conditions available to them. In contrast, the similarly small, insectivorous fence 
lizards encountered a microclimate that was 39° warmer and 36 per cent less humid. 

Neither traps nor recorders accounted for all the individuals living nearby. 

Museum of Vertebrate Zoology, Berkeley, California. Received October 29, 1957. 



359 



PREY SELECTION AND HUNTING BEHAVIOR 
OF THE AFRICAN WILD DOG' 

RICHARD D. ESTES, Division of Biological Sciences, Cornell University, Ithaca, Nevv York 
JOHN GODDARD, Game Biologist, Ngorongoro Conservation Area, Tanzania 

Abstract: African wild dog (Lijcaon picttis) predation was observed in Ngorongoro Crater, Tanzania, 
between September, 1964, and July, 1965, when packs were in residence. The original pack of 21 dogs 
remained only 4 months, but 7 and then 6 members of the group reappeared in the Crater at irregular 
intervals. The ratio of males: females was disproportionately high, and the single bitch in the small pack 
had a litter of 9 in which there was only one female. The pack functions primarily as a hunting unit, 
cooperating closely in kilhng and mutual defense, subordinating individual to group activity, with strong 
discipline during the chase and unusually amicable relations between members. A regular leader se- 
lected and ran down the prey, but there was no other sign of a rank hierarchy. Fights are very rare. A 
Greeting ceremony based on infantile begging functions to promote pack harmony, and appeasement 
behavior substitutes for aggression when dogs are competing over meat. Wild dogs hunt primarily by 
sight and by daylight. The pack often approaches herds of prey within several hundred yards, but the 
particular quarry is selected only after the chase begins. They do not run in relays as commonly sup- 
posed. The leader can overtake the fleetest game usually within 2 miles. While the others lag behind, 
one or two dogs maintain intervals of 100 yards or more behind the leader, in positions to intercept the 
quarry if it circles or begins to dodge. As soon as small prey is caught, the pack pulls it apart; large 
game is worried from the rear until it falls from exhaustion and shock. Of 50 kills observed, Thomson's 
gazelles (Gazella thomsonii) made up 54 percent, newborn and juvenile wildebeest {Connochaetes 
taiirmus) 36 percent. Grant's gazelles (Gazella granti) 8 percent, and kongoni (Alcelaphus buselaphus 
cokei) 2 percent. The dogs hunted regularly in early morning and late afternoon, with a success rate 
per chase of over 85 percent and a mean time of only 25 minutes between starting an activity cycle to 
capturing prey. Both large and small packs generally killed in each hunting cycle, so large packs make 
more efficient use of their prey resource. Reactions of prey species depend on the behavior of the wild 
dogs, and disturbance to game was far less than has been represented. Adult wildebeest and zebra 
(Equus burchelli) showed little fear of the dogs. Territorial male Thomson's gazelles, which made up 
67 percent of the kills of this species, and females with concealed fawns, were most vulnerable. The 
spotted hyena (Crocuta crocuta) is a serious competitor capable of driving small packs from their kills. 
A minimum of 4-6 dogs is needed to function effectively as a pack. It is concluded that the wild dog 
is not the most wantonly destructive and disruptive African predator, that it is an interesting, valuable 
species now possibly endangered, and should be strictly protected, particularly where the small and 
medium-sized antelopes have increased at an alarming rate. 



The habits of the African wild dog or 
Cape hunting dog (Lijcaon pictus) have 
been described, sometimes luridly, in most 
books about African wildlife. Accounts by 
such famous hunters and naturalists as 
Selous (1881), Vaughan-Kirby (1899), and 
Percival (1924), repeated and embellished 
by other authors, have created the popular 
image of a wanton killer, more destructive 
and disruptive to game than any other 
African predator. 

^ Field work supported by the National Geo- 
graphic Society; also by grants from the New York 
Explorers Club and the Tanzania Ministry of 
Agriculture, Forests and Wild Life. 

52 



Because of its bad reputation, the wild 
dog was relentlessly destroyed in African 
parks and game reserves for many years. 
In Kruger National Park, for instance, it 
was shot on sight from early in the present 
century up until 1930 as part of an overall 
policy to keep predators down. In Rhode- 
sia's Wankie National Park some 300 wild 
dogs were killed by gun and poison be- 
tween 1930 and 1958. 

Acceptance of modem concepts of wild- 
life management has finally brought an 
end to the indiscriminate destruction of 
wild dogs and other predators in most, if 
not all, African national parks. There is now 



360 



The African Wild Dog • Estes and Goddard 53 



a general awareness among game wardens in sanctuaries, paid very little attention to 

of the predator's role in regulating popula- cars and could be watched undisturbed 

tions, which perhaps began with Stevenson- from within 30 yards or less. It was also 

Hamilton ( 1947 ) , Warden of Kruger Park feasible to keep pace with the pack during 

for almost 30 years, who related the alarm- chases over the central Crater floor, either 

ing increase of impala {Aepijceros me- driving parallel to the leader at a distance 

lampus) to the disappearance of the park's of 100-200 yards or following behind and 

formerly large wild dog packs. to one side so as not to get in the way of 

While the wild dog has benefited from other pack members. To locate the pack 

more enlightened concepts of game man- initially, we often drove to an observation 

agement, its reputation, still based on pop- point on a hill and scanned the Crater with 

ular writings and myth, remains unchanged, binoculars and a 2