Biology of bats [1 - 3, 1 ed.]

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Stereoradiograph of fossil bat, about 50 million years old, described in Chapter 1. Two times natural size. Cf, fourth caudal vertebra; HI, left humerus, partly opaque to x-rays; Tir, right tibia, distal end; Wr, right wrist.

Biology of Bats Volume I

Edited by

William

A.

Wimsatt

Division of Biological Sciences Cornell University Ithaca, New York

1970

Academic

Press

New York and London

COPYRIGHT © 1 9 7 0 , BY ACADEMIC PRESS, INC. ALL RIGHTS RESERVED NO PART OF THIS BOOK MAY BE REPRODUCED IN ANY FORM, BY PHOTOSTAT, MICROFILM, RETRIEVAL SYSTEM, OR ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION FROM THE PUBLISHERS.

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United Kingdom Edition published by

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LTD.

LIBRARY OF CONGRESS CATALOG CARD NUMBER:

PRINTED IN THE UNITED STATES OF AMERICA

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List of Contributors Numbers in parentheses indicate the pages on which the authors' contribu­ tions begin. Robert J. Baker, Department of Biology, Texas Technological College, Lub­ bock, Texas ( 6 5 ) Wayne H. Davis, Department of Zoology, University of Kentucky, Lexington, Kentucky ( 2 6 5 ) Donald R. Griffin, The Rockefeller University, and New York Zoological Society, New York, New York ( 2 3 3 ) Glenn L . Jepsen, Department of Geological and Geophysical Sciences, Prince­ ton University, Princeton, New Jersey ( 1 ) Charles P. Lyman, Department of Anatomy, Harvard Medical School, and Museum of Comparative Zoology, Harvard University, Boston, Massachu­ setts ( 3 0 1 ) Robert T. Orr, California Academy of Sciences, San Francisco, California ( 2 1 7 ) Robert M. Rosenbaum, Department of Pathology, Albert Einstein College of Medicine, New York, New York ( 3 3 1 ) Terry

A. Vaughan, Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona ( 9 7 , 1 3 9 , 1 9 5 )

ix

Preface

Bats had mastered flight eons before man's own lineage began. Their unique volitional mode was obviously advantageous, for adaptive radia­ tion within the group has been little short of extraordinary. Today Chiroptera represent the second largest order of mammals in number of species and the largest in overall abundance; excluding man, and pos­ sibly rodents, they are also the most widely distributed land-based mammals. Bats are relatively inconspicuous only because they are active by night, hidden by day, and wary of human contact. Possibly these are the reasons they were not studied as vigorously as other mammals before the turn of the century. Since then, however, the striking, and sometimes bizarre specializations of bats and a growing awareness of their impor­ tance to the economy and health problems of man have stimulated an increased scholarly interest in the group so that today our knowledge of Chiroptera has grown to sizeable proportions. Unfortunately a great deal of basic information is not readily acces­ sible to those who lack good library facilities or the time and patience required to extract it from the extensive literature where it has lain scattered and unsystematized. To be sure, some excellent books have been produced which cover selected topics in considerable depth, but the few that achieve a broader coverage are compendious and, for the most part, limited in detailed reference value. No single information source which is both sufficiently comprehensive and detailed to meet adequately the multidisciplinary reference requirements of zoologists, teachers, and others concerned with the general biology of Chiroptera has been written. The present multivolume treatise is an attempt to fill this reference gap. "Biology of Bats" treats in detail most of the basic anatomic, physiological, behavioral, and ecological characteristics of the group. It includes data on evolution, karyology, principles of classifica­ tion, zoogeography, bioeconomics, and an analysis of procedures and problems involved in the care and management of bats in the laboratory. The aim has been to provide a balanced and authoritative account of all major facets of chiropteran biology, exclusive of systematics which are dealt with adequately in several recent monographs. xi

XÜ

PREFACE

The chapters have been prepared by qualified experts in their respec­ tive fields. Authors were encouraged to present what they wished in whatever manner they deemed appropriate, the only constraint being that the intended reference value of the work be preserved. Many have included new observations and viewpoints, and each has documented his contribution with an extensive bibliography of important references from the literature. No formal attempt was made to unify nomenclatural terminologies throughout the volumes. In the few cases where generic or specific names cited from the older literature have been changed the interested reader will usually be able to determine current designations by consulting available sources on the systematics of Chiroptera. Un­ avoidably, the sequence in which various subjects are presented is some­ what haphazard, but insofar as possible an attempt was made to group related subjects together in the individual volumes. Although a "definitive" bat book can never be written as long as scholars continue to probe unexplored facets of chiropteran biology, it is probable that much of the basic information contained in these vol­ umes will remain current for some time. It is hoped that the discussions presented here will assist in the identification of promising areas for future research and perhaps help generate new enthusiasm for multidisciplinary studies of these extraordinary mammals. I am grateful to many colleagues and associates in bat studies—too numerous to name individually—who perceived the need for a "Biology of Bats," and provided the encouragement without which I would not likely have organized a work of this dimension. I owe special thanks to the contributors not only for their enthusiastic acceptance of the idea and their tangible collaboration, but also for their patience with delays and their willingness to update their chapters as needed until the vol­ umes could go to press. The staff of Academic Press has been enormously helpful in all phases of production and, opportunely, indulgent with the ineptitudes of an inexperienced editor. Mrs. Barbara Thorp gave invalu­ able assistance with the proofreading and rectification of manuscript copy and with many other routine but essential tasks. Mrs. Almita Ann Proto provided secretarial assistance and helped in the preparation of the Subject Indexes.

Chapter 1

Bat Origins and Evolution Glenn L. Jepsen

I. II. III. IV. V. VI. VII. VIII. IX. X. XI. XII. XIII. XIV. XV.

First Bats and Men What Are Bats? Bats through Time Taxa of Bats Fossil Bats Designs of Wings Caverns and Crevices Bats and Birds Bat Hand-Wings or Wing-Hands Gliders Don't Fly and Vice Versa The Forefinger, Index of Function Neck Bones Stages to Flight Icaronycteris index "First" Bat at Present References

1 5 7 8 10 22 24 32 36 40 46 1

3

57 60 ^2

I. First Bats and Men There never was a first bat. This chapter is an exposition on the oldest-known bat, not the primordial chiropteran, and a discussion of the efficacy of classic taxonomy in its application to petrified bats and other taxa in evolutionary sequences. For simplicity I have tried to avoid 1

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GLENN L . JEPSEN

most of the specialized jargon of the paleontological trades, as well as the false accuracy and the metaphysics that try to creep into state­ ments about fossilized phylogenies of bats and of men and of other forms whose genealogies have emotional attachments. For analogies to illustrate the concepts of bat evolution the records of other groups, especially rodents and horses and multituberculates (see Chart 1 ) , are cited. Anyone who expects, from the title of this chapter, a bone by bone account of all fossil bats has been unfortunately misled, because this is a broad sweep, past many details, toward speculations which future discoveries may confirm or falsify. This procedure is quite differ­ ent from that of taxonomists who make tight little taxa for single teeth. For brevity parts of this chapter are condensed to an almost telegraphic style. Bat skeletons are so diversified in details from group to group that a fractional bony part may not be as representative of a whole animal as an analogous fragment would be in a less variant group such as, for example, horses or men. For this reason, particularly, the study of many small bits of fossil bats does not yield as much information about bat evolution as does the examination of a single whole specimen. Fortu­ nately, the earliest known bat, from sediments of an Early Eocene lake in Wyoming, is also the most complete fossil chiropteran skeleton, and it is the basis for many of my presumptions about the origin and develop­ ment of bats. It has been briefly described (Jepsen, 1966), with figures that were, regrettably, inadequate to show many of its interesting qualities. Special­ ists on bat morphology have recently asked many questions about numer­ ous structures on this skeleton (Princeton Museum of Natural History No. PU18150), and, therefore, special efforts have been made to illustrate here its most significant features. To this end some of the photographs have been taken in stereo pairs to present three-dimensional aspects of the specimen, especially to experts on various bony elements of bats. (A simple stereoscope, to attain the effect of three dimensions from the photographs, will be required by some viewers, and others, with a little advice from anyone who is practiced in unaided stereo viewing, will not need instrumental help.) The indicated magnification for each figure is approximate. These photographs (Figs. 4-18) by David C. Stager and Willard Starks and the accompanying drawings (Figs. 1-3) by Mrs. Elton J. Hansens constitute by themselves a wordless essay that reveals much more than any text about the natural wonder and splendor of this most venerable bat. Some obscure details of its bony architecture were re­ vealed by the skill of W. Landon Dennison and William Snyder in

180

135

53

36

25

13?

3?

PALEOCENE

EOCENE

OLIGOCENE

MIOCENE

PLIOCENE

PLEISTOCENE

1

@

(

Q

y

Plagiomene

Planetetherium

Paramys a t a v u s

Archaeopteropus

Icaronycteris

of some

l 7 ) Hvmrnthflrnim

[^6J

©

(3)

(2)

Chart 1. Approximate ranges (heavy vertical lines) in geologic time and earliest known records (circles) vertebrate taxa. (Uyracotherium, oldest known genus of perissodactyl, occurs also in early Eocene strata.)

TRIASSIC

JURASSIC

CRETACEOUS

TERTIARY

QUATERNARY

1. BAT ORIGINS AND EVOLUTION 3

4

GLENN L . JEPSEN

making x-ray photographs, and good ideas about its position in nature were generously given by Robert H. Baker, Margaret W. Cross, Karl F. Koopman, Paul McGrew, Bernard Sige, Robert C. Stones, Terry A. Vaughan, and many other thinkers who are interested in bat study. Concepts of an original or prime bat have been the source of much conjecture and of many publications that ignore the real difficulties of the idea of the beginning bat. Like the first man the first bat is an arbitrarily defined section of a vast family tree, a selected segment of an evolutionary cord which was composed of uncountable fibers of com­ plex materials and integrated processes. Popular demands for definitions of the initial man or bat have created wholly artificial semantic structures that conceal more than they reveal about nature as it is. Genetic materials in bats and men are, of course, as old as those of any organism; all are equally ancient but they have differentiated into multiple kinds of organizations whose relationships are now obscure. Geological and biological processes of the present are, presumably, con­ tinuations of those of the past, with current elaborations normal to a continuity of events wherein each successive stage employs the incre­ ments of those preceding it. Thus, although the physical processes may remain uniform the products continually vary, as a chain reaction. Paleontological chronology is founded upon this principle, and, of course, so is the whole idea of ongoing evolution. A bat is a way of life, a way so alien to mans way that we have great difficulty in comprehending it and about which, therefore, we have developed many aversions and superstitions. Man mirrors good and evil in his anthropic view of the form and the social traits of the bats that he demonizes or deifies (Allen, 1939, pp. 14-17; Peterson, 1964, pp. 1-10). The fact that no love is lost between humans and chiropts is principally mans loss; it has delayed the extensive studies that bats deserve until now it may be too late to save them from our pollution or to study them as the fascinating and elegant bits of nature that they are. Bats and people obviously share some physical attributes, and men have long wanted to extend the similarity by flying like bats. More than two centuries ago Linnaeus, in his system of static taxonomy, classi­ fied Vespertilio as one of four genera of primates. And to the most antique group of bats yet known, represented by the tiny delicate petri­ fied skeleton that evokes artistic esthesia in everyone who sees it, I have given the generic name Icaronycteris in allusion to the old Greek myth about a youth who tried to fly. Examination of these fragile bones expands the meaning of artist Georgia O'Keeffe's comments about the

1.

B A T ORIGINS AND

EVOLUTION

5

beauty of old bones and the sensation that they are strangely more alive than living animals. The only known species of Icaronycteris has been christened index in reference to the important and informative tiny claw on the forefinger of its wing. Bats are very old. Their style of volitation, with its attendant morpho­ logic and behavioral commitments, was fully developed as a highly suc­ cessful vital technique long before man s own antecedent gene kit had produced even a little leaping lemur. Bats (with their incredibly complex and refined neural and audio-response systems) and pre-men knew each other for many scores of millions of years before mans brain had reached even the minimum size that we now call human. Among the many interesting opportunities for man's present and future superbrain are attempts to answer the question "What is a bat?" II. What Are Bats? What are they? Bats are a vast number of peculiar taxonomic groups. The study of their origins and evolutions may need special considerations in the application of primary taxonomic techniques to their living and their extinct forms. Obviously, as anyone can see, and as some critics of paleontology have emphasized, fossils are the only direct record of ancient bats (and men), and these brittle skeletal remnants are a very small representation of whole animals (although much larger than the fractions that are studied by specialists in some biochemical techniques). Known bits of petrified primates are many thousands of times more numerous than the small number of fossil bats that have been collected, and as the discoveries of man's old relatives (ancestral and collateral) increase, the confusions about their relationships also grow. One appar­ ently irremediable and subtle source of troublesome semantic disorder in taxonomic statements is the plain fact that a word or a number that "stands for" an organismic type or sort cannot change but the organism can and does evolve through a kind of continuum of very small genetic and phenotypic steps—if our general beliefs about mutation and natural selection are correct. (Blackwelder, 1967; Buck and Hull, 1966; Colless, 1967; Hull, 1966; Hennig, 1966; Michener, 1963, Simpson, 1961, 1963; and many other authors have discussed some of the troubles and oppor­ tunities of taxonomic activities.) Unfortunately, no one has yet devised a taxonomic system which can be used successfully to classify organisms in accord with the loosely designed and rarely tested but well-known "biologic definition" of living

6

GLENN L . JEPSEN

species ("actually or potentially interbreeding populations") and also in accord with the facts of evolutionary change. Many efforts to reconcile these two aspects of taxonomic purpose and practice have led to exten­ sive and fruitless debate. If biologists continue long enough to be inter­ ested in the taxonomy of organisms they will observe at some unpre­ dictable time in the future that the physical attributes of some species no longer conform to the original descriptions of them. This is another way to repeat and emphasize the truism that the present is merely a layer between pasts and futures and that organisms evolve whereas taxonomic nomina do not, and to express regret that the Linnean system was devised in the belief that species are eternally fixed and not limited by time. The concept of species as discrete and discontinuous entities in nature has resulted in past decades in the publication of monumental trivia, and the concept still persists when authors confine their attention to taxonomic devices for manipulating living forms (Mayr, 1968) and fail to look at nature's depth in time. Students of fossil mammals can occasionally see little increments of morphologic modification in an obvious ancestral-descendant series whose bones are found in sequential sedimentary strata—layers that may represent thin slices of time. Such observable sheets of the record, although very rarely seen in long-continued piles, clearly reveal the fact that if we had all the skeletons of all man-lines or of all bat-lines of phylogeny we could not divide them into separate species. Writers who ignore this fact and disregard time throw the vast majority of orga­ nisms out of serious taxonomic consideration and rarely realize that their reasoning logically leads to a belief that the individuals in one generation of a natural population can be members of species which are different from those of their parents or offspring. This is an illogical confusion of F generations and F generations. Bats are so unlike other mammals that to understand their lives and their geologic history and to classify them adequately we need much more information than that at hand about their natural history and their morphology. Various aspects and parts of bat-being that may yield taxonomic and evolutionary notions are their skeletal, muscular, neural, circulatory, digestive, urogenital, and respiratory systems, their food, reproductive, metabolic, thermoregulatory, and other habits, their parasi­ tology, their geographic distribution, and the peculiarities of their karyology, immunologic reactions, and endocrine chemistry. And, of course, much more knowledge would be necessary to know a whole bat, quick or dead. x

x

1.

B A T ORIGINS AND

EVOLUTION

7

III. Bats through Time Specialists in studies and concepts of fossil vertebrates become unu­ sually habituated to thoughts about long periods of time and about the vast numbers and complexities of biochemical and ecologic events that are represented by even small changes in the morphologic attributes of evolving populations. To the modern student of fossil horses the differ­ ences between the oldest (Paleocene) species of Hyracotherium (eohippus, dawn horse) and any subsequent descendant species are so numer­ ous as to be almost beyond comprehension, although a brief and casual examination of the bones does not reveal much complexity or difference between chronologically adjacent species. When the first attempts were made to think of the relationships of genetics to paleontology, of the organization of gametic chemicals to living form, a naive habit developed of equating gene to character as a one-to-one relationship, almost as simple as "a gene for an eye and a gene for a tooth" to rephrase an Old Testament formula. "Fifty to fifty-five million years ago" rolls liltingly off the tongue of geologists to indicate the moment when the hands of the geological clock passed from the Paleocene Epoch to the Eocene Epoch in the early Tertiary Period, but does such a span of time have any special meaning to them? No one I know can think of a million years without using some kind of a mnemonic device. "A million inches is about sixteen miles, the distance from home to office." A million dollar bills, end to end, would reach by road from Denver or Boston to Chicago. Just as geological processes in a region accelerate or decelerate so do biological processes vary chronologically .or sequentially in rate and also from group to group of organisms and from organ to organ in a phyletic line. Some animals, like certain opossums (or parts thereof) have remained structurally rather static since Cretaceous times (75 mil­ lion years ago), apparently adjusted to persistent environmental and functional conditions. Other kinds of animals have sprinted. Although some teeth of living opossums differ but little from those of early Tertiary forms, the dentition of Equus is so unlike that of Hyracotherium that, lacking intergraded stages, the relationships of the Recent to the early Tertiary horses of 500,000 centuries ago would probably be unsuspected. Despite the apparent evolutionary speed of the equids, the modifications have actually been gradual. If a photograph of each horse that has lived since Early Eocene time were on a sheet of the thickness of this one, the stack of pictures would be (at a low estimate) more than

8

GLENN L . JEPSEN

fifteen million miles high, and if we made a portrait of only one horse only once every two years during the slow gradual modifications of the group, this geological stroboscopic record would pile up more than a mile high. Another exercise in imagination that may help indicate the magnitude and taxonomic complexity of phyletic evolution also uses imaginary horses. Visualize again all the horses that ever lived, from eohippus to Equus, in the form of a solid column, marching shoulder to shoulder, head to tail, about 75 miles wide (greater than the distance from New York to Philadelphia) and moving at a speed of 6 miles per hour. Allow 5 feet for the average horse length. It will require about 90 years for the column to move past you in the reviewing stand. Where could you draw a line between any two taxa? Probably the minute changes from generation to generation would not be sensed by an observer, and classi­ fication into subgroups would be quite impossible except by wholly arbitrary means; there would be no natural precise genetic or morpho­ logic boundaries in the chemicophysical continuity. This vision, imper­ fect though it is, indicates some of the weaknesses in the practice of selecting the gaps in the fossil record as convenient divisions between species. Although the inadequacies of using morphologic hiatuses in phylogenetic lines as taxonomic expedients are obvious, these blanks in pre­ history are nevertheless widely (and, at present, necessarily) used as boundaries between observable (and definable) anatomic stages. No other systems that are acceptable to systematists have been developed. As Hennig (1966, p. 193) states "In dealing with the classification of fossils, typological systematics lives on the incompleteness of the fossil record. The more numerous and completely preserved the fossils, the greater the difficulties of typological systematics become, whereas the difficulties of phylogenetic systematics decrease." IV. Taxa of Bats Obviously the taxonomy of fossils has to be based almost entirely upon morphologic characteristics but the "biological definition" of spe­ cies formerly achieved such popularity that some paleontologists tried to estimate, from study of skeletal structures, the degree of its appli­ cability to fossil taxa, which are far more numerous than extant forms; and to make decisions based upon it about the natural limits of species. These exercises in futility and frustration were much more art than

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craft but they did emphasize the fact that the conceptual boundaries of "biological species" are inapplicable to most species of living animals as well as extinct forms because the observations and experiments that are necessary to establish the facts or potentials of interbreeding cant be or haven't been made. Thus the concept has become a nebulous kind of theoretical model which usually mirrors nature poorly if at all. Another facet of the biological definition states that the natural popula­ tions which constitute a species are "reproductively isolated from other such groups." By this statement (also based upon time-ignoring factors) every part of a family tree or phylogeny is one species because, of course, in a genetic lineage no form can be reproductively isolated from its ancestors or its descendants. Taxonomic practices that split sections of the genetic continuum into discrete parts in order to erect arbitrary taxa are circumventing the problems and creating false boundaries. To repeat, no satisfactory simplistic solution to these problems is at hand, and some taxonomic specialists have retreated from trying to de­ vise answers because the complexities of the genetic-morphologic-phylogenetic systems appear to be too extensive to respond to current methods of study. How, then, can a fossil species of vertebrate be defined? Various in­ tricate methods of dimensional and statistical analyses have been devised to express the differences in form of whole skeletons or of parts of them. Unfortunately, no phylogenies are now complete enough (or ever will be) for the practice of describing species as discrete aggregates of organisms to be wholly discarded in favor of a truer picture of evolv­ ing populations. At present a fossil "species" is all the organisms that are regarded by experienced taxonomists as worthy of formal recognition as a distinct kind, a morphologic point in time. Frequently, in this highly subjective concept, which is considerably better than the archaic practice of treating a specimen as if it were a species, human minds and eyes act as highly trained computing devices to perceive differences of form which characterize the individual organisms in a segment of a phylogenetic sequence. Bat taxonomy, based upon the unique anatomy of living and fossil bats, is informative in several ways in spite of its deficiencies. All mem­ bers of the order Chiroptera fly with moving wings. No other mammals do so although some are accomplished gliders (and some authors refer to the parachute membranes as "wings"). The two suborders of bats, Megachiroptera and Microchiroptera, differ in many anatomical and functional features. Megabats (with a few exceptions) have simple teeth, large eyes, possess a claw on the index finger, eat fruit, and live in

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GLENN L . JEPSEN

the Old World tropics. Microbats have diversified and complex teeth, small eyes, lack an index claw, eat insects and other animals (although a few indulge in different diets), and are more widely distributed than any mammalian taxon on this planet other than man. Many writers about bats have said that the big fruit bats are probably more primitive than the small insectivorous kinds. "Primitive" in this context frequently is intended to suggest "older" or "more ancient" or "prior" or "ancestral stem form" as well as "less highly organized ana­ tomically" or "less complexly related to environments" or having "charac­ ters of common inheritance." Judgments about these same attributes are frequently used also as the basis for drawing "family trees" of living forms, without reference to prior or ancestral forms. Most of these neogenealogic charts are short on information; they are useful mainly as exercises in organizing arrays of graded structures and they can contain slanted and misleading directives about "courses of evolution" and about genetic relationships and evolutionary rates. Fortunately this kind of phylogenetic arboriculture, wherein family trees are patterned solely upon living forms as a means of indicating degrees of relationship of fossil forms, is not as common a diversion as it used to be. Too many of such imaginary arrangements have proved to be wrong when gene­ alogies became better established through the discoveries of "missing links." In some groups of mammals the records of the fossil forms are thin indeed, a situation which leads taxonomists to try to weigh and assort the characters of living forms in order to "establish" phylogenetic trees and then ". . . an attempt should be made to incorporate recog­ nized fossils" (Martin, 1968). Only rodents outrank bats in the number of living genera and species (Simpson, 1945; Walker, 1964; S. Anderson and Jones, 1967). There are about 350 genera of rodents and half as many, about 175, genera of bats. (The numbers fluctuate from time to time and from author to author.) Next in order of decreasing number of genera are the car­ nivores with only about 100. In number of species the rodent-to-bat ratio is nearly the same, 2 to 1 (about 1685 and 875), as the ratio of genera. V. Fossil Bats Only a few extinct bat genera are known, probably about twenty. This is a ratio of recovered dead forms to known living forms of approxi­ mately 1 to 9, whereas the corresponding ratio for fossil to live rodents

1.

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11

is about 1 to 1.2. Bats, in fact, rank below all other orders of living mammals in the ratio of extinct to modern genera. (Monotremes, with no known extinct genera, and hence virtually no firm ancestral history, are an obvious exception.) In other words, bat fossils are extremely rare, and most of them are fragments that, of necessity, have been de­ scribed piecemeal, one by one, or in small collections rather than as a whole group. Descriptions of most of the known pre-Pleistocene bats appear in a few works^which are listed in bibliographies in recent pub­ lications (such as Dechaseaux, 1958; Jepsen, 1966; Sige, 1968; Viret, 1955). A few of these titles are given in the Reference section of this chapter (Friant, 1963; Handley, 1955; Heller, 1935; Lawrence, 1943). Only in a few places such as Bouzigues, France (Sige, 1968) are fossil bats a substantial part of a paleofaunule. Pleistocene and subRecent cave deposits do, of course, in many places contain large numbers of bat bones, but these are too similar to living forms to yield much information about the subject of this chapter. Indeed, most of the prePleistocene bats, except where they have been relatively abundant in European fissure deposits and lignites (Bouzigues, Phosphorites, Geiseltales) are usually taxonomically refractory. The bones are small, disso­ ciated, crushed, usually brittle and difficult to prepare for study, and they are not numerous enough to provide satisfactory bases for "specific diagnosis." For their classification, as for many other fossil vertebrates, the category of species has little real meaning, and the perception of differences between "species" becomes more intuitive than objective. This is not the place for an extended discussion of this fact but in many studies of fossil mammals the attempt to differentiate between "specific characters" and "generic characters" is merely a futile attempt to fit an archaic model of neobiologic taxonomy to paleontology. The late Professor W. B. Scott and I (1936) discovered, when we were preparing a monograph on early Oligocene mammals, that the species and subspecies categories were comparatively unimportant to our re­ search because many of the described "species" were really indetermi­ nate and were far too numerous to reflect real past ecologic conditions. For our conclusions at that time the genus was the significant unit, as it is for most studies of fossil bats, especially because they are rare and fragmentary. Several taxa of extinct bats are each represented by a single specimen. In such cases, of course, there is little reason to differentiate between specific and generic attributes, and, usually, no good basis for doing so. In the taxonomic records of some kinds of fossil mammals the males and the females have probably been placed in different taxa, particularly

12

GLENN L . JEPSEN

in the case of groups that had strong sexual dimorphism. Among the fractions of bones of multituberculates (classified as eccentric little, batsized, mammals that died out in Eocene time after more than one hun­ dred million years of vigorous family history, as indicated in Chart 1) which have been recovered in great numbers from quarries in northwest­ ern Wyoming we sometimes find pairs of types of teeth that are similar in general but also different in detail and size. These variations are such that they do not appear to be reflections of morphologic differences between species, but rather between genera or sexes (Jepsen, 1940, p. 257). Most bats show very little external sex dimorphism beyond the primary differences associated with sex organs, and the homologous bones that I have examined of Recent male and female bats appear to be almost identical in configuration and in degree of variation. This similarity is not remarkable but it at least diminishes the opportunities, in classifying fossil bats, of confusing sexes with species and genera. The described specimen of Icaronycteris index has a small bone of proper shape and position to be a baculum and is therefore believed to be a male. Among some modern bats the bones appear to vary more from individual to individual than do the bones of some other animals, but I have not studied enough samples to state this as a firm conclusion or to derive meaning from it. By the time in paleobiology history that I. index was a segment in the phylogeny of chiropts the whole vast galaxy of morphic, behavioral, and ecologic characteristics that distinguish bats from nonbat predeces­ sors had already been achieved. It is reasonable to assume that PU18150 is not a freak but a normal or average member of its taxa. It was much closer skeletally to modern bats than to a "generalized quadrupedal insectivore." It is not a taxonomic bifurcation, a crotch in the family tree, as Archaeopteryx (see Chart 1) is so frequently said to be. It is not a "missing link" between shrews or anything else and bats, but already a true bat. It cannot be used sensibly as a kind of midpoint in triangulating or extrapolating from living bats to it and then on back­ ward in time to a quadrupedal insectivore, from a hand-winged animal to one with a terrestrial forefoot. Nevertheless some inferences about "speed" or rates of evolution of bats are supplied by the fact that Icaronycteris index had reached its elegant degree of bat-status at the time it did in early Eocene (early Tertiary) time. It indicates that some bats had already evolved almost to their present grade of organization while horses were the size of modern dogs and mans ancestors were no larger than small monkeys.

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EVOLUTION

13

We know one species of "first horse" and one of "first bat." There were, undoubtedly, more species of each, although it is unlikely that in early Tertiary times bats and horses were as diversified as they became at the acme of their evolutionary careers which, for bats, seems to be now. From early Eocene to the present bats have lost from 16 to 32% of the number of bones in their hands (assuming that some living small bats are direct descendants of Icaronycteris index), while 63% of the forefoot elements of horses have disappeared, and man has remained pliably "primitive" by not discarding any of his ancestral hand bones. The increase in palmar area and in length of arm from an insectivore forefoot to a bat wing must be among the greatest increases in relative size of a single structure in mammalian history. An almost complete skeleton of an insectivore in the Princeton collection (No. PU14526) from the late Paleocene Polecat Bench formation of northwest Wyoming appears to be a "normal" and "primitive" (no parts "lost") insectivore with relatively large strong hind limbs for leaping, and of a size, overall, much bigger than Icaronycteris index from the Green River formation of southwest Wyoming. The length of the hind leg (femur plus tibia) of PU14526 is almost twice that of I. index whereas the front leg (hu­ merus plus radius) of the latter is about 2 times as long as that of the insectivore. The middle toe (ankle to tip of claw) of PU14526 is 3y times as long as this digit in I. index and the middle finger (wrist to claw tip) is % as long as that of I. index. The tip of nose to base of tail length of the latter is % as great as that of PU14526, whose tail, in turn, is 4 times longer than I. index's tail. Bodies of bats and leapers do indeed develop differentially for different ways to make a living. Men and horses are now much bigger than any known Eocene primates or ancestral equines, respectively, but Icaronycteris index was larger than some modern microbats. Among them the limits of size differ­ ence are comparatively far greater than the dimensional extremes from the smallest to the largest of wild horses or of wild men. The biggest megachiropteran is many times the size of the most minute microbat. Variation among kinds of living bats forms troublesome problems of taxonomic manipulation whereas, in contrast, horses are now curiously stereotyped. No wild horse either lacks a tail or has one that is longer than his body. Neither does any equine have a chinfold that can be elevated to go over the top of the head. Centurio does. No horses habitually eat fish, or blood, or lizards, as some bats do. Bat species differ greatly from each other not only in bulk of indi­ viduals but they show wide ranges of difference also in many other 2

14

GLENN L . JEPSEN

anatomic and physiologic attributes such as relative proportions of head, wings, body, legs and feet, and tail; they have greatly diversified physi­ ognomies, numbers and shapes of teeth, ears, nasal and mouth lobes, food and digestive habits, reproductive customs, thermoregulatory char­ acteristics, vocalizations, habitat preferences, and endo and ecto para­ sites. Patterns of flight and of anatomical devices associated with vocal­ ization are also extremely varied. Many features of bat distributions and habits are conditioned, directly and through food chains, by climate and weather and light conditions at different latitudes. Bats achieved their remarkable variety with the loss or reduction of some parts and with the elaboration of the remaining elements, in a kind of evolutionary development which is sometimes called "Williston's Law." Occasionally the "lost" parts show up in an individual animal such as Julius Caesar's polydactylous horse, and are regarded as exam­ ples of atavism. Bat's teeth, their food masticating apparatus, show a far greater range of varieties than do the dentitions of rodents or perissodactyls or primates. This fact suggests but, of course, does not prove that bats have had a longer time than the other groups to enter diversified dietary niches. From the known fossil record the rodents appear to have had a rapid morphologic diversification and a vast population explosion at about the time that Icaronycteris index was a vital species. Parallelism and wide diversities of habit and function mark the evolution of rodents. Bats, for their practices in torpor and other activities, are sometimes regarded as having imperfectly controlled body temperatures but the rodent Ηeterocephalus has ". . . the poorest capacity for thermoregula­ tion of any known mammal" (McNab, 1966, p. 712). The early Tertiary rise of rodents occurred more or less apace with the decline of multituberculates, previously mentioned, a vigorous and diversified order, with many members, that had flourished at least since mid-Mesozoic time. Rodentlike in habitus, they have been called ecologic ancestors of rodents or pre-rodent analogs of rodents. Multituberculates and rodents almost certainly were in vigorous competition with each other for certain places in nature, as several authors (Hopson, 1967; Jepsen, 1949; Landry, 1965, 1967; Van Valen and Sloan, 1966) have noted in their search for explanations of the fact that rodents now are nearly the only mammalian occupants of many territorial areas on and partly under the ground, and in the bushes and trees that were previ­ ously the home sites of multituberculates (and perhaps of other small mammals like primates and insectivores). As far as we know none of these groups were either flyers or gliders. Perhaps the bats beat them

1.

B A T ORIGINS AND

EVOLUTION

15

to the volant mammalian niches and defended these regions against invasion. Not a trace of a rodent that is surely older than the late Paleocene species Paramys atavus (see Chart 1) has been discovered. Some au­ thorities (see Wood, 1962) in discussing the great blank in the record of earlier ("first") rodents have wondered if members of the order were actually in existence for a long time and simply have not been found or if they branched suddenly into being from another order. More fossils are needed to extend backward in time the geological documents of rodent genealogy and, unquestionably, they will be found. At present, however, there is no direct evidence to support a belief (conjecture) that rodents were abundant and diversified before late Paleocene or that they were an early derivative from any of the highly developed and intricately interrelated and numerous populations of primates of mid-Paleocene age. Members of several of these prosimian branches had long procumbent gliriform anterior lower incisors and were thus equipped by part of their dental hardware to gnaw in rodentlike fashion. The resemblances were probably superficial. None of the known Tertiary rodent competitors among primates and multituberculates were gifted with incisors that grew from persistent pulps and formed self-sharpening chisels. What is the significance of these observations to the origin and evolu­ tion of bats? Rodents and bats, the two orders of mammals with the greatest number of living genera and species are, as far as their fossil records go, about equally old, appearing in late Paleocene and early Eocene, respectively (see Chart 1), long after the oldest known primates and multituberculates had become numerous and diversified. By the time that rodents, in our discovered records, were becoming abundant and ecologically varied, the bats were already totally volant, and were, compared with rodents, highly precocious. Living "flying" squirrels are obviously quite adequate as gliders but rodents have never evolved a true flyer with wings. Most rodents are not habitually insectivorous as are most microbats and hence are not in competition with them for food. And, although many rodents have their maximum activity periods at night their sensory equipment for food gathering is quite different from the refined acousti­ cal apparatus of microbats. Rodents apparently never have had the ca­ pacity to echolocate in bat fashion, although other small Tertiary mam­ mals may have had this ability if brain configuration (development of acoustic colliculi) is a reliable indication (Jepsen, 1966, p. 1338). This observation suggests another question. Were the early primates

16

GLENN L . JEPSEN

the prime competitors of pre-bats for food and territorial rights? Primates were abundant in mid and late Paleocene time. Quarry samples in the Polecat Bench formation in northwestern Wyoming sometimes contain more jaws and teeth of primates than of any other order, and the kinds of primates are also more numerous than are the subordinal taxa of other orders. Obviously the question has no substantial answer but it leads again to the other question, When were bats first volant, and why? Whenever it was, in the Mesozoic or Tertiary, flight was no novelty in locomotion even then. Many kinds of animals, in fact more than one-half of known living species, mainly insects, have become flyers in their struggle for existence. The repeated speculation, as a presumed example of rapid evolution (see Mayr, 1963, p. 617), that bats originated suddenly in the Paleocene Epoch (which lasted perhaps ten million years between Fig. 1. Reconstruction of axial skeleton and limbs of right side, dorsal aspect, Icaronycteris index, PU18150. 1.5 X . 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

second and third upper incisors upper canine coronoid process of dentary lateral process of atlas axis seventh cervical vertebra twelfth rib first lumbar vertebra seventh lumbar vertebra sacrum first caudal vertebra third caudal vertebra thirteenth caudal vertebra clavicle scapula pectoral ridge of humerus shaft of humerus radius ulna carpus (wrist) metacarpal of first digit (thumb) second phalange (cfow) of first digit metacarpal of second digit proximal (first) phalange of second digit second (middle) phalange of sec­ ond digit

26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45

third (distal) phalange (claw) of second digit metacarpal of fifth digit proximal (first) phalange of fifth digit second (middle) phalange of fifth digit third (terminal) phalange (chw) of fifth digit iliac crest of pelvis acetabulum obturator foramen ischium femur patella tibia fibula tarsus metatarsal of first digit second phalange (claw) of first digit metarsal of fifth digit proximal (first) phalange of fifth digit second (middle) phalange of fifth digit third (terminal) phalange (claw) of fifth digit

Fig. 1. 17

Fig. 2. Reconstruction of right side of skeleton of Icaronycteris index, PU18150, 1.5X. (Some bones are foreshortened.)

18 GLENN L. JEPSEN

ORIGINS AND

(Some bones are fore­

BAT

Fig. 3. Right side of a skeleton of Myotis myotis, 1.5χ, redrawn from de Blainville (1840). shortened. )

1. EVOLUTION 19

DIMENSIONS ( M M ) O F P U 1 8 1 5 0 ,

Icaronyctens index*

Entire specimen length 125.0 Skull length (anterior incisor, 12, to posterior border of occipital condyle) J a w length (anterior incisor, il, to rear border of condyle) 15.3 Upper tooth row length ( I 2 - M 3 ) 9.3 Lower tooth row length ( i l - m 3 ) 9.3 Upper molars ( M 1 - M 3 ) , midline 3.7 Lower molars ( m l - m 3 ) , midline 4.5 Total length of the 7 cervical vertebrae 9.9 Total length of the 12 thoracic vertebrae 18.1 Total length of the 7 lumbar vertebrae 16.7 Total length of the 3 sacral vertebrae 5.8 Total length of the 13 caudal vertebrae 52.4 Lengths of wing elements: Humerus 34.3 Metacarpal 2 28.5 Ulna 28.0 Metacarpal 3 40.1 Radius 48.0 Metacarpal 4 39.0 Metacarpal 1 3.5 Metacarpal 5 38.0 Proximal phalange, digit 1 5.7 Proximal phalange, digit 2 4.9 Proxmal phalange, digit 3 10.9 Proximal phalange, digit 4 11.5 Proximal phalange, digit 5 10.1 (L) Second (terminal) phalange, digit 1 2.7 Second (middle) phalange, digit 2 4.9 Second (middle) phalange, digit 3 18.8 (L) Second (middle) phalange, digit 4 16.1 (L) Second (middle) phalange, digit 5 12.2 (L) Third (terminal) phalange, digit 2 1.5 Third (terminal) phalange, digit 3 0.4 (L) Third (terminal) phalange, digit 5 0.3 (L) Lengths of hind foot elements: Femur 19.8 Metatarsal 2 3.2 Fibula 18.4 (L) Metatarsal 3 3.3 Tibia 18.3 (L) Metatarsal 4 3.4 (L) Metatarsal 1 2.8 Metatarsal 5 3.1 Proximal phalange, digit 1 3.4 Proximal phalange, digit 2 2.4 Proximal phalange, digit 3 2.5 Proximal phalange, digit 4 2.5 Proximal phalange, digit 5 2.6 (L) Second (terminal) phalange, digit 1 2.5 Second (middle) phalange, digit 2 2.5 Second (middle) phalange, digit 3 2.5 Second (middle) phalange, digit 4 2.7 Second (middle) phalange, digit 5 2.7 Third (terminal) phalange, digit 2 2.3 Third (terminal) phalange, digit 3 2.3 Third (terminal) phalange, digit 4 2.1 (est.) Third (terminal) phalange, digit 5 2.1 (est.) Ratios of dimensions ( X 100) Humerus: radius 71.5 ( R ) , 7 2 . 8 (L) Femur: humerus 57.7 ( R ) , 53.2 (L) a

20.1

Right side of paired elements unless indicated by L .

Fig. 4.

Head dorsal aspect of Icaronycteris index, PU18150.

4χ.

At atlas Cp coronoid process of left dentary Ax axis 12 second upper right incisor C upper canines H>2,3 left lower incisors c left lower canine L locator bristles (installed as "landmarks" to indicate same spot on opposite sides, dorsal and ventral, of the skeleton) Lc internal side of condyle of left dentary (protruding through skull roof) m3 third lower right molar (protruding through skull roof) PI left premaxilla Rc external (labial) part of condyle of right dentary (protruding through skull roof) Sc semicircular canal (right anterior vertical, protruding through skull roof) So supraoccipital crest Ζ zygomatic arch 20

21

Fig. 4.

BAT ORIGINS AND EVOLUTION

22

GLENN L. JEPSEN

the Mesozoic Period and the Eocene Epoch) lacks supporting evidence of any kind. At present, bat history has a completely open end, in the distant past, that only more fossils can close. The baseless speculation of a "probably Paleocene" origin of bat flight is repeated by Peyer (1968, p. 226). If bats successfully flapped their wings before the insectivores spawned the primates that may have spawned the rodents, the search for compelling competitions that may have been associated with the origin of bats must go deeper into the geobiologic record and look at other possible agents, at small mammals such as antique insectivores or marsupials (or the subeutheres whose known geologic ranges are restricted to the Mesozoic) and also look at submammalian taxa like reptiles and birds. But here we are in an area of such rarefied facts that at present we must substitute flights of imagination for evidence on the causes of bat flight. Peyer's observation (1968) that insectivores and bats and primates have similarly simple "enamel relations" in teeth may be significant in tracing ordinal relationships and times of origins. VI. Designs of Wings Wholly independently bats and birds and reptiles invented wings, using different designs to flap differently in the same air. We don't know when any of the vertebrate true flyers originated or how they took to the air. Of the three groups the Mesozoic reptilian pterosaurs (see Chart 1) became the most "highly specialized" in aerial adaptation. Durable wing membranes extended from their long strong fourth fingers to the body and to the hind legs which, like the feet, were so reduced and gracile that they apparently had no use except as rods and hooks for suspension of the body from rocks and plants (Hankin and Watson,

Fig. 5. An Ax C Cp Fp Gl i3 L Ld

Head, ventral aspect. 4χ.

angular process of right dentary axis upper right canine coronoid process of left dentary postglenoid foramen glenoid fossa third lower left incisor locator bristles labial surface of left dentary

M3 m3 Oc P4 p3 SI Vc Vd Ζ

third upper right molar third lower left molar occipital condyles fourth upper right premolar third lower left premolar left stylohyal vertebroarterial canal of atlas ventral border of right dentary zygomatic arch

23

Fig. 5.

BAT ORIGINS AND EVOLUTION

24

GLENN

L.

JEPSEN

1914). How these animals managed any kind of locomotion is a mystery in mechanics. The larger ones, fish eaters probably, have been called reptilian analogs of albatrosses. Some of them were probably hairy and may have been warm-blooded in response to the problems of metabolism that they faced as volant vertebrates. If bats gained wings early enough, in the Mesozoic, they may have been in territorial and dietary rivalry with the flying reptiles which, as a group, had a known temporal range through most of the Jurassic Period and through the Cretaceous Period, a total duration of more than one hundred million years. In fact if bats were a sufficiently ancient mammalian novelty they may have had interlocking and reciprocal ecologic connections not only with birds and small pterosaurs but also with moths and other insects. Each of these groups might have affected the others' courses of evolution. Surely some living bats and moths have special anatomic and behavioral features that are essential to their cur­ rent biotic relationships to each other. In the worlds of some microbats there are remarkable varieties of body temperature fluctuations, correlated especially with habits of flying and with periods of inactivity and of torpor. It would be satisfying to be able to indicate some Mesozoic or earliest Cenozoic occurrences in climate or air conditions or habitat controls that could have had a causal relationship to the eccentricities of bats' thermal behavior, but no such factors of influence are known. VII. Caverns and Crevices To the varied modern conditions of temperature and humidity in the caves and crevices where they spend most of their time, many small bats have made various ethologic and anatomic responses. Some of the behavioral consequences and morphologic correlatives of roosting and landing and launching in caves and crevices have been skillfully pre­ sented by Vaughan (1959). Of necessity the entire way of life of bats is modified by these habitats, in the functioning of temperature-regulat-

Fig. 6.

Upper right teeth. 11 χ .

C canine Ld labial surface of left dentary Ml first molar Vd ventral border of right

M3 third molar P2 second premolar P4 fourth premohr dentary

25

Fig. 6.

BAT ORIGINS AND EVOLUTION

26

GLENN

L.

JEPSEN

ing metabolic systems, in respiration, and in reproductive habits. Caves and crevices were available for occupation many hundreds of millions of years (probably billions) before there were any bats in them. Caves are a stable habitat, shielded from some of the natural forces that influ­ ence life in less protected environs. At present we can only speculate about the long-time effects of cave occupation by bats. Perhaps certain mutagenic factors such as cosmic rays may have unusual relationships to the evolution of cave bats. Very little is known (or agreed to), how­ ever, about maximum natural rates of evolution (Smith, 1968) or about the relationships of "observed" rates in phenotypes and the theoretical rates at the molecular level. Very few kinds of animals are cave dwellers now; perhaps formerly there were more and they could successfully resist the incursions of expanding groups. Even today not much is known about cave life; it is very difficult to investigate. Caves are used occasionally as temporary shelters by several kinds of vertebrates such as turtles, snakes, mar­ supials, porcupines and other rodents, raccoons, bears and hyenas and other carnivores, but bats are apparently the only terrestrial (or aerial) mammals that have taken advantage of their capacity for echolocation to find satisfactory continuous and extensive refuge in caves. Whether this shift of habitat occurred through strife or in peace the records do not yet reveal, and probably never will. The near absence of natural enemies in caves must have had profound effects upon the ecologic and social habits of bats; only in cave conditions could they indulge in such long periods of torpor and hibernation. Nor do we know whether the atmosphere in caves, with its special qualities of air circulation and composition, was a particular attraction to animals with the energic properties and dietary habits of bats. Bats themselves have effects on the atmosphere of caves (see Constantine, 1958; Mitchell, 1964). Bartholomew et al. (1964) have concluded that to the largest and to some of the smallest fruit bats of Australia ". . . the major challenge

Fig. 7. Crowns of lower righ t teeth penetrating skull roof. βχ. C c 12 il,2,3

M3 tips of roots of third upper upper canines right molar lower canines (tip of right ml ,2,3 first, second, third lower right one is broken and dis­ molars placed ) Nl left nasal bone second upper right incisor Fl left premaxilla stubs (bases) of lower in­ cisors p3,p4 protoconids of third and fourth lower right premolars

Fig. 7.

1. BAT ORIGINS AND EVOLUTION

27

28

GLENN L . JEPSEN

presented . . . by the physical environment is high summer tempera­ tures" (p. 198). Bat ancestors may have become permanent cave dwellers at an early date in their phylogeny, perhaps to escape avian predators. Fully evolved owls (Wetmore, 1938) and vultures were contemporaries of bats in early Tertiary time and probably in the preceding Cretaceous period. In caves bats could conserve energy and moisture between the periods of high activity when nocturnal moths and other insects were available in the air for food and when most birds (and, perhaps, pterosaurs) were not on the wing as competitors. Many widely distributed insects such as moths, butterflies, bees, wasps, dragonflies, owl-flies, and lacewings are effectively "warm-blooded" (Adams, 1969) in their ability to raise their thoracic temperatures above ambient levels to optimum temperatures for flight (which are about the same as the "normal" temperatures of many mammals) by fast lowamplitude contraction of the flight muscles ("shivering"). These insects, while flying, are able to maintain the requisite temperature levels in conditions of varying thermal loads and different environmental tempera­ tures (Adams and Heath, 1964). Insects with this kind of endothermic (or homeothermic) capacity have " . . . a degree of freedom from en­ vironmental thermal conditions which approaches that of small birds and mammals" (p. 22). This phenomenon may be much more widespread, among insects, than present observations indicate, and it may be related significantly to the nocturnal habits of insectivorous bats. If so it supplies a "positive" or attracting factor in natural selection for the initial development of the abilities of bats to feed in the air on the wing. Whether bats readily detect the infrared radiations of warm moths is a subject for future consideration. It has been suggested by Heath and Adams (1967) that these radiations may be used by moths in conjunction with pheromones as aggregating signals; and this possibility raises the question of whether bats are able to intercept such signals and use them to advantage.

1

Fig. 8. An C Cp c il,2,3

Left dentary. 5% χ .

angular process of left dentary upper left canine coronoid process lower canine first, second, and third lower left incisors Ζ

ml,2,3 Mf p2,3,4 Vd

first, second, and third lower left molars mental foramina second, third, and fourth lower left premolars ventral border of right dentary

zyp omatic arch

Fig. 8.

1. BAT ORIGINS AND EVOLUTION

29

30

GLENN L. JEPSEN

Although the development of endothermy and of nocturnal habits by insects enables them to avoid the predations of diurnal (day-feeding) birds it exposes them to the predatory capacities of insectivorous bats. This consideration may suggest that birds were a controlling factor in the escape of insects to nocturnalism which, in turn, attracted the primor­ dial bats to night-feeding. This comment grossly simplifies the probable complexities of the processes, but it suggests, however tenuously, that birds evolved earlier than bats did and that insectivorous bats were antecedent to fruit bats. Insects have acquired various kinds of volitional and autonomic behavioral systems that act as bat-evading (escape) mechanisms, and the development of such structures as scales by insects may also be partly a function of the predator-prey relationship. Microbats, regarded as being among the most imperfectly homeothermic of mammals, do of course develop their energy budgets correlative with climate, food supply, and behavior. They have various adaptations and activity patterns that fit their caloric utilization in periods of flying, of torpor, and of aggregation in caves. If body heat was a critical factor in bat existence in caves then population density has had an unusual survival value in the evolution of bats. The habit of clustering in a hibernaculum, however, may be a social expression more than a means of preventing the loss of body heat (Stones and Wiebers, 1965, p. 162). Bats do not build nests in caves, nor can they store energy sources such as insects or fruit in caves or crevices. The major expenditures of energy by bats occur in relatively short periods of the day and of the year when they are flying outside of caves. Hahn (1908, p. 152) estimated that a cave bat spends about five-sixths of its life hanging head downward in almost motionless dormancy in the dark. This energy conservation may be a factor in the great longevity, for mammals of their size, of some bats. Pre-bats presumably were more perfectly homeothermic than living forms are and had a different distribution of insulating hair and epi­ dermis. Why and when did some of them select caves or retreat into them and begin the series of intricate adjustments and refinements of Fig. 9. Ab Ac Cv Gf Gt

Right shoulder without acromion process of humerus. 5 χ .

axillary border base of (removed) acromion process clavicle glenoid fossa of scapula greater tuberosity (trochiter) of humerus

Hh If Sf Sp St

head of humerus infraspinous (postspinous) fossa supraspinous (anterior) fossa spine of scapula supraglenoid tuberosity

Fig. 9.

CO

δ

Ο

32

GLENN L . JEPSEN

anatomy and habit that are parts of bat existence? Nothing in geology gives a definitive answer. Years and days were almost the same lengths in Mesozoic and early Tertiary time as they are now. No known condi­ tions in nature have been recognized as compelling causes for the origin of bats. The energic costs of living seem not to have changed during the emergence of bats from nonbat ancestors. Heat conservation or thermal control is a major factor of natural eco­ nomics not only in cave-inhabiting bats but in all bats, big and little, because the wings present so much surface to the surrounding atmo­ sphere. The feathers of avians form an effective insulating device that some specialists on fossil reptiles believe was developed as a protective and insulating armor in the evolution of birds (from archosaurs) before they became warm-blooded. Pre-avians were thus able to maintain con­ stant body temperatures, prior to the time that any birds were able to fly. VIII. Bats and Birds In attempting to rationalize about the beginnings of bats it may be meaningful to compare living chiropts (especially microbats) with flying birds. Both the similarities and the differences in the two groups may contribute some information to the subjects of times and modes of origin and of the major reasons for flight in the two groups. For each of the following pairs of opposed qualities the bat characteristic is stated first. For simplicity and in order to avoid endless minor qualifications and exceptions (some of which are applicable to nearly every item on the list) the entries are greatly abbreviated. It is common knowledge, for example, that most fruit bats are stationary feeders (see item 22) and that some bats do not echolocate and some birds do (see item 30). (1) Hair: feathers; (2) viviparous: oviparous; (3) nonnucleated red blood cells: nucleated erythrocytes; (4) teeth: edentulous; (5) no air sacs: air sacs extensively developed; (6) no reduction of tarsal bones: reduction and fusion; (7) parts of all five fingers present: only three

Fig. 10. Right shoulder with acromion process on humerus. 5 χ . Ac Cv

acromion process clavicle

Gt Hh Hp

greater tuberosity humerus

head of humerus pectoral ridge of humerus

(trochiter)

of

B A T ORIGINS

AND

EVOLUTION

Fig. 10.

1.

33

34

GLENN L . JEPSEN

fingers represented; (8) urinary bladder: none; (9) feet small, "weak": big, "strong"; (10) big external ears: no projecting earlobes; (11) use hind limbs in flight: do not; (12) body thin dorsoventrally: thick; (13) small keel on sternum: large; (14) head flat: high; (15) no renewable flight structures: wing feathers renewed; (16) "poor" insulation: "good"; (17) use forelimbs in terrestrial and arboreal locomotion: do not; (18) little sex dimorphism: extreme differences in sexes; (19) dull colors: bright; (20) wings can work independently of each other in flight: cannot; (21) very maneuverable in flight habits with flexible wing membranes: much less so with stiff feathers; (22) feed during nocturnal flight: rela­ tively stationary diurnal feeders; (23) many muscles involved in flight: few; (24) live in crevices and caves: in trees and on ground surfaces; (25) don't build nests: do and have reduced mobility when brooding; (26) long gestation period: short time for incubation; (27) hibernate: do not; (28) roost heads downward: heads up; (29) hang by feet: perch upright; (30) highly developed auditory response (echolocating) system: do not echolocate, but are more sight-oriented; (31) no alula: "bastard wing" present; (32) comparatively low rate of reproduction: high; (33) smaller range of ambient temperature tolerance: tropical to subpolar distribution; (34) smaller range of size: hummingbirds to moas; (35) smaller range of rate of wingbeats: much greater range, slow flaps to hovering. (Specialists will think of many other differences.) One of the most obvious class distinctions between bats and birds is the habit of lactation by bats and the absence of similar exudation for neonates by birds. The social structures of families, of clans, and of entire populations are conditioned by this fundamental difference, and it has significant implications in speculations about the origins of bats and of birds. Also obvious is the very important fact that bird and bat brains are quite dissimilar in configuration and function. Each of these neural centers, to state a truism, was capable throughout its evolution of operating in a way appropriate to each morphic and be­ havioral stage. To be a microbat a bat brain was necessary, with the

Fig. 11. Right carpus. About 7 χ.

Mm Prl

metacarpals of first digit (thumb) and second and third digits magnum proximal phalange of first digit (thumb)

R Se Sr Td Tm Urn

radius sesamoid bones scapholunar trapezoid trapezium unciform

AND

EVOLUTION

Fig. 11.

B A T ORIGINS

36

GLENN L. JEPSEN

development of acoustical areas that were capable of functioning in the techniques of echolocation. For many years the belief was often repeated that Archaeopteryx was really a kind of flying reptile with a reptile's brain and a bird's feathers. Recently Jerison (1968) has reexamined and reinterpreted an endocranial cast of this bridge-bird and has concluded that Jurassic Archaeopteryx has a brain in . . an intermediate stage of evolution, clearly nonreptilian, more or less avian, but not modern" (p. 1382). Some bats, like some birds, apparently have strong territorial affilia­ tions, have widely varied food habits and food-getting structures, have hollow bones, are powerful vocalizers. Thus, in summary, there are many differences and few similarities in the ways that bats and birds solved similar problems of aerodynamics and got into the air. Birds developed terrestrial bipedal locomotion and freed the forelimbs for flight; bats redesigned the fore and hind legs and feet for multiple duty. IX. Bat Hand-Wings or Wing-Hands A common assumption that the bat's wing has become almost useless for anything but flight (see Winge, 1941, p. 255 et seq.) is not sustained by observation. In fact, both fore and hind limbs of bats have many varied functions. Wings continue their use as forelegs and hands in ambulation and they are employed in fast locomotion or scuttling on the ground and in swimming. They help in catching insects (Webster and Griffin, 1962), in hanging from and walking along cave walls and ceilings; and in controlling body temperature by radiation. They act as fans, as insulating overcoats and windbreaks and raincoats, and as areas for evaporation. Some megabats create their own microcaves or controlled environment capsules by the way they wrap their wings about their bodies, and, in some microbats, the dorsal (outer) layer of the

Fig. 12. Right CI Η 1c Mc2-5

calcite filling of cavity in humerus humerus index claw (ungual phalange of second digit) metacarpals of second to fifth digits V varves (layi

bow area. Pr2-5

4χ.

proximal phalanges of second to fifth digits R radius S2-5 second (middle) phalanges of second to fifth digits Se sesamoid bone U ulna ? of sediments)

BAT ORIGINS AND EVOLUTION

37

>—ι

38

GLENN L . JEPSEN

dual wing membrane is comparatively nonvascular, apparently serving as an insulating sheet over the highly vascular ventral (palmar) layer. Bats, apparently, have almost literally always had their best foot forward. Many aspects of the evolution of the patagium of bats should be considered. Did it originally have some functions other than that of a flight structure and is its present development merely an extensive remodeling and refinement of its primordial construction for other utili­ zation such as aggressive threat display? If so, which, if any, of its modern functions were the first ones? These questions may seem non­ sensical, but the wing was a foot before it was a wing, and no other mammals have evolved anything even remotely resembling a flapping wing except in science fiction and in religious art. For a leg and foot to become a mammalian wing the selection pres­ sures must have been compelling and continuous. How long in time was the foot in transition from walking to flying? What were its functions during this period? For lack of evidence to the contrary, and because there are so many difficulties and unknowns in our attempts to answer these questions I am assuming that the bat wing evolved only once, that a schism into megachiropts and microchiropts occurred after the time that mammalian wings evolved from feet. This belief could be falsified by future discoveries of fossils but not, presumably, by any studies on living bats although there are many profound differences between megabats and microbats. Especially notable dissimilarities may be seen in their auditory and thermoregulatory systems, their visual apparatus (but see Suthers, 1966), reproductive systems and habits, food habits, hanging postures, geographic distribution, and habitat selections. The oldest known fossil megachiropt apparently is the early Oligocene Archaeopteropus (see Chart 1) from Italian lignites (K. Anderson, 1912; Meschinelli, 1903; Dal Piaz, 1937), about 35 million years old. A. transiens was a large bat, with a wingspread of about a meter (as stated by Dal Piaz, 1937, p. 4 ) , a long tail, and well-developed calcars or spurs on its heels. It probably had a long and clawed index finger as well as teeth with pointed cusps, but the poor preservation of part

Fig. 13. Η Ic

Index claw bone (terminal phalange) of second digit of right manus. 34χ.

humerus index claw bone (ungual or third phalange of second digit) Pn perforation

S2 second (middle) phalange of second digit U ulna

Fig. 13.

1. BAT ORIGINS AND EVOLUTION

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GLENN L . JEPSEN

of the incomplete skeleton has precluded rigorous study of dental and other details. The specific name referred to the nomenclator's belief that the specimen was intermediate between the megachiropts and the microchiropts, but most taxonomists now prefer to regard it as a megabat. In length the humerus and radius of A. transiens are each about 2y times the size of these elements in Icaronycteris index, and the femur and tibia in the Italian form are 3 times the length of the corresponding bones in I. index. And this latter ratio holds for wingspread if Archaeopteropus transiens really did measure a meter between wing tips. Living megabats as a subordinal group are curiously stereotyped and invariant, as compared with the multitudes of wide diversities among microchiropts. All modern megachiropterans are classified as members of one family, the Pteropodidae (sometimes spelled Pteropidae) whereas the microchiropterans are usually divided by taxonomists into about fifteen or sixteen (Miller, 1907) families. Icaronycteris index as a species may have been directly ancestral to all or to some living microbats or megabats or to none of our contempo­ rary chiropts. It is surely related, at least collaterally, to some existing bats, and it, like every other mammalian species, represents a transitory moment in a long phylogenetic line or cord wherein the genetic fibers vary in length and no two segments are precisely alike. Some parts (some threads) of the genome of I. index certainly still function in the genetic stuff of modern bats, and other biochemical fractions have ceased to operate as they did 50 million years ago, in the phenomena of natural selection, through the ceaseless evolutionary pulse of genome-phenomegenome. Throughout the geologic history of bats (and of all other com­ plex animals) the filaments of the phylogenetic cords constantly undergo partial mutative extinction and partial viable transformation in the origin of new forms—of new "species." A skeleton of an old dead bat doesn't give much direct information about the details of genie history although it may be richly informative about broad evolutionary generalities. 3

X. Gliders Don't Fly and Vice Versa Bat evolution, from ground or branch to air, was a short distance up or down in space but a vast distance in genetic alteration and funcFig. 14. Clawlet (ungual phalange) of left anterior fifth digit ("little finger"). 41 χ. CI, Calcite filling of second phalange; S5, second (middle) phalange; T5 terminal phalange (clawlet).

B A T ORIGINS

AND

Fig. 14.

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EVOLUTION

41

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GLENN L.

JEPSEN

tional design. Frequently this transmutation is assumed to have occurred quickly, in the all-or-nothing contention that a nonaquatic animal either walks or flies and that intermediate gliding grades must be evanescent because they are mere passageways from one stabilized organization to another, from life as terrestrial or arboreal animals to that as winged bats. The invalid and fallacious analogies of all-or-nothingness in the development of the vertebrate eye and of the rattlesnake's keratinous buzzer are sometimes introduced for support of this erroneous princi­ ple—whose content of teleology and orthogenesis discredits it for most vertebrate paleontologists. It is factually weak for the simple reason that life as a gliding or volplaning mammal seems to be a durable plateau of structure, a function-environment organization which has been established several times—by marsupials, by rodents, and by dermopterans, among living forms. [At least two groups of reptiles have become gliders without becoming flyers (see Colbert, 1966, 1967).] For effective use of the skin patagium that extends from neck to forelimb to hind limb to tail (if a tail is present) mammalian gliders require strong front and back feet to launch from and to land on tree branches or other areas. Although the gliding dermopteran Cynocephalus (or Galeopithecus) which is wholly misnamed "the flying lemur," is said to be ". . . almost a bat in some respects" (Allen, 1939, p. 175) or illustrative of ". . . an intermediate stage in the development of flight" (Romer, 1959, p. 297), it may be as closely related to rats as to bats. Its handweb or chiropatagium includes the thumb and the four fingers whereas in bats all or at least part of the thumb is free. And, of course, the large forefoot of dermopterans is not truly winglike in the sense that a bat's is. Darwin, in the "Origin," classed the flying lemur ("once ranked amongst bats") with the insectivores but observed that it has Fig. 15. A Ap Ca Cd Cf F G Hf 11 It

Pelvis, dorsal aspect. About 3 . 7 5 χ .

acetabulum anterolateral process of seventh lumbar vertebra calcaneum first caudal vertebra fourth caudal vertebra fibula greater (major) trochanter of femur head of femur crest of right ilium ischial tuberosity

Ls Mtl Mt5 Ο Prl Sa S2-5 Ti Τ2

seventh lumbar vertebra metatarsal of first digit (big toe) metatarsal of fifth digit obturator foramen proximal phalange of first digit sacrum second (middle) phalanges of second to fifth digits tibia terminal phalange (claw) of sec­ ond digit

B A T ORIGINS

AND

EVOLUTION

Fig. 15.

1.

43

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GLENN L . JEPSEN

no living link to other insectivores and that if its fingers and connecting membranes were greatly lengthened by natural selection it could have been converted into a bat. Of course, but he did not suggest any pres­ sures for the change. Now the "flying lemur" is the only living form in the order Dermoptera. Not to my knowledge has anyone made a detailed and thorough com­ parison of dermopteran and chiropteran structures and functions al­ though many authors have noted superficial likenesses. The obvious ana­ tomic resemblances are probably "homeomorphic similarities" (or repeti­ tions) rather than sequential stages in the evolution of flight. No one now believes that dermopterans and chiropterans are closely related, for they most probably have had entirely separate phylogenies since Paleocene time. Plagiomene multicuspus (see Chart 1), approximately contemporary with early Eocene Icaronycteris index, appears to have been a direct ancestor or collateral relative of the modern dermopterans and already had digitate margins on the lower incisors, perhaps the beginning of the unique "comb incisors" of the living form. Planetetherium mirabile, the best presently known nominee for a tree-dwelling ancestor of Vlagiomene, comes from a late Paleocene coal bed in Mon­ tana in a faunule that includes the oldest known rodents. Morphologically and genetically and phylogenetically the distance from a gliding habit to a bat-flying habit among known mammals is so immense that a development of the former may almost be said to preclude the probability of further development in the same phyletic line to the latter. As Moody (1962, p. 505) observed "gliding does not provide the means for entering the flying insect-eater niche." The mor­ phology-habit plateau of several living mammalian gliders seems to in­ dicate that they are successfully adjusted to continued existence as such in their firm ecologic niche. A glide distance by a "flying lemur" of 136 m has been reported (Walker, 1964, p. 180) and giant "flying" squirrels of S. Asia have been observed to glide on favorable air currents as far as 4500 m (p. 716). Neither of these eutheres nor the "flying" Fig. 16. A Ap Cf F Fl G

Pelvis, ventral aspect. About 3.75χ.

acetabulum anterolateral process of seventh lumbar vertebra fourth caudal vertebra fibula lesser trochanter of femur greater trochanter of femur

Hf Ls Ο Ps Sa Sp

head of femur seventh lumbar vertebra obturator foramen pubic symphysis sacrum spine of pubis

Fig. 16.

1. BAT ORIGINS AND EVOLUTION

45

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GLENN L . JEPSEN

marsupials, Acrobates, Petaurus, and Schoinbates are known to forage or eat while volplaning; the whole function of the glide seems to be transportation. Most gliders appear to be firmly committed to having slender, long, and strong fore and hind legs, plantigrade and pronograde feet, to occupying open arboreal habitats, and to eating mainly vegetable food, although some Acrobates are known to eat various insects, and some Petaurus catch flying moths by leaping after them, and will eat other small animals. All living dermopterans, the arboreal colugos of Asia, are poor candi­ dates for the development of true flight in the future. They are nocturnal herbivores, are said to be slow moving and unable to stand erect, and they cling head-down or head-up (see Findley, 1967, p. 108) by their claws in tree cavities during the day. It is almost as logical to think of dermopterans as being derived from bats as it is to entertain the idea of a dermopt-to-chiropt lineage. In the transformation from terrestrial forefoot to aerial wing, bats used all five metacarpals and all the phalanges of the standard mam­ malian hand, two in the thumb and three in each of the other four digits (phalangeal formula 2-3-3-3-3). Icaronycteris had the full comple­ ment of these bones (although the terminal or ungual members of digits III, IV, and V were mere nubbins) but all the living small bats have "lost" some finger ossicles. Somewhere along the genealogic line when bat hands were evolving up to flight some ancestral genomes failed to hand down some bones. XI. The Forefinger, Index of Function If Icaronycteris is ancestral to any or all of the living microchiropterans why did it possess a strong and separate clawed index finger whereas

Fig. 17. A

Ca Cf Cu F Hf Mtl-5 Ν Ο

acetabulum calcaneum fourth caudal vertebra cuboid fibula head of femur metatarsals of first to fifth digits navicular obturator foramen

Feet.

5χ.

Prl-3,5 Ps Sa S2-5 Tl-5 Ti

proximal phalanges of first to fifth digits pubic symphysis sacrum second (middle) phalanges of second to fifth digits terminal phalanges (claw bones) of first to fifth digits tibia

Fig. 17.

1. BAT ORIGINS AND EVOLUTION

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GLENN L. JEPSEN

their index finger is reduced to the small incomplete clawless digit that is closely associated with the strong third finger as a brace along the leading edge of the wing? Some authors have effortlessly assumed that the index claw of Icaronycteris was a useless vestigial structure well on the way to being mutated out through selection. This theory, of course, is possible only retrospectively. When it is regarded without commitment to its future disappearance the taloned index digit of Icaronycteris may be seen as a comparatively strong, powerfully mus­ cled, and highly functional part of the bat, a sharp-pointed finger for catching insects and other prey, impaling grubs, feeding, climbing, walk­ ing, clinging, piercing, scraping, grooming, and for offense and defense, with possibly, some advantageous properties of weight distribution and aerodynamics for a flying animal. Retention of the whole index finger, relatively no larger than that of Icaronycteris, by living megabats may be cited as proof of its continued selective value for some functions. The index claw of Icaronycteris is much larger and more powerful than the highly functional thumb claw of some living microchiropts. Small size doesn't mean ineffective. In fact, the chain of three phalanges in the index finger of Icaronycteris was about twice as long in ratio to overall body size, head to toe, as my index finger in the corresponding ratio. In the ratio length of ungual phalanx to overall body height Icaronycteris and I are almost exactly the same. In life this ossicle of I. index had a horny claw, sheathing the end of the bone, that was much larger, proportionately, and much more effective, for multiple duties, than my fingernail. This sheath greatly increased the total length of the claw, perhaps making it two times as long as the bone is alone. Although the index (second) finger and thumb on a wing of Icaronyc­ teris were not long enough to touch each other they probably could flex toward each other close enough to pierce and hold small fruits Fig. 18. Skeleton, ventral aspect. 1.5χ. Ax Ce Cf Cs Cv F Η Hf Ld Lf Ls

axis seventh cervical vertebra fourth caudal vertebra coracoid process of scapula clavicles fibula humerus head of femur labial surface of left dentary first lumbar vertebra seventh (last) lumbar vertebra

Ma Ms Prl R RU2 Sa Sr Ti X

manubrium (episternum) mesosternal segments proximal phalange of first digit (thumb) radius twelfth rib sacrum scapholunar tibia xiphisternum

49

Fig. 18.

1. BAT ORIGINS AND EVOLUTION

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GLENN L . JEPSEN

or large insects and carry them to the mouth. And, of course, the first and second digits of the two wings could act together effectively as two hands, each with two short fingers. It is not possible from the bones of Icaronycteris to determine the degree to which the thumb and index finger were free of the flying membrane. The extent of freedom of these structures varies greatly in the megachiroptera. Icaronycteris may have reached the stage of bat evolution wherein the hind feet were assuming the functions of hands as the wings became more efficient structures for flight. In the reduction of digit II the whole structure and function of the distal part of the leading edge of the wing was involved. Today bats apparently fly with the thumb extended forward; perhaps Icaronycteris flew with both the thumb and the index finger outstretched, and both may have had some effect as airfoils, like the alula of birds. The aerodynamic efficacy of the index finger of Icaronycteris was influenced by its degree of freedom—the extent and manner of its attach­ ment to the propatagium. It is unlikely that it formed a leading edge wing slot that would prevent stalling turbulence, which seems to be the effect of the bird's alula. The thumb of Icaronycteris is nearer the position of the alula on avian wings than is the end of digit II. This index finger did, of course, have an effect upon the distribution of wing weight and of balance and upon the mechanics of movement. It is diffi­ cult, however, to see how the complete index digit would have any effect upon echolocating techniques unless it could have been a ner­ vously sensitive area or especially associated with airstream responses. Bader and Hall (1960) found extreme variation in phalanx 1 of digit II and concluded that factors which normally operate to control or limit bone development in this area of bats are missing or peculiarly modified and that it is hence a field of relaxed selection. Through a different interpretation it might be regarded as a field of very active, and hence variable, selection, if the leading edge of this part of the wing is asso­ ciated with the development of airstream effects and neural responses or with the use of the wing in securing food in flight. Megabats retain the whole index finger and do not flick flying insects into the mouth or into the cupped uropatagium as do microbats. Fruit bats that do not feed while on the wing would not benefit by having the high ma­ neuverability of insectivorousflight-feedingbats. Study of the bone of the terminal phalange of the index digit of Icaronycteris indicates that the keratinous sheath that originally enclosed it was sharply recurved but that it was not "hooded," not set in a basal groove in the proximal part of the bone, as it is in Pteropus. In Icaronyc-

1.

B A T ORIGINS AND

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51

tens this claw is smaller than the claw on the thumb, but probably had a sharper point and a greater leverage advantage in flexing by the flexor longus digitorum. In Pteropus the ungual phalange of digit II (the index claw bone) is small, irregular, variable and in the several specimens that I have measured is about one-third as long as the thumb claw. In Icaronycteris the index claw bone is more than half the length of the thumb claw bone. Terminal phalanges on digits III, IV, and V are so small in Icaronyc­ teris index that they are difficult to study. They do, however, all have similar forms and true articular surfaces to hinge against the distal ends of the phalanges proximal to them. And they are truly ossified, with compact outer layers around inner cancellate bone; they apparently are not merely proximal ossified parts of slender cartilaginous rods such as those that occur in some bats. These ossicles in Icaronycteris may have been tipped with keratinous sheaths as true claws are, and they may have been used as firm parts of the landing gear of Icaronycteris. Digit III, compared with this finger in many modern bats, is very strong and short, appropriately designed for the same function. XII. Neck Bones The configurations of the cervical vertebrae of bats (and other animals) control and limit the movements of the head and neck, and this kind of functional osteology is clearly shown in the correlations of verte­ bral structures with the roosting habits of megabats and microbats. Both groups hang by their supinated hind limbs, with their legs straight above their suspended bodies. Megabats habitually keep their heads in an upside down position. They eat in this attitude, observe their world from it and launch themselves from it (whether they are free-hanging from branches of trees or have their backs to a vertical surface of a tree or other shelter) by releasing the grasp of their feet and falling or pushing or flapping into the flight position wherein the head is topside up. Megabats thus hold their heads in either of two positions, crown up or crown down, depending upon their activities. Microbats (with an exception or two) suspend themselves with their ventral side toward whatever vertical surfaces they are hanging against, such as trees or rock walls. This position is similar to that of their prebat days as arboreal insectivores scampering up and down trees. It necessitates a backward, snout-raising flexure of the neck so that the head is held right side up, the reverse of the megabat position,

52

GLENN L.

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when the animal looks outward. Even when hanging in open spaces away from walls the microbats frequently assume this attitude to survey the surroundings. It has several apparent advantages. The fur-insulated (and concealingly colored) back of the animal is always away from a wall and the wings can be wrapped around to protect the belly side, which sometimes has nursing young bats clinging to it. From this posi­ tion the bat can spring right-side-up into space by pushing the wings or the abdomen and perhaps the tail against the wall. And, when landing to hang by its hind limbs the bat can turn in a horizontal plane when it reaches a selected site and grasp whatever it chooses to be suspended from. Hence, a microbat has its head habitually oriented in only one position—crown up. Perhaps this is necessary for the production and reception of bat noises in echolocating and in communicating with other bats. A disadvantage of this attitude may be in the fact that the wings cannot be used as readily as can the wings of megabats to cover the head. For the neck to be extremely flexed in the microbat head-up position all the cervical vertebrae have special constructions that are lacking in the megabats. In some microbats on the medial ventral region of the second to the fifth cervicals there is a posteriorly directed extension (hypophysis) of the centrum which underlies the anterior ventral border of the next posterior vertebra and is accommodated by a little hollow thereon. These small accessory processes and furrows keep the adjacent vertebrae partly interlocked when the head is raised. Megabats appar­ ently lack these structures. If a microbat's cervical vertebrae are flexed in the opposite (the megabat) direction, chin toward chest, the little projections cause the centra of adjacent vertebrae to be pried away from each other and the zygapophyses on the sides of the neural arches become disengaged because the posterior zygapophyses do not extend posteriorly as far as the centrum projections do. Icaronycteris index has only one set of the projection-and-recess structures, between the second and third vertebrae, where there is a slight development of it. Additional modifications that permit the heads-up flexion of the neck are seen in the shape of the neural arches. These are very slender trans­ verse bars without neural spines except on the second cervical vertebra in some microchiropts. In I. index there are no neural spines on the neck vertebrae (although one may have been on the axis originally) and the gracile arches occupy less space along the dorsal side of these bones than the interarch spaces do. Some living microbats show similar proportions, but in megabat skeletons that I have examined the cervical neural arches are broad bands that do not permit extreme flexion of

Fig. 19.

Skeleton, dorsal aspect. 2χ,

of Icaronycteris

index, PU18150.

(Overall

length of skeleton, 125 mm.)

1. BAT ORIGINS AND EVOLUTION

53

the neck when the head is raised. Structures of the cervical neural arches in some tree shrews and in the Paleocene insectivore (PU14526) are similar to those of megabats, quite unlike the vertebrae of microbats. From these observations it may be concluded that I. index could easily flex its neck as living microbats do, and that is could also hold its head in the position that is habitual with megabats. A second major function of the flexibility of the neck in microchiropts may be a scanning action of the head during flight. XIII. Stages to Flight How fast and by what stages did bats enter the nocturnal, insect-eat­ ing, volant mammal niche? About these subjects there has been curiously little diversity of speculation; most of the concerned authors have be­ lieved that some arboreal insectivores, perhaps a small population group, passed very rapidly (tachytelicly or by "quantum evolution") through a gliding stage and quickly perfected the structures for flight. No one has successfully proposed any kind of selection pressure that would be effective in the change from one niche to the other; whether the bridging group would be pulled by advantages in the new milieu or pushed by disadvantages in the old. Arboreal niches and gliding niches are well established, widely occupied, and durable. Why should a ground-living or a tree-climbing insectivore (whether or not it ate in­ sects ) begin to parachute or fly? By combining observations and reasonable inferences about extinct and living insectivores and bats it is possible to hypothesize a series of stages of evolution from pre-bat to bat. In this highly imaginative exercise some negative evidences may be significant. (As they were in the incident of the dog in the night. "But Holmes, the dog did noth­ ing." "Exactly, Watson, that is the incident.") Why are there no bats that are powerful leapers and none that perch like birds? Why are no bats blind? Why are there, as Lyell asked Darwin, no nonvolant bats? Why are none aquatic? Or edentulous? Why don't any of them have a prehensile or bushy tail or a large sternum? Why don't they hang habitually by their front limbs, and why aren't more of them diurnal rather than nocturnal? Why are no Megachiroptera native to the New World? Why don't more vertebrates, including birds, live in caves? Why were no insectivores left to continue as viable intermediates at any of the stages between wholly non-bat and pure bat? Static stages are, of course, artifacts in these conjectures about the

54

GLENN L.

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changes in the histories of bats because even at the most extreme speed of evolution the natural modifications must be slow to permit viable integration of all the genetic and functional factors that are part of the intricacies of being a bat. The more complex a piece of biotic ap­ paratus becomes, the greater is the chance of disorder, and the more precisely must the parts be adjusted for proper operation. Echolocating bats are unusually complicated parts of nature, they are not simply, as some writers have stated "insectivores with wings" nor are they merely airborne mice. Apparently no other grade of mammal has ever had so many eccentric and extremely "specialized" characteristics combined into such a highly "successful" organism. In these "stages" all bat systems were, of course, in the process of continual genetic change and integra­ tion; the statement that "a calcar developed in stage three" does not mean that there was no sign of the "spur" in earlier forms; only that it became noteworthy, in these speculations, at that stage. Selection, the constant monitor, acted ceaselessly, of course, on every phenotype, and not directly on any of the constantly mutating genotypes. Stage 1 was the (imaginary) pre-bat, a small inconspicuous, insectivore-like, nocturnal inhabitant of the ground-bush-tree regions in tem­ perate areas. Omnivorous, it ate small tough-skinned fruits and softshelled nuts and seeds, eggs, insects, arachnids, small birds, lizards, frogs, and fish. It made short leaps from higher to lower levels to catch prey with its large (and, possibly, webbed) front feet, and could run fast on the ground or scamper up trees and rocks into small holes and crevices for refuge and for roosting. During its seasonal hibernation and its daily periods of energy-conserving torpor in cavities its body temperature markedly decreased. Its hind legs and feet could be ex­ tended outward (laterally) from the body when it moved around in crevices. Its big toes were opposable, and it could run vertically (squir­ rel-fashion) down a tree or rock wall, belly toward the wood or rock surface, with the hind feet rotated (supinated) and extended backward. It could hang by its hind feet, in the same attitude, and watch activities by flexing its neck and raising its head into a right-side-up position, and could leap (launch itself) from this ready-posture toward a nearby target. [Muul (1968) observed caged flying squirrels hang by their hind legs and use their forefeet to captureflyinginsects.] The tail of the pre-bat was long, may have been hairy, and perhaps had tactile functions. Compensating for its small eyes and "poor" ocular equipment the animal had a rich and loud vocabulary and it practiced echolocation, as do some modern insectivores, for which it had the requisite vocalizing and auditory and neural structures. In the full denti-

1.

B A T ORIGINS AND

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55

tion of 44 teeth the W-pattern of the sharp-cusped upper molars was well developed. No elements of the primary euthere skeleton had been lost or gained. This animal probably had a relatively short life span, with high rates of energy expenditure, and with a large intake of food, and its young were necessarily precocious to escape from predators such as birds (or prebirds), other mammals, and, possibly, pterosaurs and carnivorous gliding and leaping reptiles. Instant activity and escape were its major factors of preservation, but it also had the teeth, claws, and muscles to protect itself and to expel territorial trespassers. It was incon­ spicuous. (Some living bats seem to have protective or concealing colora­ tion and may be mimics of other objects. It has been suggested that small bat bodies in crevices or on trees may look, to some predators, like cockroaches or other large insects, that some bat faces or parts thereof resemble moths, and that perhaps suspended megabats could be mistaken for hanging coconuts or other plant pendants.) There is no evidence that the flying insect-eater, crevice-and-cavedwelling niche was either occupied or vacant when pre-bats or bats moved into it, whether it presented problems in territorial competition or offered dietary opportunities and immediate tenancy. In Stage 2 the webbed large hands (or small wings) which were used principally in catching flying prey, and the little skin flaps extending from arms to sides of the body enabled the sub-bat to be very briefly sustained in the air by rapid flapping, after a jump from the ground or from a branch to catch an insect. This action avoided a crash landing, and the animal lit lightly on all fours. The thumb and index fingers were shorter, in adults, than the other digits of the manus, and had a wide variety of functions, as they still do in megabats. Because both the thumb and the index finger continued to be extensively involved in many terrestrial activities such as climbing and grooming they had less function as aerial aids, in this sub-flight stage, than did the elongat­ ing digits III, IV, and V. The latter three fingers, slender and webbed, were still clawed and they retained enough flexibility to grasp insects and convey them to the mouth. Thus, as the elements of the manus developed a division of labor, they simultaneously experienced a multi­ plication of function. Correlated with the shapes of habitation space in crevices and grottos and with living conditions therein the animal became operationally and anatomically flatter, the hind legs extended laterally rather than directly downward under the body and there was an attendant in­ creased rotation of the femur and supination of the hind foot. As the forefoot became more winglike the hind limb assumed some of the

56

GLENN L.

JEPSEN

functions that were formerly performed exclusively by the front foot such as grooming and food grasping and holding. With continued selec­ tion toward volantism the incipient patagium extended as a little skin fold from the body to the splayed hind legs which thus became partly involved in the developing flight mechanisms, as did the tail when the membranes developed still further. The big toe was shorter than the other digits of the pes which were about equal in length and formed, functionally, a single hook for suspension of the body from cave walls or other rough surfaces. Food specialization began. Some forms preferred fruit, after finding initially that it was a good source for worms and bugs, and, in accord with such dietary changes, new dental types appeared. Various develop­ ments of the limbs and tail were correlated with divergences in regimen. For some functions wherein the rear limbs required freedom of action, such as eating fruit while suspended by one foot from a branch, the tail and the uropatagium were reduced; .modern fruit bats (with one exception) are nearly tailless. Neural and circulatory and thermoregula­ tory systems evolved in pace with the developing wings which, as they enlarged, served several purposes in addition to those related to flying. Many muscles became involved in flight. The precocious young sub-bats developed a habit of clinging to their mother with their big thumbs and large feet and their slender bent-hook milk teeth. Cave-inhabiting groups continued the heads-right-side-up position in roosting, made refinements in launching techniques from it and in land­ ing procedures to it, and perfected their echolocation abilities in foraging for brief periods at night outside of the caves. They thus were able to avoid the heat of daylight hours, to take advantage of the nocturnal habits of certain insects, and to avoid food competition with birds. Fruit eaters, hanging by their hind feet in trees, developed the habit of keeping the head upside down (not raised to a right-side-up position) even while eating and grooming. They ceased the practice of echolocation. Morphologic diversity developed as habits and sense systems, especially for seeing and hearing, became specialized in various subniches. Stage 3 was a continuation of refinements to the present condition of bats. The wings grew, developed elastic fibers, and became specialized for different speeds and loadings, "lost" some bones and added cartilagi­ nous extensions to others, the femur rotated farther, a calcar developed and helped control the uropatagium during flight. Ears diversified for various functions of sound focusing and tuning, and in some bats became useful parts of the flight surfaces. In the thoracic area some of the vertebrae fused, as did the sternal segments, and formed a more solid

1.

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EVOLUTION

57

lung box. Factors favoring reduction in body and increased flight power were refined. Although they have become specialized and diversified flyers many bats still retain good ability to crawl, scamper, and cling. Through energy conservation or for other reasons their individual lives have become greatly extended beyond that of their ancestral insectivores. This total metamorphosis may have occurred quickly but we lack any kind of time gauge in the record—and the record is very fragmen­ tary, in part as a result of bats' small size and their choices of places to live. As the strange bat-world developed, its idiosyncracies affected every part of every bat-animal, as well as its relationships to the other animals and plants within its ecologic realm, either directly or through chain effects. Somewhere in the development of bats the bat-flies became parasitic on bats. Bats are now the exclusive hosts to these peculiar dipterans as well as to other parasites (Ryberg, 1947), but we don't know how or when this relationship began or to what degree either member of this host-parasite pair has conditioned the existence of the other. XIV. Icaronycteris

index

For specialists on bat osteology the accompanying stereophotos and drawings will reveal or wordlessly describe many anatomical details and dimensions of Icaronycteris index (as exemplified by the Eocene skeleton PU18150), for comparison with the functional osteology of other bats. Hundreds of measurements of this skeleton have been taken, and many ratios calculated, in the effort to ally the fossil specifically with living bats. These observations and figures have not led to many clear-cut conclusions; the kinds of modern bats are so numerous and so many of them share certain characteristics with each other and with fossil forms that no firm pattern of evolution from I. index to any other particu­ lar fossil or living bat is evident. Of course I. index has not been com­ pared directly with the bones of all other Tertiary bats or with all living kinds, nor does such an extensive exercise in comparative anatomy have much promise at this time of commensurate revelation. We need many more, and more complete, bat fossils from rocks of earlier and of later Tertiary time before the habits of the branches of the genealogic tree of chiropts can be seen. Bat sizes and habitats, decay and erosive processes through time, and the gamble of paleontologic discovery all combine to make future knowledge of bats' past unpredictable. These early speleologists already exemplify the incredible durability of some

58

GLENN L.

JEPSEN

genomes in the development of the elegant anatomic and social organiza­ tions of miniature mammals, and they will contribute much more to our knowledge of whole-animal evolution when we advance the studies of their present and their earlier forms as part of natural history. Of the fifteen families of microbats listed by Koopman and Cockrum (1967) fossil representatives of only six are known; the other three-fifths of the families have no known ancestry in the current taxonomy of bats. Icaronycteris index was a true flyer although it lacked many of the advanced specializations of some extant bats, and it retained some "prior" skeletal structures that are not found (to my knowledge) in living bats. It probably could run or scamper or scuttle very effectively as a quadru­ ped on the ground and on trees and rock walls, and habitually made more use than any living bats do of their wings as front feet in this kind of locomotion. Fortunately, the skeleton reveals more than does any other single body-system about the habits and ecology of dead bats; without it a bat is a shapeless puddle of protoplasm. In addition to the skull Icaronycteris index had at least 253 bones and 38 teeth in its solid skeleton, and all these except a few of the 44 sesamoids in the wings and feet have been studied on one side or the other (or both) of PU18150. Axial bones are as follows: 1 skull (counted as a single element), 2 dentaries, 7 cervical vertebrae, 12 thoracics, 7 lumbars, 1 sacrum, 13 caudals, 7 hyoid bones, 1 manubrium, 5 mesosternal segments, 1 xiphisternum, 1 baculum?, and, on each side, 12 ribs, a scapula, clavicle, humerus, radius, ulna, scapholunar, cunei­ form, pisiform, trapezium, trapezoid, magnum, unciform, 5 metacarpals, 14 wing-phalanges, ilium, ischium, pubis, femur, patella, tibia, fibula (missing on right side), astragalus, calcaneum, cuboid, navicular, 3 cuneiforms, 5 metatarsals, and 14 foot-phalanges. From nose tip to tail end and from limb girdles to limb ends Icaronyc­ teris index has the following distinctive combination of qualities, with the few that are especially characteristic of Megachiroptera indicated by (Μ) (other symbols are those used in the figures): long and moder­ ately narrow head; premaxillaries not united at midline ( M ) ; premaxillaries probably have palatal as well as facial branches; lacrimal foramen and posterior opening of infraorbital foramen apparently above Ml; dental formula (2.1.3.3.)/(3.1.3.3) = 3 8 ; diastema between upper in­ cisors; one root on P2 and p2, two on p3 and p4, three on P3 and P4; W-shaped labial wall of upper molars; angle formed by line from protoconid to paraconid with line from protoconid to metaconid is about 40°; metaconid and long deep talonid basin ("postfossid") on p4; long nasal bones ( Μ ) ; shallow eye-orbits; no postorbital processes on frontals

1.

B A T ORIGINS AND

EVOLUTION

59

or jugals; zygomatic arch slender, long, complete; very small sagittal and occipital ridges; palate projected rearward slightly beyond posterior molars ( M ) ; well-ossified hyoid bones; stylohyals long, slender, articulat­ ing with bullae; dentary body long, low, slender; mental foramina below i3 and p2; ascending process of dentary broad anteroposteriorly, with high, rounded superior border ( M ) ; condyle of dentary well above line of tops of molar cusps; angle of dentary hook-shaped, pointed; vertebral formula 7-12-7-3-13 or 14; no vertebral fusion except in sacrum; very slender neural arches on cervical vertebrae; no coalesced ribs; segments (seven) of sternum not fused; mesosternum not keeled; pubic bones loosely united at symphysis; pubic spine short, robust; long and free tail; 5th to 7th caudal vertebrae larger than others; tail tapers abruptly near tip; large supraglenoid tuberosity on scapula; coracoid process of scapula long and slender, not bifid; clavicle heavy, not expended at ends; high flangelike deltoid crest on straight slender humerus; trochiter of humerus large, articulates with scapula; trochin prominent but not as large as trochiter; relatively short straight radius; most of shaft of radius is round, flattens dorsoventrally at distal end; no trace of sesamoid at proximal end of ulna; large scapholunar; sesamoids associated with all (very flexible) metacarpophalangeal joints; claw of thumb not hooded; claw on independent index finger ( Μ ) ; digital formula 2-3-3-3-3 (wing) and 2-3-3-3-3 (foot); all claws of wings and feet compressed laterally; decreasing order of finger length 3-4-5-2-1; femur comparatively robust; femur with distinct very short neck between head and shaft; femur head and neck at angle to shaft; fibula slender, well developed; fibula slightly longer than tibia; tibia shorter than femur; metatarsal I shorter and heavier than others; big toe shorter than other toes; no calcar; clawlets on digits III, IV, and V; decreasing order of toe length 4-3-2-5-1. Characteristics of Icaronycteris index that might be called "primitive" or "generalized" or lacking specialization among bats are (1) the large number of teeth, (2) "insectivorous" shapes of teeth, (3) uncoalesced ribs and vertebrae and sternal segments, (4) shapes of centra and neural arches of cervical vertebrae, (5) lack of prominent keel on mesosternum, (6) long tail, (7) shape of scapula, (8) relatively short radius, (9) index claw, (10) complete phalangeal formula, (11) head and neck of femur at angle to shaft, (12) big toe shorter than others, (13) no calcar, (14) low aspect ratio of wings (estimated to have been between 2.75 and 2.84). More extended studies of the skull of PU18150 are necessary to obtain full information from it. Preliminary research, however, indicates that

60

GLENN L.

JEPSEN

it, like many another skeletal element of I. index, combines features which are widely distributed among living bats. Efforts to study the origin and development of these osteologic features in bats will continue to be frustrating until more good fossils are recovered. The fragmentary nature of the geologic history of the chiroptera also make it difficult to perceive and trace their geographic movements, however tempting it may be now to use them for speculations about land bridges and continental drift. A major puzzle in the disjunctive distribution of bats is the absence of big fruit bats (Pteropodidae) from the New World. If bats are old enough to have witnessed major wanderings of continents their silent testimony on the subject will have to be presented through future discoveries. Laurasia and Gondwanaland are believed to have split up into subcon­ tinents (Kurten, 1967), with South America becoming independent of Africa, prior to the great mammalian radiation in late Cretaceous and early Tertiary time. Bats, among mammals, have unique opportunities for certain kinds of travel and dispersal simply because they fly. Many bat groups have not increased their territorial ranges as extensively, however, as their volantism seems to provide the means for doing. Gen­ erally, bats appear to be homebodies or migrators with fixed routes for return, and one wonders if a flyway across a water body from one roosting area to another ever was extended by slow land movements to the degree that the route became hazardous and long-term flying habits were broken. In terms of numbers of families, South America is rich bat country. More than half (eight) of the living microchiropt families (fifteen) occur there and six of these eight are not known to be in the Old World. Only two families are widely distributed now in the temperate part of the United States, and either or both of them may represent some 25 million or more generations of change from ancestral Icaronyc­ teris index. When PU18150 was buried in the sediments of Fossil Lake, however (see Schaeffer and Mangus, 1965), southern Wyoming (much lower in altitude then than now) had a humid subtropical climate like that of Alabama today (Bradley, 1929, 1964). Most groups of Recent bats prefer a tropical or subtropical biogeographic range, and perhaps they always have. XV. "First" Bat at Present Conditions in tropical and subtropical areas are notoriously hostile, unfortunately, to the many processes that preserve little mammal skele-

1.

B A T ORIGINS AND

EVOLUTION

61

tons and convert them to fossils which have chances, at any distant future time, of being studied and compared (as evolutionary dropouts) with the phenotypic products of continuous biochemical alteration in surviving phylogenetic lines. Obviously, the rates of evolution vary as organisms reach successive grades or plateaus of functional organization but this fluctuation probably results more from variation in the rates of incidence and accumulation and integration of "small" mutations (those with slight phenotypic effect) than from sudden enormous in­ creases in the "size" of morphologic effects of single mutations. Several geneticists have favored the latter concept as a theoretically possible process but vertebrate paleontologists, especially those who have ex­ amined large numbers of dated fossils from closely spaced sequences of strata, have rejected the idea as being without physical evidence or contrary to it. In an attempt to define and to deride this theory it was given the name "macrogenesis" (Jepsen, 1943, p. 526) as a com­ panion word to "microgenesis" or evolution by small changes. No one at present knows what rates have prevailed in bat evolution but the whole subject of the behavior of bats at every level of organization, biochemical to social, offers many opportunities for man to improve his knowledge about them and to overcome some of his superstitions and misinformation. A new book about evolution (Romer, 1968, p. 271) states that a bat cannot walk, that when it is grounded the best it can do ". . . is a seemingly frantic series of flopping motions in the attempt to regain flight," and a recent textbook on comparative anatomy (Baer, 1964) repeats (p. 60) a common myth that "There is no patella in the Chiroptera. . . ." These persistent fictions about bats are difficult to eradicate, especially when they bear a stamp of authority. We now know that bats were bats when men were lemuroids or less, and the family trees of the two groups, in continuous ecologic association since dinosaur days, have grown tall side by side, in the same general ecologic grove, to lofty branches of mammalian specialization: bats echolocate and fly, men think and fly. Haldane (1949, p. 408), however, observed that ". . . it is a mistake to suppose that the brain is primarily a thinking organ. Thinking is mainly, if not wholly, performed with words and other symbols." What does the future hold for the further evolution of bats? Can nature create new forms from their genetic magmas? Man has found, in computers, new symbols to think with and they obviously will help his brain to control not only his future for benefit or destruction but the condition of all his mammalian associates on this planet. Now he really needs wisdom about nature.

62

GLENN L. JEPSEN

REFERENCES

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Handley, C. O. (1955). Nomenclature of some Tertiary Chiroptera. J. Mammal. 36, 128-130. Hankin, Ε. H., and Watson, D. M. S. (1914). On the flight of pterodactyls. Aeronaut. J. 18, 324-335. Heath, J. E., and Adams, P. A. ( 1 9 6 7 ) . Regulation of heat production by large moths. 7. Exp. Biol. 47, No. 1, 21-33. Heller, F. (1935). Fledermäuse aus den eozänen Braunkohle des Geiseltales bei Halle a.S. Deut. Akad. Naturforsch. Nova Acta Leopoldina 2, Parts 3 and 4. Hennig, W. (1966). "Phylogenetic Systematics." Univ. of Chicago Press, Chicago, Illinois. Hopson, J . A. ( 1 9 6 7 ) . Comments on the competitive inferiority of the multituberculates. Syst. Zool. 16, No. 4, 352-355. Hull, D. L. (1966). Phylogenetic numericlature. Syst. Zool. 15, No. 1, 14-17. Jepsen, G. L. (1940). Paleocene faunas of the Polecat Bench formation, Park County, Wyoming. Proc. Amer. Phil. Soc. 83, 217-340. Jepsen, G. L. (1943). Systematics and the origin of species, from the viewpoint of a zoologist: Review. Amer. J. Sei. 241, 521-528. Jepsen, G. L. (1949). Selection, "orthogenesis," and the fossil record. Proc. Amer. Phil. Soc. 93, No. 6, 479-500. Jepsen, G. L. (1966). Early Eocene bat from Wyoming. Science 154, 1333-1339. Jerison, H. J . (1968). Brain evolution and Archaeopteryx. Nature 219, 1381-1382. Koopman, K. F., and Cockrum, E. L. (1967). Order Chiroptera. In "Recent Mam­ mals of the World" (S. Anderson and J . K. Jones, Jr., eds.), pp. 109-150. Ronald Press, New York. Kurten, Β. ( 1 9 6 7 ) . Continental drift and the palaeogeography of reptiles and mam­ mals. Finska Vetenskaps-societeten, Helsingfors. Commentationes Biol. 31, No. 1, 1-8. Landry, S. O., Jr. (1965). The status of the theory of the replacement of the Multituberculata by the Rodentia. J. Mammal. 46, No. 2, 280-286. Landry, S. O., Jr. (1967). Disappearance of multituberculates. Syst. Zool 16, 172-173. Lawrence, B. (1943). Miocene bat remains from Florida, with notes on the generic characters of the humerus of bats. /. Mammal. 24, No. 3, 356-369. McNab, Β. K. ( 1 9 6 6 ) . The metabolism of fossorial rodents: A study of convergence. Ecology 47, No. 5, 712-733. Martin, R. D. (1968). Towards a new definition of primates. Man [N.S.] 3, No. 2, 377-401. Mayr, E. (1963). "Animal Species and Evolution." Harvard Univ. Press, Cambridge, Massachusetts. Mayr, E. (1968). Theory of biological classification. Nature 220, 545-548. Meschinelli, L. (1903). Un nuovo chirottero fossile (Archaeopteropus transiens, Mesch.) della ligniti di Monteviale. Atti Ist. Veneto Sei., Lettere Arft, CI. Sei. Mat. Natur. 62, 1329-1344. Michener, C. O. (1963). Some future developments in taxonomy. Syst. Zool. 12, No. 4, 151-172. Miller, G. S. (1907). Families and genera of bats. U.S., Nat. Mus., Bull. 57, 1-282. Mitchell, H. A. (1964). Investigations of the cave atmosphere of a Mexican bat colony. J . Mammal. 45, No. 4, 568-577.

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Moody, P. A. (1962). 'Introduction to Evolution," 2nd ed. Harper, New York. Muul, I. (1968). Behavioral and physiological influences on the distribution of the flying squirrel, Glaucomys vohns. Misc. Puhl., Mus. Zool. Univ. Mich. No. 134. Peterson, R. (1964). "Silently, by Night." McGraw-Hill, New York. Peyer, B. (1968). "Comparative Odontology." Univ. of Chicago Press, Chicago, Illinois. Romer, A. S. (1959). "The Vertebrate Story." Univ. of Chicago Press, Chicago, Illinois. Romer, A. S. (1968). "The Procession of Life." World Publ. Co., Cleveland, Ohio. Ryberg, O. (1947). "Studies on Bats and Bat Parasites." Svensk Natur., Stockholm. Schaeffer, B., and Mangus, M. (1965). Fossil lakes from the Eocene. Natur. Hist. 74, No. 4, 10-21. Scott, W. B., and Jepsen, G. L. (1936). The mammalian fauna of the White River Oligocene, Part 1, Insectivora and Carnivora. Trans. Amer. Phil. Soc. [N.S.] 28, 1-153. Sige, B. (1968). Les Chiropteres du Miocene inferieur du Bouziques. Palaeovertebrata 1, No. 3, 65-133. Simpson, G. G. (1945). The principles of classification and a classification of mam­ mals. Bull. Amer. Mus. Natur. Hist. 85, 1-350. Simpson, G. G. (1961). "Principles of Animal Taxonomy/' Columbia Univ. Press, New York. Simpson, G. G. (1963). The meaning of taxonomic statements. In "Classification and Human Evolution' (S. L. Washburn, ed.), pp. 1-31. Aldine, Chicago, Illinois. Smith, J. M. (1968). Haldane's dilemma and the rate of evolution. Nature 219, 114-116. Stones, R. C , and Wiebers, J. E. (1965). A review of temperature regulation in bats (Chiroptera). Amer. Midi. Natur. 74, No. 1, 155-169. Suthers, R. A. (1966). Optomotor responses by echolocating bats. Science 152, 1102-1103. Van Valen, L., and Sloan, R. E . (1966). The extinction of multituberculates. Syst. Zool. 15, No. 4, 261-278. Vaughan, T. A. (1959). Functional morphology of three bats: Eumops, Myotis, Macrotus. Publ. Mus. Natur. Hist. Univ. Kans. 12, No. 1, 1-153. Viret, J. (1955). Chiropteres fossiles. In "Tratte de Zoologie" (P. P. Grasso, ed.), Vol. XVII, Pt. 2, pp. 1845-1853. Masson, Paris. Walker, E. P. (1964). "Mammals of the World," 2 vols. Johns Hopkins Press, Baltimore, Maryland. Webster, F. Α., and Griffin, D. R. (1962). The role of flight membranes in insect capture by bats. Anim. Behav. 10, Nos. 3 and 4, 332-340. Wetmore, A. (1938). Another fossil owl from the Eocene of Wyoming. Proc. U.S. Nat. Mus. 85, 27-29. Winge, H. (1941). "The Interrelationships of the Mammalian Genera," Vol. I. Monotremata, Marsupialia, Insectivora, Chiroptera, Edentata. C. A. Reitzels, Forlag, Copenhagen. Wood, A. E. (1962). The early Tertiary rodents of the family Paramyidae. Trans. Amer. Phil. Soc. [N.S.] 52, No. 1, 1-261.

Chapter 2

Karyotypic Trends in Bats Robert J. Baker

I. Introduction Techniques II. Karyotypic Trends A. Diploid Number B. Fundamental Number C. Variation D. Sex Chromosomes E. Types of Chromosomal Evolution III. The Primitive Karyotype of Bats IV. Role of Karyotypes in Studying the Biology of Bats V. Specimens Examined References

65 66 67 67 67 4

78 81 81 82 83 93

I. Introduction Although morphological features have long been used in genetic, sys­ tematic, and evolutionary studies, the karyotype (chromosome mor­ phology) as an adjunct to such studies developed only after reasonably easy and consistent techniques were available. For mammals adequate techniques were not described until 1956 (Ford and Hamerton, 1956). Since that time karyological studies have developed rapidly for several mammalian groups (Matthey, 1958, 1963, 1964, 1965, 1966, 1967, 1968b). Although modifications of Ford and Hamertons procedure seem to work 65

66

ROBERT J . BAKER

extremely well in the preparation of chiropteran chromosomes, the karyotype of only 21 of the approximately 875 bat species was reported by the end of 1965. Since that time several workers have set about to rectify this situation (see Table I of reported bat chromosomes and Fig.l). Techniques The following technique for somatic chromosomes is relatively simple, requiring a minimum of equipment. With the use of a hand centrifuge it can be adapted to field situations. 1. Weigh the live animal, inject it intraperitoneally with a 0.025% Vin­ blastine (Velban of Eli Lilly & Co.) or colchicine solution at 0.01 ml per gram of body weight. 2. Two hours later sacrifice the animal and remove about % of the humerus without damaging the proximal end. Remove the flesh and a chip of bone from the proximal end of the humerus to expose the red bone marrow cavity. Flush the shaft with 3 ml of a 1.0% sodium citrate solution. Pipette vigorously to break up any cell clumps. 3. Let the resultant cell suspension set for 10-12 minutes. 4. Filter the suspension through two layers of cheesecloth and centri­ fuge at 500-1500 rpm for 4 minutes. 5. Discard as much of the supernatant fluid as possible, being careful to leave the button of cells undisturbed. Add 3 ml of freshly prepared Carnoy's fixative (3 parts absolute methanol; 1 part glacial acetic acid). Floating material and lipids may be removed at this stage. Gently disrupt the cell button with a pipette until the cell suspension is homogeneous. Allow cells tofixfor 10-12 minutes. 6. Centrifuge for 4 minutes and decant supernatant. Resuspend cells in 1.0 ml of fixative and centrifuge as before. This step is repeated 3 times. After final washing, cells are resuspended in 1.0 ml of fixative. 7. Place three or four drops of cell suspension on a clean slide and ignite. When the fire extinguishes itself, the residue is promptly slung from the slide. Four slides from each specimen are usually made. 8. Dry slides are stained with Giemsa's stain (1 part Giemsa's stock solution to 8 parts distilled water) for 15 minutes. 9. Pass slides through two baths of acetone, one of acetone and xylol (1:1), and two of xylol, then mount under a 22 X 40 mm coverslip with Permount. In reporting karyotypic data the number and sex of specimens ex-

2.

KARYOTYPIC TRENDS IN BATS

67

amined, the geographic locality(s) from which the specimens were col­ lected, and where voucher specimens are deposited should always be given. Many workers studying karyotypes have had the tendency to discard the specimens from which the chromosomes were taken. This is very detrimental to the value of the karyotypic report. There are over 800 species of bats, many of which can be correctly identified only by a specialist. If karyotyped specimens are properly labeled, and deposited in a reputable museum, the karyotypic report is still useful even if the specimen is incorrectly identified. Further, when different karyotypes are reported for the same species, voucher specimens form the bases for determining if the variation is really intraspecific or indicates specific differences. Methods of preparing study specimens are given in a publi­ cation by Hall (1962) which can be obtained from the Museum of Natural History, University of Kansas, Lawrence, Kansas. II. Karyotypic Trends A. Diploid

Number

The diploid number has been reported (including those reported here) for 126 species of bats from 13 families (Table I and Fig. 1). This value ranges from 16 to 62 for the order. The majority of the variation is not removed at the family level (Fig. 1). The range of the diploid number reported for Eutherian mammals is 14-84 (Brenner, 1946; Matthey, 1958, 1963, 1964, 1965, 1966, 1967, 1968a,b). Over half of the reported species, including bats, have a diploid number between 40 and 56 (Matthey, 1968a). Fifty species of bats have diploid numbers in this range (Table I and Fig. 1). Seventy-eight species have lower values, whereas only four species have values above this range. Obvi­ ously, diploid numbers of bats are considerably lower than for most other orders of Eutherian mammals. The mean of reported Chiropteran diploid numbers is 36.8. A bimodal curve is obvious in Fig. 1, and this probably reflects the fact that a large number of the species studied are in the families Phyllostomatidae and Vespertilionidae. B. Fundamental Number The fundamental numbers (FN) reported for bats are also given in Table I and Fig. 2. I have attempted to standardize this value by count-

X

—

—

58 58

Rhinolophidae Rhinolophus blasii R. ferrumequinum Schreber

SM

—

—

54

60

SM

58

A

—

A

—

—

A

—

A

—

A

—

A

—

A A A

Υ

—

34

58

36 36 38 60

MICROCHIROPTERA

SM SM Μ

54 68 70

MEGACHIROPTERA

FN

Noctilionidae Noctilio leporinus (Linnaeus) Megadermatidae Megaderma lyra Geoffroy

42

22 26 28 32 42

Emballonuridae Rhynchonycteris naso (Wied-Neuwied) Saccopteryx bilineata (Temminck) S. leptura (Schreber) Balantiopteryx plicata Burt Taphozous longimanus Hardwick

T. melanopogon Temminck

36

Rhinopomidae Rhinopoma hardwickei Gray

34 36 38 38 38

2N

4

3

7

—

2 0 2 1

1

&

CHROMOSOMAL DATA R E P O R T E D F O R B A T S A

3

2

0

0

1 3 1 2

1

— — —

9

and Pathak, 1968 and Pathak, 1968

Dulic, 1966, 1967 Makino, 1948

Ray-Chaudhuri and Pathak, 1966; Pathak, 1968

This paper

This paper This paper This paper This paper Ray-Chaudhuri 1966; Pathak, Ray-Chaudhuri 1966; Pathak,

Ray-Chaudhuri and Pathak; 1966, Pathak, 1968

Pathak, 1968, 1965a Pathak, 1966 Pathak, 1968, 1965b Manna and Talukdar, 1965 Makino, 1948

Authority

ROBERT J.

P. dasymallus Temminck

Pteropidae Cynopterus sphinx gangeticus Anderson Rousettus leschenaulti Desmarest Pteropus giganteus Brunnich

Family and Species

TABLE I 68 BAKER

Lonchorhina aurita Tomes Tonatia bidens (Spix) T. minuta Goodwin Mimon crenulatum (Saint-Hilaire) Phyllostomus discolor Wagner P. hastatus Pallas Phylloderma stenops (Peters) Trachops cirrhosus (Spix)

R. cornutus Hipposideridae Hipposideros ater Templeton H. fulvus Gray Phyllostomatidae Pteronotus psilotus (Dobson) P. parnellii (Gray) P. davyi Gray Mormoops megcdophylla (Peters) Micronycteris megalotis Gray Μ. nicefori Sanborn Macrotus waterhousii Gray

R. hipposideros (Bechstein)

R. euryale Blasius

— A

A A

— ST

SM SM

—

A A A

—

Μ Μ SM

1 2 2 0 3 1 0 2

1

2 1 1 2 1 1 1 2

1

60 20 56 60 60 58 58 56

SM

32 16 30 32 32 32 32 30

Μ

60

1 4 2 1 0 2 2

40

2 6 3 0 1 3 3

Capanna and Civitelli, 1964a,b Dulic, 1966; Dulic, 1967 Bovey, 1949 Capanna and Civitelli, 1964a,b Dulic, 1966; Dulic, 1967 Capanna et al., 1967 Matthey and Bovey, 1948 Sasaki, 1968

Baker, 1967 Baker, 1967 Baker, 1967 Baker and Hsu, 1970 Baker, 1967 Baker and Hsu, 1970 Baker, 1967; Nelson-Rees et al., 1968 Kniazeff et al., 1967; NelsonRees et al., 1968 Baker and Hsu, 1970 Baker and Hsu, 1970 Baker and Hsu, 1970 Baker and Hsu, 1970 Baker, 1967 Baker and Hsu, 1970 Baker and Hsu, 1970 Baker, 1967 A A A A A A A

1

— —

3 3

3 4

60 60 60 62 68 52 60

0

—

—

7 4

5 4

38 38 38 38 40 28 46 SM SM SM SM ST Μ SM

—

— —

—

A A A

A A

SM SM SM

SM SM

Pathak, 1968 Pathak, 1968

60 60 60 60 60-62

62 60

32 32

58 58 58 58 58 56 54 62

2. KARYOTYPIC TRENDS IN BATS 69

56 60 60 60 60 56 56 24-26 32 36 36 36 56 56 56 50 50 56 56 56 48 48 48 24 56 56 56 56

30 32 32 32 32 30 30 16 19 20-21 20-21 20-21 30 30 30 44 42 30 30 30 26 26 26 21-22 30-31 30-31 30-31 30-31

Vampyrum spectrum Linnaeus Glossophaga soricina (Pallas) G. alticola Davis G. commissarisi Gardner Leptonycteris sanborni Hoffmeister Anoura geoffroyi Gray

A. lituratus Lichenstein

C. trinitatum Goodwin Mesophylla macconnelli (Thomas) Artibeus jamaicensis Leach

Vampyrodes caraccioloi (Thomas) Chiroderma villosum Peters

Vampyrops helleri Peters

C. subrufa (Hahn) Sturnira lilium (Geoffroy) S. ludovici S. tildae de la Torre Uroderma bilobatum Peters

Choeronycteris mexicana Tschudi Choeroniscus godmani (Thomas) Carollia perspicillata Saussure

FN

?

ST-A A-A A-A A-A SM SM SM SM SM SM SM SM SM SM SM

?

SM ST ST ST ST ST ST ST ST ST ST ST ST ST ST A ST ST ST ST A-A SM-A A-A ST-A

?

A A A A A A

Y

Μ Μ Μ Μ SM SM

X

DATA R E P O R T E D F O R BATS

2N

CHROMOSOMAL

Family and Species

TABLE I

9 1 7 0 3 4 0 1 1 0 0 2 7 6 1 2 1 1 0 2 2 2 2 2 10 5 1 3 1