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Mhofanuraimc Nural Olling Mating:' I'n- Th Aleopard Frog, 1Ana

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Mhofanuraimc Nural Olling Mating:' I'n- Th Aleopard Frog, 1Ana THE SEXU-AL B:EHAVIOR MHOFANURAIMC NURAL OLLING MATING:' I'N- TH ALEOPARD FROG, 1ANA. PIPIENS LESTER -R. ARONSON AND G. KINGSLEY NOBLE BULLETIN.- OF THE: AMERIC-AN MUSEUM'.OF NATURAL HISTORY- VOLUME 86 : ARTICLE 3 NE-NVNKYORK. 1945 THE SEXUAL BEHAVIOR OF ANURA THE SEXUAL BEHAVIOR OF ANURA 0 2. NEURAL MECHANISMS CONTROLLING MATING IN THE MALE LEOPARD FROG, RANA PIPIENS LESTER R. ARONSON Assistant Curator, Department ofAnimad Behavior G. KINGSLEY NOBLE Late Curator, Departments of Herpetology and Experimental Biology A DISSERTATION SUBMITTED BY THE FIRST AUTHOR TO THE FACULTY OF THE GRADUATE SCHOOL OF ARTS AND SCIENCE OF NEW YORK UNIVERSITY IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY VOLUME 86 : ARTICLE 3 NEW YORK -* 1945 BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY Volume 86, article 3, pages 83-140, text figures 1-27, tables 1-5 Accepted for publication December 4, 1944 Issued November 19, 1945 CONTENTS INTRODUCTION ... .... 89 LITERATURE ..... 91 MATERIALS AND METHODS . 95 RISUME OF NORMAL MATING PATTERN . 97 MAJOR NUCLEAR MASSES OF THE FROG BRAIN. 98 EXPERIMENTAL PROCEDURES AND RESULTS . 105 Swimming Response of the Male to the Female . 105 Emission of the Warning Croak . 108 Sex Call . 108 Clasp Reflex. 109 Spawning Behavior. 110 Release after Oviposition . 113 DESCRIPTION OF OPERATED BRAINS AND SUMMARY OF BEHAVIORAL DATA 117 DISCUSSION . 129 SUMMARY AND CONCLUSIONS . 135 LITERATURE CITED . 136 ABBREVIATIONS FOR ALL FIGURES .. 139 87 INTRODUCTION ALTHOUGH SOME of the very early concepts of ine some of these concepts from the behav- the neural mechanisms controlling sexual be- ioral point of view. havior were developed from experimentation While the anuran brain exhibits a consid- on Anura, almost all the recent investigators erable amount of specialization as compared in this field have concentrated on mammals. with that of the urodele, the technical advan- The rapid progress made in the last two dec- tages gained by using the frog, particularly ades in this aspect of mammalian research Rana pipiens, were such as to make this spe- has not been paralleled in the lower verte- cies particularly desirable, at least for an in- brates. In Anura, few advances have been troductory investigation. made in this subject since the close of the In developing the project we attempted to last century. utilize, wherever possible, recent methods and Some of the earlier investigators probably techniques. Foremost among these is the pi- chose the frog because lesser technical prob- tuitary injection method developed by Rugh lems were involved in brain experiments on (1935) which made available to us an abun- this animal, but a more important reason for dant supply of sexually active leopard frogs investigating the neural mechanisms of Am- for eight consecutive months in the year. phibia is now apparent. It is generally ac- Other techniques such as the use of suction cepted that the amphibian brain closely and electrocautery for producing brain le- resembles the generalized prototype from sions, and the sectioning and reconstruction which the higher vertebrate brains developed of the operated brain enabled us to localize (Kuhlenbeck, 1921; Herrick, 1933a). Many more precisely than heretofore the function- of the ancient pathways of the amphibian ally important areas in the frog brain. Fi- brain are still recognized in the mammalian nally, the results of hours spent learning and and human brains (Papez, 1929; Ariens Kap- quantifying the normal mating patterns pers, Huber, and Crosby, 1936). Relatively (Noble and Aronson, 1942) proved to be an speaking, the frog brain is organized along invaluable aid in interpreting the effect of very elementary lines, and this is reflected in brain injury upon sexual behavior. the simple and extremely stereotyped mating The present study was designed to survey patterns which these animals exhibit. Hence in a general way the effects of brain depriva- information concerning the mechanisms of tions on various phases of the mating pattern. the innate behavior patterns of these primi- Intensive investigation of any particular tive vertebrates should be of considerable phase was left for future investigation now value in interpreting mammalian and human contemplated. brain function (Beach, 1942a) and in formu- lating general theories of the evolutionary changes in the nervous control of this very ACKNOWLEDGMENTS important aspect of behavior. This study was initiated under the guid- For many years Dr. C. J. Herrick has been ance of Dr. G. Kingsley Noble, late Curator engaged in an exhaustive study of the mor- of the Departments of Herpetology and Ex- phology of the amphibian brain, and during perimental Biology of the American Museum the course of this work he has formulated a of Natural History and Visiting Professor of number of hypotheses concerning the func- Biology of the Graduate School of New York tion of the structural elements which he de- University. Dr. Noble's inexhaustible en- scribed in such detail. However, as Herrick ergy, unending enthusiasm, and inspiration (1933a) himself expresses it, "These are in- are gratefully remembered. Sincere thanks ferences drawn from the anatomical arrange- are due to Dr. Frank A. Beach for many val- ments, and for most of them there is as yet uable suggestions made during the final little direct experimental proof." The present course of this research, and also for his very experiments were intended, in part, to exam- helpful criticism of the manuscript. Thanks 89 90 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY VOL. 86 are also due Dr. T.C. Schneirla for a critical fine histological preparations and to Miss reading of the manuscript. The generous as- Janet Roemhild for the illustrations.-L.R.A. sistance of Miss Arlene Douglis and Mrs. M. The experiments herein reported were sup- Madof in making some of the observations is ported by a grant from the Committee for acknowledged. Thanks are due to Miss Pris- Research in Problems of Sex, National Re- cilla Rasquin for the large number of very search Council. LITERATURE ROBERT BOYLE (1663), renowned physicist males which had just been separated from fe- and natural philosopher, was among the ear- males, he observed that one of the decere- liest experimentalists to investigate the be- brate animals reclasped a female. He inter- havior of frogs following the extirpation or preted this to be the result of the female's destruction of the brain. Boyle's experiments, accidentally swimming underneath the male and the studies of a number of investigators and stimulating the male's clasp reflex, that during the following century (reviewed by is, a simple local reaction rather than a gen- Eckhard, 1883), demonstrated the impor- eral response of the decerebrate male towards tance of the brain of the frog to the mainte- the female. nance of various vital functions such as heart Goltz (1869) confirmed Spallanzani's find- beat, respiration, and locomotion. More than ings relative to the tenacity of the male's a century later the great naturalist Spallan- clasp. He observed that the clasp reflex could zani (1786) demonstrated that during the be initiated by stimulation of the ventral breeding season clasping male frogs and toads pectoral skin and that frogs deprived of this would suffer excessive mutilation of their skin area no longer clasped. Moreover, a male bodies and hind limbs without releasing the could be induced to clasp the experimenter's females. When forcibly separated from the finger when it was rubbed against the pecto- females, these mutilated males soon re- ral skin. However, according to Goltz, a male clasped. Spallanzani decapitated clasping would soon release the finger, whereas when males, and found that they still remained in the pectoral region was stimulated by the amplexus for several hours, and separated back of a female, a lengthy clasp usually en- only when near death. On at least two sepa- sued. Males deprived of the cerebral hemi- rate occasions oviposition occurred while the spheres distinguished between the experi- decapitated frogs were coupling with normal menter's finger and a female as efficiently as females. These headless males fertilized the an intact male; but following ablation of the eggs, and viable tadpoles were recovered. entire brain, the animal attempted to em- Flourens (1824) was the first to report the brace and continued to clasp without discrim- loss of all spontaneous movement resulting ination, any object which touched his pecto- from forebrain extirpation, observing also that ral skin. Goltz concluded that a tonic em- the removal of only one cerebral hemisphere brace of the finger is not obtained in the caused no apparent behavioral changes. At intact animal because the brain transmits in- about the same time Desmoulins (1825), who hibitory impulses to the clasp reflex center was also studying the physiology of the anu- located in the spinal cord at the level of the ran brain, came to the opposite conclusion, brachial plexus, and at the same time the namely, that the. decerebrate frog still ex- brain sends excitatory impulses to many hibits spontaneous activity. His conclusion other centers in the spinal cord. was reached after observing the swimming Fromn other experiments investigating the activity of forebrainless animals in deep wa- functions of the forebrain Goltz (1869) ter. Here are found the beginnings of a con- stated that after various types of extirpa- troversy which has continued to the present tion, frogs lose "voluntary or spontaneous day. Desmoulins also showed that the decere- locomotion." Such frogs will not snap at in- brate frogs were not blind, for they could be sects, and during the breeding season decere- stimulated to jump accurately through a slot brate males will not pursue females. In in a board held obliquely in front of them. agreement with Desmoulins (1825) Goltz re- Most of the early investigators (Patton, ported that these forebrainless animals were 1846; Vulpian, 1866; Goltz, 1869; Onimus, not totally blind, since they avoided obsta- 1870; Steiner, 1885; Stroud, 1899) agreed cles when prodded to leap.
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