HARVARD UNIVERSITY

Library of the

Museum of

Comparative Zoology

MUS. COMP. ZOOU.

LIBRARY

MAY 2 4 1977 BREVIORA

HARVARD UNIVERSITY

MUSEUM OF COMPARATIVE ZOOLOGY

Harvard University

NUMBERS 410-436 1973-1976

CAMBRIDGE, MASSACHUSETTS, U.S.A.

1977

CONTENTS

BREVIORA

Museum of Comparative Zoology

Numbers 410-436

1973

No. 410. The Color Pattern of Scmora michoacanensis (Duges) (Serpentes, Colubridae) and Its Bearing on the Origin of the Species. By Arthur C. Echternacht. 18 pp. September 20.

No. 411. The Mandibular Dentition of Plagiomene (Dermop- tera, Plagiomenidae). By Kenneth D. Rose. 17 pp. December 28.

No. 412. Mylostoma variabile Newberry, An Upper Devonian Durophagous Brachythoracid Arthrodire, with notes on related taxa. By William J. Hlavin and John R. Boreske, Jr. 12 pp. December 28.

No. 413. The Chanares (Argentina) Triassic Reptile Fauna. XX. Summary. By Alfred Sherwood Romer. 20 pp. December 28.

No. 414. Ecology, Selection and Systematics. By Nelson G. Hairston. 21 pp. December 28.

No. 415. The Evolution of Behavior and the Role of Behavior in Evolution. By M. Moynihan. 29 pp. Decem- ber 28.

No. 416. Museums and Biological Laboratories. By Ernst Mayr. 7 pp. December 28.

No. 417. A New Species of Cyrtodactylus (Geckonidae) From New Guinea With a Key to Species from the Island. By Walter C. Brown and Fred Parker. 7 pp. Decem- ber 28.

No. 418. Morphogenesis, Vascularization and Phylogeny in Angiosperms. By G. Ledyard Stebbins. 19 pp. December 28.

No. 419. Protopiychus, A Hystricomorphous Rodent from the Late Eocene of North America. By John H. Wahlert. 14 pp. December 28.

1974

No. 420. Environmental Factors Controlling the Distribution of Recent Benthonic Foraminifera. By Gary O. G. Greiner. 35 pp. March 29.

No. 421. A Case History in Retrograde Evolution: The Onca Lineage in Anoline Lizards. L A no/is amiectens new species. Intermediate Between the Genera Anolis and Tropidodactylus. By Ernest E. Williams. 21 pp. March 29.

No. 422. South American Anolis: Three New Species Related to Anolis ni^rolineatus and A. dissimilis. By Ernest E. Williams. 15 pp. March 29.

No. 423. A New Species of Primitive Anolis (Sauria Iguanidae) from the Sierra de Baoruco, Hispaniola. By Albert Schwartz. 19 pp. March 29.

No. 424. The Larva of Sphindocis denticollis Fall and a New Subfamily of Ciidae (Coleoptera: Heteromera). By John F. Lawrence. 14 pp. June 28.

No. 425. Systematics and Distribution of Ceratioid Anglerfishes of the Genus Lophodolos (Family Oneirodidae). By Theodore W. Pietsch. 19 pp. June 28.

No. 426. Association of Ursus arctos and Arcfodus simus (Mam- malia: Ursidae) in the Late Pleistocene of Wyoming. By Bjorn Kurten and Elaine Anderson. 6 pp. Novem- ber 27.

No. 427. The Stratigraphy of the Permian Wichita Redbeds of Texas. By Alfred Sherwood Romer. 31 pp. Novem- ber 27.

No. 428. A Description of the Vertebral Column of Ervops Based on the Notes and Drawings of A. S. Romer. By James M. Moulton. 44 pp. November 27.

No. 429. Anolis rupinae new species A Syntopic Sibling of A. inonticola Shreve. By Ernest E. Williams and T. Preston Webster. 22 pp. November 27.

1975

No. 430. Anolis marcanoi new species: Sibling to Anolis cyhotes: Description and Field Evidence. By Ernest E. Wil- liams. 9 pp. March 28.

No. 431. An Electrophoretic Comparison of the Hispaniolan Lizards Anolis cyhotes and A. marcanoi. By T. Preston Webster. 8 pp. March 28.

No. 432. Evolution and Classification of Placoderm Fishes. By Robert H. Denison. 24 pp. March 28.

No. 433. South American Anolis: Anolis ihague. New Species of the Pentaprion Group from Columbia. By Ernest E. Williams. 10 pp. September 19.

No. 434. South American Anolis: Anolis parilis. New Species, Near A. tuirus Williams. By Ernest E. Williams. 8 pp. September 19.

1976

No. 435. Two New Species of Chelus (Testudines: Pleurodira) from the Late Tertiary of Northern South America. By Roger Conant Wood. 26 pp. April 8.

No. 436. Stupendetuys geographicus. The World's Largest Turtle. By Roger Conant Wood. 31 pp. April 8.

INDEX OF AUTHORS

BREVIORA

Museum of Comparative Zoology

Numbers 410-436

1973-1976

No.

Anderson, Elaine 426

Boreske, JohnR., JR 412

Brown, Walter C 417

Denison, Robert H 432

echternacht, arthur c 410

Greiner, Gary O. G 420

Hairston, Nelson G 414

Hlavin, William J 412

Kurten. Bjorn 426

Lawrence, John F 424

Mayr, Ernst 416

MouLTON, James M 428

Moynihan, M 415

Parker, Fred 417

PiETSCH, Theodore F 425

ROMER, Alfred Sherwood 413, 427

Rose, Kenneth D 411

Schwartz, Alber r 423

Stebbins, G. Ledyard 418

Wahlert, John H 419

Webster, T. Preston . ,. 429, 431

Williams, ErnestE 421, 422, 429, 430, 433, 434

Wood, Roger Conant 435, 436

B R E V I O R A

Miiseiiiii of Coiiipa]iliU&a^jv^^<2Blpgy

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us ISSN 0006-9698 ■'»^'^rfT

Cambridge, Mass. September 20,w©|^2 4^^f^tPER 410

THE COLOR PATT^^j^JW^'^O

Sonora michoacanensis i^Dugis/S^TV (SERPENTES, GOLUBRIDAE) AND ITS BEARING ON THE ORIGIN OF THE SPEGIES

Arthur C. Eghternaght

Abstract. The extensive variation in color pattern of the 31 known specimens of Sonora michoacanensis is described and a model illustrating the relationships of the major components presented. Sonora aequalis Smith and Taylor is placed in the synonymy of Sonora michoacanensis muiabilis Stickel from which it differs only slightly in color pattern. It is suggested that S. michoacanensis evolved from a bicolor, banded ancestor within the 5. semiannulata group or from a common ancestor at the southern edge of the Mexican .Plateau following habitat shifts associated with climatic changes during the Pleistocene. Sonora michoacanensis is inter- preted as an imperfect Batesian mimic of elapid coral snakes (Micrurus sp.) , intermediate irl an evolutionary sequence beginning with the bicolor, banded ancestor and leading toward a more perfect, tricolor mimic. Known locality records of S. michoacanensis are mapped and selected meristic data presented in tabular form.

Introdugtion

The genus Sonora (Serpentes, Colubridae) is represented in Mexico, at the southern Hmit of its range, by Sonora micho- acanensis (Fig. 1). Sonora m. michoacanensis (Duges) is found in arid to semiarid habitats from the upper Balsas Basin in Puebla to the lower slopes of the Sierra de Coalcoman and southeastern Colima, whereas S. m. mutabilis Stickel occupies foothills of the Sierra Madre Occidental from southern Jahsco to Nayarit and Zacatecas (Duellman, 1961; Zweifel, 1956). The principal diagnostic difference between the subspecies is that S. m. michoacanensis has an unmarked tail, whereas the tail of 6*. m. mutabilis is banded. The two subspecies will be considered together in the discussion of color pattern to follow.

The last review of this assemblage was by Stickel (1943).

BREVIORA

No. 410

106

Figure 1. Localities of documented specimens of Sonora iiiichoacanensis in Mexico. Hollow circles: 5. ?/?. michoacanensis; solid circles: S. m. muta- bilis. D. F. is the Distrito Federal.

His clear and concise discussion included a detailed description of a single unusual specimen which Smith and Taylor ( 1 945 ) subsequently named, with no further description, Sonora aequalis. Stickel had been unwilling to base a new species on the single specimen because it was of unknown provenance and because it difTered from S. m. mutabilis only in color pattern, a character known to be highly variable in S. michoacanensis. Stickel presented data on all 18 specimens of S. michoacanensis (including ^S*. aequalis) then known but was able to examine only 1 1 of these. The holotype of S. m. ?nichoacanensis was lost, and he designated a neotype (Fig. 2), and described S. m. muta- bilis. The recent discovery of a specimen intermediate in color pattern to "typical" S. m. michoacanensis and S. aequalis and the availabihty of 14 specimens of S. ynichoacanensis collected over the 30 years since Stickel's paper ha\e made possible a re-examination of the variation in color pattern of the species and a reassessment of the taxonomic status of S. aequalis. Al-

1973

COLOR PATTERN OF SONORA

Figure 2. Neotype of Sonora michoacanensis micfioacanensis, BMNH 1946. 1.14.65.

though this paper emphasizes color pattern, I have summarized meristic data for all known specimens (Tables 1 and 2) so that these data will be available to others. Counts of ventral scales were made according to the method of Dowling ( 1 95 1 ) and do not include the anal scale. Counts of subcaudal scales exclude the tip. For these reasons, data given here may differ slightly from those presented by Stickel (1943: 114-115). Where means are given for scale counts they are based only upon specimens that I was able to examine myself. The color de- scriptions are based on preserved specimens unless stated otherwise.

Acknowledgements. William E. Duellman, Richard D. Estes, Ernest E. Williams and Richard G. Zweifel have all read the manuscript in its formative stages and I am grateful for their thoughtful criticism. The research was funded in part by a grant from the Boston University Graduate School (GRS BI- .15-BIO). I am indebted to the following individuals and institutions for the loan of specimens: William E. Duellman (University of Kansas Museum of Natural History, KU), Her- bert S. Harris (Personal Collection, RS-HSH), Hymen Marx (Field Museum of Natural History, FMNH), Hobart M. Smith and' Dorothy Smith (University of Illinois Museum of Natural History, UIMNH), David B. Wake (Museum of Vertebrate Zoology, MVZ), Charles F. Walker and Scott M. Moody (Uni- versity of Michigan Museum of Zoology, UMMZ), Ernest E. Williams (Museum of Comparative Zoology, MCZ) and Richard G. Zweifel (American Museum of Natural History, AMNH). Herbert S. Harris kindly provided a color slide of a living snake, and A. F. Stimson was instrumental in obtaining data

4 BREVIORA No. 410

on, and photographs of, the three specimens in the British Museum of Natural History (BMNH). Photographs of other specimens were prepared by Frederick W. Maynard.

Variation of Color Pattern

It is almost impossible to exaggerate the extent of variation in color pattern exhibited by the series of Sonora michoacanensis presently a\'ailable for study. Only the pattern of the head and neck seem relatively invariant. There is always a dark "mask" on an otherwise pale head. The mask may include the rostral and internasal scales, but typically begins between the rostral and a line connecting the anterior margins of the orbits. This dark area surrounds the eye and may extend forward on the side of the head to include all or parts of the nasal, loreal, preocular, anterior supralabials and those in contact with the orbit, the postorbitals and the temporals. Dorsally it covers the frontal, supraoculars and (often) parts of the prefrontals, terminating with a crescentic posterior margin on the parietals. There is a black or dark brown nuchal band (coUar) separated from the mask by a light-colored band. The nuchal band may completely encircle the body or may be interrupted midventrally. The anterior margin of the nuchal band is variable in shape but the posterior margin is usually straight across. The nuchal band is followed posteriorly by a light-colored band, usually three to fixt scales wide, which is, in turn, followed by another dark band. The last is a "half-saddle," its anterior margin straight across and its posterior margin crescentic. The half- saddle may completely encircle the body or be interrupted at the midline below.

One specimen (FMNH 37141, Fig. 3A) has no pattern what- soever except that just described. All others have some dorsal banding pattern. This overall dorsal pattern ranges from one of only saddle-shaped triads consisting of a median gray band abutted fore and aft by black {e.g., AMNH 74951, Fig.'4B) to one of only broad black bands separated by a narrower gray band corresponding to the median gray band of the triads [e.g., KU 106286, Fig. 4C-4D). Individual snakes may have combinations of triads and broad black bands (Fig. SB, 3E-3F). Occasionally, the broad black bands are partially split by light pigment extending up from the venter {e.g., MVZ 76714, Fig. 3B). The light pigment (= ground color) may be ofT- white, gray, salmon or flesh-colored but to comply with Stickel's

1973

COLOR PATTERN OF SONORA

Figure 3. Sonora michoacanensis michoacanensis: A. FMNH 37141, dorsal; B. MVZ 76714, dorsal; C. UMMZ 109904, dorsal; D. UMMZ 109904, ventral; E. FMNH 39129, dorsal; F. FMNH 39129, ventral.

6 BRE\aORA No. 410

(1943) terminolog)- it is referred to as red herein. The black bands mav not reach the ventral scutes but if thev do, thev mav or ma}- not extend across them to form rings. The same is true for the black elements of the triads which may not reach the \'entral scutes, may completely ring the body in such a way that the median gray band is also a ring, or may be joined along the midventral line so that the median gray band is incomplete. All three possibilities are seen on UMMZ 109904 (Fig, 3D). If a snake has both triads and broad black bands, it is usual for the triads to be found anteriorly and the black bands posteriorly [e.g., FMNH 39129, Fig. 3Ey.

Taylor ( 1937) provides a description of color-in-life of Sonora michoacanensis michoacanensis from Guerrero and Jalisco. The ground color is red or pinkish, the dark elements of the triads black and the middle element of the triads yellow or gray- cream. A single specimen from Colima is similarly colored (Harris and Simmons, 1970), but Duellman (1961) described the middle element of the triads as white in a series of specimens from Michoacan.

A specimen of Sonora michoacanensis michoacanensis collected in Jalisco by Percy CUfton (KU 106286, Fig. 4C-4D) is un- usual in that none of the black bands is split by red and there are no triads. None of the black bands except the nuchal and that immediately posterior to it reaches the ventral scutes. The broad black bands are expanded laterally just above the ventral scutes and some contact adjacent, similarly expanded bands. The black and gray bands (black and pale salmon in this specimen) are subequal in width. This pattern is approached in MVZ 76714 (Fig. 3B) but, prior to the discover\^ of KU 106286, no S. michoacanensis were known with a pattern en- tirely of unsplit black bands alternating with gray bands of approximately equal width. In this respect, KU 106286 re- sembles Sonora aequalis (MCZ 6444, Fig. 4E-4F).

In addition to presence or absence of caudal banding, Sonora michoacanensis michoacanensis and S. m. mutahilis differ in the number of gray bands of females, the number of complete triads of males, and the number of black bands unsplit by red of males and females. Sexual differences are e\'ident for all three of these characters in S. m. mutabilis, but not in S. m. michoacanensis (Tables 1 and 2). In addition, there is a sta- tistically significant (t = 3.91, P < .01 with 23 degrees of freedom) difTerence between the subspecies in total (left plus right) number of infralabials: The mean and standard devia-

1973

COLOR PATTERN OF SONORA

Figure 4.

Sonora michoacanensis mutabilis: A. UIMNH 18754, dorsal; B. 'AMNH 74951, dorsal; C. KU 106286, dorsal; D. KU 106286, ventral; E. MCZ 6444, dorsal; F. MCZ 6444. ventral. MCZ 6444 is the holotype of Sonora aequalis.

8 BREVIORA No. 410

tions for S. m. michoacanensis are 13.5 ± 1.09, for S. m. muta- bilis 12.1 ± 0.30. The number of infralabials is not sexuallv dimorphic for either subspecies. It is notable that of the seven S. m. michoacanensis with 13 fewer infralabials, three are from near Coalcoman, Michoacan (UMMZ 106604-6), where a single specimen (UMMZ 109904, Fig. 3C-3D) has one irregu- larly shaped caudal band, possibly indicati\-e of intergradation. Three other specimens with fewer than 14 infralabials (KU 23791, MCZ 33650) or indications of low numbers of infra- labials (MVZ 45123) are from near Chilpancingo, Guerrero. The seventh such specimen is the missing holotype from "Michoacan" [Cope, 1884(1885)].

The Taxonomic Status of Sonora aequalis

The only known specimen of Sonora aequalis (MCZ 6444)^ is recorded as being from Matagalpa, Nicaragua, but Stickel ( 1 943 : 117) concluded that Matagalpa was most likely only the shipping point for material collected by W. B. Richardson. Other specimens in the same bottle as the snake and the locality label were two Eurneces lynxe lynxe (fide Joseph R. Bailey in Stickel, 1 943 : 1 1 8 ) , a lizard ^vhose range overlaps that of Sonora michoacanensis mutabilis. This and other evidence led Stickel to conclude that MCZ 6444 was found within or near the range of S. 7n. mutabilis. The pattern of MCZ 6444 consists of 26 black bnnds and 25 gray bands, the bands being all of ap- proximately the same width (the basis for the name aequalis). None of the black bands is split by red but se\'eral are xentrally concave (Fig. 4F). The nuchal band completely rings the body, but details in this region are obscure because of damage to the specimen. None of the black bands on the body reaches the venter and none is expanded laterally as in KU 106286. The cephah'c pattern is the same as that of S. michoacanensis and the tail is banded in triads as is characteristic of S. m. mutabilis. The specimen is badlv faded and no colors other than black and gray are apparent.

In vie\'/ of the great \'ariation in dorsal body pattern evident within the su}:)species of Sonora michoacanensis, it does not seem to mc that the differences between S. aequalis and S. m.

\Stickcl (1943: 117), in error, recorded tlu- snake as ;iii uiicatalogued specimen in the University of Michi,gan Museum of Zooloi^v. How and whv it got to Michigan and thence back to the Museum of Comparative Zoolog\' remains a mystery.

1973 COLOR PATTERN OF SONORA 9

mutabiUs are great enough to warrant taxonomic recognition of S. aequaUs. These differences are certainly no more startling than those of the almost patternless FMNH 37141 (Fig. 3A). KU 106286 (Fig. 4C-4D) seems to be a logical intermediate in pattern between S. m. mutabilis and S. aequalis. Extensive collecting in Mexico and Nicaragua over the last 30 years has brought to light no additional specimens of S. aequalis, but a number of additional specimens of "typical" (if that word is admissable) S. michoacanensis have been collected in Mexico. Of course, no additional specimens similar to FMNH 37141 have been found either.

It may be questioned whether it is any more justifiable to "sink" a species on the basis of one specimen (KU 106286) than it was to name one in the first place [S. aequalis, MCZ 6444). But the discovery of KU 106286 has provided an im- portant link in what appears to be a continuum in pattern variation extending from the pattern (or, rather, lack of pat- tern) exhibited by FMNH 37141 to that of MCZ 6444 with the presence or absence of caudal banding superimposed. The possibility that KU 106286 is a hybrid of S. aequalis and S. m. mutabilis cannot be ruled out, but its likelihood is reduced by the absence of additional specimens of S. aequalis in collections made over the past 30 years.

Relationships of the Components of Color Pattern AND THE Origin of Sonora michoacanensis

Figure 5 illustrates my concept of the relationships of the various components of dorsal color pattern of Sonora michoa- canensis. Certainly no ontogenetic sequence is impHed, but the initial stages (Fig. 5A-5B) may be interpreted to suggest some- thing of the origin of the species. The ancestor of S. michoa- canensis may have been patterned verv^ much like MCZ 6444. Progressive erosion of the broad black bands (Figs. 5B-5D) would yield triads (Fig. 5E). A complex genetic mechanism would allow indi\ddual snakes to have various combinations of triads and unsplit black bands or triads in varying numbers and of varying distances apart. With the exception of the virtually patternless FMNH 37141, the most consistent element of color pattern is the gray band between adjacent unsplit black bands or as the median element in a triad (Stickel, 1943: 116).

The banding pattern of MCZ 6444 is very similar to that of the banded forms belonging to the Sonora semiannulata group

10

BREVIORA

No. 410

Figure 5. Diagiammatic representation of color pattern variation of Sonora michoacanensis. The arrow spans one complete triad. Black r^ black, white :z= white or yellow, stippled rzz red. Upper figure of each pair, lateral view; lower figure, dorsal view.

of southwestern United States and northern Mexico (Stickel, 1938: 184-186; Stebbins, 1966). MCZ 6444 and all Sonora michoacanensis have 15 dorsal scale rows with no reduction as do some members of the S. semiannulata group. Sonora michoacanensis is distinguishable from members of the S. semi- annulata group in morphology of the hemipenis (Stickel, 1943: 112), but the two groups are very similar in scutellation, teeth, dentigerous bone structure, microscopic scale striation and, generally, color pattern (Stickel, 1943: 110). It seems reason- able to assume that, as Stickel ( 1 943 : 118) seems to have suggested, S. michoacanensis had its origin within the S. semi- annulata group or that the two groups had a common ancestor. Members of the Sonora semiannulata group are presently found (Stebbins, 1966) in the southern Warm Temperate and Subtropical Climatic Zones as broadly mapped by Dorf (1959: 198). These major climatic belts shifted southward \vith glacial

1973 COLOR PATTERN OF SONORA 11

advance during the Pleistocene (Dorf, 1959: 195) and the range of the S. semiannulata group or its ancestor may have been depressed southward into the area presently occupied by iS*. michoacanensis. Sonora michoacanensis may have differ- entiated as a relict at the southwestern fringe of the Mexican Plateau when climatic zones retreated northward with retraction of ^Visconsin glaciation.

The Selective Significance of the Color Pattern

OF Sonora michoacanensis

A number of New World colubrid snakes have tricolor band- ing patterns which are reminiscent of the red, black and yellow or white patterns well known among the highly venomous coral snakes (Elapidae). Considerable circumstantial evidence has accumulated that the colubrids are mimics of those coral snakes with which they are sympatric and are thus avoided by those predators which have learned to avoid coral snakes (Dunn, 1954; Hecht and Marien, 1956; but see Brattsrom, 1955). Three kinds of mimicry in snakes have been recognized ( Wickler, 1968: 118). Batesian mimicry where the model is highly venomous and the mimic nonvenomous, Miillerian mimicry where both models and mimics are highly venomous and rein- force one another, and Mertensian mimicry where the model is highly \'enomous and the mimic mildly venomous. Sonora michoacanensis I?, a Batesian mimic of coral snakes of the genus Micrurus (Hecht and Marien, 1956: 345).

The ranges of several species of Micrurus overlap or are con- tained within the range of Sonora michoacanensis (Roze, 1967). The basic color pattern of these elapids is one of black rings bordered on either side by narrower yellow or white rings, these triads being separated along the body by red. The order of the colors in the triads is, therefore, different from that of S. michoa- canensis. This difference is probably of little significance insofar as mimicry is concerned, as the distinction is difficult to make, even for a trained obser\'er, when the snakes are come upon suddenly or when they are moving. Potential predators pre- sumably have the same difficulty and Hecht and Marien (1956: 339) present evidence that the order of the colors is less im- portant that the presence of the bright, contrasting colors themselves. In other words, the mimic need not be an exact renlica of the model to gain a selective advantage.

The concept of Batesian mimicry requires that the mimic be

12 BREVIORA No. 410

less abundant than the model. If relative abundance in museum collections is an accurate reflection of relative abundance in nature, this requirement is met in that Micrurus is much better represented. It should, however, be noted that Sonora michoacanensis is a secretive species and may not be as rare as collections indicate. In a few areas where collecting has been repeated or intensive, small series have been obtained (see list of specimens ) .

There are two alternative hypotheses concerning the origin of mimicry- : 1 ) The mimic evoh es in a single step by mutation (Goldschmidt, 1945), and 2) the mimic evolves gradually through selection of modifier genes improving upon an original mutant that had itself a shght selective advantage (Fisher, 1930; E. B. Ford, 1953). Sheppard (1959) strongly supports the second hypothesis and suggests that mimetic patterns are con- trolled by supergenes that have evolved stepwise. Recent experi- mental work by H. A. Ford (1971) supports the alternative of gradual evolution and pro\ides evidence that bird predators avoid a new partial mimic, strongly preferring a familiar non- mimetic form of prey.

If my interpretation is correct, Sonora michoacanensis evolved from a bicolor, banded ancestor belonging to the S. semiannulata group. Although bicolor members of this group are sympatric with a coral snake {Micruroides euryxanthus) over much of their range, relative numbers of specimens in museums suggests the colubrid to be much the commoner snake. Thus, Batesian mimicry could not develop. To the south, however, the Pleisto- cene rehct population ancestral to S. michoacanensis may have been small relative to the populations of Micrurus with which thev evolved. If this was indeed the case, S. michoacanensis may as yet have not been perfected as a mimic and should be considered as intermediate in an evolutionary sequence leading from a nonmimetic, bicolor, banded ancestor toward a snake with a pattern of only triads. As there seems to be no geo- graphic trend in color pattern except the presence or absence of caudal bands and the generally better mimetic pattern of male S. m. mutabilis (see below), the gradual perfection of mimicry seems to be proceeding over the entire range of S. yyiichoacanensis. The extreme variability in color pattern evi- dent in the present population would result from lack of fixation at each of the major and minor gene loci responsible for pattern. This di\ersity of pattern would be tolerated because all of the intermediate types are to some degree mimetic except those that

1973 COLOR PATTERN OF SONORA 13

have bicolor banding patterns {e.g., MCZ 6444 and KU 106286) or are nearly patternless {e.g., FMNH 37141). Such extremes are expected at low frequencies where inheritance is polygenic and where fixation has not occurred ( Strickberger, 1968). The pattern of S. michoacanensis may be regarded as both protective in a mimetic sense and as concealing or dis- ruptive (Brattstrom, 1955). Hecht and Marien (1956: 346) have suggested that, "Banding may be an intermediate step through which a disruptive pattern is converted to a ringed, warning pattern, but functioning in both ways." It seems equally likely that the disruptive stage is intermediate to banded and tricolor, warning patterns.

An interesting and unexplained observation is that male Sonora michoacanensis mutabilis are, by virtue of having more complete triads (Table 2), better mimics than females and than both sexes of S. m. michoacanensis. Among butterflies, mimetic patterns are often sex-limited to females, as are other, nonmimetic, polymorphisms (Sheppard, 1959: 137). E. B. Ford (1953) has attributed this phenomenon to the importance of visual stimuli in the courtship of butterflies. Females make a choice of mates largely on the basis of visual cues and Ford (1953: 68) reasons that a new color pattern in males might not stimulate a female to copulate. In moths, where olfactory courtship stimuli largely replace visual cues, both sexes may be polymorphic (Sheppard, 1959: 137). Noble (1937) reviewed the role of sense organs in the courtship of snakes and concluded that chemical and tactile senses play the primary^ roles in sex discrimination and courtship, respectively. Vision was found to be important only in that movement attracts snakes during the breeding season. Nothing at all is known of the behavior of S. michoacanensis, but it seems unlikely that the sexual dichromatism of S. m. mutabilis serves as an aid to sex dis- crimination or courtship. There are no clues as to why sexual dichromatism should be pronounced only in S. m. mutabilis and not in S. m. michoacanensis.

The color pattern variation exhibited by Sonora michoa- canensis is at least equaled by that of Sonora aemula Cope of southern Sonora and Chihuahua, Mexico (Bogert and Oliver, 1945: 374; Zweifel and Norris, 1955: 244; Nickerson and Heringhi, 1966: 136). Sonora aemula is rare in collections (Nickerson and Heringhi knew of only ten specimens), but it, like S. michoacanensis, is probably locally more abundant than collections indicate. Five of the known specimens were found

14 BREVIORA No. 410

in or near Alamos, Sonora. The species is sympatric with both Micruroides and Micrurus and one specimen {e.g., Arizona State University No. 6611; Nickerson and Heringhi, 1966, fig. 1) may ha\e typical MicruroidesAik^ triads (white-black-white), S. 7nichoacanensis-\ike triads (black-white-black), or expanded triads (black-white-black-white-black) like some Micrurus from southern Mexico and Guatemala. The area between the triads is red. Mimicry in S. aemula may be at the same stage of de- velopment as that which I have suggested for S. michoacenensis, as may mimicry in some species of the venustissimus and annu- latus groups of the genus S cap hiodonto phis in Central America (Taylor and Smith, 1943). Scaphiodontophis is a Batesian mimic of both Micrurus and the mildlv colubrid Erythrolarnprus (Hecht and Marien, 1956: 342).

Known Specimens of Sonora michoacanensis

The holotype of Contia michoacanensis Duges (Cope), 1884 (1885) (= Sonora michoacanensis) has been lost, and Stickel (1943: 113) designated BMNH 1946.1.14.65 as neotype. BMNH specimens have been recatalogued since Stickel's (1943) paper and both old and new catalogue numbers appear in the listing to follow. Stickel ( 1943 : 115) examined an uncatalogued specimen of S. m. mutabilis in the American Museum of Natural History which was "tied with" (Stickel, 1943) AMNH 19714- 19716, but the present whereabouts of this specimen is unknown (W. H. Stickel and R. G. Zweifel, personal communications). Zweifel (1956: 6) has questioned the locality data of all four specimens. They are said to haxe been collected in Distrito Federal, Mexico, but this is far remo\'ed from the range of the subspecies as presently understood from well-documented speci- mens (Fig. 1) and they are given as "Locality Unknown" below. Stickel ( 1 943 ) cited specimens in the collections of E. H. Taylor and H. M. Smith by field number. These speci- mens have all been deposited in museums, and both field numbers (preceded by "HMS") and museum catalogue num- bers are gi\en below.

Sonora michoacanensis michoacanensis (18). COLIMA: Between Tecoman and Boca de Apiza, RS 596 HSH. GUERRERO: Chilpancingo Region, KET 23790-1, MCZ 33650, MVZ 45123; 16 km^ S Taxco, UTMNH 25063 (HMS 5440, holotype of Sonora erythrura Taylor, 1937); locality unknown, unnumbered specimen in the Museo Alfredo Duges,

1973 COLOR PATTERN OF SONORA 15

Colcgio del Estado Guanajuato. MICHOACAN: Apatzingan, FMNH 39128-9; Apatzingan, Hacienda California, FMNH 37141; 3.2 km E Coalcoman, 1364 m, UMMZ 109904-6; 12.2 km S Tzitzio, 1121 m, UMMZ 119457; 16 km S Uruapan, MVZ 76714; locality unknown, BMNH 1946.1.14.65 (formerly BMNH 1903.3.21, neotvpe), the holotype (presumed lost). PUEBLA: 10 km SE Matamoros, UIMNH 41688.

Sonora michoacariensis rnutabilis (13). JALISCO: near Magdalena, FMNH 105296 (HMS 4659, paratype), FMNH 105257 (HMS 4661, holotvpe), UIMNH 18754 (HMS 4660, paratvpe); 6.5 km S Tecalidan, MVZ 71356. NAYARIT: Jesus Maria, AMNH 74951. ZACATECAS: 8.8 km S Maya- hua, 1212 m, KU 106286; Mezquital de Oro, BMNH 1946.1. 14.63 (formerly BMNH 92.10.31.42, paratype), BMNH 1946.1.14.64 (formerly BMNH 91.10.31.43, paratype). LO- CALITY UNKNOWN: AMNH 19714-6 (paratypes), speci- men "tied with" AMNH 19714-6 (presumed lost), MCZ 6444 (holotype of Sonora aequalis Smith and Taylor).

Literature Cited

BOGERT, C. M., AND J. A. OLIVER. 1945. A preliminary analysis of the

herpetofaima of Sonora. Bull. American Mus. nat. Hist., 83: 297-426. Br.\ttstrom, B. H. 1955. The coral snake "mimic" problem and protec- tive coloration. Evolution, 9: 217-219. Cope, E. D. 1884(1885). Twelfth contribution to the herpetology of

tropical America. Proc. American phil. Soc, 22: 167-194. DoRF, E. 1959. Climatic changes of the past and present. Contrib. Mus.

Paleont. Univ. Michigan, 13: 181-210. Bowling, H. G. 1951. A proposed standard system of counting ventrals

in snakes. British J. Herp., 1: 97-99. DuELLMAN, W. E. 1961. The amphibians and reptiles of ISIichoacan,

Mexico. Univ. Kansas Publ., Mus. nat. Hist., 15: 1-148. DUNN^ E. R. 1954. The coral snake "mimic" problem in Panama.

Evolution, 8: 97-102. Fisher, R. A. 1930. The Genetical Theory of Natural Selection. Oxford:

Clarendon Press, xiv + 291 pp. Ford, E. B. 1953. The genetics of polymorphism in the Lepidoptera.

Advance. Genet., 5: 43-87. Ford, H. A. 1971. The degiee of mimetic protection gained by new

partial mimics. Heredity, 27: 227-236. GoLDSCHMiDT, R. B. 1945. Mimetic polymorphism, a controversial chapter

of Darwinism. Quart. Rev. Biol., 20: 147-164, 205-250. Harris, H. S., and R. S. Simmons. 1970. A Sonora michoacanensis michoa-

canensis (Duges) from Colima, Mexico. Bull. Maryland herp. Soc.

6: 6-7.

16 BREVIORA No. 410

Hecht, M. K., and D. Marien. 1956. The coral snake mimic problem:

A reinterpretation. J. Morph., 98: 335-365. NiCKERSON, M. A., AND H. L. Heringhi. 1966. Three noteworthy colubrids

from southern Sonora, Mexico. Great Basin Nat., 26: 136-140. Noble, G. K. 1937. The sense organs involved in the courtship of Storeria, Tliamnophis and other snakes. Bull. American Mus, nat. Hist., 73:

673-725. RozE. J. A. 1967. A checklist of the New World venomous coral snakes (Elapidac) , with description of new forms. American Mus. Novitatcs,

No. 2287, 60 pp. Shei'pard, p. M. 1959. The evolution of mimicry; a problem in ecology

and genetics. Cold Spring Harbor Symp. Quant. Biol., 24: 131-140. Smith. H. M., and E, H. Taylor. 1945. An annotated checklist and key

to the snakes of Mexico. U. S. natl. Mus. Bull., No. 187, iv + 239 pp. Stebbins. R. C. 1966. A Field Guide to Western Reptiles and Amphibians.

Boston: Houghton Mifflin Co., xiv + 279 pp. Stickel, W. H. 1938. The snakes of the genus Sonora in the United States

and Lower California. Copeia, 1938: 182-190. . 1943. The Mexican snakes of the genera Sonora and

Cliiouactis with notes on the status of other colubrid genera. Proc.

biol. Soc. \Vashington, 56: 109-128. Strickberger. M. W. 1968. Genetics. New York: The Macmillan Co.,

X + 868 pp. Taylor. E. H. 1937. A new snake of the genus Sonora from Mexico, with

comments on S. miclioacanensis. Herpetologica, 1: 69-73. , and H. M. Smith. 1943. A review of American sibynophine

snakes, with a proposal of a new genus. Univ. Kansas Sci. Bull.,

29: 301-337. WiCKLER. "\V. 1968. Mimicry in Plants and Animals. New York: "World

Univ. Lib., McGraw-Hill Book Co., 255 pp. ZwEiFEL, R. G. 1956. Additions to the herpctofauna of Nayarit, Mexico.

American Mus. Novitates, No. 1953, 13 pp. , AND K. S. NoRRis. 1955. Contribution to the herpetology

of Sonora, Mexico. American Midi. Nat., 54: 230-249,

ADDED IN PROOF: Mr. Scott AL Moody has kindly called my attention to an additional specimen of Sonora michoacanensis miitahilis obtained too late for inchision in this study. The snake (UMMZ 131666) is typical of the subspecies and was found at Prcsa de El Molino. El Molino in Jalisco, Mexico.

1973

COLOR PATTERN OF SONORA

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Museum of Comparative Zoology JAM? 1974 ^

HAftVARO

us ISSN 0006-9698

CambSB^?^ Number 411

THE MANDIBULAR DENTITION OF

PL A GIOMENE (DERMOPTERA, PLAGIOMENIDAE)

Kenneth D. Rose^

Abstract. The peculiar bilobate lower incisors and the anterior lower premolars of the Early Eocene genus Plagiomene are described for the first time. Several groups of mammals have independently acquired incisors with divided crowns, but available evidence suggests that any resemblances to Plagiotnene, except in the case of Recent dermopterans, can be attributed to convergence. Nevertheless, the close resemblance between the incisors of Plagiomene and those of certain Recent elephant shrews (Macroscelididae) may be indicative of similar incisor function. The hypothesis that Recent dermopterans (Galeopithecidae) are descended from Plagiomene or a closely allied form (a view previously based primarily on molar morphology) is strengthened by the specimens described here. A brief review of fossil forms that have been referred to the Dermoptera is presented, and it is concluded that, at present, only two fossil genera, Plagiomene and Planetetherium, can with reasonable probability be assigned to the Dermoptera.

Introduction

The Early Eocene genus Plagiomene has been widely re- garded as an early member of the Dermoptera, a view based on the molar morphology, which is similar to that in living der- mopterans. Fossil evidence of dermopteran e\'olution is ex- tremely scarce. Although Plagiomene is better known than any other fossil forms that may be considered Dermoptera, it is represented only by dental and gnathic remains. Previous litera- ture on fossil dermopterans (known forms of which are all assigned to the family Plagiomenidae) is minimal, and has been

^Department of Vertebrate Paleontology, Museum of Comparative Zoology, Harvard University.

2 BREVIORA No. 411

restricted to descriptions of parts of the dentition. None of the anterior dentition has been described or adequately figured be- fore, although the unusual incisors ha\'e been noted pre\'iously (Jepsen, 1962, 1970; Van Houten, 1945). The nearly complete lower dentition of Plagiomene described here (PU 14551, right mandible, and PU 14552, associated left mandible) is significant in pro\iding new e\idence that Plagiomene is related to and possibly ancestral to extant dermopterans. In addition, an in- complete right mandible, PU 13268, provides the first knowl- edge of the deciduous premolars in Plagiomene.

Comparative material of Plagio?nene and other forms has been examined during this study. Abbreviations used in the text are as follows:

AMNH American Museum of Natural Historv, New York MCZ Museum of Comparative Zoology (Mammalogy Col- lection), Harvard Uni\ersity, Cambridge, Massachusetts PU Princeton University Museum, Princeton, New Jersey YPM Peabodv Museum of Natural Historv, Yale Uni\er- sity. New Haven, Connecticut

Description

The lower dental formula of Plagiomene, 3.1.4.3, deduced by Matthew (1918) from f ragmentar\^ specimens, is confirmed bv PU nos. 14551 and 14552 (see Fig. 1 ).

The three lower incisors (Figs. 1, 2, 4) of Plagiomene are semiprocumbent, with broad, bilobate crowns, of which the mesial lobe is the larger. Faint longitudinal depressions on the lingual sides of these larger lobes in Ii and U (see Fig. 1 lower) are potential sites for further digitation of the incisor crowns. The crowns are slighth- convex on the buccal surface and somewhat concave lingually. The incisors diminish in size from U to U, Ii being considerably larger than L,. They have an oval, mesio- distally compressed cross section at the root. In the absence of the crowns, Matthew (1918) inferred from the roots that the incisors were small and unspecialized. The specimens discussed here show this inference to have been incorrect. Expansion of the incisors (mostly mesiodistally) occurs at the base of the crowns and increases towards the tip. There are no cingula. A small wear facet on the labiodistal surface of the mesial lobe of left Ii suggests that upper incisors may have occluded with the lower incisors. This is of interest because in the Recent forms, in

1973

DENTITION OF Plagiomeue

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BREVIORA

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1973

DENTITION OF Plagiomeue

' Figure 3. Occlusal view of right mandibular dentition, PU 14551.

BREVIORA

No. 411

5/^tA

Figure 4. Comparison of lower left incisors (I, at top) of Plagiomene (above) and Cynocephalus (below) .

1973

DENTITION OF Plagiomene

TABLE I

MEASUREMENTS (in mm) OF MANDIBULAR TEETH

OF PLAGIOMENE

PU 14552

PU 13268 (Deciduous teeth)

Ix

maximum mcsiodistal length

2.3

maximum height of crown

3.4

(measured Ungually)

I2

maximum mesiodistal length

2.0

maximum height of crown

2.5

(measured lingually)

I3

maximum mesiodistal length

1.4

maximum height of crown

1.8

(measured lingually)

c

maximum length

2.0

maximum breadth

1.4

Px

maximum length

1.7

maximum breadth

1.3

P:

maximum length

2.8

2.3 (dP,)

maximum breadth

2.0

1.2 (dP,)

P3

maximum length

3.7

3.5 (dP3)

maximum breadth

2.3

2.0 (dPa)

P4

maximum length

4.3

4.3 (dP,)

maximum breadth, trigonid

2.8

1.9 (dP,)

maximum breadth, talonid

3.2

2.3 (dP,)

M,

maximum length

4.3

maximum breadth, trigonid

3.0

maximum breadth, talonid

3.5

M.

maximum length

4.0

maximum breadth, trigonid

3.1a

maximum breadth, talonid

3.3a

M3

maximum length

3.9

maximum breadth, trigonid

2.4

maximum breadth, talonid

2.4

a,— approximate (tooth damaged)

which P is lost and P is reduced, the anteriormost upper teeth have migrated distally, so that the lower, comblike incisors meet an edentulous area during centric occlusion. The most com- plete upper dentition known for Plagiomene, AMNH 15208 (Szalay, 1969: 241), shows diminishing tooth size anteriorly, however, and does not preserve any incisors (except possibly

8 BREVIORA No. 411

P). This may indicate reduction or loss of the anterior upper teeth as in extant dermopterans.

The single-rooted lower canine (Fig. 1) of Plagiomene is premolariform, consisting of a large anterior cusp, which rises above the crowns of the incisors and of Pi, and a prominent but low heel. A low, incipient cusp is observed on the anterior border. The canine is laterally compressed and its root is ellip- tical in cross section.

The first premolar is a small, single-rooted tooth bearing one major cusp that may be followed by a much lower, small cusp- ule. Behind this is a still lower, incipient talonid cusp.

P2 (Figs. 1-3), a much larger tooth than Pi, is double-rooted and "premolariform-semimolariform" (as defined by Szalay, 1969: 199). The prominent protoconid is preceded by a dis- tinct though much smaller and lower paraconid, which is situ- ated directly anterior to the protoconid (not anterolingual to it, as in the teeth behind P2). The talonid is much broader and longer than in Pi, but still consists of only a single distinct cusp, homologous to the hypoconid.

The third premolar is semimolariform. The protoconid is the largest cusp, and there is a conspicuous, lower paraconid an- terolingual to it. A less prominent metaconid de\'elops from the posterolingual border of the protoconid. Some individuals {e.g., YPM nos. 24966 and 24971) have a small, lower cuspule anterior to the paraconid. The trigonid is somewhat extended anteroposteriorly and there is no trigonid basin. The talonid is well de\'eloped, with both hypoconid and entoconid prom- inent, and with a rudimentary^ hypoconulid. The talonid basin is closed posteriorly but is open anteriorly in a deep buccolingual valley separating the trigonid and the talonid. This feature is more strongly expressed in the molariform teeth.

P4 is fully molariform, differing from Mi chiefly in its slightly smaller size, but these two teeth are frequently almost indis- tinguishable. The three trigonid cusps and two main talonid cusps of P-i are large and sharp; the hypoconulid is lower and smaller. Some specimens {e.g., YPM 23578) have a small entoconulid anterior to the entoconid.

The lower molars have been pre\'iously figured and described (Matthew, 1918), but a few features may be noted. M1-3 are very similar to each other. The trigonid cusps are high and sharp; the metaconid is usually as high as the protoconid or higher, and the paraconid is somewhat lower. In the talonid a

1973

DENTITION OF Pldgiomene

0

5MM

Figure 5. Right mandible with functional deciduous premolars (dPj.^) and unerupted jjemianent P2_4; Mj is in process of eruption. Lateral view of PU 13268.

pronounced entoconulid is anterior to the entoconid on M2 and Ms, and it is present on Mi in some individuals. Posterior to the hypoconulid, the postcingulid rises in a broad cusphke projec- tion. This is well developed in Mi and M2 and, to a lesser ex- tent, in P4. In Ms the hypoconulid forms a small third lobe. Ms is usually narrower buccolingually than the other molars. The enamel of the molariform teeth is moderately crenulated, particularly in the talonid. A prominent ectocingulid is present on P3-M3 and posteriorly on P2. The posterior premolars and the molars clearly demonstrate a tendency toward polycuspida- tion, a characteristic of the Plagiomenidae.

The deciduous premolars preserved in PU 13268, dP2-4 (see Figs. 5 and 6), are in general similar to their adult replace- ments. They possess the same cusps in approximately the same positions but are relatively longer anteroposteriorly and more cqmpressed buccolingually. The talonid of dP2 is more molari- form than in P2, exhibiting both a hypoconid and a small ento- conid. The talonid of dPs is similarly more expanded than that of the replacing tooth. In the trigonid of dPs the paraconid and metaconid are somewhat more distinct and better separated from the protoconid than in the permanent Ps. In dP4 as well, the talonid is elongated and expanded relative to its condition in P4, and the hypoconulid is much more pronounced, almost forming a small third lobe as in Ms.

10

BREVIORA

No. 411

Figure 6. Occlusal view of PU 13268.

Discussion

Incisor specializations comparable to those occurring in Pla* giomene are found in several other mammals. Incisors with digitate crowns have evolved independently in several unrelated groups, including Carnivora, Notoungulata, Macroscelidea, Der- moptera, and Insectivora. Among these, carnivores such as Canis and Ursus show tendencies toward digitation of the in- cisor crowns, but to a less marked degree than in Plagiomene, and there is surely no relationship involved. Patterson (1940) described the deciduous incisors of the notoungulate "Progaleo- pithecus" (^ Archaeophylus), so-named by Ameghino in refer- ence to the dermopteran-like, pectinate incisor crowns, but there is no reason to believe that Plagiomene is in anv wav related to the Notoungulata.

Among the Insectivora, Nesophontes, a recently extinct Antil- lean form (McDowell, 1958: fig. 3), possesses bilobate incisors very similar to those in Plagiomene. Tenrec also shows a slight tendency toward digitation of the incisor crowns. There is little resemblance of the lower cheek teeth or the upper dentition of these forms to Plagiomene, however. The superficial similarities again may be attributed to convergence.

1973 DENTITION OF Plagiomeue 11

Certain Recent elephant shrews (Macroscelididae) bear a remarkable likeness to Plaoiomene in the conformation of the incisors; the most striking examples are Petrodromus and par- ticularly Rhynchocyon. In the former, the crowns of the per- manent incisors are bilobate, while the milk incisors {e.g., MCZ 26113) may have three or four lobes. The lower incisors of Rhynchocyon are the closest to Plagiomene of any forms exam- ined. They are, however, all approximately of equal size in Rhynchocyon, in contrast to the decrease in size from Ii to Is in Plaoiomene. The remainder of the macroscelidid dentition is

quite unlike that of Plagiomene. The most obvious contrasts are the loss of M3 (in the majority of known macrosceHdids, including both genera mentioned here) and the peculiar struc- ture of the molariform teeth (PI, MJ, M?.). Macroscelidids are not common in the fossil record, and of those known (Patterson, 1965; Butler and Hopwood, 1957), none show any particular resemblance to Plagiomene. The family is unknown outside Africa. Therefore, the similar form of the incisors in some Recent macroscelidids is surely not indicative of any close relationship, although it may reflect functional similarities.

Matthew (1918: 599) noted that the molars of the talpid Myogale [^= Desmana) were of somewhat similar structure to those of Plagiomene. Although he viewed this as "perhaps sig- nificant of a real though remote affinity" {ibid.: 600), the resemblances do not extend to the other teeth. It is unlikely that Plagiomene is related to talpids.

Plagiomene has most frequently been compared with the living dermopterans, Galeopithecidae {e.g., Matthew, 1918; Romer, 1966; Szalay, 1969; Jepsen, 1970; among others), and alliance with this group still appears to be the most likely possi- bility. Matthew (1918) first suggested a relationship between the two groups after studying the molars of Plagiomene, which be described as "unlike any placental molars known to me except those of Galeopithecus" {ibid.: 601). Indeed, the mo- lariform teeth (P4-M3, as in Plagiomene) of extant dermopter- ans show many features in common with Plagiomene: prominent conules; absence of hypocone; paracone and metacone situated well lingual to the buccal margin; low paraconid; presence of an entoconuHd; talonid and trigonid separated by a deep bucco- lingual valley; and crenulated enamel. Furthermore, PJ and, to a lesser extent, P3 are molarized as in Plagiomene. Although

12 BREVIORA No. 411

the lower incisors of galeopithecids exhibit less resemblance to those of Plagiomene than do most of the forms discussed above, the long time inter\'al separating these two forms must be taken into account. It seems highly probable that the comblike in- cisors of galeopithecids must ultimately have been deri\'ed from incisors with divided crowns such as those present in Plagiomene (see Fig. 4). In fact, the form of I3 in extant dermopterans is an approximate morphologic intermediate between the form of the incisors in Plagiomene and the pectinate condition of Ii and I2 in the living forms. The dental formula of the Galeopitheci- dae differs from that of Plagiomene, in the loss of two ante- molar teeth ( probably Pi and P2 ) ; this is easily explained, however, for the reduction or loss of teeth is common in species that evolve enlarged, specialized teeth, such as the pectinate in- cisors of galeopithecids. In summary, the new evidence pro- vided by the anterior dentition of Plagiomene strengthens the view that it is in or near the ancestry of the Recent Dermoptera.

This view, however, has been questioned recently. Van Valen (1967) regarded the Dermoptera as a suborder of the Insecti- vora. He suggested {ibid.: 271) that the Galeopithecidae may have been derived from Adapisoriculus (or an unknown related form) rather than from the Plagiomenidae, which he considered to be "unrelated to the Galeopithecidae" (although including both Plagiomenidae and Galeopithecidae in the same super- family of the Dermoptera, and placing Adapisoriculus in a suborder separate from the Dermoptera).

From the preceding discussion, it is clear that incisors with di\ided crowns have arisen independently in many unrelated mammals and that such incisors function in various ways. Al- though incisors of different general morpholog)^ are included in this discussion, some of those mentioned above exhibit close resemblances to those of Plagiomene. Based on these similari- ties, incisor function in Plagiomeiie may have been close to that in Nesophontes, Petrodromus, and Rhynchocyon, and probably not so much like that in extant dermopterans. Unfortunately, little is known of incisor use in anv of these forms. Flvinsr lemurs are reported to use their comblike incisors "in scraping the green coloring out of leaves" (Gregory, 1951: 387, quoting H. C. Raven), in ingesting leaves (Winge, 1941), or in groom- ing (Wharton, 1950). They are strictly herbivorous, feeding mainly on leaves, but including shoots, buds, soft fruit, and coconut blossoms in their diet (Wharton, 1950; Walker et al.,

1973 DENTITION OF Plapiomeue 13

&'

1964; Medway, 1969). In contrast, macroscelidids are pri- marily insectivorous, feeding largely on ants (Brown, 1964), but almost nothing is known of how macroscelidids use their incisors.

Hiiemae and Kay (1973) stress that incisors frequently func- tion in processes other than food ingestion and, in fact, that minimal use of incisors during ingestion in primitive mammals provided the opportunity to develop incisor specializations un- related to feeding. Therefore, it may not be correct to speculate that the diet of Plagiomene was similar to that of macroscelidids (indeed, differences in premolar and molar morphology would seem to be against siich a supposition) ; but it does seem likely that in both there are similarities of incisor function.

Fossil forms that have been assigned to the Dermoptera are rare and are represented solely by jaws and teeth. Only two monotypic genera, Plagiomene (from the Early Eocene of Wyo- ming) and Planet ether ium} (from the latest Paleocene of Mon- tana), can with reasonable assurance be referred to the family Plagiomenidae, the only known family (in addition to the Re- cent Galeopithecidae) referred to the order. Planetetherium (Simpson, 1928, 1929; Szalay, 1969) is almost certainly the direct ancestor of Plagiomene. It is known from only one lo- cality, the Eagle Coal Mine at Bear Creek, Montana, where it occurs in carbonaceous shale just above the coal layer (Van Valen and Sloan, 1966). The site evidently represents an an- cient swamp, and many of the mammals present (including Planetetherium) were probably arboreal (Simpson, 1928; Van

^Giasse (1955: 1727, fig. 1698) reproduced drawings of isolated incisors, from Simpson (1928: figs. 12 and 13) , and attributed the incisors to Planete- therium. This is apparently an unintentional error, which may have oc- curred because the description of the incisors (which Simpson, p. 14, stated "cannot be definitely classified or correlated with cheek teeth as yet") im- mediately followed the discussion of Planetetherium in Simpson's paper. Simpson believed that the incisors in question belonged to insectivores or primates, but he suggested no association with Planetetherium. The mor- phologies observed differ substantially, indicating that more than one taxon is involved. Inasmuch as Planetetherium is the most abundant form at Bear Creek, it seems not improbable that it is among the forms represented by the incisors. Szalay (1972: 25, figs. 1-9) has recently referred one of these incisors, AMNH 22153, to the primate Carpolestes, a common occurrence at Bear Creek. There is little evidence to confirm this allocation and, in fact, the morphology of AMNH 22153 may be closer to what might be expected in Planetetherium than in Carpolestes.

14 BREVIORA No. 411

Valen and Sloan, 1966; Jepsen, 1970). Planetetherium is by far the most commonly found member of the Bear Creek fauna. Se\'eral isolated teeth from the Early Eocene of France are the basis for a new genus and species being described by D. E. Russell, P. Louis, and D. E. Savage (in press) and regarded by them as a plagiomenid dermopteran. Casts of the teeth show features that suggest to me, however, that the new form may be neither a plagiomenid nor even a dermopteran. More complete evidence may in the future substantiate allocation of this form to the Plagiomenidae, but I do not believe that presently avail- able evidence is sufficiently convincing for such an assignment. L. S. Russell (1954) proposed Thylacaelurus montanus based on a maxillary fragment from the Kishenehn Formation (Late Eocene ?), British Columbia, which he believed to have mar- supial affinities. Although the specimen probably represents a placental (McKenna, in Van Valen, 1965: 394), Van Valen's (1967) allocation of the genus to the Plagiomenidae is unjusti- fied (see also Szalay, 1969: 242). Its relationships will remain obscure until further material is available.

Van Valen (1967) referred the Mixodectidae to the Der- moptera. This move also seems unwarranted, but the resem- blance of Elpidophorus to the plagiomenids may be significant. This comparison is not new. Simpson (1936) first discussed this similarity and suggested that Elpidophorus pro\ided a suitable structural intermediate between the two families, but he rejected Elpidophorus as an ancestor of Planetetherium on the grounds that they were approximate contemporaries. This objection is no longer valid, howe\^er, for the range of Elpidophorus has since been extended back at least into Torrejonian time. Szalay (1969) reviewed the status of relationships between the Plagio- menidae and the Mixodectidae and concluded that a\'ailable evidence does not support such ties. Nevertheless, the cheek teeth (both upper and lower) of Elpidophorus are quite similar to those of Plaoiomene, sufficientlv close to susrsrest that more than con\'ergence may be involved. It is possible that Elpido- phorus lies in or near the ancestry of the Plagiomenidae (cf. Sloan, 1969: fig. 6).

The Picrodontidae were placed in the Dermoptera by Romer (1966), but I concur with Szalay (1968: 32) that there is no evidence to support this.

If the Plagiomenidae are truly related to the living fiying lemurs, as seems probable on the basis of dental e\idence pre-

1973 DENTITION OF Plagiomeue 15

sented above and by Matthew ^1918) and Szalay (1969), the Dermoptera have been distinct from other mammalian groups since at least Late Paleocene time. Recent dermopterans have acquired a peculiar suite of specializations (including in par- ticular the dental specializations and the patagium) which is not found in other mammals. In view of these considerations, recog- nition of ordinal status for the Dermoptera (as accepted by Simpson, 1945; Grasse, 1955; Butler, 1956; Walker, 1964; An- derson and Jones, 1967; among others) seems fully warranted.

Acknowledgments

I am indebted to G. L. Jepsen and V. J. Magho, Princeton University, for granting me the privilege of studying and de- scribing the Princeton specimens of Plagiomene. G. L. Jepsen also furnished me with drawings of the specimens prepared several years ago by R. Bruce Horsf all.

Donald E. Savage kindly sent me a copy of a manuscript (Russell, Louis, and Savage, in press) describing a new form from the Eocene of France. Casts of the new specimens were generously provided by D. E. Russell. I am grateful to Russell, Louis, and Savage for graciously permitting me to include herein a dissenting view on the allocation of this new species.

My appreciation is also extended to the following, who have given me access to specimens under their care: Mary Dawson, Carnegie Museum; Parish A. Jenkins, Jr., Department of Verte- brate Paleontology, Museum of Comparative Zoology; Malcolm McKenna, American Museum of Natural History; C. W. Mack, Department of Mammalog)^, Museum of Comparative Zoology; and Elwyn Simons, Peabody Museum of Natural History.

Finally I would like to thank Thomas M. Bown, John G. Fleagle, F. A. Jenkins, Jr., G. L. Jepsen, and especially Br\an Patterson for critically reading the manuscript and offering help- ful suggestions and stimulating discussion. Laszlo Meszoly pre- pared the drawings; photographs are by A. H. Coleman. The illustrations were made possible through National Science Foun- dation Grant GB-30786 to A. W. Crompton.

Literature Cited

Anderson, S., and J. K. Jones, Jr. 1967. Recent Mammals of the World. New York: Ronald Press. 453 pp.

16 BREVIORA No. 411

Brown, J. C. 1964. Observations on the elephant shrews (Macroscelididae)

of Equatorial Africa. Proc. zool. Soc. London, 143(1): 103-120. Butler. P. M. 1956. The skull of Ictops and the classification of the

Insectivora. Proc. zool. Soc. London, 126(3): 453-481. Butler, P. M., and A. T. Hopwood. 1957. Insectivora and Chiroptera

from the Miocene rocks of Kenya Colony. Fossil Mammals of Africa,

no. 13. London: British Museum (Nat. Hist.) , 35 pp. Grasse, p. 1955. Ordre des Dermopteres. In Grasse, P. (ed.) , Traite de

Zoologie. Paris: Masson, pp. 1713-1728. Gregory, W. K. 1951. Evolution Emerging. Vol. I. New York: Mac-

millan. 736 pp.

Hiiemae, K. M., and R. R, Kay. 1973. Evolutionary trends in the dynamics of primate mastication. Fourth Internat. Cong. Primatology. Cranial- Facial Biology Symposium, M. R. Zingeser, ed. Basel: Carger. 30 pp.

Jepsen, G. L. 1962. Futures in retrospect. Yale Peabody Museum Report for 1962, 3: 8-21.

. 1970. Bat origins and evolution. In "Wimsatt, W. A. (ed.) ,

Biology of Bats. Vol. L New York: Academic Press. 64 pp.

Matthew, W. D. 1918. Part V — Insectivora (continued), Glires, Eden- tata. In Matthew, W. D., and Walter Granger, A revision of the Lower Eocene Wasatch and Wind River faunas. Bull. Amer. Mus. Nat. Hist., 38: 565-657.

McDowell, S. B., Jr. 1958. The Greater Antillean Insectivores. Bull. Amer. Mus. Nat. Hist., 115: 117-214.

Medwav, L. 1969. The "Wild Mammals of Malaya. London: Oxford

University Press. 127 pp. Patterson, B. 1940. The status of Progaleopithecus Ameghino. Field

Museum Nat. Hist., Geol. Ser., 8(3) : 21-25. . 1965. The fossil elephant shreAvs (Familv Macroscelidi- dae) . Bull. Mus. Comp. Zool., 133 (6) : 297-336. RoMER, A. S. 1966. Vertebrate Paleontology. Chicago: Univ. of Chicago

Press. 468 pp. RussrLL, D. E., P. Louis, and D. E. Savage, (in press) . Chiroptera and

Dermoptera of the French Early Eocene. Univ. Calif. Publ. in Geol. Sci. Russell, L. S. 1954. Mammalian fauna of the Kishenchn Formation.

southeastern British Columbia. Ann. Rep. nat. Mus. Canada for 1952-

1953, 132: 92-111. Simpson, G. G. 1928. A new mammalian fauna from the Fort Union of

southern Mcmtana. Amer. Mus. Novitates, No. 297: 1-15. â–  . 1929. A collection of Paleocene mammals from Bear

Creek. Montana. Ann. Carnegie Mus., 19: 115-122. . 1936. A new fauna from the Fort Union of Montana.

Amer. Mus. Novitates, No. 873: 1-27. . 1945. The principles of classification and a classification

of mammals. Bull. .\nRi. Mus. nat. Hist. 85: 1-350.

1973 DENTITION OF Plagiometie 17

Sloan, R. E. 1969. Cretaceous and Palcocene terrestrial communities of

western North America. Proc. North Amer. Paleont. Conv., part E:

427-453. SzALAY, F. S. 1968. The Picrodontidae, a family of early Primates. y\mer.

Mus. Novitates, No. 2329: 1-55. . 1969. Mixodectidae, Microsyopidae, and the insectivore-

primate transition. Bull. Amer. Mus. nat. Hist., 140: 195-330. . 1972. Paleobiology' of the earliest Primates, hi Tuttle, R.

(ed.) , The Functional and Evolutionary Biology of Primates. Chicago:

Aldine, pp. 3-35. Van Houten, F. B. 1945. Review of latest Paleocene and early Eocene

mammalian faunas. Journ. Paleo., 19(5): 421-461. Van Valen, L. 1965. Paroxyclaenidae, an extinct family of Eurasian

mammals. Journ. Mammal., 46(3) : 388-397. . 1967. New Paleocene insectivores and insectivore classi- fication. Bull. Amer. Mus. nat. Hist., 135: 219-284. Van Valen, L., and R. E. Sloan. 1966. The extinction of the multi-

tuberculates. Syst. Zool., 15 (4) : 261-278. Walker, E. P., et al. 1964. Mammals of the World. Vol I. Baltimore:

Johns Hopkins Press. Wharton, C. H. 1950. Notes on the life history of the flying lemur.

Journ. Mammal., 31: 269-273. Winge, H. 1941. The Interrelationships of the Mammalian Genera. Vol. I,

Copenhagen: C. A. Reitzels Forlag. (English translation.)

B R E V I 0 R A

V

iMu s^fftff^Tf Comparative Zoology

J^H^ t974

US ISSN 0006-9698

Cambridge, Mass. 28 December 1973 Number 412

HARVARD

um^m^c

OMA VARIABILE NEWBERRY, AN UPPER DEVONIAN DUROPHAGOUS BRAGHYTHORAGID ARTHRODIRE, WITH NOTES ON RELATED TAXA

William J. Hlavin^

and John R. Boreske, Jr.^

Abstract. All known gnathal elements of the durophagous aithrodire Mylostoma from the Late Devonian (Famennian) Cleveland Shale of Ohio show that the inferognathal and posterior palatopterygoid elements increase in size and maintain a constant shape during growth, Avhile the anterior palatopterygoids are paired elements in the juvenile condition which fuse into a single median gnathal in the adult. Dinognatlius is a synonym of Mylostoma. Mylosioma variahile, Mylostoma eurhinus, and Mylostoma new- berryi are here considered the only valid taxa. Mylostoma eastmani from the Grassy Creek Shale of Missouri (Famennian) is now considered a syno- nym of M. variahile; it was based on undiagnostic gnathal characters. The fusion of anterior gnathal elements is suggested as a possible origin of the median gnathal in the enigmatic arthrodire Biingartius and possibly also in the selenosteid Paramylostoma.

Introduction

, Newberry (1883: 146) described a left inferognathal from the Cleveland Shale member of the Ohio Shale Formation ( Late Devonian, Famennian) as Mylostoma variahile, referring to it as a "dipterine ganoid" on the basis of the similarity of its gnathal element to those of Dipterus and Ceratodus. In 1893, a concre- tion containing the virtually complete cranial, thoracic, and

^Cleveland Museum of Natural History, Cleveland, Ohio, and Boston Uni- versity, Boston, Massachusetts.

^Museum of Comparative Zoology, Harvard University, Cambridge, Mas- sachusetts.

2 BREVIORA No. 412

ventral shield of a single indi\'idual ^vas collected from the Cleve- land Shale exposures at Brooklyn, Ohio, and was obtained by the American Museum of Natural History, with the counterpart being acquired by the Museum of Comparati\'e Zoology. Dean ( 1901 ) described both specimens as Mylostoma variabile, placing the taxon within the Arthrodira. Eastman (1906) reviewed the jaw mechanics of Mylostoma as well as the morphology of its gnathal elements and concluded that Mylostoma was an arthro- dire with a gnathal apparatus specialized for crushing.

Hussakof (1909: 268) described Dinognathus ferox as "an imperfectly definable genus and species of arthrodire" on the basis of an isolated median gnathal. Eastman (1909) made a hypothetical reconstruction by placing the Dinognathus ferox t\pe of dentition over the inferognathals of Mylostoma terrelli and placing the posterior palatopter)'goids of M. terrelli on the labial side of the Dinognathus ferox median gnathal. Dunkle and Bungart (1945) described Dinognathus eurhinus, a second species of Dinognathus, on the basis of a median gnathal with general morphology differing from that of D. ferox, but with features giving evidence for a similar function.

A recently discovered specimen (CMNH 8120) represents a complete set of jaw elements of an adult Mylostoma variabile. This specimen, along with other specimens in the Museum of Comparative Zoologv (MCZ), American Museum of Natural History ( AMNH),'bberlin College (OC), and the Cleveland Museum of Natural History (CMNH) has enabled this study of the morphology of the functional region of the inferognathals and palatopterygoids through various size-growth stages. Evi- dence of the fusion of the anterior palatopterygoids has been observed in the adult, aiding in the synonymy of mylostomatid taxa that were based oh undiagnostic character-states of the anterior palatopterygoids.

Order Arthrodira

Family Mylostomatidae

Mylostoma variabile Newberry, 1883

Mylostoma variabile Newberry, 1883: 146 Mylostoma terrelli Newberry, 1883: 147 Dinognathus ferox Hussakof, 1909: 268 Mylostoma eastmani Branson, 1914: 62

Holotype. OC 1 300, left inferognathal.

Paratypes. MCZ 1435, left anterior palatopterygoid ; MCZ

1973 MYLOSTOMA VARIABILE 3

1436, right posterior palatoptcrygoid ; AMNH 42G, left anterior paIatopter)goid ; and AMNH 43G, right anterior palatopter)'- goid.

Type locality and horizon. Sheffield Lake, Ohio. South Shore of Lake Erie, T 7 N, R 17 W, Lorain County, Ohio; Cleveland Shale member of the Ohio Shale Formation.

Age. Famennian ( Late Devonian ) .

Hypodigm. Cleveland Shale member of the Ohio Shale For- mation, Ohio: AMNH 7526, nearly complete disarticulated cra- nial and thoracic shields (counterpart = MCZ 1490) ; CMNH 8129, left and right inferognathals, left and right posterior pala- topterygoids, median gnathal; AMNH 7915, 10701, CMNH 6094, median gnathals; MCZ 1429-1431, CMNH 5080, 5150, 5177, 6095, 6224, 7256, 7643, 7705, OC 1483, inferognathals; AMNH 44G, 3290, 3588, 3591, MCZ 1437-1438, 13271- 13274, OC 1301, 1429, CMNH 5022, 5795, 7694, palatoptery- goids. Huron Shale member of the Ohio Shale Formation, Ohio: MCZ 13275, right inferognathal. Grassy Creek Shale Formation, Missouri: University of Missouri collections, median gnathal, posterior palatoptcrygoid.

Revised diagnosis. Cranial shield having a wide lateral width and short anteroposterior length similar to that of the titanich- thyids. Postorbital element bordered posteriorly by paranuchal; centrals not in contact with marginals and are anteriorly sep- arated by pineal. Anterior palatopterygoids of juvenile fuse to form median gnathal in adult. Suborbitals narrow and long, orbits large. Median dorsal short without well-developed keel. Median gnathal of Mylostoma variabile possessing a greater width than length and less deeply excavated on either side of the longitudinal ridge than that of Mylostoma eurhinus.

Systematic Discussion

The holotype of Mylostoma variabile Newberry (1883: 146) is a left inferognathal, the size of which indicates that it belongs to a young adult of the species. The paratypes, comprising the anterior and posterior palatopterygoids, are characteristic of the known palatopterygoids of Mylosto?na. Dean (1901) described the most completely known specimen of M. variabile (MCZ 1490, AMNH 7526). This specimen represents a young in- dividual of the species ( Plate 1 ) . All of the elements comprising the upper and lower jaw apparatus are well preserved and are

4 BREVIORA No. 412

the basis for Eastman's (1907) reconstruction of the mylosto- matid dentition.

A second species, M. terrelli Newberry (1883: 147), repre- sents the left inferognathal (MCZ 1430) of an individual larger than the holotype of M. variabile. Hussakof (1909: 268) be- lieved the specific variations in this specimen could be attributed only to an age difference in M. variabile, and recommended that M. terrelli become a synonym of M. variabile.

A third species of Mylostoma, M. newberryi Eastman (1907: 224) is based on a pair of dental elements identified as the anterior portions of left and right inferognathals (OC 1302) and the posterior portion of a smaller left inferognathal (MCZ 1439) . These dental elements were originally described by Newberry (1889: 165) as belonging to M. variabile because of their dis- tinctive narrowness and triangularity, which he believed demon- strated diversity in the species. Earlier, Eastman (1906: 22; fig. E) figured these plates as pre-anterior palatopterygoids as part of his reconstruction of the upper dentition of M. variabile. This reconstruction is misleading since these pre-anterior pala- topterygoids are not present in the MCZ 1490 and AMNH 7526 specimens. We believe that Eastman realized this a year later and established M. newberryi to include these "extra" plates. Morphologically, the dental plates represent the functional region of the inferognathal in a juvenile mylostomatid, having a very thin and narrow attachment with the blade of the inferognathal. This functionally weak attachment between the two areas in this bone may be a result of either an extremely early growth stage or a pathologic condition, the latter being here suggested as an explanation for the abnormal osteological conditions in the jaw elements of the dinichthyid Hussakofia ( Cossmann ) .

Branson (1914) described Mylostoma eastmani on the basis of an isolated posterior palatopterygoid from the Famennian Grassy Creek Shale of Louisiana, Missouri. This specimen, along with an element referred to by him as an "occipital" (= nuchal) of Dinichthys rowleyi (correctly identified as a Dinognathus-\ike median gnathal by Dunkle and Bungart, 1945), comprises the only known occurrence of Mylostoma outside the Ohio Shale Formation. The character-states established by Branson (1914) for Mylostoma eastmani are undiagnostic since they do not differ from those of M. variabile, and we therefore include Mylostoma eastmani as a synonym of Mylostoma variabile. This occurrence, however, extends the distribution of this genus outside of the Appalachian Basin onto the mid-continent.

1973

MYLO STOMA VARIABILE

/0^mm:\

••.'••-•;;5-i>-!'>.\ v';-,! '• -J'-;''-".-;;;.' • /

Figure 1. Median gnathal elements (after Dunkle and Bungart, 1945) : A, Mylostoma (= Dinognathus) eurhinus CMNH 5063; B, Mylostoma varia- bile {= Dinognathus ferox) CMNH 6094; d = dorsal, v = ventral.

6 BREVIORA No. 412

Hussakof (1909: 268) described Dinognathus ferox (Fig. IB) from a single median gnathal (AMNH 7915) resembling the mvlostomatid dentition but ha\ins: uncertain affinities. Eastman (1909) felt that D. ferox represented the fused part of the an- terior palatopterygoids of an adult Mylostoma, but he lacked the appropriate specimens needed to prove this hypothesis. Dunkle and Bungart (1945), in describing Dinognathus eurhinus from a median gnathal (CMNH 5063; Fig. lA), did not advocate Eastman's ideas on fusion of the anterior palatopterygoids and opposed his hypothesis on anatomical grounds, which they felt were contradictory to the generalized pattern of jaw elements in all arthrodiran fish. They considered his reconstruction of the Dinognathus median gnathal as a dorsal gnathal element of Mylostoma to be invalid, arguing that the median gnathal could not have been derived from the fusion of the anterior pair of mylostomatid palatopterygoid elements.

A recently discovered specimen (CMNH 8129; Plate 2) rep- resents a complete set of gnathal elements belonging to an adult M. variabile. This specimen consists of typical right and left inferognathals, right and left posterior palatopterygoids, and a Dinognathus ferox median gnathal. The discoxery of this speci- men, which lacks the anterior palatopterygoids but has posterior palatopterygoids and inferognathals associated with the D. ferox median gnathal element, confirms Eastman's hypothesis that the median gnathal of D. ferox represents the fusion of the anterior palatopterygoids in the adult mylostomatid (Fig. 2). A survey of all known existing mylostomatid palatal dental plates shows them to fall into three size categories : ( 1 ) the posterior pala- topterygoids, having a size-growth range from ju\^enile to adult, (2) the anterior palatopterygoids, all representing juvenile speci- mens of varying degrees but none approaching the adult size of their corresponding posterior palatopterygoids, and ( 3 ) the me- dian gnathals or fused anterior palatopterygoids, which all cor- respond to the adult size of the inferognathals and posterior pab.- topterygoids of the genus Mylostoma.

In \iew of this evidence, it is su2:s:ested here that the taxonomv of the Mvlostomatidae ma\ be revised as follows: the 2:enus Dinognathus becomes a synonym of Mylostoina; Mylostoma variabile, the type species, includes also Dinognathus ferox, Mylostoma terrelli, and Mylostoma eastmani as synonyms; "Dinognathus'' eurhinus becomes a valid species of Mylostoma; Mylostoma newberryi, a species known only from the anterior portions of its inferognathals, is included within the M}losto-

1973

MYLOSTOMA VARIABILK

A

B

Figure 2. A, Eastman's (1907) reconstruction of the upper jaw apparatus of Mylostoma variabUe, displaying the paired anterior palatopterygoids (AP) of the juvenile condition (reconstruction based on AMNH 42G-43G, 3591, and MCZ 1437) ; B, Reconstruction of the tipper jaw apparatus of Mylo- stoma variabile, displaying the median gnathal (MG) of the adult condition (fused anterior palatopterygoids; reconstruction based on CMNH 8129) ; PP = posterior palatopterygoids.

8 BREVIORA No. 412

matidae but its affinities with the other species of Alylostorna cannot be determined until additional material becomes avail-- able.

Comparison With Other Arthrodires Having A Similar Jaw Apparatus

As presently constituted, the family Mylostomatidae embraces the following genera: Mylostoma (= Dinognathus), Dinomylos- toma, and possibly Tafilalichthys. Eastman (1906) described Dinomylostoma, which is restricted to the medial Frasnian Shales of New York and Kentucky, as being phylogenetically the most primitive of the mylostomatids. Although incompletely known, it is morphologically and chronologically transitional between Dinichthys and Alylostoma. The inferognathal elements possess a flat, narrow oral surface, not yet expanded as in Mylostoma. The blade-length comprises approximately 45 percent of the inferognathal, displaying the generalized condition of the ad- ductor mandibulae muscles in the Frasnian mylostomatids, as compared to the 60 percent blade-length attained by the arched forward inferognathal elements of the Famennian Mylostoma. According to Dunkle and Bungart ( 1 943 ) , this specialized con- dition increases the length of the adductor mandibulae muscles to produce a more powerful bite. The anterior dorsal gnathal elements of Dinomylostoma display features transitional between the dinichthyid anterior supragnathals and the mylostomatid anterior palatopterygoids. The posterior gnathal elements, how- ever, have become completely specialized into well-defined my- lostomatid posterior palatopterygoids. This gnathal condition is paralleled to a less specialized degree by the Frasnian pholidosteid Malerosteus, described by Kulczycki (1957) from the Holy Cross Mountains of Poland.

It is interesting to note that the enigmatic arthrodire Bungar- tius perissus Dunkle, which is known from a single complete adult specimen, lacks the anterior supragnathal element. The jaw elements preserved represent the corresponding right and left inferognathals, the posterior supragnathals, and a wtII- developed median gnathal. In this case, Dunkle (1947: 104) considered the "anterior supragnathal element either \estigial or completely absent." The absence of the anterior supragnathal elements in the adult Bungartius parallels the absence of these elements in the adult Mylostoma. The median gnathal is uniquely restricted to these two genera and we believe it has developed

1973 MYLOSTOMA VARIABILE 9

through the fusion of the anterior supragnathal elements during srrowth. This condition mav occur also in the selenosteid Para- mylostoma Dunkle and Bungart, in which the jaw mechanism is represented by an inferognathal specialized for crushing, and an associated posterior supragnathal. The anterior supragnathal and/or median gnathal is unknown in this genus.

The gnathal condition, suggesting a durophagous habit, while not exclusively restricted to the Mylostomatidae as demonstrated by Bungartius, Paraniylostoma, and Malerosteus, has achieved its highest degree of specialization in the genus Mylostoma. This gnathal condition as manifested within other families of arthro- dires is believed to represent diverse attempts of broader adapta- tion and efficiency of the feeding mechanisms at the pachyosteo- morph le\el of organization as suggested by Miles (1969).

On the basis of an isolated cranium, Lehman (1956) de- scribed Tafilalichthys lavocati as a new brachythoracid arthro- dire from the Famennian of Southern Morocco. Obruchev (1964), in his review of this genus, suggested that Tafilalichthys lavocati might be a mylostomatid, since the cranium is morpho- logically similar to that of Mylostoma as described by Dean (1901). No gnathal elements are yet known from T. lavocati, and therefore no positive assignment to the Mylostomatidae can be made at this time. However, the close relationship of the North American Famennian arthrodiran taxa to the Moroccan arthrodiran remains, as well as a review of the Cleveland Shale Arthrodira, will be of considerable interest in documenting the phylogenetic and paleozoogeographic relationships within the Mylostomatidae.

The stratigraphic range of Mylostoma is relatively short, re- stricted to the Famennian (Late Devonian) time in North America. At this time the brachythoracid arthrodires achieved their highest level of adaptive radiation before extinction.

ACKNOW^I.EDGMENTS

Thanks are due to J. -P. Lehman and Daniel Goujet ( Museum National d'Histoire Naturelle, Paris), Farish A. Jenkins, Jr. and Robert H. Denison (Museum of Comparative Zoology), Richard Estes (Boston University), and William E. Scheele (Cleveland Museum of Natural History) for their helpful sug- gestions. This research was supported in part by grants from the Albion Foundation and Sigma Xi to Hlavin.

10 BREVIORA No. 412

Literature Cited

Branson, E. 1914. The Devonian fishes of Missouri. Univ. Missouri Bull.,

15(31): 59-74. Dean, B. 1901. On the characters of Mylostoma Newberry. Mem. New

York Acad. Sci., 2 (3) : 101-109. DuNKLE, D. 1947. A new genus and species of arthrodiran fish from the

Upper Devonian Cleveland Shale. Cleveland Mus. Nat. Hist. Sci. Publ.,

8(10) : 103-117. , AND P. BuNGART. 1943. Comments on Diplognathus mirabilis

Newberry. Cleveland Mus. Nat. Hist. Sci. Publ., 8 (7) : 73-84.

AND . 1945. Preliminary notice of a remarkable

arthrodiran gnathal plate. Cleveland Mus. Nat. Hist. Sci. Publ., 8 (9) :

97-102. Eastman, C. 1906. Structure and relations of Mylostoma. Bull. Mus. Comp.

Zool., 50(1).: 1-29. . 1907. Mylostomid dentition. Bull. Mus. Comp. Zool., 50 (7) :

211-228.

1909. Mylostomid palatal dental plates. Bull. Mus. Comp.

Zool., 52 (14) : 261-269.

HussAKOF, L. 1909. The systematic relationships of certain American arthrodires. Bull. Amer. Mus. Nat. Hist., 26: 263-272.

KuLCZYCKi, J. 1957. Upper Devonian fishes from the Holy Cross Moun- tains (Poland) . Acta Pal. Polonica, 2 (4) : 285-380.

Lehman, J.-P. 1956. Les arthrodires du Devonien Superieur du Tafilalet (Sud marocain) . Notes Mem. Serv. Geol. Maroc, 129: 1-70.

Miles, R. 1969. Features of placoderm diversification and the evolution of the arthrodire feeding mechanism. Trans. Roy. Soc. Edinburgh, 68 (6) : 123-170.

Newberry, J. 1883. Some interesting remains of fossil fishes, recently dis- covered. Trans. New York Acad. Sci., 2: 144-147.

. 1889. The Paleozoic fishes of North America. Monog. U.S.

Geol. Surv., 16: 1-340.

Obruchev, D. 1964. Class Placodermi. hi Osnovy Paleontologii 11. Mos- cow: Nauka, pp.1 68-260.

1973

MYLOSTOMA VARIABILE

11

'T" *^yf^»^

^_ — I

ocrri

B

Plate 1. Mylostoma variabile (displaying cranial, thoracic, and ventral shields) , juvenile: A, MCZ 1490; B, counterpart AMNH 7526; SO = sub- orbital.

12

BREVIORA

No. 412

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r"'^^*^

"|gi-v

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Plate 2. Mylostoma variabile CMNH 8129; jaw elements of an adult showing left and right infeiognathals (IG) , left and right posterior pala- topterygoids (PP) , and a median gnathal = fused anterior palatopterygoids (MG) .

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CAMBRiDGKajl^j^f^gl*^, December 1973 Number 413

THE GHANARES (ARGENTINA)

TRIASSIG REPTILE FAUNA

XX. SUMMARY

Alfred Sherwood Romer

Abstract. A brief account is given of the geologic setting of the Tiiassic tetrapod faunas found in South America; the nature of the Chanares reptile fauna is summarized, and this fauna is compared with other Triassic as- semblages in South America and other continents.

In nineteen pre\'ious papers in the Museum of Comparative Zoology Breviora^; an account has been published of the reptile fauna ifrom the Triassic Chafiares Formation of Argentina col- lected by the La Plata-Harvard expedition of 1964-65; this series includes, in addition to papers written by myself, contribu- tions by C. Barry Cox, Parish A. Jenkins, Jr., James A. Jensen, and Arnold D. Lewis. Except for a future detailed study of the skull of the cynodont Pro baino gnat hus by Edgar F. Allin and myself I have no further plans for publication on the Chafiares fauna. The present paper is intended to furnish a short summary of the results of the 1964-65 expedition. Except for a few forms recently described from the Chanares Formation, a recent paper by Bonaparte (1972) gives a succinct summary of all known reptiles from the South American Triassic, so that detailed ref- erences are unnecessary below.

As noted in previous papers in this series, I am deeply in- debted to the National Science Foundation for grants for collec- tion, preparation, and publication of the Chanares fauna.

Geologic Setting Until the last few decades, almost nothing was known of the

^Breviora Nos. 247, 252, 264, 295, 333, 344, 352, 373, 377, 378, 379, 385, 389, 390, 394, 395, 396, 401, and 407.

2 BREVIORA No. 413

Triassic tetrapod faunas of South America. Now, however, tetra- pods are known from fi\e discrete areas of Argentina and south- ern Brazil:

( 1 ) The El Tranquilo Formation of Santa Cruz Province of Patagonia. From the upper part of this formation, ob\'iously of Late Triassic age, have been collected prosauropod dinosaur remains. These ha\'e been studied by Casamiquela, but the results have not been published; they appear to pertain to the European genus Plateosaiirus.

(2) The Puesto Viejo Formation, in southern Mendoza Prov- ince. Undescribed fragmentary remains are present in the lower part of the formation; from the upper part, Bonaparte has described a primitive but somewhat specialized traversodontid gomphodont Pascualgnathus and, most interestingly, forms in- distinguishable from Cynognathiis and Kannemeyeria, the most characteristic genera of the Cynognathus zone of the Upper Beaufort beds of South Africa. The Scythian age of this forma- tion is obvious.

(3) The Cacheuta Basin. In the precordillera west of Men- doza is a series of beds of Triassic age, the Cacheuta Series. I have elsewhere (Romer, 1960) given a brief resume of the geology. Four formations have long been recognized; in ascend- ing order they are the Las Cabras, Potrerillos, Cacheuta and Rio Blanco; recently a basal Rio Mendoza Formation has been dis- tinguished. Rusconi, in various publications (as Rusconi, 1951) has described \'ertebrates from these beds, including various fishes, many of uncertain systematic position, and from the Cacheuta Formation, flat-skulled amphibians of the genus Pel- orocephalus [Chigutisauriis], which, although comparable in many regards to the brachyopids of other Gondwana continents, appears not to pertain to that group. Reptilian remains are rare; in the older collections there was, apart from a few scraps, only the postcranial skeleton of a primiti\c thecodont, Cuyosuchus. More recently an indeterminate jaw from the Potrerillos Forma- tion has been described as Colbertosaurus, and Bonaparte has described the gomphodonts Andescynodon and Rusconiodon and a kannemeyeriid dicynodont, Vinceria from the Rio Mendoza Formation. Because the flora of the Cacheuta Series is of the Dicroidium type present in the Late Triassic, Stipanicic (1969) believes the Cacheuta beds to be relati\elv Late Triassic in as^e. Howe\er since the Dicroidhim flora extends well down toward the level of the Upper Beaufort beds of South Africa, Bona- parte's belief (1966, etc.) that part of the Cacheuta Series is

1973 CHANARES SUMMARY 3

relatively Early Triassic in age is reasonable. Unfortunately the reptile fauna is as yet too fragmentary in nature for adequate comparisons to be made.

(4) Santa Maria Formation. From this Triassic formation in southern Brazil a few bones were early sent to the British Mu- seum; major collections were later made by and for Huene, whose full results were published in 1944; further collections have been made by Price and White for Harvard University, by Colbert for the American Museum, and by Price for the Bra- zilian Geological Survey. The Santa Maria Formation has been described by Beltrao ( 1 965 ) and by Bortoluzzi and Barbarena (1967). The vertebrate remains are confined to the upper part of the formation, and there is no known difference in the age of the beds between the three major collecting areas — near the city of Santa Maria, in the region of Chiniqua, west of that city, and in the Candelaria region, well to the east.

The fauna is varied, but the nature of preservation is such that structural details are frequently obscure and many forms are imperfectly known. Included are the procolophonid cotylosaur Candelaria; the rhynchosaur Scaphonyx [Cephalonia] ; a number of thecodonts including Cerritosaurus, Rauisuchus, Prestosuchus, Hoplitosuchus, Procerosuchus; a fragmentary postcranial skeleton that appears to be a primitive saurischian, Staurikosaurus and a questionable second dinosaur, represented by a few vertebrae and limb bones; two carnivorous cynodonts, Chiniquodon and Belesodon; the gomphodont cynodonts Traversodon and Gom- phodontosuchus; the dicynodonts Barysoma, Dinodontosaurus and Stahleckeria.

As discussed later, the Santa Maria Formation seems surely to be equivalent to the Los Rastros Formation of the Talampaya basin.

(5) The Talampaya basin or Villa Union-Ischigiialasto cuenca. This is the largest and most richly fossiliferous of the bope-bearing South American Triassic areas. It lies on the boundary between La Rioja and San Juan provinces, between the Sierra de Safiogasta on the east and the Rios Bermejo and Guandacol on the west, and extends from the region of Villa Union on the north to the Sierra de Valle Fertil on the south. Faults are numerous, but in general the Triassic beds can be grouped in two areas, east and west of the flat alluvium-covered Talampaya plain, the two areas being essentially the two limbs of a major syncline, with various formations present in reverse order on the two sides of the plain. The area to the west of the

4 BREVIORA No. 413

plain is the better known and here the formations identified are much thicker than on the east. This region was explored by earlier geologists, but first adequately studied by Frenguelli ( 1 946 ) ; his account has been modified and corrected by later workers, such as Groeber and Stipanicic (1953) and Ortiz (1968). To the northwest, in the region of Cerro Bolo there is an exceedingly thick series of beds that appear to extend con- tinuously upward from the Carboniferous "Paganzo I" to the Late Triassic; this region was studied by de la Mota, whose work, unfortunately, remains unpublished. To the southwest the series, as far as published results are concerned, terminates below in the presumed Triassic "Paganzo III." For much of the west- ern border this last is absent; if included, the major formations, in descending order, are :

Los Colorados Formation,

Lschigualasto Formation,

Los Rastros Formation,

Tarjados Formation (= Paganzo III).

As described by Frenguelli, the Los Colorados beds were termed the Gualo Formation, a mistake corrected bv Groeber and Stipanicic. The lower part of the Los Rastros Formation was synonymized by Frenguelli with the Ischichuca Formation; as pointed out by Ortiz this is incorrect, for the type Ischichuca, in the Cerro Bolo region, is synonymous with the main carbon- bearing beds of the Los Rastros. The lowest redbeds were thought by Frenguelli to represent the Permian "Paganzo II,'' whereas, as Ortiz states, they are the redbeds of "Paganzo III," or Tarjados.

Fragments of vertebrate skulls were reco\'ered by Frenguelli from the Ischisfualasto Formation and described bv Cabrera in 1943. The richness of fossils in this formation was disclosed by the Har\'ard-Buenos Aires Museum expedition of 1958 (Romer, 1966). For many years, from 1958 on, the lschigualasto beds were worked by expeditions from the Instituto Lillos of Tucu- man, at first under O. A. Reig, later with great success by J. F. Bonaparte. The rich reptile fauna includes the rhynchosaur S ca phony x: the thecodonts Proterochampsa, Saurosuchus, Ven- aticosuchus, Triassolestes, Aetosauroides and Argentinosuchus ; the rare saurischian dinosaurs Herrerasaurus and {?)Ischisaurus; the ornithischian Pisanosaurus ; fragmentan- remains perhaps representing the carnivorous cynodont Chiniquodon; the gom- phodonts Exaeretodon, Proexaeretodon and Ischignathus; the

1973 CHANARES SUMMARY 5

dicynodont Ischigualastia. Except for representatives of Ischi- gualasto forms in transitional beds, no reptiles are known from the Los Rastros beds or the underlying Tarjados Formation. Abo\e the Ischigualasto Valley rise the high clifTs of the Los Colorados. Except for a single dicynodont, Jachaleria, the faunal content of most of the thick series of Los Colorados redbeds is unknown; from the few meters available at the summit of the cliffs Bonaparte has described (1972b) a fauna of very late Triassic age, including the thecodonts Riojasuchus, Pseudhes- perosuchus and N eoaetosauroides ; the primitive crocodilian H emiprotosuchus ; the prosauropod Riojasaurus; and fragmen- tary materials comparable to Tritylodon.

We are here concerned mainly with beds lying to the eastern side of the basin, which was little studied by earlier workers; Jensen and I (1966) have discussed the geology here. Most of the formations present can be matched with those on the west side of the \alley, although they appear to be much thinner here. The formations present (all adequately represented along the course of the Arroyo de Agua Escondida) are, in descending crder :

-Los Colorados Formation,

Ischigualasto Formation,

Los Rastros Formation,

Chafiares Formation,

Tarjados Formation,

Talampaya Formation.

These formations are presumably underlain by the Carboni- ferous and Permian beds of "Paganzo F' and "Paganzo II," which are exposed on the slopes of the Safiogasta Range, east of a major north-south fault at the western margin of the moun- tains; in the area studied, however, we have not seen a contact between "Panganzo II" and the base of the Talampaya beds. The latter formation is best exposed in the clifTs forming the walls of the "Puerta de Talampaya," where 180-200 meters of these beds are present. They mainly consist of soft sandstones, but with occasional "cobbles." No fossils of anv sort have been found. They appear to be purely continental in nature and are not improbably Early Triassic in age, or possibly Late Permian.

Unconformably above the Talampaya beds are the hard sand- stones of the Tarjados Formation, some 385 meters in thickness at the i\rroyo de Agua Escondida. These beds correspond, ap- parently, to part or all of the sandstones elsewhere termed

6 BREVIORA No. 413

"Panganzo III." For the most part they are red, but in the southern part of the area studied the upper beds are white in color. Fossils are rare, but a few fragmentary dicynodont re- mains have been found in the upper layers. They are presumably Early Triassic in age.

On the irregular upper surface of the Tar j ados sandstones lie unconformably the 75 meters of the volcanic ash deposits constituting the Chaiiares Formation. The uppermost layer of the Tar j ados, about half a meter thick, forms an uneven, undu- lating surface of hard resistant materials suggesting hydrothermal action. Obviously there was major volcanic activity in the region at that time. The Chaiiares sediments show none of the laver- ing that would be expected if the ash had been laid down in water; presumably there was merely a covering of the then existing surface with tremendous quantities of volcanic ash in Pompeii-like fashion. Bearing out such a conclusion is the fact that no trace of water-dwelling amphibians or fishes have been discovered in the Chaiiares and — more significant — almost all the numerous reptile remains found are in the lowest few meters of the ash deposits. Apparently the ash falls resulted in the local extermination of the vertebrate fauna.

As Jensen and I noted in 1966, it is not customary' in Argen- tina to give a formation name to a set of beds of such limited thickness. I believe, however, that it is warranted in this case because of the distinctive nature of the sediments, and most especially, because of the vertebrate fauna contained in them. Bonaparte (1967) suggested that the Chaiiares beds are equivalent to those of the Ischichuca Formation, the type section of which lies in the Cerro Bola region. However, both Ortiz (1968) and I (1971) have shown that this is incorrect. Bona- parte informs me that light-colored beds, which may be compa- rable to those of the Chaiiares, are present below the typical Los Rastros in the southwestern part of the basin, and that he has collected reptiles of Chafiares type there. I have not \'isited this area. Ortiz includes these beds in the Los Rastros Formation, and if one does not wish to distinguish a separate Chafiares Formation, one might include it in the Los Rastros — despite the marked contrast in the nature of the sediments — but could not, of course, consider these beds as part of the so-called "Ischichuca."

Conformably above the Chafiares ash beds are the Los Rastros sediments of shales, clays, and sandstones, with intercalated carbonaceous layers, similar in nature to the beds of this forma-

1973 CHANARES SUMMARY 7

tion in the western part of the basin. Because of numerous faults it is impossible to determine the thickness of the Los Rastros in this region, but it is obviously much less than the estimated 600 meters found west of the Ischigualasto Valley.

Only a limited exposure of Ischigualasto Formation sediments is present in this region; the thickness observed is but 175 meters, as compared with 400-500 meters in the type area. Abo\'e the Ischigualasto Formation are present Los Colorados beds, only 95 meters thick; whether this is the total amount originally deposited or whether they were originally thicker and later reduced by erosion before deposition of overlying Tertiary sediments is uncertain.

The Chanares Fauna

Below are listed the reptiles discovered in the 1964-65 expedi- tion and described in earlier papers in this series. A few forms are represented by fairly complete specimens; others are known only from fragmentary materials. Much further collecting is possible; one may hope that if and when such collecting can be done, much better material of many of the forms already de- scribed may be obtained and additions be made to the faunal list:

Dicynodonts :

Chanaria platyceps Dinodontosaurus brevirostris Dinodontosaurus platygnathus Kannemeyeriid indet.

Gomphodont cynodonts: Massetognathus pascuali Massetognathus teruggii Alassetognathus major Megagomphodon oligodens

, Carnivorous cvnodonts: Probelesodon lervisi Probelesodon minor Probainognathus jenseni

Thecodonts :

Luperosuchus fractus Lagerpeton chanarensis Lagosuchus talampayensis Lagosuchus lilloensis Chanaresuchus bonapartei

8 BREVIORA No. 413

Gualosuchus reioi Gracilisuchus siipanicicorum Lewimchus admixtus

Dicynodonts. In contrast to the wealth of dicynodonts in the later Permian, the group in the typical Triassic deposits is re- stricted to a few forms of relatixely large size (their place as herbivores appears to ha\e been taken oxer mainly by rhyncho- saurs and gomphodonts). In the Chanares beds such forms are present, but only in modest numbers, dicynodont specimens constituting but perhaps 5 percent or so of the total of reptiles collected. A few postcranial remains suggest the presence of a kannemeyeriid ; apart from this, three types of dicynodonts are present, all of which are assigned by Cox to the characteristically Middle Triassic family Stahleckeriidae — Chanaria platyceps, Dinodontosaurus platygnathus, and D. brevirostris. Chanaria is a form not present elsewhere; howe\er, the Dinodontosaurus species are quite similar to the genotypic form from the Santa Maria Formation ( presumably of somewhat later age ) .

As also mentioned below, ecologic factors tend to separate stratigraphically and topographically the three common herbi- vore groups — dicynodonts, gomphodonts and rh) nchosaurs — of the South American Middle Triassic fossiliferous areas. In the Santa Maria beds, dicynodonts and rhynchosaurs are, so to speak, "allergic" to one another; rhynchosaurs abound in the deposits near Santa Maria city but are unknown in the two other major fossil beds in this formation where dicynodonts are abundant. At Ischigualasto all known dicynodonts ha\e been found in a stratigraphically narrow band, about half-way up the formation, and quite distinct from higher levels where gompho- donts abound, and frotn lower levels where rhynchosaurs are plentiful. Ill the Chanares beds, as noted abo\e, almost all fossils are from the lowest part of the formation, but 1 ha\e the impression that all dicynodonts collected were from the \ery base, within a meter or two of the unconformity with the Tarjados sandstones, whereas other types tended to occur up to a dozen or so meters higher.

Gomphodonts. Gomphodont cynodonts arc the dominant herbivores in the Chanares beds; more than half of all specimens collected in the 1964-65 expedition were members of this group. Nearly all clearly pertain to a single genus, Massetognathus. In the first box of fossils received in Cambridge, Massachusetts, there was present a considerable series of specimens that seemed to sort out clearly into two size groups, and hence I descril^ed

1973 CHANARES SUMMARY 9

them as belonging to two species, M. pascuali and M. teruggii. As I noted later, the full collection, when received, broke down such a clear distinction. Dr. James Hopson tells me that in primitive African cynodonts which he has been studying, a very considerable size range is to be found; this suggests that M. pascuali and M. teruggii merely represent populations of two sizes of the same species. However, as my tables show, the size distribution is heavily weighted above the peak that one may reasonably believe to represent mature adults, and the presence of two common species of Massetognathus is still a not unreason- able assumption. Still further, the size range of specimens that seem to belong to this genus is such that I find it impossible to believe that the amount of growth necessary to reach the size of the largest specimen can have been possible if a single species (or even two species) had been present, and hence have with some confidence given the name Massetognathus major to this relatively enormous skull.

Nearly all the gomphodonts in the collection appear to be reasonably assignable to a single genus. However, two rather large individuals are clearly distinctive, and I have given the name Alegagomphodon oligodens to this rare form.

The Chafiares gomphodonts are clearly members of the family Traversodontidae, a group to which all known South American gomphodonts belong ( and also forms present in the Manda beds of East Africa). In the Santa Maria beds of Brazil gomphodonts are less common, and are represented mainly by the genus Traversodon. This genus may well have descended from Mas- setognathus, but its remains are too poor to allow a detailed com- parison. The Ischigualasto traversodontids are obviously much more ad\'anced types.

Rhynchosaurs. Quite as significant as the presence of certain forms in a given formation is the absence of expected types. Most Triassic reptile faunas, except those of the very earliest and very latest parts of the period, are notable for the presence of rhynchosaurs, often in great abundance. In our Chafiares col- lections there is not the slightest trace of a rhynchosaur ( despite the fact that identifiable elements of this type of animal, most especially upper tooth plates, are readily preserved and readily recognized ) .

Why are no rhynchosaurs present? It is not because they had not yet evohed, for although the Chafiares beds date from a fairly early time in the Triassic, primitive rhynchosaurs were already present in the Cynognathus Zone, definitely earlier, and

10 BREVIORA No. 413

were abundant in the Manda beds of East Africa, which (as discussed later) are probably somewhat earlier than the Chaiiares Formation. Quite certainly rhvnchosaurs had evolved bv the time of formation of the Chaiiares beds and (although there is no proof) may have been present in Argentina at that time.

Their absence here is quite surely, as I have suggested else- where (Romer, 1973), attributable to some ecologic factor. Rhynchosaurs and gomphodonts, in South American deposits at least, seem to be basically incompatible.^ In the Ischigualasto beds, rhvnchosaurs are exceedingly abundant in the lov/er part of the formation, but in our 1964-65 expedition we found no specimens in the upper half of the beds. On the other hand, on our expedition we found gomphodonts to be very rare in the lower part of the Ischigualasto Formation but very abundant in the upper half of these deposits. Rather surely the contrast is related to the type of plants present; the rhynchosaurs fed on some type of plants having a hard-shelled "seed" for which the "cracking" dentition of these forms was a necessity; the gompho- donts, as the grinding character of their teeth and the absence of a cracking device indicate, fed upon some different types of plant materials. In the Santa Maria Formation, gomphodonts are not as conspicuous as in the Ischigualasto and Chanares beds, but such gomphodonts as are present there are absent in the beds near Santa Maria city where rhynchosaurs alone are present. If, as is probable, rhynchosaurs were present in South AmxCrica in Chanares times, they would presumably have been of a relatively primitive type, comparable to Stenaulorhynchus of the Manda beds rather than the more advanced genus present at Santa Maria and Ischigualasto.

Carnivorous cynodonts. In the Permian and earliest Triassic the typical carnivores are therapsids; during the Triassic car- ni\orous therapsids are reduced and disappear, to be replaced by archosaurs (but giving rise to the earliest mammals before dis- appearing completely). In the Chaiiares beds, thecodont archo- saurs were becoming abundant, but carni\orous cynodonts were still present and modestly abundant. They are interesting in being more ad\'anced than Thrinaxodon and Galesaurus of the earliest Triassic and without the somewhat specialized features seen in Cynognathus, the common form in the Late Beaufort of South Africa. Probelesodon lewisi is quite clearly ancestral to

'Charig tells mc, however, that there is no evidence for this in the Manda beds of East Africa.

1973 CHANARES SUMMARY 11

Belesodon of the somewhat later Santa Maria beds; apparently two species are present, P. lewisi, fairly common, and a smaller form, Probelesodon yninor. More interesting is Probainognathus, in which a starthng advance is the presence of a socket — a glenoid cavity - — in the squamosal for attachment of the jaw. This, however, is only a half-way stage in the development of the mammalian system of jaw suspension, for this glenoid is for the reception of an articular body of the lower jaw formed by a fusion of the posterior elements of the reptilian jaw type; the dentary bone, which in mammals articulates with the squamosal, is as yet not quite in touch with the squamosal. The teeth of Probainognathus are usually worn and show only the main fore-and-aft row of cusps present in the teeth of primitive mam- mals and seem to lack the row of basal "cusplets" found in early mammals. For this reason it was thought for a time that Pro- bainognathus could not be on the direct line of ascent to mam- mals. However, Hopson has studied a little-worn dentition in which these cusps are present and hence it may be reasonably considered to be a true pre-mammal, or at least very close to the actual ancestral line.

Thecodonts. Although carnivorous cynodonts still survived, thecodonts were well on their way toward succeeding them as dominant carnivores. In earlier years we knew little of this group except for a few primitive forms in the Early Triassic and ( apart from the specialized phytosaurs) only a few survivors in the Late Triassic, where the thecodonts were already being succeeded by the dinosaurs descended from them. One could have rea- sonably assumed that were Middle Triassic beds well known, the thecodonts would be discovered to be a varied group, with a variety of forms leading in different directions — toward ptero- saurs, bird ancestors, crocodilians and dinosaurs. Our increased knowledge of Middle Triassic fossil deposits in recent decades has gone far toward verifying this assumption, for although many phyletic lines are far from clear, it is obvious that during the middle part of the Triassic the thecodonts were undergoing a rapid radiation into a wide diversity of types. The only large Chaiiares form is Luperosuchus, represented only by an incom- plete skull, which appears to be a member of the prestosuchid (or rauisuchid) assemblage, of uncertain relationship. No close affinities are known for Lewisuchus or the two small long-legged types, Lagosuchus and Lagerpeton, represented mainly by hind legs. Chanaresuchus and Gualosuchus are long-snouted, prob- ably amphibious forms related to Cerritosaurus of the Santa

12 BREVIORA No. 413

Maria and Proterochampsa of Ischigualasto; once suggested as crocodilian ancestors, the proterochampsids do not seem to be related to that group, but are not impossibly related to the phytosaur pedigree. A progressive form is Gracilisuchus, related, it would appear, to Ornithosuchus of the later Triassic, which has suggestive resemblances to primitive theropods, although it is far from certain that the ornithosuchids are ancestral to these dinosaurs. The Chanares thecodonts, as was stated, increase con- siderably our knowledge of thecodont diversity, but as vet do little toward establishment of any major archosaur evolutionary lines.

Comparison With Other Faunas

As knowledge of Middle Triassic faunas has increased, ideas as to the stratigraphic position and interrelations of these faunas ha\e been expressed by a variety of workers, such as Bonaparte, Colbert, Cox, Reig, and myself. I shall here merely consider the interrelationships of these faunas from the point of view of the Chanares assemblage. I have recently re\iewed the Triassic faunas in a plenary paper (1972) for the Second Gondwana Symposium, and hence full documentation here seems unneces- sary.

As I pointed out some years ago (1966) Triassic faunas may be roughly divided into three successive groups, (A) early, (B) intermediate, and (C) late, although it is obvious that such distinctions cannot be completely clear-cut, and transitional assemblages may be expected. A-type faunas have long been known from the Upper Beaufort beds of South Africa, contain- ing mainly therapsids, although with early members of other groups, notably thecodonts. C-type faunas are almost ubiquitous, being known from redbeds Late Triassic deposits in Eiuope, North America, South Africa, China, and (now) South Amer- ica. In such faunas dinosaurs are already prominent, and their thecodont predecessors are still present, whereas therapsids are practically extinct (although the earliest mammals descended from them have now appeared ) .

As to B-type faunas, these were until recently almost entirely unknown, since deposits of Middle Triassic age in the northern continents are mainly marine, and in South Africa the Molteno beds, of Middle Triassic age, appear to be nearly barren of fossils (although footprints are abundant). What should one have expected in B-type faunas? Ob\'iously, a transition between

1973 CHANARES SUMMARY 13

A and C, with a gradual reduction of therapsids and an increase in archosaurs, including a variety of thecodonts and the begin- nings of the dinosaurs. The B-type faunas now known from the southern continents do show these expected transitional features. But, in addition, they show positive characteristics of their own, in the great flourishing of gomphodont cynodonts and rhyncho- saurs - — groups that had their beginnings in the A-type faunas of the Early Triassic but seemed of little importance.

Let us first consider the South American situation. A-type faunas are certainly present in the Puesto Viejo Formation and not improbably in the Cacheuta series, as Bonaparte believes (although the evidence is still scanty). The C-type is present both in the upper part of the Los Colorados Formation, as now being developed by Bonaparte, and in the El Tranquilo Forma- tion. Between, we have in Argentina the succession Chanares- Los Rastros-Ischigualasto, three formations that lie conformably one above the other in the Talampaya basin. The Los Rastros beds are almost barren of fossils, but it is, I think, generally agreed that the Santa Maria Formation of Brazil is equivalent, and thus, for vertebrates, our sequence may read Chafiares-Santa Maria-Ischigualasto. All three clearly include B-type reptile faunas. ^

The Chaiiares beds, earliest of the three, clearly are an early part of the B complex. The gomphodonts are members of the traversodontid family, and the diademodontids and trirachodon- tid types present in the Scythian Cynognathus beds of South Africa appear to be extinct. The carnivorous cynodonts are of relatively ad\anced types — rather more advanced than Cyno- gnathus. Rhynchosaurs are absent, but this, as noted above, ap- pears to be due to some ecological factor, since primitive rhynch- osaurs were already present in the A-type Cynognathus zone. And, while few thecodonts were present in the Cynognathus zone, thev are here alreadv varied in nature and in some cases at least, of a progressive type.

The Santa Maria beds are quite surely later in age than the Chafiares beds but, just as the presumably equivalent Los Ras- tros beds lie in the break above the Chaiiares, the fauna of the Santa Maria beds follows that of the Chafiares with some ad- vances but without any major change. Among the dicynodonts, Dinodontosaurus continues Httle changed into the Santa Maria. Of gomphodonts, the Santa Maria Traversodon, although poorly known, may well be descended with litde change from Mas- setognathus. The Santa Maria carnivorous cynodont Belesodon

14 BREVIORA No. 413

appears to be but an enlarged edition of Probelesodon of the Chanares. In both Chanares and Santa Maria beds, most of the thecodonts are imperfectly known, but it is very probable that, given more adequate material, several close comparisons may come to be made, and Cerritosaurus of Santa Maria is very similar structurally to Chanaresuchus of the earlier formation. As Cox (1968) states, "the Chafiares fauna is only slightly earlier than that of the Santa Maria." The only advance of any note is that here (as might be expected) we have the first sign of the evolution of dinosaurs from thecodonts in Staurikosaurus Colbert and possibly the fragmentary materials described by Huene as Spondylosoma.

Next above the Los Rastros Formation, without disconformity, lies the Ischigualasto Formation, from which a very considerable fauna is now known. The only dicynodont, Ischigualastia, is a large form of no particular stratigraphic significance. Gompho- donts of several genera — Exaeretodon, Proexaeretodon, Ischig- nathus — are exceedingly abundant, especially in the upper part of the formation. All are traversodonts that are more advanced than those of the Chanares and Santa Maria beds. Carnivorous cynodonts are rare and represented only by fragmentary remains that ha\e been referred to the Santa Maria genus Chiniquodon. Thecodonts are, again, fairly common and \'aried. Saurosuchus is a relative of Luperosuchus of the Chanares but of larger size; Proterochampsa is similarly a large member of the Chanare- suchus-Cerritosaurus group. Triassolestes, originally thought to be a dinosaur, is probably a thecodont, but perhaps a crocodi- loid relative. Interesting is the presence of Aetosauroides, first representative of a thecodont type that was to continue, ap- parently little changed, to Late Triassic times. Of dinosaurs we now have (although as rarities) the probable saurischians Her- rerasaurus and Ischisaurus and, most interestingly, the oldest known ornithischian, Pisanosaurus. Despite advances, we have a close tie with the Santa Maria in that the common Ischigua- lasto rhynchosaur Scaphonyx (thoroughly studied in an unpub- lished thesis by Sill) is almost indistinguishable from the species present in the Santa Maria. Chatterjee (1969) has suggested that the Santa Maria localities containing Scaphonyx are later than those containing the remainder of the fauna. But there is no geological e\idence to support this suggestion; all the verte- brate fossils, rhynchosaurs, dicynodonts and others, appear to come from the relatively thin upper portion of the Santa Maria Formation. In sum, the fauna of the Ischigualasto Formation

1973 CHANARES SUMMARY 15

is ad\'anced over that of the Santa Maria, but the difference is not great, as Bonaparte has noted.

We lack any means of correlation of these South American beds with the standard marine series, but since these faunas are ob\'iously post-Scythian and pre-Norian, it is natural to suggest a one-to-one correlation of Chanares-Santa Maria-Ischia^ualsto with Anisian-Ladinian-Carnian. I have in the past expressed doubts as to whether the horizon of the Ischigualasto Formation was as high as the Carnian. In the European Keuper reptile remains are known only from the upper, Norian, part of the sequence and we have no knowledge of the reptile fauna of Carnian times. Further, in the Ischigualasto Valley the Los Colorados redbeds tower for some 400-500 meters above the top of the Ischigualasto beds and, except for a single dicynodont, our knowledge of the Los Colorados fauna is derived from the vcv)^ topmost beds of this formation, so that it is possible that the lower part of these beds are of Carnian age. However, consid- eration of the faunas found in India and the northern continents (discussed below) suggests that our B-type faunas continued into Carnian days. It is thus very likely that the age of our B-type Middle Triassic faunas conflicts with the classic division of the Triassic into lower, middle and upper. Stratigraphically the Middle Triassic includes Anisian and Ladinian, while the Upper Triassic includes Carnian, Norian and Rhaetic ; as regards verte- brates it is probable that the Middle Triassic includes Carnian and Anisian and Ladinian as well, with the "upper" C-type faunas restricted to the Norian and Rhaetic.

If one wishes to compare the Chaiiares and other South Amer- ican B-type faunas with those of other continents, one naturally turns first to South Africa, since current theories of continental drift suggest that in the Triassic South America and Africa were closely apposed to one another. If this was the case one would expect similarities between the faunas of the two continents. But even if the South Atlantic were then nonexistant, there would remain a considerable distance between the Talampaya basin, and even the Santa Maria region, and the fossiliferous beds of east and south Africa. One should expect that there might be a considerable difference between the reptile faunas of these regions just as there is today a very considerable difference between the reptile faunas of, for example, California and the Atlantic coast areas of North America.

The African beds concerned are ( 1 ) the Molteno beds of the

16 BREVIORA No. 413

Stormberg Series cf South Africa, (2) the Ntawere beds of Zambia, and (3) the east African Manda beds.

The Molteno beds are quite surely Middle Triassic in age and should contain a fauna of the B-type. But while footprints are tantalizingly abundant, actual fossils are rare, and such few as ha\'e been described are of uncertain stratigraphic position and may either come from the top of the Cynognathus zone (as in the case of a cynognathid) or from the base of the redbeds (as in the case of a traxersodont gomphodont ) .

The Ntawere beds are as yet not fully explored and as yet little material has been described [cj. Cox, 1969). Two zones appear to be present. The lower, in which Diademodon is present, may well be equivalent to the upper part of the Cynognathus zone, with an A-type fauna. The upper zone fauna includes two dicynodonts — the stahleckeriid ^ambiasaurus and the kanne- meyeriid Sangusaurus, two traversodont cynodonts, Luangwa and a second form as yet undescribed, and fragments of theco- dont«;. In default of fuller data, the age of this fauna is difficult to determine. The presence of traversodonts suggests the B-type; but tra\ersodonts occur at an Early Triassic age in Argentina and may well ha\ e been as early in appearance in Africa.

Of especial interest is the Manda Formation of east Africa, from which a very considerable fauna is known, owing to col- lections made for Huene, by Parrington, and by an English ex- pedition a decade ago. Unfortunately much of the known ma- terial is undescribed or described in only preliminary fashion. I am indebted to A. J. Charig for the faunal list given here. There are three dicynodonts, Kannemeyeria, Tetragonias, and a third undescribed form. No carnivorous cynodonts are as yet described, but gomphodonts are numerous and \aried, including the diademodontids Theropsodon and {?)Aleodon, the triracho- dontid Cricodon and a \arietv of traversodontids of which the only remains as yet described are assigned to four species of the Q:enus Scalenodon. Some seven thecodonts have received names, including the prestosuchids Mandasuchus and (?)Stag?iosuchus, and fi\e further genera not assigned to families — Parringtonia, Teleocrater, Hypselorhachis, Nyasasaunis and Pallisteria. The abundant rhynchosaur remains pertain to the primitive genus Stenaulorhynchus.

The abundance of gomphodonts and rhynchosaurs indicates that we are dealing with a typical B-type fauna, and the presence of Kannemeyeria and of diademodontid and trirachodontid gomphodonts suggests a relati\'ely early age. The fauna is ob-

1973 CHANARES SUMMARY 17

\iouslv earlier than that found at Ischia^ualasto, and the Santa Maria and Chanares faunas are the two South x\merican as- semblages with which comparisons might reasonably be made. On the whole, it is the Chanares fauna that seems to be the closest. The absence of rhynchosaurs in the Chafiares beds re- mo\'es one basis of comparison which might have been hoped for. Not improbably some of the Manda thecodonts will show aflfinities to Chafiares genera when fully described. Crompton tells me that some of the Manda gomphodont specimens are closely comparable to Massetognathus, but here again we must await further publication. It is not unreasonable to expect that when the Manda fauna is fully described it will prove to be rather similar to that of the Chanares, but of a somewhat earlier date.

In more northern regions — India, Scotland and Nova Scotia — are assemblages that contain characteristic elements of the B-type fauna but are usually considered as of Late Triassic age. In the Maleri beds of India only three named tetrapods are present. These are : ( 1 ) a stereospondylous labyrinthodont ge- nerically identical with Metoposaurus, common in the Upper Triassic of both Europe and North i\merica but otherwise un- known in presumed "Gondwana" areas; (2) a phytosaur, diffi- cult to assign to a given genus (the systematics of phytosaurs are in a confused state) but representing a group unknown else- where in "Gondwana" areas except in Morocco; (3) a rhyncho- saur Parasuchus [Paradapedon] of an advanced type which Chatterjee believes related to Scaphonyx of South America and Hyperodapedon of Elgin. The presence of a metoposaur and phytosaur in a supposed Gondwana region presents an interesting geologic problem, but the question of the age of the Maleri is almost equally interesting.

The Maleri is considered to be "Upper" Triassic; but while "upper" in a stratigraphic sense, it may well represent a Carnian fauna of our B-type. As regards phytosaurs, they are unknown in Europe before the Norian, but this group obviously had a long antecedent history (disregarding the question of the age of Mesorhinus) . Metoposaurs, again, are "Upper" Triassic, but it is not improbable that there may have been older antecedent stages in the development of these peculiar stereospondylous labvrinthodonts.

Rhynchosaurs, in the form of the advanced genus Hyper- odapedon, are present in the Elgin beds of Scotland, which Walker (1961) believes to be of Norian age. His conclusions

18 BREVIORA No. 413

mav be correct, and this mav mean a late survival of rhvncho- saurs in Europe. But it must be pointed out that there is no trace of a rhynchosaur in the Norian Keuper of continental Europe, and hence it may be suggested that the Elgin beds are pre-Norian, perhaps Carnian in age. The Elgin fauna is a sparse one; there is nothing to represent the typical dinosaur fauna of the continental Norian (the systematic position of Ornithosuchus is questionable ) . Walker's correlation with the Norian is based mainly on the presence of Stagonolepis, a close relative of Aetosaurus of the continent. But we now know that the aeto- saurid pattern was already present in the Ischigualasto beds in the form of Aetosauroides [Argentinosuchus], which is still in- completely known but appears to be a fully developed member of this group.

Most interesting is the report by Baird (1962 and in litteris) of the presence in beds in Nova Scotia which have been corre- lated with the Newark series of the Atlantic seaboard of the United States, of both of the most characteristic elements of the B-type fauna — - rhynchosaurs and a gomphodont jaw ! The Newark is a characteristically C-type series, as witnessed not so much by the rare dinosaurian fossil remains as by the vast num- bers of dinosaur footprints. Are we dealing in these Nova Scotia finds with a very late sur\d\'al of gomphodonts and rhyncho- saurs? Or — more probably, I think ^ — these supposed Newark equi\'alents in Nova Scotia may, in their lower beds, extend downward from Norian to Carnian age, into the time of exist- ence of the B-faunas. Parenthetically, while the familiar red Triassic deposits of the western United States — Chinle, Dockum, Popo Agie — are usually considered as of quite Late Triassic age, we find in them mainly metoposaurid amphibians and phy- tosaurs, and little representation of the abundant dinosaurs found in the European Norian, the redbeds of South Africa, the Late Triassic of China and, apparently, in the Newark series proper. Ls the nature of the faunas of these western beds associated with ecological factors or are they of pre-Norian age?

References Cited

Baird, D. 1962. Rhynchosaurs in the late Triassic of Nova Scotia. Gcol. Soc. Amer. Spec. Paper, 73: 107.

Beltrao, R. 1965. Paleontologia de Santa Maria e Sao Pedro do Sul, Rio Grande do Sul, Brasil. Bot. Inst. Cien Nat. Univ. Fed. Santa Maria, 2: 1-114.

1973 CHAN ARES SUMMARY 19

Bonaparte, J. F. 1966. Chronological survey of the tetrapod-bearing Tri- assic of Argentina. Brcviora, Mus. Comp. Zool., No. 251: 1-13.

. 1967. Comentario sobre la "Formacion Chanares" de la

cucnca Triasica de Ischigualasto-Villa Union (San Juan-La Rioja) . Acta Geol. Lilloana, 9: 115-119.

— ■ 1972a. Annotated list of the South American Triassic

tetiapods. Proc. and Papers Second Gondwana Symposium (South Africa, 1970) , Pretoria: 665-682. . 19721^. Los tetrapodos del sector superior de la forma-

cion Los Colorados, La Rioja, Argentina. (Triasico Superior) . I Parte. Opera Lilloana, XXIIL 1-183.

BoRTOLUZZi, C. A., AND M. C. Barbarena. 1967. The Santa Maria beds in Rio Grande do Sul (Brazil) . Proc. Intern at. Symp. on Gondwana Strat. and Paleont.: 169-195.

Cabrera, A. 1943. El primer hallazgo de terapsidos en Argentina. Notas, Museo La Plata, 8, Paleont., No. 55: 317-331.

Chatterjee, S. 1969. Rhynchosaurs in time and space. Proc. Geol. Soc. London, No. 1658: 203-208.

Cox, C. B. 1968. The Chanares (Argentina) Triassic reptile fauna. IV. The dicynodont fauna. Breviora, Mus. Comp. Zool., No. 295: 1-27.

. 1969. Two new dicynodonts from the Triassic Ntawere forma- tion, Zambia. Bull. Brit. Mus. (Nat. Hist.) , Geol., 17: 255-294.

Frenguelli, J. 1946. Consideraciones acerca de la "Serie de Paganzo" en las provincias de San Juan y La Rioja. Rev. Mus. La Plata (N.S.) , Geol., 2: 313-376.

Grober, p. F., and P. N. Stipanicic. 1953. Geografia de la Rej)ublica Argentina. Buenos Aires, H (Primera Parte) : Triasico: 13-141.

Ortiz, A. 1968. Los denominados estratos de Ischichuca como seccion media de Formacion Los Rastros. Actas IH Jorn. Geol. Argentina, 1: 333-339.

RoMER, A. S. 1960. Vertebrate-bearing continental Triassic strata in Men- doza region, Argentina. Bull. Geol. Soc. Amer., 71: 1279^1294.

. 1966. The Chanares (Argentina) Triassic reptile fauna. L

Introduction. Breviora, Mus. Comp. Zool,. No. 247: 1-14.

— ' . 1971. The Chanares (Argentina) Triassic reptile fauna. IX.

The Chanares Formation. Breviora, Mus. Comp. Zool., No. 377: 1-8.

1972. Plenary paper. Tetrapod vertebrates and Gondwana-

land. Proc. and Papers, Second Gondwana Symposium (South Africa, 1970). Pretoria: 111-124.

. 1973. Middle Triassic tetrapod faunas of South America. Act.

IV Congr. Latin. Zool. (Caracas, 1968), II: 1101-1117. , and J. A. Jensen. 1966. The Chanares (Argentina) Triassic

reptile fauna. II. Sketch of the geology of the Rio Chanares-Rio Gualo region. Breviora, Mus. Comp. Zool., No. 252: 1-20.

20 BREVIORA No. 413

RuscoNi, C. 1951. Laberintodontes Triasicos y Permicos de Mendma.. Rev.

Mus. Hist. Nat. Mendoza, 5: 33-158. "

Stipanicic, p. N. 1969. Las sucesiones Triasicas Argentinas. Gondwana

Stratigraphy, I. U. G. S. Symposium (Buenos Aires, 1967): 1121-1150. Walker, A. D. 1961. Triassic reptiles from the Elgin area: SMgdnolepis,

Dasygnathus and their allies. Phil. Trans. Roy. Soc, London (B) , 244:

103-204. \ • ■■

c

B R E V I 0 R A

]ffV^^liii^Y^^^^â„¢^P^^^*^'^^ Zoology

IAN 7 1974

US ISSN 0006-9698

Cambridge, Mas^. 28 December 1973 Number 414

UNIVfiRSlTt:

ECOLOGY, SELECTION AND SYSTEMATICS

Nelson G. Hairston^

Abstract. Three different kinds of ecological relationships between newly separated species are examined, with the aim of establishing their expected effects on the systematic differences between the species involved. In cases of slight difference between the habitats of two products of recent speciation, selection can be expected to favor specific competitive mechanisms, but taxonomic differences would be expected to be slight, and examples of hybrid superiority would be common. Where the habitats of the two species are markedly different, as along a steep ecological gradient, adaptation to the different places will result in species that become broadly overlapping in habitat, and taxonomically different in many clearly adaptive characters. Although this latter process leads to species with somewhat different food habits, it would not lead to food specialization, even if the two species were originally limited in abundance by food and in competition for it. True food specialization, in the form of monophagy, is most likely to evolve in the presence of a superabundance of several kinds of food, owing to in- creased efficiency of handling, digestion and metabolism, and is improbable among species in competition for food. Closely related monophagous species should differ maikedly in a few characters, and hybrids should be inferior. Examples of the three situations are described, plethodontid salamanders being used for the first two and leaf-mining insects for the third.

Introduction

Classically, the relationship between systematics and ecology has been approached by first taking systematics as the exploration of genomic diversity, and then turning to ecology for explana- tions that were secondary to the origin of differences. This approach is epitomized by the recent comment to me that the reproductively isolated entities within Paramecium aurelia could

^Museum of Zoology, the University of Michigan

2 BREVIORA No. 414

now be considered species because their isoenzyme patterns are visibly different. Such a viewpoint surely gets the classification much too far away from the biology. As an antidote, I propose to examine the relationship from the standpoint that ecology provides the set of opportunities that can be exploited by diversi- fication of the genome. The approach is not original, as it is the basis for the idea of adaptive radiation, but the impact of ecology on systematics deserves reexamination. In this, we should separate the passive background from the active; that is, those factors that set the conditions, and those that are able and likely to respond by evolving themselves. These two classes, unfortu- nately, will not remain constant for us. For example, it would be agreed that the distinction between nonliving and living parts of the environment might provide such a preliminary classifica- tion, but as far as I can discover, this is not the case. The dis- tinction between the vegetation on one hand and the climate and substrate on the other is clear enough. The physical gradients provide the passive background, making physiological demands on a potential additional plant species, and the various com- peting species of plants provide the acti\'e counteradapting back- ground, making ecological demands.

However, when we consider the active and passive background of animals, particularly carnivorous ones, the distinction between plants and the physical environment becomes less important than the distinction between both of those on the one hand and other animals on the other. Indeed, there are few cases of terrestrial predators which are distributed concordantly with even the dominant plants, and when this coincidence does occur, the plants are used in a nonliving context, as when they are required for nest sites.

This example provides the opportunity to emphasize the dis- tinction between selection for physiological adaptation and selec- tion in response to the ecological pressures of competition and predation. It is to the latter to which I wish to address myself principally, but I first give an example of the simultaneous opera- tion of both. This will be followed by a description of what seems to me to be an unusual opportunity to investigate the ecological interaction between one species and several geograph- ically varying populations of another, closely related one. From that, I hope to be able to generalize some about a fruitful in- vestigation of other kinds of systematic consequences of ecological phenomena.

1973 ecology and systematics 3

^,: An Analysis of the Exploitation of a

: ' Undimensional Gradient

As has been emphasized by Dunn (1926), (Hairston, 1949), Organ (1961) and others, the evolution of the Dusky Sala- manders of the genera Desmognathus and Leurognathus is de- scribable in terms of adaptation to a linear series of habitats from aquatic to terrestrial.

This unidimensional array of pertinent physical environments facilitates the analysis of each species' most immediate biological environment: namely, its closest relatives.

My own early analysis showed that the coexistence of five species was possible, when they used the entire physical gradient from completely aquatic to terrestrial. The species involved are Leurognathus marniorata, Desmognathus quadrainaculatus, D. monticola, D. ochrophaeus and D. wrighti. The distribution of the four species of Desmognathus is shown in Figure 1. With no further information, however, it was not possible to determine whether more species could be accommodated in this presumably competitive series.

Some years later. Organ was able to provide a tentatively negative answer when he investigated the ecological distribution of the same four species of Desmognathus in an area where a fifth species, D. fuscus, was found. He found that at nearly every location, the maximum number of species present was four. D. fuscus could coexist either with D. quadramaculatus at high elevations or with D. monticola away from large streams at lower elevations but not with both.

Thus, the limit imposed by the presumably competitive rela- tionships seems to have been reasonably well established, but a more detailed look at the data suggests that steepening of the moisture gradient may reduce the number of species that can be accommodated from the competitive standpoint. At high eleva- tions, atmospheric moisture, however expressed, is as great far from water as it is over a stream at low elevations (Hairston, 1 949 ) . This correlates very well with the combined vertical and horizontal distributions of the two most terrestrial salamanders, Desmognathus ochrophaeus and D. wrighti. D. ochrophaeus is confined to a zone near streams at low elevations, none having been found more than 15 feet from a stream at elevations below 3000', but its distribution is unrelated to surface water above 4500 feet. D. wrighti, with its distribution unrelated to water in summer, apparently cannot compete with its congeners close

BREVIORA

No. 414

DISTRIBUTION OV DESMOGNATHUS

BLACK MOUNTAINS (3000-6500')

NANTAHALA MOUNTAINS (2300')

r~i

D. quadramaculatus

Ti

X

rr

^ â– 

S>

t n r~i r ]

D. monficola

V7^

I

'A

mn^

'/a

1

'//â– 

^â– y,.

1

^

D. ochrophae

I I I

I

0

cn

5- 9

10- 14

D. wrighti

15- 20- 25 + 19 24

â–¡ q

us

a.llll

D. aeneus

0 I- 5- 10- 15- 20- 25+ 4 9 14 19 24

NUMBER OF FEET FROM STREAM

Figure 1. The ecological distribution of the species of the salamander genus Desmognathiis in two different mountain ranges in North Carolina.

1973 ECOLOGY AND SYSTEMATICS 5

to Streams at low elevations, and cannot persist away from streams there because of the lower moisture.

It is therefore with some interest that one notes the coexistence of four species of Desmognathus at low elevations (down to 2200 feet) in the Nantahala Mountains. D. wrighti does not occur at low ele\'ations, but a study of the ecological distribution of the genus shows the presence of a terrestrial species, D. aeneus. This species, which is the size of D. wrighti, but more slender, was found closer to streams than wrighti usually is in summer, but clearly occupies the same general position at the terrestrial end of the environmental gradient ( Fig. 1 ) . It seems anomalous that it should be present, although D. wrighti is unable to occupy the corresponding habitat at low elevations near its range. It was postulated above that this inability is related to reduced moisture at low elevations. This suggests that there may be a climatic \'ariation that permits the existence of a low-altitude terrestrial Desmognathus in the Nantahala Mountains. An examination of rainfall records reveals that such is the case. In the Coweeta Experimental Forest, the location of the distribu- tional study, the average annual rainfall ranges from 75 inches at 2240 feet to 93. inches at 3870 feet. This is appreciably higher than the rainfall at comparable elevations elsewhere in the Southern Appalachians. For example, at the foot of the Great Smoky Mountains, Bryson City, N.C. has an average annual rainfall of 52.12 inches. At the foot of the Black Mountains, Montreat and North Fork have 53.61 and 51.78 inches respec- tively, and between the Smokies and the Blacks, the French Broad Valley receives from 38.45 inches at Enka to 47.61 at the Asheville-Hendersonville x\irport.

Among other locations at comparable elevations in the South- ern Appalachians, only the region from Brevard to Highlands, N.C. receives as much rain as the general area south and west of the Little Tennessee River. Comparable rainfall is found elsewhere only at high elevations (71.20 inches at Mt. Mitchell, 6684' in the Black Mountains, and 81.71 inches at Clingman's Dome, 6643' in the Great Smoky Mountains).

The end of the series of species seems to be determined by climate, with high rainfall permitting the addition of a small terrestrial species. On larger and higher mountains, when the tops are (or once were) covered with conifer forests and rainfall is high, the terrestrial species is Desmognathus wrighti, which is confined to elevations above 3500 feet; in that part of the moun- tains where the rainfall is high, even at low elevations, Des-

6 BREVIORA No. 414

mognathus aeneus occupies the terrestrial end of the series. In other areas, the series stops with the third species, D. ochro- phaeus. It does not appear possible for another species to enter the series in the midle, as shown by the situation with D. fuscus at \Vhite Top Mountain in Virginia. Competition thus seems to determine how similar any pair of species can be and still coexist. When the climate would require the next most terrestrial species to o\erlap the habitat of D. ochrophaeus to too great an extent, only three species are found.

This situation seems to present an unusually clear example of the e\'olutionary exploitation of a simple environmental gradient and of the limits of this diversifying exploitation that are set by competitive interactions. The limits to "species packing" are demonstrated as clearly as post-facto analysis could permit.

Moreover, it provides a miniature model for the early stages in the e\'olution and diversification of the family Plethodontidae.

Post-Speciational Events : Increased Competition or Coexistence?

The kind of analysis made in the preceding section differs from large numbers of published descriptions only in being a little more tidy than most. If the field is to progress, such state- ments will become the beginning of studies at the interface of ecologv' and systematics, rather than representing final conclu- sions. The choice among investigations of ecological distribution should depend upon the respective opportunities that they pre- sent for experimental tests of hypotheses of systematic status or ecological processes. One of the points which I wish to make most strongly is that experimentation related to ecological inter- actions can yield important information about evolutionary events, provided that care is taken to select appropriately favor- able situations for study. One such situation that seems to be especially suitable for field manipulations is represented by two species of Plethodon, an exclusively terrestrial genus of sala- manders. The location is also the Southern Appalachians.

Plethodon jordani is endemic to the southern Appalachians. Through much of its range, it is confined to higher elevations, resulting in a fragmented distribution consisting of a number of isolated populations, many of which are morphologically dis- tinct from each other. These populations have been studied repeatedly, and have been classified as belonging to as many as four distinct species (Grobman, 1944). Whenever specimens

1973 ECOLOGY AND SYSTEMATICS 7

have been taken from intermediate locations, they are inter- mediate in color between the adjacent different populations. This discovery led to the eventual inclusion of all of these popu- lations within Plethodon jordani and the recognition of seven subspecies (Hairston and Pope, 1948; Hairston, 1950). The subspecies are no longer recognized, largely because at least some of the color characters are distributed independently of one another. The situation as it is presently known is described by Highton (1970, 1971) and by Highton and Henry (1970), who add the electrophoretic patterns of plasmaproteins to the char- acters for which distributional data are available.

Plethodon glutinosus is widespread throughout the eastern United States. In the Southern Appalachians, it tends to occur at lower elevations than those at which P. jordani does, and I ha\'e suggested that the sharp altitudinal replacement of the two species is the result of competitive exclusion (Hairston, 1949, 1 95 1 ) . Although easily recognizable color differences are known for at least four geographically distinct parts of the P. glutinosus population (Highton, 1962, 1970, 1971), the population in the area discussed herein consists of only one of these. P. glutinosus is thus morphologically more uniform than is P. jordani. The above-mentioned altitudinal separation of the two species is not the case everywhere, however. Over the southeastern part of the range of P. jordani, the two species occur together over nearly the entire range of altitudes available, indicating that competition does not play a significant role in their distributions. This ob- servation, reported by me for a few vertical transects (Hairston, 1951) has been confirmed and extended by Highton. The fact that in this area P. jordani occurs at lower elevations and P- glutinosus at higher elevations than elsewhere strengthens the conclusion that in the areas of altitudinal replacement, there is intense competition in the narrow vertical zones of overlap. It is this geographical difference in ecological relationship between the two species that provides an unusual opportunity to investigate the phenomenon of competition in the field, and to obtain evi- dence on the sequence of evolutionary events accompanying competitive interactions between two similar species.

The above account is oversimplified from the taxonomic stand- point. Over most of the area west of the French Broad River, the two species are distinct, but Highton has found hybrids at appropriate elevations on some of the mountains, and intergra- dation is so extensive in the Nantahala Mountains that the local form of P. jordani was once described as a subspecies of P.

8 BREVIORA No. 414

glutinosus (Bishop, 1941). Highton has called specimens from intermediate elexations a hybrid swarm. Two detailed vertical transects in the Southeastern Nantahalas at Coweeta Experi- mental Forest show that simple explanations of the relationship are unlikely to be satisfactory. The forest has two more or less parallel roads that ascend to the top of the mountain. The roads di\'erge slowly from the foot of the mountain at 2200 feet, being a little more than one mile apart at 3200 feet and around two miles apart at the points where they reach the top of the ridge at 4100 and 4500 feet, respectively. In October, 1971, a transect was carried out along the more northern road, to be referred to as the Shope Creek Road. The con\'entional expectation would be of continuously increasing similarity to P. jordani and de- creasing similarity to P. glutinosus with increasing altitude. The comparison was made on the basis of color alone, no other known character being of value in that part of the range. Four different color characters are possible. P. jordani is character- ized by red legs and a pale belly; P. glutinosus has extensive white spotting, especially on the sides, and a black belly. A population of P. jordani 10-15 miles to the east has extensive brassy spotting on the back, as well as some white spotting on the sides, but at present seems to be distributed discontinuously from the Nantahala population. A few specimens from the transect had brassy spots, but were too few to yield meaningful informa- tion. Arbitrary scales were established to compare the relative amount of red on the legs, white spotting, and darkness of belly color. Six to 20 specimens were collected at each of 11 eleva- tions from 2200 to 4300 feet. For each collection, an average intensity of each character was established by five different ob- servers, and the results pooled. The three characters changed in exactly the same way along the transect. The results for two of them are shown in Figure 2. The reversal of the expected trend led to a transect of the southern road (Ball Creek) in 1972. The results, shown in Figure 3, conform to the original expecta- tion, but do not agree with the Shope Road transect, which was repeated in 1972 with \irtuallv identical results to those obtained in 1971 (Fig. 2).

Although the 3800-foot site is located on an east-west ridge, the same is true of all higher sites, and no obvious vegetational differences could be seen to account for the difference between the transects — impressions confirmed in the records from 69 widely dispersed rain gauges (Dils, 1957).

\Vhate\er the eventual explanation for these anomalous data.

1973

ECOLOGY AND SYSTEMATICS

ALTITUDINAL VARIATION IN COLOR CHARACTERS IN PLETHODON ALONG SHORE CREEK WATERSHED

UJ

o

Q UJ

q: o

3 O

1971 1972

^.

0

2200 2400 2600 2800 3000 3200 3400 3600 3800 4000 4200

ALTITUDE (feet)

\J

1

— 1 1

1— T

1

o

•■' '■• \

z

'

i

\

p 1

-

/

\

f

(-

1 :

/

o

1/

\ \

CL

f

\ \

_/

CO

J

/

UJ

1—

/ j

Y

•

^ 2

.

/ 1

\ >

c'

_

5

/ 1

u.

1

o

1

t-

,'

'' 1

J^

z

p"

J

y^

3

;

j

o 3

.

I

_

2

O— .

;

^,-^-'

<

-*

. y

^,---r^

_..d'

V'"'

4

,

,

•

1 1

1 '

,

,

2200 2400 2600 2800 3000 3200 3400 3600 3800 4000 4200

ALTITUDE (feet)

Figure 2. The vertical distribution of two color characters in the sala- mander genus Plethodon along the Shope Creek transect in the Nantahala Mountains in North Carolina. The scale for white spotting has been in- verted because white spots are characteristic of the low-altitude species.

10

BREVIORA

No. 414

ALTITUDINAL VARIATION IN COLOR CHARACTERS IN PLETHODON ALONG BALL CREEK WATERSHED

2300 2500 2700 2900 3100 3300 3500 3700 3900 4100 4300

ALTITUDE (feet)

2300 2500 2700 2900 3100 3300 3500 3700 3900 4100 4300

ALTITUDE (feet)

Figure 3. The vertical distribution of two color characters in Plethodon along the Ball Creek transect, for comparison with Figure 2.

1973 ECOLOGY AND SYSTEMATICS 11

they reflect complications in the relationship between the two species, and further in\'estigations may reveal or at least suggest \'ery local selective forces.

The situation in the Nantahalas gives a strong indication of close taxonomic relationship between P. glutinosus and P. jor- dani, and is thus useful information in suggesting ecological and especially evolutionary questions about the two species elsewhere in the Southern Appalachians where hybridization is absent or very rare.

Current ev^olutionary theory would explain the observed eco- logical distributions in these other areas in the following manner : assuming, as seems likely, that Plethodon glutinosus and P. jor- dani share a common ancestor in the not very remote past, the speciational event separating them left two species with adjacent geographical ranges and very similar ecological requirements. Plethodon jordani presumably occupied the southern part of the Blue Ridge physiographic province, and the relevant part of P. glutinosus occupied the adjacent part of the Piedmont prov- ince. With a warming climate, glutinosus has invaded the val- leys of the Blue Ridge province, but competition from jordani has prevented glutinosus from extending its range to the tops of at least some of the mountains, notably the Great Smoky Mountains, the Black Mountains, and the Unicoi Mountains. Throughout most of the rest of the area of common distribution, one or both species have evolved into ecologically divergent directions, with the result that competitive exclusion no longer operates, and the two species coexist over a wide range of eleva- tions. This situation would represent character displacement in the use of some ecological requirement as yet unidentified. In the areas of competitive exclusion, the vertical overlap of 200 feet represents the uncertainty of outcome of competition owing to climatic variability, P. jordani being favored by cool, wet years and P. glutinosus by the reverse conditions.

' Thus, in conventional theory and as far as numerous observa- tions have revealed, we have the same two species coexisting in some areas and in intense competition in others. Geographic variation in color of P. jordani provides independent identifica- tion of representatives from the two ecologically different popu- lations, and this and other features make it feasible to undertake experimental manipulations to test the accuracy of the interpre- tations that I and others have made of the present distributions of the local populations of the two species. This should be done by reciprocal removal experiments and by exchanging numbers

12 BREVIORA No. 414

of Plethodon jordani between the two areas of presumably dif- ferent ecological relationships. Inasmuch as they difTer in color pattern, the introduced individuals and their descendents would be readily identifiable for an indefinite number of years after the start of the experiments.

The most obvious first test of the interpretations would be to remo\'e each species separately from different plots in the differ- ent areas where competition is and is not expected. If the in- terpretation is correct, the remaining species should show a much greater response in the area of narrow vertical overlap than in the area of wide vertical o\'erlap.

Whatever the outcome of these simple removal experiments, they would help resoh^e an implicit contradiction in ecological theory. This is the conflict between the often used theory that distributional overlap between closely related species implies an appreciable amount of competition (Levins, 1968; MacArthur, 1968) and the converse that the same overlap implies that com- petition is reduced or absent (Crombie, 1947; Hairston, 1951; Brown and Wilson, 1956; MacArthur, 1972: 29 ff). This con- flict is rarely stated overtly, but its resolution could have a pro- found effect on ecological theory, including much that has been written about niche breadths and community matrices.

The implications of the simple removal experiments are more directly ecological than they are evolutionary. The combination of ecological and systematic situations provides the opportunity for more sophisticated experiments whose results could yield im- portant insights into the recent influence of natural selection on the direction of evolution in the several populations of Plethodon jordani. These experiments would consist of reciprocal trans- plants of populations of P. jordani between an area of narrow o\'erlap and one of wide overlap. The subsequent changes in the transplanted jordani populations and in the P. glutinosus popu- lations newly exposed to the foreign jordani would re\eal the direction of recent evolution with respect to interspecific com- petition.

If P. jordani from the area of wide overlap survived in the area of narrow overlap, and the P. glutinosus population in- creased, the interpretation would be that in the area of wide overlap, P. jordani has evolved so as to decrease its competitive interaction with glutinosus. If P. glutinosus has evohed in the same way, the reciprocal experiment should result in no change in the glutinosus population, and it might result in an increase in the jordani population introduced from the area of narrow over-

1973 ECOLOGY AND SYSTEMATICS 13

lap, because the jordani would not be meeting as much compe- tition as it had been experiencing before the experiment.

Con\ersely, if the P. jordani transplanted from the area of narrow o\erlap increases in the area of wide overlap at the ex- pense of the local P. glutinosus, it would be necessary to conclude that recent e\'olutionary history had produced a specialization in jordani for some specific competitive mechanism.

A decrease in and eventual disappearance of jordani moved from the area of wide overlap, combined with an increase in the local glutinosus, would be interpreted to mean the evolution of a specific competitive mechanism in that population of glutinosus.

The complete set of possible experimental outcomes and their interpretations is given in Tables 1 and 2. Specifically omitted from the tables are the highly necessary controls. For the re- moval experiments, the only controls required are undisturbed plots containing both species. The reciprocal transplantation of populations of P. jordani will require elaborate controls. First, one must be satisfied that the salamanders can be moved at all and continue to thrive. This will require transplanting animals within an area where their ecological relationships appear to be constant. Assuming the success of such an experiment, it will also be necessary to provide assurance that they are physiologi- cally capable of existing in the remote area where the competi- tive relations are presumably different. For this control, it will be necessary to first remove both species from a plot and then introduce the foreign jordani. Its survival would assure an interesting result on those plots where it was introduced into contact with glutinosus. The failure of any of these controls would of course mean that the main experiment in reciprocal transplantation of populations was a failure. This is a gamble taken by anyone planning a controlled experiment.

If the controls succeed, the experiment should permit one to choose with confidence between the following hypotheses: First, that after speciation natural selection has favored ecological diversification with resultingly greatly lowered competition and a greatly increased area of coexistence; and second, that after speciation and reinvasion, natural selection has favored the de- velopment in at least one species of mechanisms to increase its competitixe ability and thus exclude the congener from all or nearly all of its range. The ability to choose between the two hypotheses would greatly advance our ability to interpret sys- tematic-distributional data from a large array of situations where post facto conclusions are all that can be expected.

14

BREVIORA

No. 414

TABLE 1. The plan and possible outcomes with their interpretations of experimentation in the area where Plethodon jordani and P. glutinosus over- lap broadly in vertical distribution. All controls are described in the text.

MANIPULATIONS

OUTCOME

INTERPRETATION

a.

Local glutinosus has a competi-

Disappearance

tive adaptation to foreign

of moved

jordani and local jordani has

jordani.

evolved ecological character displacement.

(I)

1.

Combined with a decrease in

Replace

abundance of glutinosus, means

with

that introduced jordani had

jordani

b.

evolved a specific competitive

from area

Persistence

mechanism against glutinosus.

of narrow overlap.

of moved jordani.

A.

(II) Combined with constant gluti- nosus population, means that

Remove jordani.

local glutinosus has evolved eco-

logical character displacement.

a.

Means that there was no

No change in

competition with jordani.

2.

abundance of

Leave

glutinosus.

local

glut 171 OS us

b.

Means that there was some

alone.

Increase in abundance of glutinosus.

competition at a low level.

a.

Means that there was no

No change

competition with glutinosus.

1.

in abundance

(Reciprocal of A 2 a)

B.

Leave

oi jordani.

Remove

local

glutinosus.

jordani alone.

h. Increase in

Means that there was some competition with glutinosus at a

abundance

low level. (Reciprocal of A 2 b)

of jordani.

1973

ECOLOGY AND SYSTEMATICS

15

TABLE 2. The plan and possible outcomes with their interpretations of experimentation in the area where Plethodon jordani and P. glutinosus have a narrow zone of vertical overlap. All controls are described in the text

MANIPULATIONS OUTCOME

A.

Remove jordani.

B.

Remove

glutinosus.

I.

Replace with jordani from area of wide overlap.

2. Leave local

glutinosus alone.

1.

Leave local jordani alone.

Disappearance of moved jordani.

Persistence of moved jordani.

No change in abundance of glutinosus.

h. Increase in abundance of glutinosus.

a.

No change in abundance of jordani.

b.

Increase in abundance of jordani.

INTERPRETATION

Local glutinosus has a specific competitive adaptation to all jordani; glutinosus should increase in abundance.

(I) If glutinosus increases in

abundance or remains stable,

indicates that introduced

jordani has evolved ecological

character displacement with

respect to all glutinosus.

(II) If glutinosus decreases, indicates specific adaptation by area I glutinosus to coexist with all jordani; especially strong if combined with A 1 b (II) of Table 1.

Means that original hypothesis of competition was false. Total distribution pattern hard to interpret. Expect other bad results. Habitat disturbed?

Confirms original hypothesis of competition. Should increase more than in A 2 b of Table 1.

Means that original hypothesis of competition was false, especially with A 2 a. (Same interpretation)

Confirms original hypothesis of competition; jordani should increase more than in B 1 b of Table 1.

16 BREVIORA No. 414

Specialization and the Results of Ecological Interactions

The e\'olutionary result of competitive interactions has been the subject of a great deal of speculation, most of it stressing specialization for different resources. This interpretation requires scrutiny, since it implies that differential specialization is a prob- able result of competition for resources, and the observation of different food habits among coexisting related species has been interpreted as a\'oidance of competition.

Such an interpretation, to be accepted even provisionally, should require an examination of alternate hypotheses to explain the observation. One such hypothesis that has not been explored adequately, is that specialization carries advantages in efficiency of handling, digesting or metabolizing the food, and that com- petition need not be invoked at all. Thus, competition is easily shown not to be a necessary condition for the evolution of food specialization. The subject will be pursued to examine the ques- tion of the sufficiency of competition as an explanation. If spe- cialization for one kind of food is regarded as a derived state, as either of the aboxe hypotheses assumes, then polyphagy must be regarded as the starting point for any reconstruction. Assuming that such is the case, and that the members of a species are ex- periencing intraspecific competition for food, an individual of this species which tended to specialize would be at a disadvantage whene\er its specialty became scarce, since, in becoming a spe- cialist, it would be expected to lose some ability to handle or digest the remaining kinds of food. The only ways for such a specialist to remain at an advantage would be to begin by being so efficient at obtaining the special food as to overcome the expected periodic scarcity, or else in some way to avoid the ex- pected trade-off in efficiency with regard to other kinds of food. The probability appears to be very low in either case. Thus, for food-limited species polyphagy should be the rule.

With an initially polyphagous species that has a superabun- dant supply of food, the situation is quite different. Any geno- type increasing specialization is likely to be favored because of the benefits of increased efficiency. No penalty is attached to this tendency, because under the terms stated, none of the various kinds of food is ever in short supply. Therefore, contrary to routinely accepted theory, specialization for different foods should be characteristic of species that are not in competition, and the claim is hereby advanced that prior competition is

1973 ECOLOGY AND SYSTEMATICS 17

neither a necessary condition nor a suflficient one to explain the coexistence of closely related species each specializing on a dif- ferent food.

How is such a claim to be tested? One way would be the laborious one of field experimentation testing for the means of limitation of population size in a large series of related species, some of which were monophagous and some polyphagous. If the former are consistently limited through means other than the supply of their food resources, and the latter show a consistent tendency to be food-limited, the claim would be strongly sup- ported. Rigorous proof of a series of events in evolutionary his- tory is, of course, not possible, and in the present instance, even if the experiments had the expected outcomes, the counterclaim could always be made that the specialists had been released from competition by becoming specialists and therefore would have to be limited in abundance by some other factor.

A post facto test of the claim that food specialization implies the absence of prior competition for food can be suggested in the following manner. Among a number of species whose food is well documented, there should be no particular relationship be- tween the degree of specialization and the number of specialized species per species of food. If, on the other hand, specialization represents an evolutionary "escape" from competition for food, the advantage gained should be reflected in a tendency to be the only such species feeding on the food species in question. Thanks to an extensive table by Needham, Frost and Tothill (1928), this test can be made in the case of leaf-mining insect species. There are 435 species of plants that serve as hosts. Of these 289 are fed on by only one species of leaf miner; 82 are fed on by two species, and 64 are fed on by three or more species of leaf miners. On the hypothesis that the distribution of the insect species is by chance among the three groups of plant species, the expected distribution can be calculated by tabulating for each insect species its host plant species with respect to the number of insect species that the host plant supports. Thus, for each spe- cialist, only one plant species will appear in the table; for those feeding on two plant species, both plant species will appear in the table, and the same system continues for insects feeding on three or more species of plants; each plant species will appear separately in the appropriate part of the table. After the removal of those records involving plants determined only to genus, and prorating those appearing more than once in the table, there remain 426 records of the plant species, classified according to

18 BREVIORA No. 414

TABLE 3. The number of species of plants attacked by varying numbers of species of leaf-mining insects. The insect species have been separated ac- cording to the specificity of their food habits. The figures in the table have been calculated on the assumption of no relationship between the degree of specialization of the insect and the number of species of insects supported by its food plant (s) .

Number of species of insect per species 2 of host plant

U o - -

O a. U

^ w y:

«4-l — —

^ ^ -y.

^ (-1 ^ ^ O y.

TABLE 4. The observed distributions of plant species for comparison with the expected distributions in Table 3.

Number of species of insect per species 60 of host plant

O '> w

a- ~ '

1

9

3

or more

1

99.47

28.31

21.87

2

47.21

13.44

10.38

3 or more

136.41

38.83

30.00

*^ -y.

"ti a-

1

2

3

or more

1

94.00

37.50

18.31

9

48.00

11.00

12.10

3 or more

134.00

38.50

32.95

Z o

the number of insect species feeding on them. In the absence of a relationship between specificity of feeding by the insect and the number of insect species supported by the host, these 426 records should be distributed in the ratio 289 : 82 : 64 for each group of insects : those found on one species of plant, those found on two species and those' found on three or more species. The expected distributions are given in Table 3.

If specialized species of insects tend to specialize on plant spe- cies for which there is little competition, there should be an excess of species in the first column for species with one host, and a corresponding deficiency in the third column for the same row. That such is not the case is shown in the observed distribution (Table 4). Three of the specialists are confined to a plant spe- cies that supports them and ten other species of leaf miners; four are confined to a plant species that supports them and eight other species of leaf miners. At the other end of the scale, one species of leaf miner which lives on 37 different plant species is the only species feeding on 19 of these plants. Thus, these data

1973 ECOLOGY AND SYSTEMATICS 19

provide no support for the hypothesis that specialization for spe- cific food items arises as a direct result of interspecific competi- tion, and the data do support the hypothesis that such specializa- tion arises in the presence of ample food of various kinds. The data, incidentally, are also consistent with other kinds of evi- dence indicating that the terrestrial herbivore trophic level is predator-limited as a whole (Hairston, Smith, and Slobodkin, I960).

It is now worthwhile to examine the kinds of divergence that would be likely under the selective force of interspecific compe- tition. It is assumed, and will probably be conceded, that com- petition is likely to be most intense between close relatives, here interpreted as those most recently separated by speciation. It is further assumed that newly separated competing species will be in contiguous but largely nonoverlapping ranges. If the differ- ences between the adjacent places were great enough, the pro- cess of adaptation to the separate local conditions would be likely to result in species that were different in many ways, in- cluding the acquisition of different kinds of food, even if both species were limited in abundance by their food supplies. Selec- tion might now favor either of two quite different courses: the production of competitive mechanisms specifically against the neighboring species, or further divergence by each species in ob- taining food in those parts of the others' range most like its own. The first would sharpen the boundary between the two species, as is the case with Plethodon jordani and P. glutinosus over parts of their distribution; the second course would be expected to lead to broadly overlapping but different ecological distributions, such as are exemplified by the species of Desmognathus. These two courses, as well as the third and noncompetitive course pro- posed earlier, would have quite different consequences from the standpoint of systematics. The continued highly competitive situ- ation should result in few differences, and it is easy to imagine situations in which hybrids would be at an advantage. The two spdcies of Plethodon in the Nanthala Mountains may provide an example. Where the species become differentially adapted to place, it would be expected that many differences would be favored, and that eventually these would become the large dif- ferences that characterize higher categories. It would be easy to place Desmognathus aeneus and D. quadramaculatus in different genera, were it not for the existence of two species intermediate between them in morphology. Finally, in the noncompetitive situation, it might be expected that selection would produce few

20 BREVIORA No. 414

differences, but those would be ver\- distinct, and would be such as to put hybrids at a severe disadvantage.

What is being suggested here is that an analysis of the sys- tematic and distributional relationships provides clues to the eco- logical forces that have been operating on the species in question. In the case of one such situation, there has been proposed a series of experimental tests designed to permit a choice among the eco- logical and selectional events that led to the present systematic relationships. Without such planned experiments, we are com- mitted at best to accepting "natural experiments," the conditions of which may be unknown to us, and which nearly always lack the elements of controls and of experimental design that promote definitive answers to specific questions. Manipulations will not be possible for all situations, but if the different ecological causes and their systematic effects that I have suggested can be con- firmed for a few specific cases, predictive power would be added to the simple analyses to which we are now confined.

References Cited

Bishop, S. C. 1941. Notes on salamanders with descriptions of several new forms. Occ. Papers Mus. Zool., Univ. of Mich., No. 451: 1-21.

Brown. W. L., and E. O. Wilson. 1956. Character displacement. Syst. Zool., 5: 49-64.

Crombie, a. C. 1947. Interspecific competition. J. Anim. Ecol., 16: 44-73.

DiLS, R. E. 1957. The Coweeta Hydrologic Laboratory. U.S. Dept. Agri- culture Forest Service Southeastern Forest Experiment Station, Asheville, N.C. ii + 40 pp.

Dunn, E. R. 1926. The salamanders of the family Plethodontidae. Smith College Anniversary' Pubis, xii + 441 pp.

Grobman, a. B. 1944. The 'distribution of the salamanders of the genus PletJiodon in the eastern United States and Canada. Ann. New York Acad. Sci., 45: 261-316.

Hairston, N. G. 1949. The local distribution and ecology of the pletlio- dontid salamanders of the Southern Appalachians. Ecol. Monogr., 19: 47-73.

. 1950. Iiucrgradation in Appalachian salamanders of the

genus Plethodon. Copeia, 1950(4) : 262273.

1951. Interspecies competition and its probable influence

upon the vertical distribution of Appalachian salamanders of the genus Plethodon. Ecology, 32: 266-274. , AND C. H. Pope. 1948. Geographic variation and spccia-

tion in Appalachian salamanders {Pletfwdon jordatii Group) . Evolu- tion, 2: 266-278.

1973 ECOLOGY AND SYSTEMATICS 21 , F. E. Smith, and L. B. Slobodkin. 1960. Community

structure, population control, and competition. Amer. Natur. 94: 421- 425.

HiCHTON, R. 1962. Revision of North American salamanders of the genus

Plethodon. Bull. Fla. State Museum, 6: 235-367. . 1970. Genetic and ecological relationships of Plethodon jor-

dani and P. glutinosus in the Southern Appalachian Mountains.

Pp. 211-241 in Th. Dobzhansky, M. K. Hecht, and W. C. Steere (eds.) ,

Evolutionary Biology, Vol. 4. New York: Appleton-Century-Crofts. . 1971. Distributional interactions among eastern North Amer-

ican salamanders of the genus Plethodon. Pp. 139-188 in P. C. Holt (ed.) , The Distributional History of the Biota of the Southern Appa- lachians. Research Div. Monograph 4. Blacksburg, Va.: Virginia Poly- technic Inst.

-, AND S. Henry. 1970. Variation in the electrophoretic migra-

tion of plasma proteins of Plethodon jordani, P. glutinosus, and their natural hybrids. Pp. 241-256 in Th. Dobzhansky, M. K. Hecht, and W. C. Steere (eds.) , Evolutionary Biology. Vol. 4. New York: Appleton- Century-Crofts.

Levins, R. 1968. Evolution in Changing Environments. Princeton, N.J.: Princeton Univ. Press, x + 120 pp.

MacArthur, R. 1968. The theory of the niche. Pp. 159-176 in R. C.

Lewontin (ed.) , Population Biology and Evolution. Syracuse, New York:

Syracuse University Press. . 1972. Geographical Ecology. New York: Harper & Row.

xviii -f 269 pp.

Needham, J. G., S. W. Frost, and B. H. Tothill. 1928. Leaf-mining in- sects. Baltimore, Md.: Williams and Wilkins Co. viii + 351 pp.

Organ, J. A. 1961. Studies on the local distribution, life history, and pop- ulation dynamics of the salamander genus Desmognathus in Virginia. Ecol. Monogr., 31: 189-220.

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THE EJW^fiJ^ON OF BEHAVIOR AND THE RoKe'dF'bEHAVIOR IN EVOLUTION

M. MOYNIHAN^

Abstract. Modern behavior studies are, or should be, primarily concerned with problems of causation. The immediate causes of particular behavior patterns are being analyzed at the physiological and biochemical levels. The ultimate causes, selection pressures, are being studied by ecologists and ethologists. Unfortunately, there is little contact between the two lines of investigation at the moment. Doubtless a new synthesis will be achieved in the future. It does not, however, appear to be imminent. In the meantime, the results of behavior studies in th^ field or in the laboratory in semi- natural conditions can still be of use to the evolutionary biologist. They may be most helpful in revealing the details, mechanics, of certain ecological processes, which are themselves the regulators or determinants of evolutionary events. Some examples from recent work on cephalopods, monkeys, and birds may illustrate the sorts of data that are both available and relevant.

Introduction

I have been asked to talk about my own work on animal behavior and related subjects, and also to say something about possible further developments of behavioral studies in general. The prospect of thus anticipating the future is not entirely grati- fying. It seems to me that current research on animal behavior has reached a difficult, awkward, almost embarrassing stage. As is the case with any subject, there are numerous false starts and unrewarding pursuits. Some questions being asked by workers in the field are hardly worth posing. The answers are self- evident or easily predictable. Some other questions are devoted to more significant problems, but apparently cannot be answered with the techniques currently available, at least not the tech- niques actually being used. More important, the various kinds

^Smithsonian Tropical Research Institute

2 BREVIORA No. 415

of studies that are proving to be useful and successful are becom- ing increasingly disparate in both methods and objectives.

This anomalous situation is, of course, the result of historical factors. It might be instructive, therefore, to give a brief resume of some aspects of the past, in order to explain the present unease and to pro\'ide or re\ eal a reasonable rationale for some of the continuing work — my own included.

Many biologists, the majority of evolutionary biologists and "natural historians," probably would agree that the most stimu- lating school of behaviorists in this century was that of the "ethol- ogists." Ethology as such may be difficult to define. In theory, the term could be applied (without paying too much attention to its classical deri\ation) to the whole of the science of behavior. In fact, it is usually restricted to a particular approach to the subject, based upon Darwin (1872) and other pioneers such as Heinroth (1911), Whitman (1899 and 1919), Huxley (1914), and Craig (1918), and perhaps influenced by some early ideas of Freud or his predecessors, but largely developed in continental or Teutonic Europe in the 1930's and 1940's and subsequently widely diffused, first in the English-speaking world and then elsewhere in the next decade.

This school was distinguished by a concentration upon large segments or sequences of behavior in natural or semi-natural conditions, especially social (inter-indi\idual behavior and the reactions that were called at the time "innate," i.e., species- typical or (often by implication) species-specific. Among the better known products of the school which may ser\^e to illustrate its original range of interests were papers by Lorenz {e.g., 1931, 1935, 1941), Lorenz and N. Tinbergen (1938), N. finbergen (1932, 1935, 1936, 1939, 1940), Makkink (1936), Kortlandt (1940), Seitz (1940 and 1941), and Baerends and Baerends (1950).

Another characteristic of the first ethological studies was a pre- occupation with causes, not only long-term components such as selection pressures affecting beha\'ior in the course of evolution but also short-term or even immediate causes, external and in- ternal states and stimuli and internal mechanisms producing particular acts at particular instants in time. The latter interest entailed a considerable amount of rather ambitious and detailed model-building, the dc\elopment of concepts and terms such as "Innate Releasing Mechanism," "reaction specific energy," "dis- placement" activities, and "hierarchies" of instincts. The state of the art at this stage is beautifully summarized in N. Tinbergen

1973 EVOLUTION AND BEHAVIOR 3

( 1951 ) . Unfortunately, most of the models proved to be descrip- tive of the overt manifestations of behavior but not explanatory or usefully predictive. They did not correspond very closely to the actual e\'ents within a behaving animal. (This sort of dis- crepancy between the perceived and the real is an occupational hazard of model-building. There may be comparable gaps in ecological models — a topic that will be mentioned later. )

The responses of ethologists to their logical and methodological difficulties were exceedingly diverse :

1. The original mainstream of effort was impeded and re- duced but did not dry up completely. There were hopeful and ingenuous attempts to redefine and refine the classic concepts (see, for instance, Bastock et al., 1953; Hinde, 1954a and 1954b; Morris, 1957; Blest, 1961). Some of these attempts may have been helpful in minor ways, but I think that it would be fair to say that they did not do very much to resolve the basic dilemma. There was a push to render descriptions more precise, by adop- tion of mathematical and pseudo-mathematical means of nota- tion, often with an infusion of information theory and cybernetic terminology, and by increased* use of improved photographic and other kinds of recording equipment. Examples are too nu- merous to cite, but many can be found in recent issues of the journals "Behaviour" and "Animal Behaviour" and the bibli- ographies of the general surveys of Hinde (1970), Eibl-Eibesfeldt (1970), and Marler and Hamilton (1967). All too often, they have merely told us what we already knew or assumed, at dis- tressingly greater length and elaboration than we were prepared to cope with.

2. Perhaps a more practical response was switching of atten- tion to groups of animals and special problems that had been neglected in earlier years. Several bends in the river or new channels which are in some danger of becoming oxbows but are at least picturesque. There has been a great deal of strictly etholoarical work on a variety of "lower" mammals such as mar- supials, rodents, and carnivores [e.g., Kaufmann, in press; Klei- man, 1972; Leyhausen, 1956; Kruuk, 1972; Schaller, 1972; Ewer, 1963, 1968, and 1973), and an enormous proliferation of studies and surveys of primates {e.g., Altmann, 1967; Chance and Jolly, 1970; Crook, 1970; DeVore, 1965; Dolhinow, 1972; Imanishi and Altmann, 1965; Jay, 1968; Jolly, 1966 and 1972; Kummer, 1968 and 1971; van Lawick-Goodall, 1971; Morris, 1967a; Movnihan, in press a; Fetter, 1962; Poirier, 1972; Rey- nolds, 1968; Rosenblum and Cooper, 1968; Rowell, 1972;

4 BREVIORA No. 415

Schaller, 1963; Struhsaker, 1969). Many of these papers were indirect reflections of a strong interest in human beha\ior, both as it is and as it may be supposed to have been at some earlier time in the Pliocene or Pleistocene; and there have also been attempts to apply conventional ethological insights to some of the urgent problems of modern man {e.g., Lorenz, 1963; Russell and Russell, 1968; Morris, 1967b; Martin, 1972) with amusing results (critics have tended to dismiss both the good and bad suggestions and interpretations as impertinent sensu stricto, but it may be hoped that some of them will eventually be incorp- orated into the intellectual background of the well-informed citizen ) .

The most fashionable of the special subjects has been what might be broadly called "communication." Different aspects of the subject ha\'e been tackled at many different levels and in many different areas. There have been analyses of the various ways in which information, true or false, can be transmitted among individuals of the same or different species, and also of the means by which transmission can be prevented or inter- rupted. One of the aspects of interspecific communication that has attracted investigation and speculation is mimicr\ , not onh' the long known Batesian and Mullerian types but also aggressive and social and e\'en more recondite forms. Relevant publications include Brower et al. ( 1 960, and many other papers from the same school); Rand (1967); Robinson (1969); Moynihan (in press b), and an extensive discussion and summary in Wickler (1968). The methods by which predators discover and recog- nize prey, with or without the baffles of mimicry and crypsis, have been studied by many workers. The papers of Robinson and his collaborators {e.g., 1969, 1971a, 1971b) reveal some of the factors that may corne into play. Research on intra-specific communication has been primarily concerned with the e\en more variegated "languages" used in more complex social situations ("social" in the ever\^ day sense of the term). It has involved description, decipherment, and efforts to detect and formulate the general rules, the "grammar and syntax," of a multiplicity of signal systems. There have been sur\'eys and comparisons of the signals of different groups of animals {e.g., Tembrock, 1959; Lanyon and Tavolga, 1960; Busnel, 1963; Sebeok, 1968), some- what abstract discussion of theorv {e.g., W. J. Smith, 1965 and 1969; Moynihan, 1970; Cullen, 1972; Mackay, 1972), and detailed accounts of particular systems, ranging from the phero- mones of insects {e.g., the work of E. O. Wilson and his col-

1973 EVOLUTION AND BEHAVIOR 5

leagues) through bird "song" {e.g-, Thorpe, 1961 ; Hinde, 1969) to the non-\erbal movements and expressions of children and adults in contemporary western and other human societies {e.g., Gofifman, 1971; Blurton Jones, 1967 and 1972; Argyle, 1972; Eibl-Eibesfeldt, 1972). These studies may have implications for related fields. They have, for instance, at least made available to "real" linguists such as Chomsky, Lenneberg, etc., some useful background material and evolutionary perspective.

3. However valuable such works may be, they would appear to be di\Trsions from the classical behavioral point of view. Most active students are proceeding, and probably will continue for the foreseeable future, in one or the other of two different directions, two new mainstreams. Those who are preoccupied with immediate causes are going into physiology in earnest, lab- oratory research on hormones, nerve cells, receptor organs, at the deepest or lowest, even molecular, level. I cannot say anything about this. Results are obviously flowing in, but the subject is complex and not my major interest and I am not competent to discuss it.

4. Ethologists who are more concerned with ultimate causes are exploring connections or interfaces among behavior, ecology, and evolution.

This has been my own preference. I may, therefore, be able to illustrate sonle of the positive virtues and negative drawbacks of the approach by citing particular cases from my own experi- ence. In recent years, I have been engaged in observation and analysis of three groups of animals, cephalopods. New World primates, and passerine birds (and some "near passerines" such as hummingbirds ) , in the field in natural or semi-natural condi- tions.

Examples

1. I was attracted to cephalopods for several reasons. They provide remarkable examples of evolutionary and ecological convergence. Beginning with a molluscan body plan, they have acquired large size, good eyes, large brains, and (in many spe- cies) active and predatory habits. They have become similar to many fishes and other aquatic vertebrates in these respects. (The convergence is discussed at length in Packard, 1972.) They have also evolved unique or peculiar characters such as distinc- tive methods of buoyancy control, color changes, and jet pro- pulsion. Combinations of some of these features have finally

6 BREVIORA No. 415

allowed them to invade the laboratory, to serv^e the neurophysi- ologist. I would say, without being an expert, that some of the operations of their central nervous systems and their handling of visual information must be better known than the corresponding processes of any other animals with the possible exception of man. See, for instance. Young (1964 and 1972), Wells (1962), and the many papers of Sutherland and his co-workers.

In these circumstances, it is noteworthy that the social be- havior of cephalopods has not been studied in anything like the detail that might, off-hand, have been expected. (There are technical reasons for this comparative neglect. Most cephalopods do not li\'e long in captivity and/or are difficult to follow in the field.) Such work as has been done on the subject has been une\'enly distributed. The great majority of living species of the class can be assigned to one or the other of three diversified and flourishing orders. Using the terminology of Jeletzky ( 1 966 ) , these may be called Teuthida (including the squids), Sepiida (cuttlefishes and their relatives), and Octopida (octopi and argonauts ) . There are more or less lengthy published accounts of the social behavior in the laboratory of the common European cuttlefish. Sepia officinalis (L. Tinbergen, 1939; Holmes, 1940), and the common octopus. Octopus vulgaris (e.g., Packard and Sanders, 1971; Wells and Wells, 1972), but relatively little on other species, only bits and pieces on some reactions of a few other sepiids and octopi and several kinds of squids, mostly Loligo spp., in the laboratory or in the field (see references in Lane, 1957, and Moynihan, in press b).

I was delighted, therefore, to encounter a species of squid, Sepioteuthis sepioidea, in the San Bias Island region of the At- lantic coast of Panama which is quite unusually easy to observe in the wild under natural conditions. Mr. Arcadio Rodaniche and I seized the opportunity to look at its social behavior. We have now been observing it at monthly intervals for over two years.

The species occurs inshore in moderately or very shallow waters over turtle grass and coral. It is often extremely abun- dant. It is a true squid, but rather cuttlefish-like in shape, adapted for "hovering," and much less rapidly or continuously mobile than most other squids (see also Boycott, 1965). It is both predator, eating small fishes and crustaceans, and prey, being eaten by large fishes such as barracuda and snappers (and perhaps many other animals, including birds, Brown Pelicans, etc.). Individuals of the species tend to scatter singly or in pairs

1973 EVOLUTION AND BEHAVIOR 7

or trios to hunt more or less actively at night, but they congregate in large groups in the daytime to wait for prey to come to them. The daytime groups may be almost completely stationary for long (several hour) periods. Even when they are less sluggish, they tend to keep within rather small territories or home ranges. Groups are easily habituated to the presence of human observers. ( In fact, one of the few technical problems of working with the species is to keep from getting too close to retain perspective and an overall view.) Individuals in groups are not shy about per- forming a variety of elaborate social reactions, including the full range of "courtship" and copulatory patterns, before human ob- serv^ers. Thus, they have provided us with a superfluity of data.

What have been the results?

In one sense, they have been disappointingly conventional. The social behavior of Sepioteuthis is essentially vertebrate-like in basic articulation and organization. There do not seem to be any general principles of molluscan behavior apart from those shared by most other complex animals of other phyla. But this squid does exhibit or illustrate a whole series of interesting special adaptations which may be correlated with, causally related to, one significant aspect of its ecology — and many of which may also be characteristic of other cephalopods and for the same reasons.

S. sepioidea populations are highly structured. Not only do individuals repeatedly leave and rejoin groups, but even the groups are formed of sub-groups which may be separate at some times, with obvious hostility and territorial defense among them- selves, yet completely integrated at other times. There also are size and (presumably) age classes that assort themselves in par- ticular spatial arrangements according to particular temporal and physical circumstances. The system is both intricate and flexible, apparently at least as much so as those of such mam- malian carnivores as lions, African hunting dogs, and Spotted Hyenas.

The system is mediated by signals, both ritualized (mostly displays) and unritualized. As far as we can tell, all the signals are visual. (Cephalopods seem to be deaf, and we did not detect, see, any indications of the use of pheromones or other means of olfactory communication.) The visual signals include postures and movements and many color changes. The number of ritualized patterns is quite high. The basic components of the ritualized repertory may not be more numerous than the corresponding elements in the repertories of certain birds and

8 BREVIORA No. 415

fishes (see Moynihan, 1970), but they can be combined and recombined almost endlessly. It is not uncommon to see an animal adopt two or three, even four or five, color patterns simultaneously, each color on a particular part of the body, while performing a series of movements, especially of the fins or arms, in very rapid succession. The effect is Protean. A squid is quite able to transmit a variety of different signals in difTerent directions to difTerent recei\'ers, different kinds of onlookers, all at nearly or completely the same times. As visual signal systems go, the cephalopod versions must be unique in their combinations of speed and diversity or multiplicity and perhaps efficiency.

Comparison of the known patterns of Sepioteuthis, Sepia, Octopus, and some other cephalopods has revealed some sugges- ti\'e similarities and contrasts. Some displays are very distinct, obviously not homologous, in the different species. Others are very similar. Some of these are relatively simple. They may well have become ritualized independently in each of the phyletic lines. But at least four major displays are both extremely com- plex, exaggerated, and "unexpected," and yet strikingly similar in many details (of causation and function as well as form) in the \-arious species. These displays would appear to have be- come ritualized before the lines diverged from one another. As the divergence must have occurred well before the end of the Mesozoic, perhaps most probably in the Late Triassic, the pat- terns are not only old but also have been remarkably conservative during evolution. To my knowledge, they ha\e been more con- servative than any patterns of other groups so far recorded in the literature. One of the reasons whv some or all of them have been stable is apparent when they are compared with the other dis- plays of the same species that have changed more considerably or de\eloped more recently. The latter tend to be shown to only a few individuals or types of individuals. The conservative sig- nals, on the other hand, are designed to influence a great number and di\ersity of receivers, different age, size, and sex classes of the same species and/or individuals of other species, especially potential predators. This may be a general rule, applicable to most animals. All other things being equal, the more widely reflected or broadcast a signal, the more conservative it will be, the more narrowly reflected or broadcast, the more Ukely it is to be changeable in evolutionary time.

The role of predation should be emphasized in connection with cephalopods. There is good evidence (see Moynihan, in press c) that several or many of the living members of the class

1973 EVOLUTION AND BEHAVIOR 9

are favorite prey of marine birds and mammals almost through- out the seas and oceans of the world. They must, therefore, be themselves enormously abundant in many areas. (Common as it is, Sepioteuthis has a fairly restricted distribution in the tropical Atlantic. Other squids must have larger populations. The total numbers of cephalopods in any given area are difficult to esti- mate precisely, as many species are nocturnal and most are diffi- cult to catch with the traditional gear of marine biologists, but the birds and mammals probably are more efficient collectors.) There also is evidence that the enormous biomass of cephalopods is di\ided among fewer "packets," i.e., species, than is that of their nearest competitors, the marine fishes. This could be both cause and consequence of their relatively greater attraction for predators.

It may be assumed that many of the extinct cephalopods ex- hibited some or all of the demographic and ecological charac- teristics of their living relatives. If so, it seems likely that preda- tion pressure could have been the major impulse for a series of evolutionary events. Some of the probable steps can be listed briefly and crudely. The ancestors of the majority of living cephalopods presumably reduced, internalized, and in some cases lost, their originally external shells to gain greater maneuverabil- ity and powers of escape. This "freed" their skin for other uses, including the elaboration of color change mechanisms. The de- velopment of gregarious habits may well have been another (even earlier?) anti-predator adaptation (Brock and Riff en- burgh, 1960). The habit of living in groups puts a premium upon the development of complex signal systems. For vulnerable marine animals, a visual communication system has definite adxantages. (Visual signals can be turned off instantaneously whene\er necessary or desirable, unlike olfactory cues, and they are perhaps less apt to be noticed at a distance by dangerous receixers than are acoustic signals, especially in murky waters or around reefs or vegetation. And, of course, short range signals are perfectly adequate as long as the animals are close together. ) Once the skin has become speciaHzed for color changes, it prob- ably is not easily transformed for other purposes such as the development of new kinds of armor or spines. This restricts the choice of further anti-predator adaptations. It has already been mentioned that whatever displays may have to be shown to potential predators are conservative. As many or most of these patterns are also used in intraspecific encounters, they may tend to impede fundamental changes in the type, although certainly

10 BREVIORA No. 415

not the details, of the signal system as a whole. Other char- acters of cephalopods such as their rapid growth, relatively short life spans, special arrangements and care of eggs (see, for in- stance, Packard, op. cit., and Wells, op. cit.), and even their preference for reproducing only once in a lifetime, in "big bangs" (Gadgil and Bossert, 1970), could also be explained as responses to intense predation. (And the need to synchronize reproductive moods in a hurry, without much time for trial and error, must add another premium for both gregariousness and the elabora- tion of signals.)

The series is an illustration of some of the ways in which ecology and beha\dor can interact to determine the course of evolution, each step opening up some possibilities and foreclosing others.

2. The New World primates are a variegated family of mon- keys of some 11 to 13 genera and many species. I have obser\ed representatives of all the genera at irregular intervals over 15 years. Some species have been observed only in captivity, at the field station on Barro Colorado Island and in zoos in \Vashing- ton, London, Paris, and Amsterdam; but many others have been studied at considerable length in the wild, in the central part of the isthmus of Panama, to the west in the province of Chiriqui, and to the south in the upper part of the Amazon basin, in the Caqueta and Putumayo regions of Colombia.

For most biologists, the primary significance of the American monkeys is that they represent a wide and independent adaptix^ radiation. They have occupied most of the habitats available to primates. In this respect, they are more or less strictly equivalent to the two other radiations of modern primates, the (Recent and Pleistocene) lemuroids of Madagascar, and the so-called Old World monkeys and apes, the "Catarrhini," of tropical Asia and Africa and some adjacent areas, of which man is a specialized offshoot. The New World forms may thus provide a useful check to hypothesis and speculation about the evolution of pri- mates in general and man in particular. I should also like to claim that they are interesting in themselves.

They range from very small (the Pigmy Marmosets of the genus or sub-genus Cebuella) to moderately large (the howlers, Alouatta, and the spider monkeys, Ateles). They show a great diversity of types of locomotion, from squirrel-like scrambling and/or vertical clinging and leaping among the marmosets and tamarins {Saguinus, Leontideus, Callirnico, and Callithrix in addition to Cebuella), through quadrupedal "springing," walk-

1973 EVOLUTION AND BEHAVIOR 11

ing and pacing in such forms as Saimiri and Cebus, to brachia- tion or semi-brachiation with the supplementary use of a pre- hensile tail in Ateles. (The classification and details of locomo- tion are discussed in Erikson, 1963, and Napier and Walker, 1967.) At least two species of Cebus, capucinus and apella, come down to the ground with appreciable frequency. All or most of the species of other genera are thoroughly arboreal. One genus, Aotus, is nocturnal; the rest are diurnal. They all tend to be nearly omnivorous on occasion ; but most of the smaller forms, many of the tamarins and probably the marmosets of the genus Callithrix, seem to prefer insects whenever they can get them, while some of the larger forms are essentially herbivorous, taking various assortments of fruits of particular kinds and ages, as well as buds and leaves and even twigs and bark. At least one form, Cebuella, has specialized in sap-sucking. (The sap-sucking is described in Moynihan, in press d. The best general accounts of more conventional feeding habits and regimes, unfortunately lim- ited to the Panamanian species, are in Hladik and Hladik, 1969, and Hladik ^^ fl/., 1971.)

In the course of my own studies, I have attempted to discover and analyze the social behavior and structures of different spe- cies and combinations of species, to determine how such com- plexes are held together (or apart as the case may be), and to identify some of the selective forces involved, to tie the observed behavior to particular aspects of ecology. The results sum- marized below are taken from Moynihan (in press a) ; this book also lists references to papers and unpublished notes of other workers.

Two extreme types of intraspecific social organization can be recognized without much difficulty: the restricted "nuclear" family group and the large band. The former seems to be the basic social unit of Aotus, Callimico; two species of Callicebus, moloch and torquatus; and, in some circumstances, Pithecia monacha. Bands are characteristic of Pithecia melanocephala, Alouatta villosa, Alouatta caraya, Lagothrix, Saimiri, and some or all forms of Cebus and Ateles. As might be expected, there are intermediate conditions, complications, and exceptions. One type of intermediate is the "extended" family of some species of Saguinus, e.g., juscicollis, graellsi, midas, and Cebuella and prob- ably many other marmosets. Intermediates can also be flexible, intermittent or recurring. Small families of some species may join one another in some circumstances. It also is normal or usual for neighboring small families of most species to perform

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certain responses, e.g., anti-predator reactions, in common. (This is evidence that they do form a real social community.) Con- versely, large bands may