GILL ARCHES AND THE PHYLOGENY OF FISHES, WITH NOTES ON FiRE CLASSIFICATION OF ...

94 Pages·2004·28.18 MB·English

GILLARCHESANDTHE
PHYLOGENYOFFISHES,WITH
NOTESON FiRECLASSIFICATION
OFVERTEBRATES
...BT.1-M-
GILL ARCHES AND THE PHYLOGENY OF
FISHES, WITH NOTES ON THE
CLASSIFICATION OF VERTEBRATES
GARETH J. NELSON
Assistant Curator, Department of Ichkthyology
The American Muiseum ofNatural History
BULLETIN
OF THE
AMERICAN MUSEUM OF NATURAL HISTORY
VOLUME 141: ARTICLE 4 NEW YORK: 1969
BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY
Volume 141, article4, pages 475-552, text figures 1-26,
plates 79-92, table 1
Issued July 14, 1969
Price.' $2.00a copy
CONTENTS
INTROD.U.C..T.I..O.N................... 479
Material and Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . 479
Terminology of Gill-Arch Elements .... . . . .... . . . ..... . 480
Basibranchials 480
.........................
Basibranchial Tooth Plates ....................... . 480
Hypobranchials, Ceratobranchials, and Epibranchials 480
..
Infrapharyngobranchials and Suprapharyngobranchials .. . 481
Terminology of Current Literature . . . . . . . . . . . . . . . . . . . . . 481
Abbreviations Used in Text Figures and Plates. . . . . . . . . . . . . . . . . 483
GILL-ARCH STRUCTURE.484
Primitive Gill-Arch Dentition ......................... 486
.
Upper Pharyngeal Dentition . . . . . . . ..... 488
.............
Holosts .... . 488
.....Teleosts .. 488
.
Basibranchial .D..entition 493
.............
Primitive Teleosts . . . . . . . . . . . . . . . . . . . . . . . . . . . .493
Advanced Teleosts . . . . . . . . . . . . . . . . . . . . . . . . . . . . 497
Sarcopterygian.s.... ...... 503
.
504
Chondrosts .. .
Basibranchials 505
..
Actinopterygians . 505
.............
Sarcopterygian.s.... ...... 507
.
507
Elasmobranchiomorphs ....... . .. . .. . .. . .. . .. . . . .
Comparative Basibranchial Structure . . . . . . . . . . . . . . . . . . . . . 507
Actinopterygians 507
.
Elasmobranchiomorphs ....... .. .. . .. . 515
517
Phyletic Trends . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The Dermal Skeleton Versus the Endoskeleton. 519
Reductions of the Endoskeleton . . . . . . . . . . . . .. . ........... .. ...... .... 519
522
THE PROOTIC ARCHES.. . . . . . . . . . .. . . . ... . . . .. . ..
INETlEaRsRmEoLbArTaInOcNhSiHoImPoSrOpFhiMA.J.O.R..FIS.H.GR.OU.PS. .. .. .. . . . . . 552255
.525
Teleostomi
.525
Sarcopterygii
.526
Actinopterygii
57
Chondrostei .5........................2
....5....27
Holostei
52
Teleostei.
LCILSATSSOIFFIMCAATJIOORNGORFOVUPSEOFRCHTOREDATB.ES. R...A. ..T....E..S........... .. ..................
SUMMARY.535
.53
REFERENCES
477

INTRODUCTION
THE: DERMAL SEKELETON associated with the tooth plates of the basibranchial complex
endoskeletal gill arches of fishes is developed hasled to aconsideration of theirsupporting
in different ways and to markedly varying endoskeleton, and suggests certain com-
degrees. To date, however, this part of the parisons with elasmobranchs. For this struc-
dermal skeleton has received little study, turalcomplex a newinterpretationisoffered,
with respect either to its basic structure orto one accounting for the variation long known
its interspecific and intraspecific variability. tooccuramonggnathostome fishes. Fromthe
For teleostome fishes, osteological studies standpoint of gill-arch structure, probable
have usually dealt only superficially with the phyletic relationships among the major fish
gill arches and in many instances have not groups are expressed in a provisional higher
included any distinction between their der- classification of the vertebrates, including
mal and endoskeletal parts. Frequently, for tetrapods.
example, purely dermal elements have been
MATERIAL AND
given names more correctly reserved for
ACKNOWLEDGMENTS
endoskeletal elements. Contributing to this
confusion is the complicating fact that some Thepresentpaperisinlarge measurebased
skeletal elements of the gill arches of a given on personal examination of Recentand fossil
fish are of acompound nature, includingboth fish specimens. The techniques used are the
dermal and endoskeletal components. same as those described by the writer in
Although it breaks down at some levels of previous papers. Photographs are unre-
alizarin-stained
analysis (see, e.g., Jarvik, 1959, p. 49), a touched andingeneral are of
clear distinction between thedermal skeleton material. Specimens were made available
and endoskeleton in the head of fishes seems through thecourtesyofthefollowingpersons
both possible and necessary for routine and institutions: Dr. Reeve Bailey, Univer-
anatomical and systematic studies. With re- sity of Michigan; Dr. William Gosline and
spect to the gill arches, this distinction has Dr. Barry Muir, University of Hawaii; Dr.
long been recognized (e.g., in the works of P. Humphry Greenwood and Dr. Colin
Ridewood, 1904-1905; Gregory, 1933, p. 90; Patterson, British Museum (Natural His-
and Rauther, 1940, pp. 444-445) but gener- tory); Dr. Earl Herald, California Academy
ally has been overlooked in descriptive ac- of Sciences; Prof. Erik Jarvik, Dr. Tor
counts and in attempts to bring gill-arch 0rvig, and Prof. Erik Stensi6, Swedish Mu-
evidence to bear on questions of relationship. seumofNaturalHistory; Prof.EigelNielson,
Elsewhere (Nelson, 1966, 1967b, 1967c, Mineralogical Museum, Copenhagen; Dr.
adtoa1sclvtetgmanftrth9ioluiiaimraiaco6lwaourfccptjcbnl7shntdiiehhhlo-a,eeceoedeaalrs,smaiu,orcistanorsfacghhbicarph1onadefaesphnifti9errtusshynfde6etanheaktloir8foavccesreecelaomaitatnearltotrili)renpeoidgeotenircrftcc,iendteooeseootacrh.umltnhnictltamasapossoheo,rltatfaigiTtnealisldryphsetnwyoeeahoieeddrmnrtfyfpdlissgooaseoelveeptieurdrporeoarlatit.sgrpmselrarnhtlue,-stieitveiehganteAdnoiaonnergeuaeuooirelntcetdTntnsnlddvhsiiea,oeittceiisloasggonre,nslsfyenatrygmdtekasounbota.eadeltdsdudehrtanylleitipecphWsendmoedsstroieetasmdho,eonhsolstibntasemndeyi.osaooioitmeescfefttdmfnetrwrietTognemigfovstrritihsiotimntaalohanhllgtlss-e--hlle--e--- FwBNoffSmiaFptltofirioanowlafehhegrietreNeleebtutnlEtgutaldrhbedphueereAtofeiorresdraiwimfsio,AsSolsoiMenchmhAacmshpndearuchtaeiaeistMiicaaHspnrlvseaoetnnicuiiedrilfnhtdsa(SsdnlifcehetuNncuegeaemooabtmociarldrDtnuuot.le,sMeyeeisoenms;ud4MoorpcnoeMt.n6ifseuaffhrusa0tTwaroseleL.0omFrhnhtao7euNsoisdtfme)MApaumuUeci.ermhwtcno.mmwhsneouatMTpdeho.ttirrshrprfotaiSooaiihofi.tcaNongliamrcsNhifsmNrso,taaa,oauasLurtnIsndaHstteponucitmniueuuhlirrnhPuspdMardistecatotdppaynuyolnlhsoolylpgRunrtsysiwfrdyosdoieoHeaHWaeisi.ordlitiosponubcosbfssshgalomtmgtacptterTmodyoesuooutiorhacrsebcromnhdnaiyodne,fyygey-h-le,f.
479
480 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY VOL. 141
TERMINOLOGY OF GILL-ARCH basibranchial series in teleosts, asisoften the
ELEMENTS case, extends posteriorly beyond the paired
The following terms are applied to the fifth arch-elements and could be said to in-
endoskeletal gill-arch elements: basibran- clude basibranchials 4-6, without the im-
chial, hypobranchial, ceratobranchial, epi- plication that a sixth branchial arch some-
branchial, infrapharyngobranchial, and su- how is involved.
prapharyngobranchial. The dermal elements Thus defined, the term "basibranchial"
most conveniently are called tooth plates, or would be applicable to a cartilaginous part
gillrakers, and named according to which of a larger element, with or without ossifica-
elements support them, with the exception tion centers, to a center of ossification, and
of the plates supported by the fifth cerato- coincidentally to an independent element
branchials, called lower pharyngeal tooth (one separated from adjoining elements by
plates, and those associated with the infra- articular surfaces). Independent elementsare
pharyngobranchials, called upper pharyngeal bestreferred to as "copulae," with a notation
tooth plates. In many cases these tooth of which basibranchials they contain. Thus
plates are fused with their endoskeletal sup- the basibranchial series in teleosts may be
ports, and the compound bones are called, said ordinarilyto be formed ofthree copulae:
respectively: lower and upper "pharyngeals" one (composed of the basihyal) and two
-or "pharyngeal bones," in some cases also others, the anterior (copula 1-3) usually in-
'infrapharyngeals" and "suprapharyngeals," cluding three ossified basibranchials, and the
or "hypopharyngeals" and 'epipharyngeals." posterior (copula 4-5, or 4-6) consisting of
a single cartilage representing two or three
BASIBRANCHIALS
non-independent basibranchials.
The term basibranchial never has been
consistently and logically applied. Some BASIBRANCHIAL TOOTH PLATES
authors have used it to designate the sepa- The median tooth plates can bedesignated
rate elements of the basibranchial complex according to which basibranchial elements
of bony and cartilaginous structures; others, support them. The condition of many primi-
only for the ossifications present; others, for tiveteleosts (e.g.,Elops, pl. 79, fig. 3; Nelson,
theoretical subdivisions, cartilaginous or os- 1968a, fig. 1) includes a basihyal tooth plate
sified, that they believed were parts of some (BHP), a basibranchial tooth plate 1-3
compound element, which they believed con- (BP 1-3), and basibranchial tooth plate
tained more than one basibranchial; and 4 (B4P). In other teleosts (e.g., Osteoglossum)
still other authors, erroneously to describe a large tooth plate (BPH-3) extends from
the dermal tooth plates that overlie the the tip of the basihyal to the posterior end
actual endoskeletal basibranchials. It is evi- of the third basibranchial. The paired tooth
dent that one term cannot be used in all plates, generally associated with particular
these senses and still retain much meaning. arches, are given no special terminology.
Accordingly, basibranchial is given here a
more restricted definition, namely, the me- HYPOBRANCHIALS, CERATOBRANCHIALS,
dian part of the gill-arch endoskeleton, os- AND EPIBRANCHIALS
sified or not, that primitively lies between There is confusion in the literature con-
successive paired arch-elements, regardless cerning the terms epihyal, ceratohyal, and
of the nature of the subdivision in the basi- hypohyal, and the homology of the skeletal
branchial series. For the teleostomes, estab- elements to which these terms are ap-
lished usage dictates that a basibranchial be plied. Some authors (e.g., Harder, 1964,
given the name or number of the paired p. 27; Harrington, 1955, p. 282; Jordan,
arch-elements behind it (for elasmobranchs, 1905, p. 45; McAllister, 1968, pp. 5, 6;
see below). For teleostomes, this dictum Mujib, 1967, p. 1318; Norden, 1961, p. 688;
fairly reasonably can be applied to the Starks, 1901) have recognized the following
definition given above, with the under- paired, endoskeletal hyoid elements in tele-
standing that each basibranchial probably is ostomes: hyomandibula, symplectic, inter-
not a simple derivative of the paired arch- hyal (stylohyal), epihyal, ceratohyal, and
elements. Thus, the posterior element of the one or two hypohyals. Anatomists, however,
1969 NELSON: GILL ARCHES OF FISHES 481
have long almost universally agreed that the suprabranchial" and its shortened version
elements supporting the branchiostegal rays "suprabranchial" to replace the term "supra-
of teleostomes do not include an epihyal (a pharyngobranchial" and reintroduced the
serial homologue of the epibranchials) and in original "pharyngobranchial" to replace "in-
general have agreed that the hyomandibula frapharyngobranchial." These suggested ter-
either wholly or in part is the real epihyal minological changes are not without merit,
(Allis, 1915, p. 620; 1928; Bertmar, 1959, but at the present time important questions
p. 327; Daget, 1964, pp. 293-296; De Beer, remain to be answered concerning the homo-
1937, p. 415; Devillers, 1958, p. 612; Edge- logy of these elements in the different fish
worth, 1926; 1935, pp. 85-88; Fox, 1963, groups (Nelson, 1968b). The present paper,
p. 804; Gaupp, 1905, p. 904; Goodrich, 1930, therefore, follows the usual terminology of
p. 405; Gregory, 1933, pp. 80-81; Holmgren, infrapharyngobranchials and suprapharyngo-
1943, p. 85; Jarvik, 1954, p. 75; Parker, branchials (dating from van Wijhe, 1882,
1882, p. 165; Rauther, 1940, p. 443; Regan, p. 225).
1923, p. 450; Schmalhausen, 1950, pp. 440- Confusion about the homology of these
441). Those authors accepting this homology elements has been reviewed elsewhere (Nel-
had to find another name for the ventral son, 1968b). It may be added here, however,
arch-element that previously had been called that the tooth plates underlying the infra-
the epihyal. Usually this problem was solved pharyngobranchials frequently are confused
by calling it a "posterior ceratohyal," and with and consequently called (infra)pharyn-
callingtheold ceratohyal an "anteriorcerato- gobranchials. Partlyforthisreasonsuccessive
hyal," the assumption being that the cerato- infrapharyngobranchials are said by some
hyal ossifies in two parts. The problem with authors, erroneously, to be secondarilyfused.
this solution is that in teleostomes these two So far as known to the writer, purely endo-
parts possibly are the serial homologues of skeletal, ossified gill-arch elements (or ossifi-
the ceratobranchials and hypobranchials (see cation centers) rarely, if ever, become secon-
below, and also Daget and d'Aubenton, darily fused in Recent fishes. Even with the
1957; Nelson, 1968b). Ifso, thepaired, hyoid- involvement of the dermal skeleton, fusion
arch elements below the interhyal require re- between compound (dermal and endoskele-
naming, with the "hypohyals" given an tal) ossified elements of successive arches
entirely new name (the alternative, to re- probably never occurs, despite many state-
name the ceratobranchials and hypobran- ments to the contrary in the literature.
chials, as was done by Daget and d'Auben-
ton, 1957; see also d'Aubenton, 1961, p. 152; TERMINOLOGY OF CURRENT LITERATURE
Daget, 1964, p. 292, who used the names In the present paper an attempt is made
"ceratobranchial sup&rieur," and "ceratobran- to deal with the scattered literature on gill
chial inftrieur," respectively, would seem to arches in fishes, but little effort is directed
be an additional and needless complication). toward correcting, or even indicating, the
In the present paper aneutral terminology is individual inaccuracies in most papers deal-
applied. The ventral, paired, hyoid arch- ing with this subject. It may be mentioned
elements here are divided into medial and here that, with respect to gill-arch structure,
lateral groups, the medial in teleosts being anatomical details in the literature even of
subdivided into dorsal (which could be called recentdateseldomcanbe takenatfacevalue.
dorsohyal) andventral (ventrohyal) elements Tendingtobeespecially unreliablearepapers
(the so-called hypohyals), the lateral in most in which the dermal skeleton is not treated
teleostomes including anterior (anterohyal) as a quasi-independent system, in which
and posterior (posterohyal) elements (the so- fusions are said to occur between ossified,
called ceratohyals, or ceratohyal and epi- endoskeletal elements, or in which the
hyal). cartilaginous features of the endoskeleton
are neither studied nor described.
INFRAPHARYNGOBRANCHIALS AND
Confusion of dermal with endoskeletal ele-
SUPRAPHARYNGOBRANCHIALS
ments has caused the most difficulty. The
Jollie (1962, pp. 92, 96), for the purpose basihyal tooth plate has been called a basi-
of brevity, introduced the terms "pharyngo- hyal (Devillers, 1958, fig. 423); the basi-
482 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY VOL. 141
branchial and adjacent tooth plates have and Norman (1957, p. 217), asbeing 'united"
been termed basibranchials (Gunther and in certain Perciformes (butsee Nelson, 1967c,
Deckert, 1959, figs. 15, 16; Monod, 1963, p. 293).
figs. 39, 40; Le Danois, 1967, pls. 13, 14); As far as is known to the present writer,
thefourth basibranchial tooth plate, a fourth ossified pharyngobranchials of successive
basibranchial (Dineen and Stokely, 1954, arches never actually fuse, however inti-
fig. 8); the lower pharyngeal tooth plates mately associated they might become. With-
have been called fifth ceratobranchials out careful examination, however, it is diffi-
(Beebe, 1935a, fig. 6; 1935b, fig. 18; Beebe culttodistinguish them as separateelements,
and Crane, 1936, figs. 31, 40; 1937a, figs. 6, and they are often portrayed in an indistinct
13; 1937b, fig. 15); in lower teleosts (ostari- way (Rosen, 1962, fig. 12) or even are ex-
ophysans, osteoglossomorphs, elopomorphs, plicitly stated to include fused elements
and clupeomorphs), the often independent throughout groups in which they (in this
upper pharyngeal tooth plates have been case the third infrapharyngobranchial and
called pharyngobranchials (Mayhew, 1924, fourth upperpharyngeal tooth plate) actually
fig. 10; Joshi and Bal, 1953, fig. 8; Kirchoff, are invariably separate (cf. table 1; and
1958, fig. 27; and Kampf, 1961, fig. 30); and Liem, 1963, figs. 76-87).
inhigherteleosts thefourth upper pharyngeal Pharyngobranchials in some cases are re-
plate almost invariably has been called a duced and lost as independent elements. In
fourth pharyngobranchial. Rarely does the such cases one or more of the remaining
confusion operate in the reverse direction pharyngobranchials often are interpreted as
with toothed compound (endoskeletal and compound, including two or more pharyngo-
dermal) bones being considered purely branchials (Rosen, 1962, fig. 13). Possibly,
dermal (e.g., by Muijb, 1967, pp. 1318, inundergoingreduction thefourth pharyngo-
1320). branchial in some cases fails to separate from
A lesser source of confusion has been the the third as a distinct rudiment (see below),
possibility of fusion between endoskeletal but if so, it does not mean that the ossified
gill-arch elements of different arches. Thus portion of pharyngobranchial 3 is in any
Goodrich (1930, p. 441, also Car&usu, 1952, sense compound. In such cases the rudimen-
p. 68), implying fusion between successive tary nature of the fourth pharyngobranchial,
pharyngobranchials, stated that "thepharyn- when it occurs as a separate element in re-
gobranchials of the last three arches similarly lated forms, renders almost meaningless
any
form a toothed 'os pharyngeus superior."' In statement about its fusing with anything
the same context Gunther (1880, p. 59) re- else, and in the opinion of the present writer
ferred to them as being "more or less con- it is best considered simply absent as an
fluent," and both Regan (1913, pp. 131-132) independent element.
TABLE 1
SUMMARY OF SOME GILL-ARCH ELEMENTSG IN SOME TROPICAL FRESH-WATER FISHES
UP
BHP H3P LP 1 2 3 4 5
Nandus, Pristolepis x x x - x x T
Afronandus, Monocirrhus, Polycentropsis, Polycentrus - - x - x x T
Badis, Ophiocephalus x x - x x T
Luciocephalus - - x - x x T
Anabas, Betta, Ctenopoma, Macropodus, Osphronemus,
Trichogaster - - x - x x T
aBHP, tooth plates supported by basihyal: H3P, tooth plates supported by third hypobranchials; LP, tooth
plates supported by fifth ceratobranchials; UP 1-5, tooth plates supported by infrapharyngobranchials; T, tooth
plateanindependent element; x, tooth platefused withitsendoskeletal support; -, tooth platesabsent.
1969 NELSON: GILL ARCHES OF FISHES 483
ABBREVIATIONS USED IN TEXT LDA, lateral dorsal aorta
FIGURES AND PLATES LG, ligament
LJ, margin of lowerjaw
AF1-4, afferent arteries 1-4
LP, lowerpharyngeal tooth plates
AD, anterodorsal articularsurface
LR, lateral ridge
AV, anteroventral articular surface
M, MD, MV, in thehyoidarch, themostanterior
B1-6, basibranchials 1-6
oftheventral paired elements
B1+P, B2+P, B3+P, tooth plate fused with
MDA, median dorsal aorta
basibranchial 1, 2, or 3
MR, medianridge
B4P, tooth plate supported by basibranchial 4
MRL, medial toothrowoftheleftinfrapharyngo-
B6P, tooth plates supported by basibranchial 6
branchial 3
BH, basihyal
01, 04, calcifications corresponding in position
BH+P, tooth plate fused with basihyal
toinfrapharyngobranchials 1 and 4
BHP, tooth plate supported by basihyal
P, dermal plate
BP, basibranchial tooth plates
PA, papillae
BPI-3, tooth plate overlying basibranchials 1-3
PAR, pulmonary artery
BPH-3, tooth plate overlying basihyal and basi-
PB, perichondral bone
branchials 1-3
PH, "prehyoid' cartilages
BS, basibranchial series
PHI, pharyngobranchial 1
C, efferent arterial canal
PHH, pharyngohyal
C1-5, ceratobranchials 1-5
PS, posterior articular surface
C5+P, tooth plate fused with ceratobranchial 5
Q, quadrate
CA, cartilage
R, basibranchial rudiment
CH, ceratohyal
R1-2, right pharyngobranchials of arches 1-2
DP, dorsal process
S, sublingual bone
DS, dorsal articularsurface
S1-2, suprapharyngobranchials 1-2
E1-5, epibranchials 1-5
SD, SL, SR, SV, dorsal, left, right, or ventral
E1+P, E2+P, E3+P, tooth plate fused with
sublingual
epibranchial 1, 2, or 3
TP, paired tooth plates
EA1-4, efferent arteries 1-4
TP1-4, tooth plates of the paired series ofarches
EH, epihyal
1-4
FI-5, articular facets of paired elements of
TP2A, TP2P, anterior and posterior partsof the
arches 1-5
paired tooth plate series of arch 2
GR, gillrakers
TPI+2, tooth plates probably derived by fusion
H1-4, hypobranchials 1-4
of elements of arches 1-2
H1+P, H2+P, H3+P, tooth plate fused with
TP1+1, TP2+2, TP3+3, median tooth plates
hypobranchial 1, 2, or 3
derived by fusion of paired elements of arches
HCH, paired elements possibly including equiva-
1, 2, or3
lents of hypohyal and ceratohyal
TPH, tooth plates of the paired series of the
HH, hypohyal
hyoid arch
11-4, infrapharyngobranchials 1-4
TPM, tooth plates of the paired series of the
I2+P, I3+P, tooth platefusedwithinfrapharyn- mandibular arch
gobranchial 2 or 3 TR, transverse ridge
13+UP4, fourth upper pharyngeal tooth plate U, urohyal
fused with infrapharyngobranchial 3 UJ, margin ofupper jaw
L, LA, LP, in the hyoid arch, the paired element UP, upperpharyngeal toothplates
or elements normally supporting the branchio- UPI, 4, 5, upperpharyngealtoothplates 1, 4, or5
stegal rays VA, ventral aorta
L1-2, left pharyngobranchial of arches 1-2 VS, ventral articular surface