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/-C
MORPHOLOGY, PHYLOGENY, BIOGEOGRAPHY
AND SYSTEMATICS OF PHOXINUS
(PISCES: CYPRINIDAE)
by
XING-YU CHEN
BONNER ZOOLOGISCHE MONOGRAPHIEN, Nr. 39
1996
ZOOLOGISCHES FORSCHUNGSINSTITUT
UND MUSEUM ALEXANDER KOENIG
BONN
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MORPHOLOGY, PHYLOGENY, BIOGEOGRAPHY
AND SYSTEMATICS OF PHOXINUS
(PISCES: CYPRINIDAE)
by
XING-YU CHEN
BONNER ZOOLOGISCHE MONOGRAPHIEN, Nr. 39
1996
Herausgeber:
ZOOLOGISCHES FORSCHUNGSINSTITUT
UND MUSEUM ALEXANDER KOENIG
BONN
© Biodiversity Heritage Library, http://www.biodiversitylibrary.org/; www.zoologicalbulletin.de; www.biologiezentrum.at
—
Die Deutsche Bibliothek CIP-Einheitsaufnahme
Chen, Xing-Yu:
Morphology, phylogeny, biogeography and systematics of Phoxinus (Pisces:
Cyprinidae) / Xing-Yu Chen. Hrsg.: Zoologisches Forschungsinstitut und
—
Museum Alexander Koenig, Bonn. Bonn: Zoologisches Forschungsinst. und
Museum Alexander Koenig, 1996
(Bonner zoologische Monographien Nr. 39)
;
ISBN 3-925382-42-9
NE: GT
To my mother, father, and Jing,
for their love and encouragement.
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CONTENTS
Page
Introduction 5
Acknowledgments 5
Methods 6
Material examined ; . 8
Historical review ofPhoxinus 12
Phylogenetic relationships ofPhoxinus and the related genera 22
Monophyly ofthe Hemitremian clade and its position in the family Cyprinidae 22
Analysis oftransformation series in the Hemitremian clade 26
Phylogenetic relationships ofthe Hemitremian clade 39
Discussion 43
.
Non-osteological morphology 44
External morphology 44
Intestine and gas bladder 61
,
Osteology 67
Neurocranium 67
Viscerocranium 95
Vertebral column 121
Pectoral girdle and fin 131
Phylogenetic relationships ofthe species ofPhoxinus 141
Phylogenetic relationships 141
Discussion on the phylogenetic relationships ofthe species ofPhoxinus 144
Biogeography ofPhoxinus 145
Taxonomy ofPhoxinus 150
Key to the species ofPhoxinus 153
Species accounts 154
Phoxinusphoxinus (Linnaeus) 154
Phoxinus brachyurus Berg 161
Phoxinus issykkulensis Berg 163
Phoxinus neogaeus Cope 166
Phoxinus cumberlandensis Starnes & Starnes 171
Phoxinus tennesseensis Starnes & Starnes 175
Phoxinus oreas (Cope) 179
Phoxinus eos (Cope) 183
Phoxinus erythrogaster (Rafinesque) 188
Abstract . 194
Literature Cited 196
Appendices 215
I. Data matrix I (for Hemitremians) 215
II. Data matrix II (forPhoxinus) 216
III. Transformation series used in the analysis ofphylogenetic relationships
within Phoxinus 217
IV. List ofabbreviations 225
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INTRODUCTION
Cyprinidae, the largestfreshwaterfishfamily, isdividedintotwo subfamilies (Cavender&
Coburn 1992) with 210 genera and 2,010 species (Nelson 1994). Phoxinus, belonging to
the subfamily Leuciscinae (Chen 1987b, Howes 1991, Cavender & Coburn 1992, Co-
burn & Cavender 1992), is a small sized genus (less than 100 mm in maximum standard
length in most species) with nine species, and is the only minnow genus occurring in both
North America and Eurasia. Some species ofthe genus are widely distributed, others are
restricted to small drainage areas. For instance, P. phoxinus is widespread in Europe and
Asia (Berg 1949, Banarescu 1964), whereas P. tennesseensis is found only from the up-
perTennessee Riverdrainage ofTennessee andVirginiaofUSA(Starnes & Jenkins 1988).
Since the type species ofPhoxinus, phoxinus, was described by Linnaeus in 1758 (as Cy-
prinusphoxinus), hundreds ofpapers and books related to the genus have been published.
Most ofthe literature is records of geographical distribution, or brief descriptions of the
species ofthe genus. Only a few of these deal with anatomy and phylogenetic relations-
hips ofthe species in the genus (e.g., Gasowska 1979, Joswiak 1980, Howes 1985). Du-
ring the last two centuries, the definition ofthe genus has been an open question, and its
content has changed. For instance, P. neogaeus has been placed in four different genera
{Phoxinus, Pfrille, Chrosomus, and Leuciscus) since it was described by Cope (1869) (in
Günther 1868). A similar situation is also present in otherPhoxinus species. The unstable
taxonomic status of the Phoxinus species resulted from lack of a clear definition of the
genus, andlackofcomprehensive comparisons amongPhoxinusspecies andbetweenPho-
xinus and other related genera. Joswiak (1980) correctly pointed out that this genus "is a
focus of controversy involving the relation between Palearctic and Nearctic cyprinids".
The situation has not been improved very much since then.
The present study was designed to review the genus Phoxinus, and to provide a hypo-
thesis of its relationships with other genera and among its species. This monograph in-
cludes seven sections. A historical review of Phoxinus is presented first, followed by a
phylogenetic analysis among Phoxinus and other genera; then I report the results from the
comparative morphological study among the species ofthe genus. Based on the data from
these studies, I analyze the phylogenetic relationships among the species ofPhoxinus and
discuss the biogeography ofthe genus. Then a classification of the genus is followed by
an account ofthe nine recognized species ofthe genus.
ACKNOWLEDGMENTS
The following individuals and institutions are acknowledged for their loans or donations
ofspecimens to this project: P. Banarescu (Institute ofBiology, Bucharesti, Romania), M.-
L. Bauchot (Museum National d'Histoire Naturelle, Paris), N.G. Bogutskaya (Zoological
Institute, Academy of Sciences, St.Petersburg, Russia), K. Busse (Zoologisches For-
schungsinstitut und Museum A. Koenig, Bonn), B.W. Coad (National Museum of Natu-
ral Sciences, Ottawa), F.B. Cross, E.O. Wiley and J.T. Collins (University of Kansas,
Lawrence, Kansas), W.N. Eschmeyer and D. Catania (California Academy of Sciences,
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San Francisco), D.A. Etnier (University ofTennessee, Knoxville), K.E. Härtel (Museum
of Comparative Zoology, Harvard University, Cambridge/USA), G. Howes (British Mu-
seum, Natural History, London), S.L. Jewett (Smithsonian Institution, Washington D.C.),
E.-J. Kang (Chonbuk National University, Chonbuk, Korea), S. Kimura (Mie University,
Japan), J.G. Lundberg (Duke University, Durham, North Carolina), G. Nelson (American
Museum of Natural History, New York), T.K. Paaver (Institute of Zoology and Botany,
Academia ofSciences, Tartu, Estonia), S. Schaefer (Academy ofNatural Sciences, Phila-
delphia), B. Schatti (Museum d'Histoire Naturelle, Geneva), K.D. Vasil'eva (Zoological
Museum, Moscow Lomonosov State University), H. Wilkens (Zoologisches Institut und
zoologisches Museum, Universität Hamburg), Y.-H. Xie (Institute of Freshwater Fishery
ofLiaoning Province, China).
The Division of Biology and the Museum ofNatural History at the University of Kansas
are acknowledged for their years of support during the course ofthis project and my gra-
duate study at the University of Kansas.
I am grateful to Prof. S.-Z. Li (Institute of Zoology, Academia Sinica, Beijing) and Dr.
H.-P. Schultze (Paläontologisch-geologisches Institut und Museum, Naturkundemuseum
der Humboldt Universität, Berlin) for their helps and suggestions during this project. I am
greatly indebted to Drs. G. Arratia (Paläontologisch-geologisches Institut und Museum,
Naturkundemuseum der Humboldt Universität, Berlin), E.O. Wiley, F.B. Cross, J.S. Ashe,
andL.C. Ferrington, Jr, (University ofKansas), M. Coburn (John Carroll University, Ohio)
for their critical review and many suggestions on the draft ofthe manuscript, and to Drs.
G. Arratia and C. R. Robbins (University of Kansas) who reviewed the final version of
the manuscript.
I thank many ichthyologists for their help to access the literature. I especially thank E.B.
Böhlke (Academy ofNatural Science ofPhiladelphia) for the communication on the date
of the original description of Phoxinus neogaeus. J. Chorn and K. Shaw (University of
Kansas) are acknowledged for preparing the X-ray photographs ofPhoxinus brachyurus.
This project was partially supported by the following scholarship and agencies atthe Uni-
versity of Kansas: the International Student Scholarship, the Department of Systematics
and Ecology, the Divisions ofIchthyology and Paleontology, the Panorama Society ofthe
Museum ofNatural History, and the laboratories ofDrs. E.K. Michaelis and M.L. Mich-
aelis.
METHODS
Data Collecting
I. Measurements
Measurements were taken with Dial Calipers reading to 0.1 mm, on the left side of the
specimens. Methods for measurements follow Hubbs & Lagler (1947, 1964), except the
following which were not defined by those authors:
Prepelvic length is the distance from end of the snout to the base of the left pelvic fin.
Intestine length is the straight length ofthe intestine. Because the intestine in Phoxinus is
coiled, it was removed from the body cavity, uncoiled, and then measured.
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Length ofanterior chamber ofgas bladder is the distance between the most anterior point
to the most posterior point ofthe anterior chamber.
Length ofposteriorchamberofgas bladderis the distancebetween the most anteriorpoint
to the most posterior point ofthe posterior chamber.
Mouth angle is the angle between the dorsal surface of the head and a plane along the
dorsal margin ofthe lowerjaw.
2. Counts
All counts (e.g., branchiostegal rays, fin-rays) were conducted with aWild Microscope or
a Zeiss Microscope. The methods for different counts are described as follows:
Number of rays of paired fins were counted following Hubbs & Lagler (1947, 1964).
Number of rays of the dorsal and anal fins consists of procurrent rays (rudimentary un-
branched and unsegmented rays) and principal rays of Hubbs & Lagler (1947, 1964).
Hereafter the principal rays are referred to "rays". All procurrent rays and rays are coun-
ted. Caudal fin-rays were counted as dorsal and ventral procurrent, and dorsal and ven-
tral principal rays.
All lateral line scales were counted. Cephalic lateral line pores were divided into six sec-
tions following Reno (1969), except the preoperculomandibularcanal which is divided in-
to two sections (mandibular and preopercular sections) in the species of Phoxinus (see
below). All pores in each section were counted.
Following Chen (1988b) and Chen & Arratia (1994), all primary lamellae were counted
as the total number of the primary lamella for each olfactory organ. No secondary la-
mellae are present on the primary lamellae in Phoxinus.
Number of gill rakers on the first gill arch were counted and considered as the number
of gill rakers ofthe specimen.
Number of vertebrae includes all vertebrae (from vertebra 1 to preural vertebra 1, ural
centra not included), and are divided into precaudal and caudal ones, according to May-
den (1989). The four vertebrae associated with the Weberian apparatus were counted as
four and included in the numberofprecaudal vertebrae. The count ofvertebrae was made
on cleared and double stained specimens and some radiographs.
3. Non-osteological and osteological morphology
Non-osteological morphology was studied from 75% alcohol preserved specimens with
the microscopes mentioned above. Tubercles and scales were studied also with Scanning
Electron Microscope (SEM).
Osteological features were studied on cleared and double stained specimens prepared fol-
lowing Dingerkus & Uhler (1977), and from radiographs of some specimens.
All measurements, counts, and non-osteological data were obtained from more than five
specimens for most species studied. In most cases, more than 15 specimens for each spe-
cies were studied. Whenever possible, more than three specimens of each species were
studied in order to collect the osteological data. In most Phoxinus species, a series ofdif-
ferent sex and size was studied.
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The illustrations were prepared using microscopes with camera lucida attachment. The
photographs were taken with either camera or SEM.
Terminology
Terms for different parts of the fish body follow Cross (1967). except for a few cases
mentioned in the text (e.g.. breast scales). Terms for different structures of the olfactory
organ follow Chen (1988b) and Chen & Arratia (1994). Terms for different structures of
the gas bladder follow Bond (1979).
Phylogenetic analyses
The phylogenetic analyses follow the cladistic methodology (Hennig 1966, Wiley 1981).
Polarities ofthetransformation series weredeterminedby outgroups comparisonfollowing
Maddison et al. (1984). Ontogenetic data were also used to determine the polarities of a
few transformation series though some disadvantages might be present in the ontogenetic
criterion in the polarity determinations (Mayden & Wiley 1992).
Because no well-supported hypotheses aboutthe sistergroup ofPhoxinus are available, the
relationship among Phoxinus and other closely related minnow genera (grouped as He-
mitremians herein) are reevaluated using the Exoglossin Clade of Coburn & Cavender
(1992) as the outgroups.
According to the result from the analysis ofthe relationships among Phoxinus and other
genera (see below), Lagowskiella, Rhynchocypris, and Eupallasella were treated as the
outgroups for the polarity determination of the transformation series in the phylogenetic
analysis among the species ofPhoxinus. 210 transformation series including non-osteolo-
gical and osteological characters were analyzed.
The character states (TS) are identified as 0. 1. 2. 3. or 4. among which 0 represents the
plesiomorphic state, whereas 1, 2, 3. and 4 correspond to the apomorphic ones. These
numbers are present in square brackets following the transformation series number (e.g..
TS 100 [0]. TS 100 [1]).
PAUP (version 3.0s) (Phylogenetic Analysis Using Parsimony) program (Swofford 1991)
was used to generate the phylogenetic hypotheses presented herein for both the Hemitre-
mian Clade and the species ofPhoxinus.
Abbreviations
A list of abbreviations used in the figures and text is given in appendix IV at the end of
the book.
MATERIAL EXAMINED
Forty-seven species of Cyprinidae were studied. The species are grouped as non-Phoxi-
nus species and Phoxinus species. The non-Phoxinus species are mainly used to evaluate
the relationships ofPhoxinus with other genera, and to compare with the species ofPho-
xinus.
