sixty million years of evolution. part one: family botiidae - Travaux

Travaux du Musium National d'Histoire Naturelle
((Grigore Antipaw
Vol. XLIV
pp. 309-333
0 2002
SIXTY MILLION YEARS OF EVOLUTION. PART ONE: FAMILY
BOTIIDAE (PISCES: OSTARIOPHYSI: COBITOIDEA)*
TEODOR T. NALBANT
Motto: "The taxonomy must be an applied phylogeny"
Emile G. Racovitza (1910)
Abstract. A new classsification of cobitoid fishes is proposed based on their morphology, evolution and
phylogeny. The evolution of cobitoid loaches began in the late Palaeocene, about 60 millions years ago
from a catostomid ancestor and very soon the stem was divided in two lineages: the botiids lineage and
the nemacheilid-cobitid lineage. In early Eocene the botiids stem was divided in vaillantellin clade and
in botiin clade, both evolving slowly till present. The vaillantellins have only south east Asian genus
Vaillantella with 3-4 species. The botiids are divided in the tribe Leptobotiini with 3 east Asian genera
(Leptobotia, Parabotia and Sinibotia) and the tribe Botiini with 3 south and south-east Asian genera
(Hymenophysa, Yasuhikotakia and Botia).
Rtsumt. On propose une nouvelle classification des taxons appartenant au groupe Cobitoidae,
classification baste sur des caractkres morphologiques, sur I'tvolution et sur la phylogenie du groupe.
L' tvolution a commenct env. 60 millions d'anntes et depuis le groupe s'est djvist en deux lignes
Cvolutives: celle des fam.illes Botiidae et Namacheilidae - Cobitidae. Pendant 1'Eocene suptrieur les
Botiides se sont divistes i leur tour en Vaillantellinae et en Botiinae. Les premitres ont un seul genre
sud-est asiatique (Vaillantella) qui comprend 3-4 espkces. La famille Botiidae comprend 3 genres est
asiatiques (Leptobotia, Parabotia et Sinibotia) et Botiini avec 3 genres sud-est et sud asiatiques
(Hymenophysa, Yasuhikotakia et Botia).
Key words: evolution of Botiidae, phylogeny, classification (Pisces: Cobitoidea).
The botiids are one of the beloved group of fishes for the aquarists and also
amateur ichthyologists, due to their beautiful and attractive colours and interesting
shape of body. Their habits in aquarium made them as good companions for other
fishes such as barbs, charachoids, small catfishes etc. Unfortunately, their
systhematics was, for a long time, a controversial subject of discussion of many
students.Therefore, the main aim of this contribution is to arrange their systematics
based on their phylogeny. In this way, more than 30 of inner and outer
morphological characters of botiids and their out-groups (nemacheilids, cobitids etc)
were analysed and polarised. The results are herein presented.
MATERIAL AND METHODS
More than 300 cobitoid species (botiids, nemacheilids, and cobitids) were
examined (measured, counted for meristics, dissected, cleared and stained etc.) in
order to understand the phylogenetic value of each character. On the other hand, I
evaluated the evolution and phylogeny of lineages on the basis of earth
transformation (evolution of tectonic plates and hydrographic network), fossils
(especially suborbital spines), climatic changes and magnetic reversals.
* This paper is dedicated to the memory of Emile G. Racovitza, the forerunner of phylogenetical
systemactics.

310 TEODOR T. NALBANT
Most of the specimens came from the large loach collection "Biiniirescu-
Nalbant" (formerly ISBB), now in the National Museum of Natural History
"Grigore Antipa" Bucharest. Other specimens were obtained on loan from different
institutions (see abbreviations), such as CAS, USNM, AMNH, MNHN, BMNH,
MHNG, SMF, NRMS, ZMA, ZIAN, ZMB, NHMW, ZMC, etc. Other material was
examined and studied directly in the collections of Chonbuk National University,
Chonju (South Korea), Aristotelian University of Thessaloniki (Greece), Hacettepe
University, Ankara (Turkey), Institute of Fisheries and Aquarium, Vama (Bulgaria).
Abbreviations:
AMNH: American Museum of Natural History, New York, N. Y.; BMNH: Natural History
Museum, London; CAS: California Academy of Sciences, San Francisco, Ca; ISBB: Institutul de
Biologie Bucurevti (now in MTNB, see below); MHNG: MusCum d'Histoire Naturelle, Genhe;
MNHN: Museum National d'Histoire Naturelle, Paris; NHMW: Naturhistorisches Museum, Wien;
MINB: Muzeul National de Istorie Naturals "Grigore Antipa", Bucurevti; NRMS: Natural History
Museum, Stockholm; SMF: Senckenberg Museum u. Forschungsinstitut, Frankfurt am Main; USNM:
National Museum of Natural History, Washington, D. C.; ZIAN: Zoologiceskii Institut, Akademii
Nauk, Sankt Petersburg; ZMA: Zoological Museum, Amsterdam; ZMB: Zoologisches Museum der
Humboldt Universitat, Berlin; ZMC: Zoologisk Museum, Copenhague.
The different biogeographical concepts and unities presented in this paper are
used almost in the same sense as defined by Biinlrescu (1990, 1992, 1995).
However, there are several differences between us concerning the arrangement of
the genera and species in biogeographical unities or in evolution of the lineages.
The drawings, excepting a few, are made by the author and by Dr Rudolf
F. Mayer (Madrid) based on parts or dissected specimens, or, entire individuals.
Characters. The polarization of each feature is presented after its definition.
The nodes are characterised by their initial evolution, sometimes a few
reversals being included, plus a new specialized character.
1. Four rostral barbels (two pairs) each pair united at their base in a fleshy
mobile pad; two maxillo-mandibular barbels (one pair ) in the comer of the mouth.
Plesiomorphy, 0.
2. Four rostal barbels (two pairs) separated at their base and two maxillo-
mandibular barbels (one pair) in the corner of the mouth. Apomorphy, 1.
3. Two rostral barbels (one pair), two maxillar barbels (one pair) on each part
of upper jaw and two maxillo-mandibular barbels (one pair) in each comer of the
mouth.Autapomorphy, 2.
4. Mobile suborbital spine (ect-ethmoid bone) present. Apomorphy, 1.
5. No mobile suborbital spine (plesiomorphy, 0). In vaillantellins the absence
of this spine is secondary, representing an autapomorphy, 2.
6. Suborbital spine simple (plesiomorphy, 0). In some Bicanestrinia (Cobitis)
species the loss of the one thorn is secondary, representing an autapomorphy, 2.
7. Suborbital spine with the two thoms superimposed. Plesiomorphy, 0.
8. Suborbital spine with the two thoms in horizontal plan. Apomorphy, 1.
9. Both lips simple with no mental lobes. Plesiomorphy, 0.
10. Both lips papillous or furrowed, with well developed mental lobes,
sometimes as buttons or a fourth or fifth pair of barbel. Apomorphy, 1.
1 1. Body generally high (deep bodied species). Plesiomorphy, 0.

SIXTY MILLION YEARS OF EVOLUTION: BOTIIDAE (PISCES) 31 1
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12. Body generally low, some time serpentifom. Apomomorphy, 1.
13. Dorsal fin rays with a normal number of branched' rays, i.e. 6-16.
Plesiomorphy, 0.
14. Dorsal fin with more than 30 branched rays. Apomorphy, 1.
15. Dorsal fin placed generally in the midlle of the body. Plesiomorphy, 0.
16. Dorsal fin placed well behind the middle of the body, sometimes its last
rays above the insertion of anal fin. Apomorphy, 1.
17. Sexual dimorphism absent or not evident. Plesiomorphy, 0.
18. Sexual dimorphism present, expressed in males as osseous plates at the
base of pectoral rays or buttons on lateral parts of head and fins. Apomorphy, 1.
19. Sexual dimorphism expressed in males as a swell on each part of the body.
Autapomorphy, 2.
20. Lateral line complete and axial. Plesiomorphy, 0.
21. Lateral line incomplete, in most cobitid loaches not exceending the length
of pectorals. Apomorphy, 1.
22. Scales present on the whole body.Plesiomorphy, 0.
23. Body partially covered by scales.Apomorphy, 1.
24. Body completely nacked. Autapomorphy, 2.
25. Scales generally elongate. Plesiomorphy, 0.
26. Scales generally round. Apomorphy, 1.
27. Scales with a very large focal zone. Apomorphy, 1.
28. Body, sides of the head (sometimes on vertex) scalled. Apomorphy, 1.
29. Caudal fin well forked. Plesiomorphy, 0.
30. Caudal fin truncate or slightly rounded. Apomorphy, 1.
3 1. Stomach syphonal. Plesiomorphy, 0.
32. Stomach straight. Apomorphy, 1.
33. Long intestine with a few loops. Plesiomorphy, 0.
34. Intestine extremely long with numerous loops. Autapomorphy, 2.
35. Short and straight intestine without loops. Apomorphy, 1.
36. Gas-bladder with two developed fibrous chambers, sometimes the first
covered partially, very rare completely, by osseous substance. Plesiomorphy, 0.
37. Gas-bladder with the first part formed by two chambers placed on each
part of the vertebral column, both united by a duct and both being covered by
osseous substance (including the duct). The second chamber fibrous, reduced to a
diverticle or well developed (see also Rendahl, 1933 b and Ramaswami, 1953).
Apomorphy, 1.
38. Gas-bladder with the first chamber unique covered completely by osseous
substance, the second one a short diverticle. Autapomorphy, 2.
A study of the skeletal and muscular structures of the scapular girdle of
Rendahl (1933 a) has shown that in leptobotiins there are 11 generalized characters
(i.e plesiomorphies) and only two specialized characters (i.e apomorphies). Among
the plesiomorphic features there are: scapula without eminentia glenoidalis, the
presence of a foramen coraco-cleithralis, the presence of a musculus abductor
superficialis (pectoral rays) and the musculus abductor radialis inserted on
coracoideum. According to Rendahl, in nemacheilids there are 8 plesiomorphies and
5 apomorphies, and in cobitids there are 4 plesiomorphies and 14 apomorphies.

312 TEODOR T. NALBANT
RESULTS
The evolution ofthe cobitoid lineage. Correlations with Earth physics and
climatic changes
Wu and al., 1981, have demonstrated, on the basis of osteological characters,
that the cobitoid loaches are undoubtely placed, toghether with gyrinocheilids, on
the same big lineage of the catostomid fishes, whereas the cyprinids and
homalopterids (i.e. balitorids) form another big lineage, the sister group of the
former. Already, in Eocene fossils of the suckers were largely known in east Asia
and especially in western North America (Cavender, 199 1, 1998).
Fossils of loaches (nemacheilids) were known from Oligocene, but these
cannot be surely ascribed to these fishes (Nalbant, 1963). The first undoubtely loach
remains, of a mid Miocene age, were found in central Asia, in Kirghistan (Lebedev,
1959) and in Kazakhstan along the west Mongolian border (Sytchevscaya, 1989).
These remains represent only suborbital spines, all belonging to the genus Cobitis.
According to these results, this genus was well defined at that time (mid Miocene)
and therefore we must consider that its evolution begun much earlier, possibly in the
early Oligocene, even in the late Eocene, probably from a misgumoid ancestor. If
so, the origin and evolution of nemacheilids begun in the upper part of Palaeocene.
The primitivest lineages of nemacheilids are those of actual genera Serpenticobitis
and Ellopostoma (see PI. 7).
Serpenticobitis retains a movable suborbital spine like in botiids but somewhat
modified, i.e. the two thorns being disposed in horizontal plan like in cobitids.The
roots of the four rostal barbels are well spaced like in all nemacheilids. Another
nemacheilid feature of Serpenticobitis is the arrangement of gas-bladder based on
two anterior encapsulated chambers united by a short duct and with a very reduced
fibrous posterior chamber (see P1. 12, fig. 2 and in Nalbant, 2001, the plate). Both of
these features came from the node b ( P1. 7, see the phylogenetic arrangement of
clades) with origin in the late Palaeocene or in early Eocene. The lineage of botiids is
the least as old as nemacheilid-cobitid lineage, at the end of Palaeocene, both stems
being originated in the same node (0) possibly placed sixty million years ago. I
consider that this represents the birth moment of the loach stem (Pl. 7).
A hypothetical primitive loach had a high and compressed body, relativelly
small eyes, body completely covered by small scales, two very close rostal barbels,
but during the evolution each of them were splitted in another supplementary barbel,
two maxillo-mandibular barbels, small inferior mouth, a nearly movable suborbital
spine (ect-ethmoidal bone), forked caudal fin, gas-bladder consisting of two fibrous
chambers, the anterior one globulous and the posterior one elongated, a syphonal
stomach with a long intestine, complete lateral line and no sexual dimorphism.
In early Eocene (node a) the botiid stem was splitted and its two lineages,
Vaillantellinae and Botiinae, evolved independently. The former, vaillantellins,
aquired three autapomorphies: they lost the possibility to use a movable suborbitar
spine, an exaggerated length of body and an exaggerated length of the dorsal fin,
with more than 50 branched rays. However, they retained a number of botiin
features (see Nalbant and BiinZrescu, 1977), i. e. the arrangement of four rostra1
barbels, complete lateral line, forked caudal fin, same type of gas-bladder, body
laterally compressed, not evident sexual dimorphism.
In his "An outline of Tertia~ypalaeogeography", Adams (1981: 221) pointed
out that "The Tertiary geographical, oceanographical, climatological, faunal and
floral changes which occurred this time, were considerable and closely interrelated.

SIXTY MILLION YEARS OF EVOLUTION: BOTlIDAE (PISCES) 313
In paleogeographical terms, Cenozoic history charts the movement of the continents
and the associated alterations in the ocean basins."
The Tertiary period begun with the late Cretacic major extinctions as a result
of a considerable climatic cooling associated with a severe sea drops. After the mid
Palaeocene (see PI. 7) both curves of sea surface temperature and mean sea level
increased.
The shape and size of continents were changed and the hydrogeographic
network was modified. During Palaeocene the magnetic reversals were reduced,
generally the reverse polarity periods were dominant. Perhaps, the cobitoid stem
was born during a change of polarity and then evolved slowly towards the Eocene
epoch. Although the bradytely of its evolution, the initial cobitoid stem was splitted
in two lineages, those of botiids and those of nemacheilid-cobitids, at the border
between Palaeocene and Eocene. In the early Eocene the botiid stem was splitted
from the node a into vaillantellin lineage and botiin lineage (see above node a). Both
of these lineages evolved slowly till present without major complications. However,
probably in the late Eocene the botiin lineage was divided in two directions of
evolution by changing the karyotype (see P1. 6): leptobotiins with normal diploid
species 2n = 50 - 52 and botiins with tetraploid species 2n = 98 - 100 (Suzuki and
Taki, 1996). The single leptobotiin tetraploid genus is Sinibotia. Even
morphologically it appears very close to the botiin genus Hymenophysa. However,
due to its complicate mouth mental lobes, quite simple gas-bladder and its east-
Asian geographical distribution, I consider Sinibotia to belong rather to leptobotiins
than to botiins. The changes of karyotype in botiid fishes at the end of Eocene
appear very possible because this period was characterised by a general cooling
process, a significant decreasing sea level, quite rapid changes in polarity, followed
by a major process of extinctions (see P1. 7). The cobitid stem was originated also
towards the late Eocene. Probably, this happened when India collided the Angarian
(Asian) shield. Other changes in hydrography of this new super-continent took place
and the new lineages of fishes were able to spread in different directions.
In Oligocene period the changes of polarity were equilibrated but a severe
drops of sea level made new extinctions. Perhaps this represents the moment of the
begining of spreading and diversification of all three cobitoid stems.
The Miocene is characterised by numerous and rapid changes of polarity and
after the mid part of the period, a general deterioration of clime took place, till
present. The general sea level decreased constantly (see Berggren and
Hollister, 1974 and 1977, Briggs, 1996). All three groups of cobitoid loaches
benefited by these physical modifications to spread and diversifying. Because that
the botiids are the oldest lineage, their different elements were not be able to spread
to much towards west. Genera Parabotia, Leptobotia and Sinibotia remained
distributed only in all tributaries of the Pacific slope, whereas Hymenoplzysa and
Yasuhikotakia are distributed in south-east Asia (including the big Sunda Islands)
and south Asia till the Indus drainage (genus Botia).
Neinacheilids and cobitids radiated in all freshwaters of Euro-Asiatic
continent, from the high Hymalayan rapids to the lowland lakes and rivers of the
same continents. It is very interesting that two cobitoids penetrated in the African
shield; a Cobitis species live in a few "oueds" in north-west Africa and a
nemacheilid fish is present in lake Tana, Ethiopia, north-east Africa.