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The phylogenetic relationships of theelectric catfish family Malapteruridae(Teleostei: Siluroidei)Gordon J. Howes aa Department of Zoology, British Museum (Natural History),Cromwell Road, London, SW7 5BDVersion of record first published: 17 Feb 2007.

To cite this article: Gordon J. Howes (1985): The phylogenetic relationships of the electriccatfish family Malapteruridae (Teleostei: Siluroidei), Journal of Natural History, 19:1, 37-67

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J O U R N A L OF N A T U R A L H~STORY, 1985,19:37-67

The phylogenetic relationships of the electric catfish family Malapteruridae (Teleostei: Siluroidei)

G O R D O N J. HOWES

Department of Zoology, British Museum (Natural History), Cromwell Road, London SW7 5BD

(Accepted 7 February 1984)

Among siluroid fishes (catfishes), the Malapteruridae uniquely possess an electro- genic organ. Although much attention has been paid to the anatomy and physiology of the electric organ, little emphasis has been given to other anatomical characters, particularly with regard to their indicating phylogenetic relationships. Ten character complexes involving cranial bones, muscles, swimbladder connections and vertebral column are here analysed and compared with those of other siluroids. It is concluded that despite its obvious specializations (autapomorphies) the Malaptcruridac is basically a plesiomorphic group and that its relationships lie with some taxa belonging to the Old-World Siluridae. The Siluridae are thus a paraphyletic assemblage, with other included taxa having their close relationships with the Schilbeidae. The evolutionary potential for development of the electric organ is accounted for by the loss of a rigid connection between the pectoral girdle and the skull and the associated modification of anterior body musculature.

Introduction Of the thirty-one currently recognized families of catfishes (Order Siluriformes),

only those species comprising the family Malapteruridae possess an electric organ. This unique character has undoubtedly been known to African man since his earliest fishing activities. Indeed, if the pictogram has been correctly interpreted, then the first extant depiction of an electric catfish is that on the slate pallete of the pre-dynastic Egyptian ruler Na'rmer, c 3100BC (see Boulenger 1907, 398).

The electric catfish was first described for science by Forssk~l in 1775, mistakenly identified as Raja torpedo, then as Silurus electricus by Gmelin, 1789, and eventually being assigned its own genus, Malapterurus, by Lac~pdde in 1803.

Although four species of Malapterurus were recognized by early authors, it is now generally accepted that there are two, M. electricus (Gmelin); fig. 1, and M. microstoma Poll and Gosse 1969. Malapterurus etectricus has a widespread, Nilotic distribution and includes the three formerly recognized west African species. The species occurs over most of Central Africa, south to the Zambesi, but excludes the East Coast and Cape Provinces (sensu Roberts 1975). Malapterurus microstoma has a restricted, Zairean distribution (see Poll and Gosse 1969). There is a possibility, however, that M. electricus comprises two species (Sagua, pcrs. comm.), one of which has, at least, a Nigerian distribution.

Anatomical investigations of Malapterurus have focused principally on the electric organ, both from the morphological and functional points of view (e.g. Bilharz 1857,

¢~' 1985 The British Museum (Natural History)

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';.!:,i?; ' . % - ~ 2 ~ :.~: , ,~ ! ,L ,~ jZ~- : : ; : . . . . . . . . . . . . . - ~ . . . .

.

¢ S ~ z L ~

F~G. 1. Malapterurus electricus: drawing of a specimen from the Kaduna River, Nigeria. BMNH 1936.11.24:50. Scale, 20ram.

Johnels 1956, Bennett 1971). The swimbladder and its connections with the cranium have attracted the attention of several authors (Mfiller 1842, Sorenson 1884, Bridge and Haddon 1894, Chardon 1968), whilst the skeleton, musculature and visceral anatomy have been described in varying degrees by Bilharz (1857), CMand (1858), Kosckkaroff (1905), Regan (1911), Mahy (1970, 1974). Mahy (1974) gives historical summaries of the taxonomy and anatomy of Malapterurus.

Concerning the classification of Malapterurus, Gfinther (1864) was the first author to consider the systematic position of the taxon and assigned Malapterurus to his Stenobranchiae, a subfamily of the Siluridae. The subfamily was characterized by a short rayed dorsal fin (if present) placed on the 'abdominal' portion of the vertebral column, and gill membranes confluent with the isthmus. Included also in the Stenobranchiae were taxa now recognized as the families Mochokidae, Doradidae and Auchenipteridae.

Bridge and Haddon (1894) followed Gfinther's systematic placement and in comparing the Elastic Spring Apparatus (ESA) of the swimbladder of Malapterurus with other members of the Stenobranchiae found that of Malapterurus to more closely resemble the ESA of Synodontis than that of any other taxon. None the less, they pointed out that Malapterurus appeared to have the least modified form of ESA in any taxon known to possess the mechanism.

Only three authors appear to have seriously considered the phyletic relationships of MaIapterurus, namely Kosckkaroff (1905), Regan (1911) and Chardon (1968). Kosckkaroffpresents to what all intents and purposes is a cladogram based on cranial characters. These appear, however, for the most part to be symplesiomorphies. Nevertheless, Kosckkaroff places Malapterurus as the sister group to Clarias and recognizes as their sister-group Synodontis, Arius, Akysis, Silurus and Eutropius.

Regan (1911) stated that '... osteological characters indicate relationships to the Bagridae...'. Unfortunately, Regan did not enumerate these characters, listing instead what appear to be autapomorphies of the Malapteruridae.

Chardon's (1968) statements concerning malapterurid relationships are am- biguous. He finds possible relationships with the Siluridae, Bagridae and Pangasiidae, and his phylogram shows the Malapteruridae occupying a position somewhere between the Siluridae and Bagridae. Chardon erected the suborder Malapteruroidea to contain the Malapteruridae.

Both Regan and Chardon present a list of characters that define the Malapteruridae, viz:

1. Presence of an electrogenic organ. 2. Absence of a rayed dorsal fin and proximal pterygiophores.

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Phylogenetic relationships of the electric catfish family 39

3. Loose attachment of the pectoral girdle to the skull. (According to Chardon this is a primitive feature.)

4. Presence of an Elastic Spring Apparatus connecting the Weberian complex with the swimbladder.

5. An elongate posterior chamber to the swimbladder.

Regan (1911) lists, in addition, as specialized characters: (i) the absence of a 'pterygoid' (= ectopterygoid) and mesopterygoid (= entopterygoid) with the quadrate extending forward, external to the metapterygoid and meeting the tip of the premaxilla (ii) a strong lateral process of the sphenotic (iii) anterior compression and posterior depression of the cranium.

Chardon (1968) lists as additional specializations: (i) the reduction of the skeleton, but with closure of the posterior cranial fontanelle and hyper-development of the superficial ossification of the complex vertebrae, and (ii) the cranium partially covered by musculature.

It is not clear what Chardon means by 'faible development' of the skeleton unless he is alluding to supposed lack of supporting elements in the dorsal fin (see p. 45). Absence of a posterior cranial fontanelle and development of superficial ossification of the complex vertebra are common features amongst siluroids, which if they are derived features appear to have been developed independently in several lineages (see Howes 1983 a).

Of those characters enumerated by Regan and Chardon (listed above as 1-5), two can be considered autapomorphs, viz: the electrogenic organ and posterior chamber of the swimbladder. Nevertheless, there are features of the body musculature associated with the electric organ that appear synapomorphic with other taxa and so will be discussed below. A comparison of the swimbladder is included for sake of completeness.

Of the three remaining characters, degrees of specialization are present which indicate a closer relationship with the Siluridae and Schilbeidae than to any other group of catfishes. Evidence for this postulated relationship is derived from the cladistic analysis presented below. This methodology relies on extensive outgroup comparisons in order to make character polarity assignments. In this case 'outgroups' are considered to be all other siluroids and non-siluroid ostariophysans. The present classification of siluroids lacks any scheme of relationships; families have been recognized simply on the size of the 'morphological gap' and it is apparent that some families are not monophyletic groups (see Howes 1983a). It is only by applying the rigorous comparative treatment demanded by cladistic phylogenefic analysis that a 'natural' classification of catfishes can hopefully be achieved (Howes 1983 c).

Specimens examined The following are those specimens representing taxa cited in the text. Additionally,

many of the other specimens listed in Howes (1983 a & b) have been re-examined. All are BMNH specimens.

BAGRIDAE: Bagrus docmac 1969.3.3:10-11 (t50 mm SL); uncatalogued, 135 mm SL alizarin; uncatalogued, skeleton.

CETOPSIDAE: Paracetopsis minutus 1972.7.27:62942 (44 mm SL alizarin). CLARIIDAE: Allabenchel ys longicauda 1904.10.26:33 (skeleton); Clarias gariepinus

1907.12.2:1715-24 (64ram alizarin); 1982.4.13:3351-61 (135ram SL) C. liberiensis

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40 G.J. Howes

1902.11.12:131 (skeleton); Hetobranchus long!filis 1902.11.10:120-5 (48 and 57 mm S L alizarins).

DIPLOMYSTIDAE: Diplomystes papillosus 1889.11.14:33 (120 mm SL). HELOGENEIDAE: Helogenes marmoratus 1972.10.17:753-804 (63 and 75mm

alizarins). ICTALURIDAE: Ictaturusfurcatus 1948.8.6:221-28 (110 and 117 m SL alizarins);

I. melas 1982.11.10:525-6 (80 and 115 mm SL). LORICARIIDAE: Pterygoplichtys multiradiatus 1897.12.1:280 (skeleton). MALAPTERUR1DAE: Malapterurus electricus 1982.4.13:4798-801 (250 mm SL);

1982.4.13:3441 7 (40 and 54ram SL alizarins); uncatalogued (38 and 40mm SL alizarins); 1982.4.13:4796-7 (100 and 140 mm SL); 1863.6.16:1 (skeleton).

NEMATOGENYIDAE: Nematogenys inermis 1883.11.27:45-8 (240 mm SL); 49 (skeleton).

PANGASIIDAE: Pangasius sp. 1976.7.1:39 (94mm SL); P, sutchii uncatalogued (40 mm SL alizarin); P. buchanani 1889.2.1:2397-9 (140 mm SL).

PIMELODIDAE: Rhamdia hilarii 1879,9.10:17 (skeleton). SCHILBEIDAE: Ailia coila 1956.5.14:1-3 (alizarin); 1870.11.30:48 (skeleton);

Eutropichthys vacha 1891.11,30:162-9 (174ram SL); 170mm (skeleton); Eutropius niloticus uncatalogued (135mm alizarin; skeleton); Paraila congica 1975.6.20:592-3 (85 mm SL); Platytropius siamensis 1934.12.18:56 (195 mm SL); Physailia pellucida 1979.7.18:500 506 (66ram SL alizarin); Schilbe mystus 1982.4.13:32; 42-50 (103mm SL); uncatalogued (97, 115mm SL alizarins); Silonia silondia 1890.6.14:40 (radio- graphs); Proeutropiichthys taakree 1891.11.30:199 (skeleton); Siluranodon auritus 1907.12.2:1913 20 (126 mm SL alizarin); 1971.9,28:115 7 (100 mm SL); 1907.12.2:3764 (skeleton).

SILURIDAE: Clupiosorna 9orua 1889.2.1:2454 (radiographs); Hemisilurus heterorhynchus 1982.3.29:161-2 (radiographs); Hito taytayensis 1933.3.11:110-112 (115 & 165 mm SL); Kryptopterus bicirrhis 1982.3.20:163-7 (64 mm SL alizarin); Ompok pabo 1891.11.30:180-3 (203 mm S L); Silurichthys hasseltii 1970,9.3:178-82 (24 mm SL alizarin; 85mm SL); Siluroides hypophthalmus 1980.10.10:213 (radiograph); Silurus aristoleis 1970.9.24:319-328 (170ram SL); Silurus glanis uncatalogued (2 skeletons); Silurus triostegus 1920. 3, 3:168-76 (107 mm SL alizarin); Wallago attu 1889.9.26:48-51 (172ram SL); uncatalogued (skeleton).

TRICHOMYCTERIDAE: Trichomycterus cordovensii 1911.11.25:1-10 (31 mm SL alizarin).

Figure abbreviations AAP Adductor arcus palatini muscle AD Arrector dorsalis muscle AM Adductor mandibulae muscle

AS(AP)

ASD

AO AV Cc Cd

Adductor superficialis muscle ( = ?Adductor profundus)

Dorsal section of adductor superficialis

Adductor operculi muscle Arrector ventralis muscle Cartilaginous cup of swimbladder Cartilaginous disc

Ccm Cross-commissure C1 Cleithrum Clp Cleithral process Co Coracoid Col Coracoid lamina Cos Coracoid spur DA Deep adductor muscle DO Oilatator operculi muscle Ds Dermis Ect Ectopterygoid Ent Entopterygoid EO Electrogenic organ

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Phylogenetic relationships of the electric catfish family 41

Epo Epioccipital Op Operculum EPX Epaxialis muscle Or Orbitosphenoid EPXd divisions of deep epaxialis OS Orbital cartilage EPXt insertion tendon of outer Pop Preoperculum

epaxialis bundle Pr Proximal radial Es Extrascapular Pte Pterotic ET Extensor lemaculi muscle Ptt Posttemporal Exo Exoccipital Q Quadrate

RT Retractor tentaculi muscle Fr Frontal Sb Swimbladder HS Horizontal septum Sbc Swimbladder capsule Hy Hyomandibula SH Sternohyoideus muscle ICA lnfracarinalis anterior So Supraoccipital

muscle Sp Sphenotic LAP Levator arcus palatini muscle Spn Spinal nerve Le Lateral ethmoid Spn(e) Spinal (electric) nerve Li Liver SPMa, b, c Divisions of the epaxialis

(swimbladder) muscles Sy Symplectic Llc Lateral line canal

(ossified) Lln Lateral line nerve Ts LO Levator operculi muscle Tsl Mc Mesocoracoid V Me Mesethmoid Vp Met Metapterygoid Vp4a Mx Maxilla Ns Neural spine (numbered) Vp4p Ol Ohliquus inferior muscle

Transcapular Transcapular ligament Vertebra (numbered) Vertebral parapophysis 4th vertebral parapophysis

(anterior) 4th vertebral parapophysis

(posterior)

Character analysis The characters presented for analysis are those considered by Regan (1911) and

Chardon (1968) to define the Malapteruridae; listed above as 1-5. In addition, the suspensorium, infraorbitals and cranial muscles are considered.

The electric organ and body musculature No other siluroid is known to possess an electrogenic organ, although many, if not

all siluroids possess electroreceptive organs (see Szabo 1974). Some early investigators of the electric organ (e.g. Fritsch 1887, Bridge 1904) thought it to have been derived from the integument. Other workers (Ballowitz 1899, Stuart and Kamp 1934) believed that, as in other electrogenic teleosts, the organ was a derivative of muscle tissue. In order to settle the argument Johnels (1956) studied the ontogeny of the electric organ and concluded that it was of myoblastic origin. Johnels' evidence rested primarily on the mode of attachment of the organ to the pectoral girdle and the configuration of the surrounding body musculature. Johnels suggested that the electric organ is derived from part of the anterior musculature, and that the organ '... replaces closely in position the missing parts of the musculature, and is fixed by means of a structure identical with a muscular tendon to the very part of the shoulder girdle where the

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42 G.J . Howes

missing muscles ought to have inserted, if developed'. The question that Johnels leaves unanswered, however, is; which are those muscles missing?

In siluroids, the usual condition of the anterior body wall musculature may be illustrated by referring to Ictalurus (fig. 2 A). The division of the epaxialis and hypaxialis is indicated laterally by the horizontal septum. Anteriorly, the epaxialis continues forward above the swimbladder to insert on the cranium, whilst the hypaxialis differentiates into lateral and medial subsections. The dorsal layer (obliquus superioris sensu Winterbottom 1974) curves upward and grades into the epaxialis muscle postero- dorsally to the lateral cutaneous area. The ventral part of the muscle (obliquus inferioris sensu Winterbottom 1974) runs forward below the swimbladder and inserts on the pectoral girdle (coracoid lamina). In Ictalurus, the obliquus inferioris is further divided, the dorsal segments inserting on the cleithrum whilst the ventral inserts on to the coracoid. The ventral body muscle, the infracarinalis anterior, is feebly differentiated from the obliquus inferior and inserts musculously on to the coracoid.

The pattern of this body musculature differs in the Siluridae and Schilbeidae. In taxa of these families the anterior portion of the obliquus superioris separates into a distinct segment that lies lateral to, and intermeshes only dorsally with the epaxialis (fig. ;2 B). The obliquus inferioris is a thin muscle that inserts on to the coracoid by intermeshing with the fibres of the pectoral fin musculature, the arrector ventralis. The infracarinalis anterior is weakly developed or absent, the latter condition occurring in Silurichthys.

In the Clariidae, there is also a distinct segment of the obliquus superioris which runs well forward, beneath the pterotic, to insert on the epioccipital (fig. 2 C). Parentheti- cally, it should be pointed out that Nawar (1954) is incorrect in asserting that the epioccipital is absent in Clarias; the element is present although it is reduced.

In the Malapteruridae, fibres of the epaxialis run almost horizontally to insert along the posterior cranial border (fig. 3). The horizontal myoseptum is less clearly defined than in other siluroids owing to the diagonal strands of tendinous tissue that run from bundles of hypaxial muscle fibres and intermesh with the outer epaxial fibres. That part of the hypaxialis which in other siluroids curves upward (the obliquus superioris) is, in Malapterurus, directed antero-ventrally to insert on the lateral portion of the coracoid. That this muscle segment is indeed the obliquus superioris and not part of the inferioris is borne out by (i) the position of the 'electric' nerve, originating from a ganglion of the 2nd and 3rd spinal nerves, and which in other investigated siluroids passes between the obliquus superioris and inferioris (ii) the position of the lateral line nerve which lies exposed across the surface of the obliquus superioris and which in other siluroids exits from between the epaxialis and obliquus superior.

The obliquus inferioris in Malapterurus is similar to that of the Siluridae in overall configuration except that it is much reduced in comparison and its attachment to the coracoid is via a thin tendinous sheet that covers the protruding liver lobe; see fig. 4 and below, p. 45. The injracarinalis anterior is well-differentiated from the obliquus inferioris and inserts at the coracoid symphysis via a long, strong tendon; see fig. 4, and plate II, fig. 2 in Bilharz I857.

Thus, although Malapterurus possesses the full complement of anterior body muscles they are highly modified. Johnels' (1956) contention that the electric organ is attached to the pectoral girdle via a muscular tendon is not borne out by this study. In contrast, I find the organ to be weakly attached by connective tissue. Nevertheless, I would agree with Johnels' hypothesis that the electric organ is derived from muscle tissue and add that this tissue is the superficial part of the obliquus inferioris. Johnels'

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Phylogenetic relationships of the electric catfish family 43

HS EPX OS LIn /

~ ~ / S b

A ~,Ciii':!~?il ......... ~,

LS EPX OI .QS \ ~ " ~ Sb

~ ~ ~ ~ /

~ X ~ s -~v

C

J '\ ~ , OI Li

F1o. 2. Anterior body wall musculature of A, Ictalurus meIas; B, Silurichthys hasseItii; C, Clarias 9ariepinus. Scale, 10mm.

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LIn Ds

G. J. Howes

Epx Sb Li LO DO AM

\ Cl

EO

FIG. 3.

I OI OS Ica I I Spn(e) Malapterurus electricus, anterior body wall musculature. Scale, 5 mm.

I I FIG. 4. Malapterurus electricus, ventral view of body musculature. The left tendinous sheet of

the obliquus inferioris and the left ventral liver lobe have been excised to show the insertion tendon of the infracarinalis anterior muscle. Scale, 5 ram.

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Phylogenetic relationships of the electric catfish family 45

evidence of myoblastic origin depended partly on the 'deficiency' of the anterior body musculature. This 'deficiency' is due to a reduced obliquus inferioris; its outer part having been modified as electrogenic tissue (the organ is much thickened where it overlies the muscle). To 'replace' the outer portion of the obliquus inferioris, the obliquus superioris appears to have shifted from the upper to the lower part of the pectoral girdle, with a concomitant shift of the spinal nerve that innervates the obliquus inferioris outer layer the electric organ and exposure of the entire anterior length of the lateral line nerve. Further aspects of the electric organ are discussed on p. 65.

Whilst there is no other siluroid known to have this particular arrangement of the anterior body musculature, there are similar, although less derived, modifications in silurid and schilbeid taxa. In these groups the anterior musculature is thin, the anterior part of the obliquus superioris is a separate segment extending in some taxa as far forward as the 'posttemporal'; see fig. 2 B.

The position of the liver in Malapterurus deserves some comment at this point since it is associated with the configuration of the infracarinalis anterior muscle. It is well known that in siluroids the liver has a position atypical for teleosts (see Weber 1891, Bridge and Haddon 1894, Dutta 1924 and Hora 1937). Bridge and Haddon(1894) contended that the liver in catfishes was displaced by the lateral growth of the swimbladder and its surrounding capsule. Hora (1937) attributed the displacement to the shortening of the body cavity. Irrespective of our ignorance of factors leading to modifications of the organ, the fact remains that the anterior liver lobes in Malapterurus have been produced ventrally to such an extent that each curves around the infracarinalis anterior muscle bundle of its respective side, contacting one another in the midline (fig. 4). The liver lobes are also ventrally produced in the Plotosidae but they do not protrude below the musculature. Only in Silurus aristotelis is there anything approaching the malapterurid condition, in Silurus the lobes are pressed so firmly into the infracarinalis as to make a distinct depression in the muscles, from which they are separated by a tendinous sheet.

Absence of a dorsal fin There is no dorsal fin in the Malapteruridae. Hyrtl (1859) first noticed an internal

rudimentary spine. Gfinther (1864, 219) placed emphasis on this feature when allocating Malapterurus to his subfamily Stenobranchiae. Giinther wrote that Malapterurus ' ... belongs to this subfamily, and not to the following (Protopterodes)... by the rudimentary internal spine, which rests in the cleft of the neural process of the first vertebra, and clearly shows that if the dorsal fin had been developed, it would have been quite in the forepart of the trunk, far in advance of the ventral fins'.

The lack of a dorsal fin is not unusual amongst siluroids. It is absent in members of the Siluridae, Schilbeidae and Trichomycteridae. In members of the two former families possessing a dorsal fin, it is invariably small, i.e. pauciradiate.

The dorsal fin is variably developed amongst siluroids. For example, in the Clariidae it extends along most of the dorsum and often is confluent with the caudal fin. In the Plotosidae, in addition to the short based dorsal fin, there is a second many- rayed fin similar to that of the Clariidae. In the Mochokidae, one genus Mochochus, possesses a second fully rayed, short-based dorsal fin.

In most siluroids the first and second dorsal fin spines are pungent, the former small, but the latter long and often serrated along both the anterior and posterior margins. The articulation of the first and second spines is often complex and incorporates a locking mechanism to retain the second spine in an erect position. The locking

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46 G.J. Howes

mechanism, which has been explained by Alexander (1965), depends on the first and second proximal radials having broadened dorsal surfaces and on the support of nuchal plates which according to Alexander (1965) are derived from supraneurals.

In the Diplomystidae, generally considered the plesiomorphic group of siluroids, there are well-developed dorsal fin spines, proximal radials and every indication that a fin spine locking mechanism is present (Alexander 1965, 115). The Diplomystidae differs from most other families possessing an elaborate dorsal fin in that the anterior proximal radials articulate with the sixth and seventh neural spines rather than with the fourth and fifth. Nevertheless, the fourth and fifth neural spines of Diplornystes are angled backwards almost to touch the anterior proximal radials (see Alexander 1965, fig. 9). The long space between the fourth neural spine and the cranium is occupied principally by the expanded third neural spine and a supraneural (see Fink and Fink 1981, fig. 17). In 'advanced' siluroids the space between the cranium and the 4th neural spine has all but disappeared; in Malapterurus electricus the 3rd neural spine is sometimes represented by a slight process on the neural complex (see Chardon 1968, fig. 156). Thus, there is a long gap between the third and fifth spines. Between the fifth and sixth neural spines and articulating with the bifurcation of the fifth, is a narrow lamellate bone with a cartilaginous base (fig. 5). It is this element that Hyrtl (1859) described as a rudimentary interneural spine. It is not figured by Chardon (1968), but appears in Mahy's (1974) figure 18 A, although it is not labelled. The position of this bone suggests that it is a proximal radial.

In the Siluridae and Schilbeidae there is also a long gap between the cranium and 1st proximal radial, and some variability as to which neural spine contacts the 1st proximal radial; viz:

Siluridae: in Silurus glanis and S. aristotelis there are two proximal radials lying between the sixth and eighth neural spines; in Ompok pabo there are from three to five proximal radials, the first and second ligamentously united distally, the first articulating with the bifurcation of the seventh neural spine (fig. 6); in Kryptopterus bicirrhis there is a single proximal radial between the sixth and seventh neural spines which articulates with a rudimentary dorsal fin spine; in Hito taytayensis there are three radials, the first lying between the sixth and seventh neural spines; in Hemisilurus hypophthalmus where the dorsal fin is lacking, the two specimens examined show

~-Pr Vp4 " ~ V p 6

I

F~G. 5. Malapterurus electricus, complex vertebra, in lateral view. Scale, 1 mm.

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Phylogenetic relationships of the electric catfish family 47

f

~Ns7

I I

7

b

FIG. 6. Dorsal fin supports of (above) Hemisilurus heterorhynchus and (below), Ompok pabo. Scales, 10 mm. Drawn from radiographs, and shown in median sagittal section; radials are stippled.

different conditions; in one there are two reduced proximal radials (fig. 6), and in the other a single radial articulating with the seventh neural spine.

Schilbeidae: in Schilbe, Eutropius and Platytropius all of which have well-developed dorsal fin spines, the fourth neural spine is elongate and strongly bifid (fig. 7). The antero-dorsal part of the first proximal radial lies between the bifurcation of the fourth spine but its distal tip contacts the reduced fifth neural spine. Eutropichthys also has a well-developed dorsal fin spine, but unlike other schilbeids, the first and second proximal radials lie between the ninth and tenth neural spines. In Physailia, where the dorsal fin is absent, there is a single rudimentary proximal radial between the fifth and sixth neural spine, reminiscent of that in the Malapteruridae. In Siluranodon where the dorsal fin spine is weak, the proximal radial is broad and situated between the fourth, to which it is sutured, and the fifth neural spines. In Clupiosoma the dorsal fin arrangement is unlike that of any other schilbeid, having well-developed nuchal plates and a strong articulation of the first proximal radial with the fourth neural spine. According to Tilak (1964) in Ailia, the second to fifth neural spines are bifid, the proximal radial articulating with the fifth neural spine. In Silonia, the fourth to sixth neural spines are bifid with the proximal radial contacting the fourth neural spine.

To summarize: in the Siluridae, the first proximal radial lies between either the sixth and seventh or the seventh and eighth neural spines, whereas in the Schilbeidae, the radial lies between the fourth and fifth, or fifth and sixth spine (exceptionally in Eutropichthys between the ninth and tenth).

In the Clariidae, the fourth neural spine contacts the supraoccipital leaving a long gap between it and the fifth neural spine. The first proximal radial lies between the

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FI6. 7.

Ns9 ~Ns6

Ns7 UNs11

Dorsal fin supports shown in lateral view of(above) Schilbe mystus and (below), Clarias 9ariepinus. Neural spines 7-9 in Schilbe and 8-10 in Clarias are bifurcate.

seventh and eighth neural spines. In Clarias all the neural spines anterior to the first proximal radial and the one or two following it are bifid (fig. 7). In the majority of siluroids the anterior eight or nine neural spines are bifid. Bifurcation of the neural spines seems an essential feature in providing a rigid support for the (often) expanded proximal radials and associated musculature. The fact that in clariids the anterior neural spines retain their bifurcation although not actually supporting radials, whereas, apart from the last one or two, those associated with the dorsal fin elements are not bifid, suggests loss of the anterior parts of the 'original' dorsal fin. The anterior one or two dorsal fin rays may well be remnants of the posterior portion of the original dorsal fin, coupled as they are with bifid neural spines, in which case they represent the last few rays of the 'original' fin. The elongate dorsal fin in clariids is undoubtedly a de novo development, the origin of which is, as yet, unclear.

It seems a well-founded assumption that the dorsal fin in the Malapteruridae has been lost and that such is the case in those silurid and schilbeid taxa where it is also lacking (see Fink and Fink 1981,342). Absence of a dorsal fin in some members of the Trichomycteridae is also considered to be loss. Trichomycterid dorsal fins have different characteristics to those of other siluroids. Usually, in these fishes the dorsal fin lies posteriorly, its origin is above the 24th or 25th vertebra. Baskin (1973) hypothesized that this posterior position was derived. I concur with this suggestion, although it seems more likely that the posterior shift was not from an anteriorly placed fin, such as occurs in the Diplomystidae and most other siluroids but from a centrally placed fin such as occurs in the Nematogenyidae and Helogenidae. In these two latter families the dorsal fin originates in the middle of the dorsum, above the 10th-14th vertebrae. I suggest that

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Phylogenetic relationships of the electric catfish family 49

the Nematogenyidae and Helogenidae exhibit the plesiomorphic siluroid dorsal fin position. In favour of this hypothesis I advance the observations that, (1) the position of the dorsal fin equates with that in non-siluroid ostariophysans that have dorsal fins; (2) the lack of pungent spines in the dorsal fin and do not have an expansion of the anterior spine bases; (3) the proximal radials rudimentary; (4) only the anterior neural spine, be it the fourth or fifth in Trichomycteridae, Nematogenyidae and Helogeneidae is bifid and supports the tendinous part of the supracarinalis anterior muscle instead of a bony element; the plesiomorphic condition in ostariophysans is for the anterior neural spine to support the medial myoseptum.

Also to be noted in the context of dorsal fin position is the peculiar arrangement in loricarioids where the first proximal radial lies anterior to the seventh neural spine. It is the 10th~0th neural spines that are bifid, whereas none of those anterior to the seventh show any sign of bifurcation. This arrangement suggests a backward progression of the dorsal fin from the plesiomorphic nematogenyid condition.

The arrangement of the neural spines in the Diplomystidae where the fourth spine is not, or is barely, in contact with the first proximal radial suggests an 'intermediate' stage in the anterior progression of the dorsal fin elements. The ultimate stage is one where the first radial is supported totally by the fourth neural spine, the condition in the majority of siluroids possessing highly developed spine locking mechanisms. It would seem, therefore, that this condition is synapomorphic for the Diplomystidae and other siluroids, with the exception of the Loricarioidei (sensu Howes 1983b) and the Helogenediae, which retain the primitive dorsal fin arrangement, or else a separately derived condition.

The pectoral girdle, its muscles and attachments to the cranium Bridge and Haddon (1894, 175), Regan (1911) and Chardon (1968) have all drawn

attention to the loose connection of the pectoral girdle with the cranium in Malapterurus. This is in contrast to the condition in the majority of siluroids where the union is a rigid one. Before commenting on the way the girdle is attached to the cranium (discussed under the 'posttemporal') there are other aspects of the girdle's osteology and myology that must be considered.

Although several authors have described the pectoral girdle and its musculature in various siluroids there has been no broad-based comparative analysis. The closest approach is that of Alexander (1965) who described the girdle of Diplomystes and compared it with a variety of Old and New World catfishes as well as with characoids. Tilak (1963) studied the siluroid girdle 'in relation to taxonomy'. Tilak's concept of a generalized siluroid pectoral girdle was, however, an amalgam of the features he had observed in only those taxa he studied. Brousseau (1978) made a detailed study of the osteo-myology and neurology of the ictalurid pectoral girdle. Fink and Fink's (1981) discussion of the siluroid girdle centred on its connections with the cramium (see below).

Accepting the Diplomystidae as representing the plesiomorphic type of siluroid girdle (see Alexander 1965), the following features are noteworthy in comparison with that of the Malapteruridae. In the Diplomystidae and also in the Nematogenyidae and Trichomycteridae, a medial cleithral lamina is absent, the cleithra are joined syndesmotically at their tips and are broadly divergent.

The medial face of the girdle has a large foramen formed dorsally by the horizontal cleithral lamina and ventrally by the vertical coracoid lamina. In most other siluroids there are well formed medial (horizontal) cleithral lamina with, usually, a long

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50 G.J. Howes

syndesmotic, or rarely, sutural symphysial connection (see Skelton 1981, fig. 17). There is no symphysial connection in the Malapteruridae, the cleithral lamina being widely divergent from one another. In no other siluroid investigated are the cleithra separated and this condition must be considered autapomorphic for the Malapteruridae.

The horizontal coracoid lamina in Malapterurus is broad and connected to its partner in the midline via a long dentate suture. This is the condition found in the majority of siluroids. In the Diplomystidae, Nematogenyidae, Helogeneidae and Trichomycteridae, a horizontal coracoid lamina is lacking. In the Siluridae the lamina is poorly developed and is connected anteriorly syndesmotically to its antimere. In Silurus there are, however, indications of a dentate border suggestive of a former suture.

Within the Schilbeidae there is some variability in the length and development of the coracoid suture. In Physailia the coracoids are sutured for only part of their lengths, whereas in Schilbe and Eutropius there is a strong dentate suture over their entire lengths. Tilak (1963) considered separation of the coracoids to be primitive, but Alexander (1965, 119) thought that it is possibly a secondarily derived condition, although he did not provide any evidence in support of this view. The widespread occurrence of a complete midline connection in siluroids suggest that this is the plesiomorphic condition. Moreover, the 'remnants' of a suture on the coracoid lamina of Silurus are indicative of secondary loss. Further evidence would be gained from ontogenetic series of Silurus.

In nearly all siluroids there is a spur of bone connecting the posterior part of the coracoid lamina with the medial ventral border of the cleithrum. Alexander (1965) referred to this as the coracoid abductor bridge'. The bridge serves to separate the arrector ventralis and arrector dorsalis muscles. It is absent in the Malapteruridae, Nematogenyidae and Trichomycteridae, where its absence is associated with a reduction of those muscles it normally separates (see below).

Pectoral musculature The nomenclature of pectoral musculature adopted here is that of Winterbottom

(1974). The pectoral fin muscles of siluroids are rather complex with, usually, several separate sections of the main abductor musculature present. The following brief description of the pectoral musculature encountered in most siluroids is based principally on that of Bagrus (Bagridae) and shown in fig. 8.

The sternohyoideus muscle covers a large part of the anterior surface of the medial, i.e. horizontal, cleithral lamina, often with fibres extending along the lateral border of the horizontal cleithral limb. A large muscle passes through the cleithral-coracoid foramen to insert on the ventro-lateral aspect of the pectoral spine boss. This muscle corresponds with Dubale and Rao's (1961) adductor superficialis, Alexander's (1965) extensor and Winterbottom's (1974) arrector dorsalis.

Lying ventro-medially another large muscle extends from the coracoid, passes through the mesocoracoid-coracoid arch and inserts on the dorsomedial aspect of the pectoral spine boss. This muscle corresponds to Dubale and Rao's (1961) adductor profundus, Alexander's (1965) 'adductor of the spine' and possibly to Winterbottom's (1974) adductor superficialis. Winterbottom, however, states that there is no insertion of the muscle on the marginal ray, and in siluroids the muscle may thus incorporate the adductor profimdus sensu Winterbottom.

A postero-dorsal portion of the adductor superficialis runs from the vertical lamina of the cleithrum, and from the mesocoracoid to insert on the dorsal surfaces of the radials and fin rays. This muscle appears to correspond with Dubale and Rao's (1961)

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Phylogenetic relationships of the electric catfish family 51

FIo. 8.

CI ~

C I p /

H

AD

/%///;:////Y/JJ~

AD

I I

AS / CO AV Pectoral girdle musculature of (above) Bagrus docmac in dorsal view, and (below)

Nematogenys inermis in medial view. Scales, 5 mm.

dilatator posterior, Alexander's (1965) 'adductor of rays' and incorporates Brousseau's (1978) 'deep adductor'.

Separated from the arrector dorsalis and adductor superficialis by a ventral process of the coracoid is a muscle that serves the ventral surfaces of the fin rays. This muscle corresponds to Dubale and Rao's (1961) abductor superficialis internus and externus, Alexander's (1965) 'abductor of rays', and Winterbottom's (1974) arrector ventralis.

In the Malapteruridae (fig. 9), the muscle arrangement outlined above is modified so that (1) the sternohyoideus covers the entire dorsal and lateral aspects of the cleithral lamina (2) there is no cleithral-coracoid foramen, the arrector ventralis being separated from the arrector dorsalis by a small vertical coracoid lamina (3) the arrector dorsalis is reduced in size and originates from the cleithral lamina just anterior to the mesocoraeoid.

Absence of a coracoid-cleithral foramen occurs also in the Nematogenyidae. In contrast to the condition in the Malapteruridae, however, the arrector dorsalis is a large muscle and extends along the cleithral wall well in advance of the mesocoracoid (fig. 9).

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FI~. 9.

G[

\ \Av

Pectoral girdle musculature of Malapterurus electricus in medial (above) and ventral (below) views. Scale, 5 ram.

In the Nematogenyidae, the lack of a cleithral-coracoid foramen is plesiomorphic since, as in the Diplomystidae and Trichomycteridae, there is no medial coracoid lamina (see above). In the Malapteruridae, the foramen appears to have been lost secondarily. Evidence to support this view is that, at the point of origin of the arrector dorsalis, the cleithrum is often foraminate or the bone is thinned.

The 'posttemporal' The difficulties concerning the homology of the so-called posttemporal in siluroids

have been commented upon by Lundberg (1975), Fink and Fink (1981) and Howes (1983 a). Evidence presented below suggests that the element in question is, indeed, the posttemporal.

In Malapterurus the 'posttemporal' is triangular shaped laterally, its upper part loosely articulated with the cranium. Regan (1911) in referring to its attachment comments '... the upper limb of the supracleithrum (here 'posttemporal') articulating in a socket between the posttemporal (here extrascapula) and the epiotic ...'. The socket

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Phylogenetic relationships of the electric catfish family 53

noted by Regan is formed by a notch in the posterior border of the pterotic and a slight lateral protrusion of the epioccipital (fig. 10).

It is not unusual in siluroids for an epioccipital process to contact or overlap the upper limb of the 'posttemporal'. In Bagrus the dorsolateral part of the epioccipital has a prominent process (fig. 10), and among the Pimelodidae, Rhamdia hilarii has a ventrolateral portion of the epioccipital formed into a process that overlaps the 'posttemporal' limb (fig. 10). Nevertheless, the notched border of the pterotic and dorsolateral process of the epioccipital in the Malapteruridae are features encountered otherwise only in the Siluridae (see Regan 1911, 560).

The usual condition of the 'posttemporal' in siluroids is for it to be firmly united with the posterior border of the cranium (the pterotic and/or epioccipital). In taxa where the 'posttemporal' is loosely attached to the skull, i.e. Malapteruridae, Siluridae, Schilbeidae, Diplomystidae, Bagridae (some taxa), and Helogeneidae, there is a ligamentous connection with principally the epioccipital but also with the pterotic (see condition in WaUago, fig. 10).

In the Malapteruridae, the ligament from the 'posttemporal' is also connected with thc cartilaginous bloc of the anterior ramus of the fourth parapophysis (see below p. 56 and fig. 12). With respect to its ligamentous attachment the 'posttemporal' in siluroids corresponds to that in other otophysans where the bone is also firmly united to the

E )o Es

/ ' Vp4 S

Ptt ~ ' / E p , o ~ / ~!ii i :,;i;!~::::.:

FIG. 10. Posttemporal articulation in A, Malapterurus electricus (posterior); B, Bagrus docmac (posterior); C, Rhamdia hilarii (dorsal) and D, Wallago attu (dorsal). Scale, 5 mm

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Fr

.~0 C

S

Ccm. )o

CI

FIG. 11.

LIc

Malapterurus electricus, posterior cranial region in dorsal view. Scale, 5 ram.

epioccipital via ligamentous tissue. Thus, if this ligamentous attachment to the epioccipital is a homologous feature, then the bone in siluroids must be considered a posttemporal.

From the configuration of the cranial sensory canals Lundberg (1975) reasoned that in siluroids the plate-like bone often found lying between the pterotic, epioccipital and supraoccipital is the posttemporal. Fink and Fink (1981) disagreed and regarded it as the extrascapular. In so doing, Fink and Fink noted that the extrascapular nature of the bone would be corroborated should it be found to be associated with a canal system representing the cross-commissure. Bamford (1948) pointed out the absence of a cross- commissure in siluroids--the parietal being absent--but considered that the remnants of the system were represented by pit line organs associated with the plate-like bone (Bamford's tabular). In Malapterurus there is an undoubted epidermal canal system which apparently represents the occipital cross-commissure (fig. 11). An epidermal extension of the pterotic canal passes latero-posteriorly across the face of the 'posttemporal'; it is joined by another epidermal canal emanating from the posterior pore of the plate-like bone. The united canals terminate in an epidermal pore above the posterior edge of the operculum. The association of the plate-like bone with the occipital canal and its link with the supratemporal canal indicates that the plate-like bone is in fact the extrascapular and that the loosely connected bone lying posteriorly and joining the cleithrum is the posttemporal.

The loose connection of the posttemporal with the cranium in the Malapteruridae and Siluridae is regarded as synapomorphic. Unlike other taxa where the posttemporal-cranial attachment is weak, the posttemporal is restrained only by

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Phylogenetic relationships of the electric catfish family 55

Vp4a S P M c SPMb Ptt

"//// ..,,, .... % . .... •

":; t r :~ / ~ C d

" ' ", ' X \Cc Vp4p

I ~a

~p

FIG. 12. The complex vertebra and its muscle and swimbladder associations in (above) Malapterurus electricus and (below) Silurus 9lanis, dorsal views. Scale, 10 mm.

ligamentous connections and its dorsal tip rises above the surrounding bones that form its 'socket'.

The medial arm of the posttemporal (transcapular) that connects the bone to the basioccipital has, in the Malapteruridae and Siluridae, a ligamentous connection. Such a connection is not unusual in siluroids and appears also as a prominent feature in schilbeids where in Ailia the transcapular is absent. Absence of the ligament appears to be a derived feature correlated with the loose articulation of the posttemporal with the cranium.

Further observations on the pectoral girdle are presented on p. 65.

Elastic spring apparatus of the swimbladder Malapterurus possesses an Elastic Spring Apparatus (ESA) associated with the

swimbladder. Bridge and Haddon (1894) give a detailed description of the mechanism. Alexander (1965) presents a concise account of the ESA, and Howes (1983 a) gives a summary of its distribution throughout the siluroids. In short, it is a mechanism whereby the distal tips of the anterior ramus of the fourth parapophyses are flexible and

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56 G.J . Howes

are attached to the tunica externa of the swimbladder. Protractor muscles connect the ramus with the cranium and their contraction serves to pulsate the swimbladder.

Alexander (1965) and Howes (1983a) conclude that the ESA has evolved independently in several lineages. Alexander's conclusion was based on functional hypotheses, Howes' similar conclusion was based on the numerous conflicting synapomorphies in those taxa possessing an ESA.

The ESA of the Malapteruridae appears to be a rather primitive form of the mechanism. The complex vertebra comprises five fused centra. The parapophysis of the fourth centrum has a narrowly triangular anterior ramus (the Mfillerian ramus, see Howes 1983 a, 26) the distal tip of which bears cartilaginous extensions. The ventral surface of the complex vertebra bears a deep superficial ossification (see Howes 1983 a, 28 for definition) which forms an aortic canal. The distal connections of the M/illerian ramus are complex. Between the tip of the dorsal part of the M/illerian ramus and the posttemporal lies a cartilaginous nodule which also contacts the epioccipital process (fig. 12). A ventral extension of the cartilaginous nodule curves latero-posteriorly to cup the antero-lateral part of the swimbladder (Cc, fig. 12). The ventral part of the Mfillerian ramus is formed into a cartilaginous disc and this attaches to the anterior wall of the swimbladder (Cd, fig. 12).

A thick protractor muscle connects the cranium with the M/illerian ramus. Bridge and Haddon (1894) show the muscle as a single element, but in fact it is more complex, comprising three sections, (1) a dorsal, superficial layer of fibres running from the posterior border and lip of the epioccipital to cover the M/illerian ramus (SPMa, fig. 12); (2) a deeper portion extending from the lower posterior face of the supraoccipital and inserting along the ventral margin of the Mtillerian ramus (SPMb, fig. 12); (3) a medial portion running diagonally from the lateral face of the fused third and fourth neural complex and inserting on the medial part of the M/illerian ramus (SPMc, fig. 12).

There has been no broad survey of siluroid swimbladder muscles so little can be said about their homologies. It appears likely that they are derived from epaxial musculature. Support for this assumption comes from the arrangement of the anterior epaxialis in the silurids, Silurus and Wallago. As in the Malapteruridae there is a division of the medial epaxial musculature. An outer segment runs from the epioccipital to insert on the anterior ramus of the fourth parapophysis; a medial segment runs from the neural complex and supraoccipital to insert along the medial face of the fourth parapophysis (EPXd. fig. 12).

In both the Siluridae and Schilbeidae the anterior ramus of the fourth parapophysis curves around the anterior wall of the swimbladder. In Silurus the anterior ramus is flexible and separated by a narrow space from the swimbladder wall. There is no complex division of the anterior epaxiatis in the schilbeid taxa examined and the anterior ramus is less flexible. Without comparative data on swimbladder muscles it cannot be said whether the similar configuration in the Siluridae and Malapteruridae is synapomorphic, but this appears likely.

Posterior chamber of the swimbladder In the Malapteruridae there is a long posterior chamber to the swimbladder. It is

broad, slightly depressed and extends as far posteriorly as the 16th to 18th vertebrae. The posterior chamber joins the anterior chamber via a wide neck, internally the posterior chamber is divided medially by a vertical septum.

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Phylogenetic relationships of the electric catfish family 57

Although a common feature of other otophysans, a two-chambered swimbladder is unusual amongst siluroids, occurring elsewhere only in the Pangasiidae and Ictaluridae.

In the Pangasiidae the posterior chamber is short, and somewhat flattened, divided by a vertical septum and containing vermiculate septa (see Bridge and Haddon 1894). The Ictaluridae contains two species possessing a two-chambered swimbladder, Ictalurusfurcatus and I. balsanus (see Lundberg 1970). Only I. ji~rcatus was available for examination in which the swimbladder comprises approximately equal-sized chambers divided by a narrow constriction; septa are absent from both chambers.

Unlike the swimbladder in malapterurids and pangasiids, that ofictalurids appears to be of simple construction and greatly resembles that of characoids and cyprinoids. The malapterurid and pangasiid swimbladder is both flattened and transversely extended with complex septal divisions. It may be that the ictalurid swimbladder represents a plesiomorphic siluroid condition, but it seems certain that the malap- terurid and pangasiid swimbladder is specialized. In view of synapomorphies relating the malapterurids with non-pangasiid taxa an independent derivation of this swimbladder type is assumed, and the respective conditions in malapterurids and pangasiids are regarded as autapomorphic.

Suspensorium Regan (1911) claimed that the ecto- and entopterygoids are absent in the

Malapteruridae. Howes (1983a) commented on the difficulties of identifying the palato-quadrate elements in siluroids. These difficulties are resolved in part from a study of the malapterurid condition.

Mahy (1974, fig. 14) depicts the hyomandibular arch ofMalapterurus electricus and M. microstoma. However, Mahy's interpretation of the elements constituting the arch differs substantially from mine.

In a small specimen ofM. electricus (40 mm SL), the hyomandibula is quite distinct dorsally from the metapterygoid (fig. 13). There is a long anterior process of the hyomandibula that extends along the dorsal border of the metapterygoid, but the posterior border of the metapterygoid is not free and is fused with the hyomandibula. Mahy (1974, fig. 14) clearly shows a suture between the metapterygoid and the hyomandibula, yet in his diagram of M. microstoma he depicts a large cartilaginous zone between the bones.

The quadrate in all my specimens is not the shape shown by Mahy. The anterior border of the quadrate curves almost at right angles to the articular surface of the bone. In the specimen illustrated (40 mm SL) there is a foramen in the anterior border, in other specimens there are two or three foramina or at least a fretting of the bone (see fig. 13). The anterior medial face of the quadrate is thickened and a distinct vein of bone marks the edge of this thickening. The thickened part of the quadrate articulates with the broad entopterygoid (identified by Mahy as the ectopterygoid). Between the quadrate, the hyomandibula and the preoperculum lies a well-developed symplectic. Mahy shows a sensory canal running through the quadrate; this is obviously the preopercular canal, but he has failed to show the suture between the quadrate and preoperculum. Mahy (1974, fig. 14) identifies in M. electricus the anterior part of the quadrate as the ectopterygoid but fails to note the suture between the quadrate and entopterygoid, the latter bone not being mentioned. In M. microstoma however, Mahy incorrectly identifies the entopterygoid as the ectopterygoid.

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/ \ Met Ent

P

Sy ~ Q ~

E n t ? I I

Fie. 13. Suspensorium of Malapterurus electricus. Above (left), lateral view of the entire arch and (right) medial view of anterior elements of a specimen 40 mm SL. Below, medial view of anterior elements of a specimen 55 mm SL. Scale, 3 mm.

FIG. 14.

Me

Le__

Pmx Ux

Pal

Position of the palatine in Malapterurus electricus. Scale, 1 ram.

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Phylogenetic relationships of the electric catfish family 59

In some specimens a small bone lies in the connective tissue between the anterior pterygoid elements and the lateral ethmoid (fig. 13). Mahy (1974, fig. 6) labels this bone as a prevomer. It corresponds to the element discussed by Howes (1983 a, 31) in certain pimelodids and identified as a sesamoid ossification or a dermopalatine.

In discussing the interpretation of the siluroid pterygoid elements (Howes 1983 a) the possibility was raised that what has been interpreted as the anterior extension of the hyomandibula is in fact the metapterygoid. That view is given weight by the condition in Malapterurus where the dorsal part of the metapterygoid is a distinct element, but the lower part is fused to the hyomandibula and forms the 'hyomandibula' extension.

Work in progress on an ontogenetic series of Corydoras paleatus (Family: Callichthyidae) also suggests that the metapterygoid and the hyomandibula originate from a single endochondral anlage. The presence in Malapterurus of an anterior foramen in the quadrate, the thickening of that area and the articulation of the dorsal surface of the 'quadrate' with the entopterygoid are features that indicate the anterior part of the quadrate is in fact, a fused (or undifferentiated) ectopterygoid. Regan's (1911) statement to the effect that the quadrate 'extends forward external to the metaptery- goid' is incorrect in the sense that the quadrate extension lies laterally to the entopterygoid.

The palatine in Malapterurus is a small bone with a posterior facet that articulates with the antero-lateral portion of the lateral ethmoid (fig. 14). Unlike the condition in most other siluroids the bone is directed toward the midline so that its anterior portion lies in front of the lateral ethmoid. The statement of Fink and Fink (1981, 319) that 'In siluroids the palatine extends posterior to its articulation with the lateral ethmoid ...' holds for the majority of siluroids, but there are several exceptions. In Silurus, Kryptopterus and Ompok (all Siluridae) and Physailia (Schilbeidae), the palatine is small and only partially ossified, lying anterior to the lateral ethmoid (see Juge 1899, Gosline 1975, 22). In the Loricariidae the palatine is generally large and abuts upon the leading edge of the lateral ethmoid (see Howes 1983 b, figs 16-18). This is also the case in the majority of Trichomycteridae (Baskin 1973). In these families, however, the palatine is either rod-shaped with flattened tips, or is broad and flat. In the plesiomorphic Diplomystidae, the palatine had a medially directed posterior stem with a broad flat part lying anterior to the lateral ethmoid. Gosline (1975, 12 13) gives a concise description of the palatine and its attachments. Whilst he acknowledges the complexity of the diplomystid palatine, Gosline refrains from judging it to be an advanced or primitive condition. The close resemblance of the anterior part of the palatine and its relationships with the lateral ethmoid to that of the Nematogenyidae, Loricariidae and Astroblepidae (a group of taxa recognized as monophyletic on other grounds; see Howes 1983 b) leave one in no doubt that it is a derived feature. The retention of the posterior stem of the palatine in the Diplomystidae is considered plesiomorphic, since it is commonly developed in the majority of siluroids and other otophysans. On grounds of commonality, the plesiomorphic siluroid palatine is regarded as being rod-shaped and articulating with part of, or the entire lateral ethmoid border. I view the anteriorly placed, truncated palatine of the Malapteruridae and Siluridae as a synapomorphy.

Frontal and sphenotic The frontal of Malapterurus has an excessively narrow dorsal surface and is directed

sharply ventrad to contact the obito- and pterosphenoids. That part of the frontal bearing the postero-lateral canal is extended laterally and curved anteriorly (figs 11 & 15). The anterior extension comprises only the bony canal, and its tip supports a ring of

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5

A

13

3 I

FIG. 15.

G

2

Infraorbitals (numbered) of A, Malapterurus electricus; B, Schilbe mystus; C, Silurus gtanis. Scale, 10 ram.

connective tissue encircling the eyeball. The curved border of the frontal serves as a site of origin for the adductor mandihulae muscles (see Stix 1956, 60 and below, p. 62).

Mahy (1974) incorrectly identifies the anterior extension of the frontal as part of the pterosphenoid but the line he shows as a suture between the 'pterosphenoid' and the frontal is merely the edge of the frontal canal. Mahy does not indicate the very marked midline suture of the frontal bones and thus shows the two actually separate frontals as a single element.

The sphenotic also is produced laterally and juxtaposed to the extended part of the frontal canal so that together they form a thick, laterally curved stem of bone (figs 11 & 15).

The only other siluroid known to me in which the frontals develop a similar configuration to Malapterurus is Ageneiosus (Family Ageneiosidae). In this genus the

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Phylogenetic relationships of the electric catfish family 61

frontal canal also extends laterally and curves forward. Unlike Malapterurus, the curvature is acute rather than semi-circular and the association of the frontal with the sphenotic is not intimate because the sphenotic is not extended laterally.

One of the characters Regan (1911) uses to define the Malapteruridae is '... sphenotic sends out a strong lateral process to above the eye'. Regan, had, however, obviously confused the sphenotic with the frontal (it is virtually impossible to discern the suture between the bones on the dry skeleton Regan used). The relative length of the sphenotic in Malapterurus is exceeded only by that in some members of the Siluridae and Schilbeidae. In the silurid genera Silurus, Wallago and Kryptopterus the sphenotic extends so far anteriorly that it contacts the lateral ethmoid. Although Tilak (1963, 437) considered this a primitive character, it is obviously synapomorphic for those taxa in which it occurs, given its absence in other siluroids and ostariophysan outgroups.

Occipital region and cranial excavation The supraoccipital of Malapterurus has a strong median ridge and a slight posterior

crest. A supraoccipital crest is uncommon in siluroids where in the majority of taxa the bone is triangular, flat and extends posteriorly to meet the first nuchal plate. In the Siluridae, Schilbeidae, most Bagridae, Nematogenyidae and Diplomystidae, there is a supraoccipital crest which in some taxa is a short, vertical posterior process. A crest is most likely a plesiomorphic feature as it is widespread throughout otophysans, and indeed, teleosts. Alexander (1965, 125) regards the small crest in Malapterurus as a rudiment of the supraoccipital process which in many siluroids extends backward to contact the first nuchal plate.

The excavation of the postcranial region in the Malapteruridae, commented upon by Regan (1911) and Chardon (1968), appears to be a derived feature. 'Excavation' refers to the depression of the supraoccipital, posterior part of the frontal, pterotic and epioccipital. A similar concavity in these elements occurs in the Siluridae and Schilbeidae. Tilak (1963), erroneously remarks that there is practically no excavation of the occipital region of the skull in the Siluridae.

In the Siluridae and Schilbeidae, the cranial depression is filled by the anterior continuation of the epaxiaIis musculature, whereas in the Malapteruridae, the excavation provides the site of origin for the enlarged adductor mandibulae muscles (see p. 62). As in the majority of siluroids the epaxialis of Malapterurus inserts along the posterior border of the cranium; see for example, Stix 1956, figs 10 & 11.

Thus, although sharing with the Siluridae and Schilbeidae an excavated cranial surface, the Malapteruridae lacks the derived feature of epaxialis intrusion. Whether, in the Malapteruridae, the epaxialis insertion along the posterior cranial border is plesiomorphic, or whether it is a secondary reduction due to expansion of the adductor mandibulae musculature is unresolved.

Infraorbital bones In the Malapteruridae, the infraorbitals are reduced to ossifications around the

laterosensory canal, a common condition amongst siluroids. The first infraorbital is anteriorly bifurcate with terminal pores. The gap between the terminal pores of all the infraorbitals is connected to a dermal tube that opens as a lateral pore. The posterior border of the third infraorbital is fastened by a thick ligamentous band to the coronoid process of the dentary (fig. 15 A). A similar ligature occurs in the Siluridae and Schilbeidae. In Silurus, the third infraorbital is elongate and both it and the fourth infraorbital are firmly fastened to the coronoid process (fig. 15 C). In Wallago the

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second infraorbital is widened and contacts the premaxilla, whilst the third infraorbital extends posteriorly to the level of the articulation of the lower jaw. Firm attachment of the infraorbitals to any part of the lower jaw is absent in other siluroids investigated and it is assumed to be synapomorphic for the Malapteruridae, Siluridae and Schilbeidae.

Cranial muscles As compared with other siluroids (see Howes 1983 a), the Malapteruridae has a

primitive arrangement of the cranial and hyoid musculature. Three features are, however, derived: (1) the extensive development of the adductor mandibulae complex (2) a reduction in size of the levator arcus palatini, and (3) the configuration of the dilatator operculi muscle.

The adductor mandibulae covers the cranium, originating from the frontal (see fig. 16 and Stix 1956). Insertion is on to the lower jaw, the upper fibres of the muscle mass running into connective tissue covering the dorsal surface of the mandible as in Nematogenys (see Howes 1983 b, fig. 7).

The retractor tentaculi is well-developed and extends from the hyomandibul a to insert on the maxilla. The adductor arcus palatini is a long-based muscle extending from the parasphenoid and prootic to insert along the dorsal margin of the pterygoid bones. The extensor tentaculi runs forward from the orbitosphenoid to insert on the postero- medial border of the palatine. The levator arcus palatini (fig. 17) is a small conical muscle extending from the lateral extension of the sphenotic to insert on the foot of the hyomandibula. The origin of the dilatator operculi covers a long portion of the frontal. The muscle is broadly triangular and passes beneath the bridge formed by the sphenotic-frontal extension (fig. 17). Some fibres of the dilatator operculi extend from

Le

Pal

AO LO

Mx

FIG. 16.

AM RT

I I

Superficial cranial musculature ofMalapterurus electricus shown in dorso-lateral view. Scale, 5 ram.

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Phylogenetic relationships of the electric catfish family

AAP Do /

63

PA

) MX

[' I

\ RT

' AM LO \LAP FIG. 17. Deep cranial musculature ofMalapterurus electricus shown in dorso-lateral view. The

adductor mandibulae muscle has been cut through; the two branches of the maxillaris nerve, above and below the retractor tentaculi, and the mandibularis nerve are shown in black. Scale, 5 ram.

the sphenotic bridge and join the muscle just prior to its insertion on the opercular process.

Amongst siluroids, reduction of the levator arcus palatini to the extent seen in the Malapteruridae is known only in the Nematogenyidae and Loricariidae. In view of other synapomorphies uniting these two families (see Howes 1983 b), it seems unlikely that the condition in the Malapteruridae can be regarded as synapomorphic and it is considered that reduction of the muscle has occurred independently.

Origin of the jaw musculature from the cranial roof is not a condition unique to the Malapteruridae, and occurs in the Diplomystidae, Ictaluridae, Cetopsidae and some Bagridae. Lundberg and Baskin (1969, 36) and Lundberg (1970) viewed this condition as derived. On the basis of the differing configurations of the musculature, and the distribution pattern of other synapomorphies I would consider that the feature is homoplastic in these groups.

C o m m e n t a r y By its very nature, as the only family of electrogenic catfishes, the Malapteruridae

must be considered as specialized. Nevertheless, in many respects it is relatively plesiomorphic when compared with such supposedly generalized groups as the Bagridae and Diplomystidae. The few characters analysed here are only those which have revealed indications of phyletic affinity. A larger number, involving for example,

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64 G . J . Howes

the ethmoid region, jaws, branchial and hyoid arches and their muscles, pelvic girdle and caudal fin skeleton are all plesiomorphic.

Those characters interpreted as synapomorphies point to a relationship with the Siluridae and Schilbeidae. However, the distribution of the characters is such that a closer relationship with either one or the other family cannot be ascertained. Indeed, indications are that the Siluridae and Schilbeidae, as currently defined are paraphyletic groups. In the literature, the only character that distinguishes the Siluridae and the Schilbeidae is the presence, in the latter, of nasal barbels. Nasal barbels are present in other siluroid groups including the Malapteruridae and may well be a plesiomorphic feature. In most Siluridae, the first proximal radial lies between the sixth and eighth neural spines whereas in the Schilbeidae it is between the fourth and sixth. The former is probably the derived condition [see p. 47) and may be a significant character in recognizing one monophyletic group. On the basis of the synapomorphies identified herein, Silurus and Wallago are recognized as twin-taxa, forming the sister-group to Malapterurus. Further cladistic treatment of the 'Siluridae' and 'Schilbeidae' is necessary to resolve the wider relationships of this tripartite assemblage.

Malapteruridae

Obliquus superioris muscle with separate anterior segment. Liver lobes associated with the infracarinalis anterior muscle. Dorsal fin absent; radials reduced

Coracoids united by a long median suture (plesiomorphic).

Loose attachment of the posttemporal to the cranium. Complex division of the swimbladder protractor muscle.

M/illerian ramus of fourth parapophysis free and forming an ESA.

Palatine reduced and without a posterior or lateral extension; entirely anterior to the lateral ethmoid.

Sphenotic elongate, laterally curved.

Siluridae Schilbeidae

Present Present

In Silurus only. Absent

Dorsal fin absent in some taxa;

radials reduced in all. radials reduced in

Weakly united, no interdigitation in Wallago. In Silurus and Wallayo. In Silurus and Wallago.

some. Weakly to firmly united.

Variable, but never complete ankylosis. Absent

Mtillerian ramus curved wall of the swimbladder; marked flexibility of the ramus in Silurus and Wallago.

Reduced and mostly cartilaginous.

Elongate and contacting the lateral ethmoid in Silurus, Wallago and Kryptopterus.

around the anterior

slight flexibility.

Variable, from rod- like with lateral contact with the lateral ethmoid, to cartilaginous and extending anterior to the lateral ethmoid.

Anteriorly lengthened but not contacting the lateral ethmoid.

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Phylogenetic relationships of the electric catfish family 65

Occipital region of the cranium excavated; occupied by adductor mandibulae musculature.

Third infraorbital attached to the lower jaw by a ligament.

Extensively Partially to excavated; extensively

excavated; occupied by epaxialis muscle.

Present; Present; additionally, the first infra-orbital is elongated.

Although the Malapteruridae is unique amongst siluroids in possessing an electrogenic organ, electroreceptive systems are widespread within these fishes; see Szabo 1974, Kalmijn 1974. The distributional patterns of electroreceptor organs on the bodies of catfishes are known for only a few species (Szabo 1974). Such similar patterns may be rewarding indicators of phyletic relationship, as will knowledge of their gross morphology, i.e. whether pit-like or ampullary. Kalmijn (1974) recognizes that catfishes are '... endowed with a true electric sense'. It is not surprising therefore that there is an electrogenic catfish but rather that it is unique.

Apart from Lissmann (1958) few authors have speculated on the evolution of electrogenic organs. Possibly most teleosts are electrogenic to varying degrees. Bioelectric DC fields are generated by muscle contractions causing rythmic impedance variations in the skin (see Kalmijn 1974). It may be visualized that the fishes' sensitivity to this passive field could have become receptive to disturbance in the field with a subsequent development of a feedback response to the disturbance.

In the case of the electric catfish, where the electrogenic organ is derived from the anterior body musculature, it seems a prerequisite that the muscle is released from the pectoral girdle. The outstanding feature of siluroids is the rigid framework formed by ankylosis of the pectoral girdle with the cranium and the vertebral column. The apparent functional purpose of this strong framework is to support the locking devices of the fin spines, suggesting that in siluroids it is those elements that have a dominant functional role. One may speculate that the phyletic loss of such presumably, highly effective anti-predatory d6vices could only be sustained in those taxa able to adopt some other equally effective device such as shoaling. Indeed, it is only in the mid-water, shoaling catfishes that highly ossified fin spines and rigid pectoral girdles are lacking. It is suggested that the benthic, solitary habits of the Malapteruridae are secondarily derived, the protective bony armour of their ecological counterparts having been 'replaced' with an electric field.

Acknowledgments I offer my sincere thanks to Drs. Humphry Greenwood, Keith Banister, Richard

Vari and Carl Ferraris Jr. for their pertinent and helpful comments which have done much to improve the manuscript.

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