BULLETIN OF MARINE SCIENCE, 60(1): 89-99, 1997

LARVAE OF FOUR LATES FROM LAKE TANGANYIKA

Izumi Kinoshita and Kalala K. Tshibangu

ABSTRACT Larvae of endemic Lales microlepis, L. anguslifrons, L. mariae and L. slappersi from Lake Tanganyika are distinguishable using body form, head spination, fin completion sequence, and distribution pattern of melanophores. The sequence of ontogeny in Tanganyika Lales was closer to marine than to fresh waters fishes. Of this group, larvae of L. microlepis had unique characters, i.e., an elongate spine develops at the angle of the preopercle and pelvic rays develop precociously in conjunction with anterior dorsal rays. When these ontogenetic char- acters were polarized and larvae of Indo-Pacific Lales were treated as an outgroup for larvae of Tanganyika Lales, we speculate that L. microlepis are most specialized in the extant Lales group and Tanganyika Lales did not form a monophyletic subgenus Luciolales.

Recently the centropomid subfamily Latinae including the genera Lates and Psam- moperca was given full familial status (Latidae) (Mooi and Gill, 1995). The genus Lates is represented by nine species, of which seven species occur in African fresh waters: L. microlepis, L. angustifrons, L. mariae, L. stappersi, L. niloticus, L. ma- crophthalmus and L. longispinis (Greenwood, 1976). The former four species are endemic to Lake Tanganyika and were hypothesised to form the subgenus Luciolates separated from the subgenus Lates (Poll, 1953; Greenwood, 1976). These fishes, which live in pelagic waters of the lake, are economically important protein sources for the people of the region (Coulter, 1991b). There is some information on the ecology and fisheries of these species including the description of larvae (Poll, 1953; Coulter, 1970, 1976, 1991a, 1991b; Chapman and Van Well, 1978; Ellis, 1978; Pear- ce, 1985); however, Poll's (1953) specific identification of larvae is problematic. During a joint project of Japan and Zaire on ecological, limnological and ich- thyological research in Lake Tanganyika and its environs, we collected numerous Lates larvae representing four species. The purpose of this paper is to describe their early developmental stages with remarks on possible specialization of Lates microlepis based upon ontogenetic information.

MATERIALS AND METHODS

A total of 145 larval and juvenile Lates microlepis (2.3-5,9 mm), 137 L. angustifrons (2.1-7.8 mm), 185 L. mariae (2.4-12.1 mm) and 25 L. stappersi (3.1-14,7 mm) were collected with a plankton net or seine net in Uvira waters, Zaire, in the northern part of Lake Tanganyika, from May to July 1988. Collection methods and sites are detailed in Kinoshita (1986) and Tshibangu and Kinoshita (1995). All specimens were preserved in 10% formalin in the field, and transferred to 80% ethanol, sorted and measured according to Okiyama (1988) under a stereomicroscope using an ocular microm- eter in the laboratory, Unlabeled lengths are body lengths (notochord length in preflexion and flexion larvae, standard length in postflexion larvae and juveniles). Some specimens were stained with cyanine and drawn with the aid of a camera lucida. For evaluation of phylogenetic relationships in the present study, the cladistic methodology was adopted (Henning, 1966).

RESULTS Identification.-The four types of specimens were recognized as Lates because of their resemblance to known larvae and juveniles of L. japonicus (Kinoshita et aI., 1988) and L. calcarifer (Leis and Trnski, 1989). Juveniles could be identified to each species on the basis of the adult morphological characteristics (Poll, 1953): L. stappersi, by its elongated body; L. mariae, by having nine dorsal spines (other species, seven or eight spines); L. angustifrons, by its caudal fin and body shape;

89 90 BULLETIN OF MARINE SCIENCE, VOL. 60, NO. \, \997 and L. microlepis, by its caudal-fin shape. Identifications of earlier larvae were verified by melanophore patterns traced back from juveniles. Descriptions (Figs. 1-4).--GENERAL MORPHOLOGY.Corresponding morphometric data are summarized in Table 1. Larvae are laterally compressed in all four species. The head is robust, with a large, oblique mouth and large eyes in L. microlepis, while moderate in the other species. The body is deepest in L. microlepis, and most slender in L. stappersi, throughout the larval and juvenile stages. The shape of body is moderate in the other two species, but in the juvenile stage, it is slightly deeper in L. angustifrons than in L. manae. Guts of all species are tightly coiled, and reach about 50% NL in larvale and 60-70% SL in juveniles. Total myomeres number 22- 23 in L. microlepis and 23-24 in the other species. FIN FORMATION.Flexion begins at ca. 4 mm in L. stappersi, and at 3 mm in the other species, and is complete at ca. 5.5 mm in L. stappersi, and at ca. 5 mm in the other species. Full caudal principal rays are completed at ca. 6 mm in L. microlepis and L. angust(frons, and at ca. 7 mm in L. mariae and L. stappersi. In L. microlepis, the pelvic fin begins to develop more precociously in conjunction with the first dorsal fin th;ill the second dorsal and anal fins at ca. 4 mm, and full complements of these fin rays are present at ca. 5 mm. Second dorsal and anal anlagen are found at 4-5 mm; their incipient fin rays begin to differentiate from posterior to anterior, and full complements of the dorsal and anal-fin rays are present at ca. 6 mm, in the other species. The pelvic bud differentiates at ca. 5, 7 and 7 mm, its rays start to develop at ca. 6, 9 and 7 mm, and complete at ca. 7, 11 and 11 mm, in L. angustifrons, L. mariae and L. stappersi, respectively. A few incipient rays appear in the pectoral fin at ca. 5, 5, 7 and 5.5 mm; a full complement is present at ca. 6, 7.5, 9 and 8-11 mm, in L. microlepis, L. angus- tifrons, L. mariae and L. stappersi, respectively. Thus, L. microlepis attains the juvenile stage more precociously than the other species. HEADSPINATION.Initially in L. microlepis, there are three spines on the pre- opercle, the one at the angle being the longest. The number of spines increases gradually during ontogeny to six. There are four and three spines of approximately equal size on the preopercle, and the numbers of spines on the preopercle increase during ontogeny to six, in the other species. Two small spines are visible on the posterior margin of the interopercle near its junction with the subopercle in L. microlepis, but these spines are absent in the other species. A single spine is present on the posterior margin of the opercle and posttemporal in all species. PIGMENTATION.In the preflexion and flexion stages, small melanophores are found on the lower end of the preopercular ridge and under the throat, chin, abdomen, and rectum, in all species. Characteristically, melanophores are densely distributed over the trunk in L. microlepis and over the tail in L. angustifrons. Melanophores are found as two distinctive spots on the ventral margin of the tail in L. mariae; however, these spots are absent in L. stappersi. In the postflexion stage, melanophores are distributed on the head in all species. They extend back- ward along the midline of the tail in L. microlepis; increase in number on the lateral midline, and dorsal and ventral margins of the tail in L. angustifrons; occur on the lateral midline of the caudal peduncle, forming a single row in L. mariae; and are visible on the dorsal margin of the trunk and extend backward, covering the whole dorsal head to caudal peduncle in L. stappersi. In the juvenile stage, melanophores shrink individually and become more numerous dorsolaterally, forming four incomplete vertical bands on the trunk and tail in L. angustifrons; shrink individually, expand allover the body in L. mariae; and become heavier KINOSHITA AND TSHIBANGU: LARVAL LATES FROM LAKE TANGANYIKA 91

Figure L Developmental stages of Lates microlepis from northern part of Lake Tanganyika. A) 2.8 mm preflexion larva; B) 4.5 mm flexion larva; C) 5.0 mm postflexion larva; D) 5.9 mm juvenile. 92 BULLETIN OF MARINE SCIENCE, VOL. 60, NO. I, 1997

Figure 2. Developmental stages of Lales anguslifrons from northern part of Lake Tanganyika, A) 3.0 mm preflexion larva; B) 4,6 mm flexion larva; C) 6.4 mm postflexion larva; D) 7.5 mm juvenile. on the lateral body, shrinking individually along the myosepta in L. stappersi, Melanophores on the fin membrane appear on the first dorsal, anal, pectoral and pelvic fins in the juvenile stage of all species, These melanophores are developed on the first dorsal and pelvic fins in the flexion stage in L. microlepis, a unique feature of this species, Distinction among Four Species of Lates.-Table 2 summarizes morphometric and pigmentation characteristics useful in distinguishing larval and juvenile stages among four species of Tanganyika Lates. The following keys are devised using characters listed in Tables I and 2. KINOSHITA AND TSHIBANGU: LARVAL LATES FROM LAKE TANGANYIKA 93

Figure 3. Developmental stages of Lates mariae from northern part of Lake Tanganyika. A) 3.1 mm preflexion larva; B) 5.2 mm flexion larva; C) 6.0 mm postflexion larva; D) 10.9 mm juvenile.

KEy TO PREFLEXION AND FLEXION LARVAL STAGES lao Melanophores densely distributed on lateral trunk L. microlepis lb. Melanophores absent or sparse on lateral trunk...... 2 2a. Melanophores densely distributed on lateral tail L. angustifrons 2b. Melanophores absent or sparse on lateral tail 3 3a. Some melanophores on ventral margin of tail L. mariae 3b. No melanophores on ventral margin of tail L. stappersi

KEy TO POSTFLEXION LARVAL AND JUVENILE STAGES

lao Body depth, more than 36% SL L. microlepis 94 BULLETIN OF MARINE SCIENCE, VOL. 60, NO.1, 1997 A

Figure 4. Developmental stages of Lates stappersi from northern part of Lake Tanganyika. A) 3,2 mm preflexion larva; B) 4,3 mm flexion larva; C) 5,6 mm postflexion larva; D) 11.1 mm juvenile. lb. Body depth, less than 32% SL 2 2a. Melanophores dense along dorsal margin of body L. stappersi 2b. Melanophores less dense on dorsal margin of body ...... 3 3a. Some melanophores on dorsal margin and lateral midline of caudal peduncle large and dis- tinctive L. mariae 3b. Melanophores on caudal peduncle small and scattered L. angustifrons

DISCUSSION Lower percoids from other fresh water systems usually exhibit delayed fin-ray completion (after 15 mm), and their larvae have minimal head spination, con- KINOSHITA AND TSHIBANGU: LARVAL L4TES FROM LAKE TANGANYIKA 95

Table I. Morphometric and meristic data for Lates species from Lake Tanganyika (J = juvenile stage, L = larval stage, La = Lates angustifrons. Lma = L. mariae, Lmi = L. microlepis, Ls = L. slappersi)

Species Lmi La Lma L, Body lengths (mm) Preflexion 2.3-3.4 2.1-3.4 2.4-3.5 3.1-4.2 Flexion 3.0-5.0 3.1-5.0 3.4-5.4 3.8-5.6 Postflexion 4.7-5.0 4.6-6.4 5.2-9.4 5.4-7.8 Juvenile 5.1-5.9 6.9-7.8 9.1-12.1 11.0-14.7 Proportions to body (%) Head L 26-35 20-39 22-35 23-34 J 36-39 36-37 34-36 34 Preanal L 53-63 53-67 46-63 46-58 J 66-69 66-67 62-66 61-63 Body depth L 26-36 16-27 19-25 17-25 J 37-39 28-32 24-26 20-21 Meristic characters (after Poll, 1953) 0 VII-VIII, 12-13 VIII, 12-13 IX, 10-13 VIII,9-10 A III, 8-9 III, 7-9 III, 8-9 III, 9-10 Shape of caudal in adult Forked Rounded Truncate Forked

sisting of only a few small spines along margins of the preopercle (Uchida, 1935; Imai and Nakahara, 1957; Auer, 1982). On the other hand, marine lower percoids usually attain the juvenile stage at sizes under 10 mm (Johnson, 1984). In Tan- ganyika Lates species, head spination is conspicuous and similar marine lower percoids (Figs. 1-4, Table 1). This family were probably present in the proto- Tanganyika region at the beginning of rifting, because Lates fossil remains have been recorded from a Miocene lake (Greenwood, 1976). Since this family is evidently of marine origin, Coulter (1991c) speculated that the ancestors of the extant species migrated the Zaire River from the sea at some later period of a marine transgression and were either present in its upper reaches before Lake Tanganyika formed or they entered the lake subsequently during a time when the lake the Zaire were connected. Thus, it seems that rapid development and head spines are characters that evolved in marine ancestors and are retained in extant freshwater species. This interpretation should be consistent with the following cladogram. The early developmental stages of four species of Lates in Lake Tanganyika could be readily identified despite their close relationship (Figs. 1-4). The distinct nature of the Lates species of Tanganyika probably reflects their adaptive radia- tion. In particular, the morphology of L. microlepis larvae is unique. In Latidae, early stages of two species have been described; L. calcarifer from India, Aus- tralia, Papua New Guinea and Thailand (Ghosh, 1973; Moore, 1982; Kosutarak and Watanabe, 1984; Leis and Trnski, 1989), and L. japonicus from Japan (Ki- noshita et aI., 1988). Therefore, relationships within Tanganyika Lates was ana- lyzed using nine characters (Table 2), polarized by comparison with larvae of Indo-Pacific Lates as an outgroup (Fig. 5). There were almost no differentiation in the character states exhibited by the Indo-Pacific Lates and L. angustifrons (Table 2), and these taxa represent an unresolved trichotomy with the other three Tanganyika Lates (Fig. 5). Thus, Indo-Pacific Lates plus L. angustifrons constitute the sister group to the other three Tanganyika Lates. L. mariae and L. stappersi share synapomorphy (1/) (Fig. 5). L. microlepis has many autapomorphies (12' 2, 32, 4, 5, 62), and is hypothesized to be the most specialized in Lates group (Fig. 96 BULLETIN OF MARINE SCIENCE, VOL. 60, NO. I, 1997

j

E ..J KINOSHITA AND TSHIBANGU: LARVAL LATES FROM LAKE TANGANYIKA 97

Indo- Poc:ific Lates Tanganyika Lates

L. japonicus L. caTrorifer L. angustiftuns L. mariae. L. stapperm. L. microl.epis

Figure 5. Cladogram of relationships hypothesized using ontogenetic information within the Lales. based on Indo-Pacific Lales as outgroup. Numbers refer to characters in Table 2: I, = synapomorphy for L. mariae and L. slappersi; 12• 2. 3" 4. 5 and 62 = autapomorphies for L. microlepis; 3, = autapomorphy for L. calcarifer; 6, and 8, = autapomorphies for L. mariae; 7 = synapomorphy for L. mariae. L. stappersi and L. microlepis; 82 and 9 = autapomorphies for L. stappersi.

5). Thus, there seems to be no justification for Greenwood's (1976) hypothesis which places Tanganyika Lates in a monophyletic subgenus (Luciolates). Juveniles of L. angustifrons and L. mariae inhabit weed beds in shallow coasts (Kondo and Abe, 1995). L. angustifrons juveniles often remain in a head-down position parallel to a leaf of weed, and appear camouflaged by the leaves due to vertical bands on their bodies. Similar habitats are shown by larval and juvenile L. japonicus, which inhabit eelgrass beds of estuaries in Japan (Kinoshita et aI., 1988). Thus, L. angustifrons resembles L. japonicus not only morphologically but ecologically. Coulter (1991a) reported that littoral weed beds are important nurs- eries for L. microlepis as well as L. angustifrons and L. mariae. However, we never observed L. microlepis in weed zones. We caught 44 juveniles (8.4-49.2 mm) of L. microlepis under drifting weeds off the Uvira coast in Zaire on 24 November 1979. Some of these juveniles had entered the hollow stalks. This observation suggests that drifting weeds in pelagic waters may be an important habitat for juvenile L. microlepis. L. stappersi larvae inhabit pelagic waters, and never immigrate to the nearshore, not even as juveniles (Coulter, 1991a). The pattern of dense melanophores along the dorsal margin of the body of juveniles (Fig. 4D), suggests that L. stappersi leads a neustonic life. This black back is frequently found in neustonic larvae from the sea such as Cololabis saira (Scomberosocidae), MugU cephalus (Mu- gilidae) and Hexagrammidae (Uchida, 1958; Haryu, 1988; Senou and Kinoshita, 1988), probably as an adaptation to life on the surface exposed to the direct rays of the sun (Moser, 1981).

ACKNOWLEDGMENTS

We express gratitude to M. Okiyama. A. C. Gill. J. Olney. W. J. Richards, J. S. Burke and H. Kawanabe for their critical reading the manuscript. N. Abe, S. Fukudome, M. Hori, T. Kondo, Y. Niimura, K. Yamaoka. M. Yuma and the staff of Uvira Station helped us in many ways, to whom we 98 BULLETIN OF MARINE SCIENCE, VOL. 60, NO. I, 1997 are indebted. This study was supported partly by a Joint Study Project from the Japan International Cooperation Agency.

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DATE ACCEPTED: June 6, 1996.

ADDRESS: (I.K.) Fisheries Research Station, Kyoto University, Maizuru, Kyoto 625, Japan; (K.K.T.) Uvira Station, Department of Hydrobiology, Zaire Research Center of Natural Science, P.O. Box 254, Bujumbura, Burundi.