228 BULLETIN OF MARINE SCIENCE, VOL. 59, NO. I, 1996

nutmeg, Cancellaria cooperi Gabb, parasitizes the California electric ray, Torpedo californica Ayres. BioI. Bull. 172: 362-366. Parth, M, 1992. Some notes on the Colubraria Schumacher, 1817, with description of Colu- bra ria brinkae, spec. nov. Spixiana IS: 213-220. Ponder, W. F. 1968. Anatomical notes on two of the Colubrariidae (Mollusca, Prosobranchia). Trans. Roy. Soc. New Zealand, Zool. 10: 217-223. Taylor, J., N, Morris and C. Taylor. 1980. Food specialization and the evolution of predatory pro so- branch gastropods, Palaeontol. 23: 375-409.

DATEACCEPTED: July 7, 1995.

ADDRESSES: (P.B.) Museum National d'Histoire Narurelle, 55 rue Buffon, 75005 Paris, France. (D.P.) 6800 S,W. 40 St" #499, Miami, FL 33155-3708.

BULLETIN OF MARINE SCIENCE. 59(1): 228-234. 1996

OCCURRENCE OF SCHINDLER'S , GENUS (TELEOSTEI: GOBIOIDEI), AT A SMALL REEF IN THE MOUTH OF THE KOSI ESTUARY, KWAZULU-NATAL: A FIRST RECORD FOR SOUTHERN AFRICA

Shael A. Harris and Digby P. Cyrus

Schindler's fishes, genus Schindleria, are small paedomorphic gobioids (John- son and Brothers, 1994) characteristic of Indo-Pacific coral reefs (Watson, 1989). Two species have been identified: Schindleria praematura and S. pietschmanni (Watson et aI., 1984). Since these are transparent when alive and are among the smallest of fishes (Gosline and Brock, 1960) they are unsampled, or under- sampled and easily overlooked in the conventional sampling procedures of gill, seine and trawl netting. However, they have been collected in samples from several areas of the Pacific Ocean such as the Hawaiian Islands (Schindler, 1932; Gosline and Brock, 1960; Watson and Leis, 1974; Watson, 1989), New Guinea (Giltay, 1934), Tahiti and Somoa (Bruun, 1940), the Tasman Sea (Bruun, 1940), the Coral Sea (Great Barrier Reef), French Polynesia (Dufour and Galzin, 1993; Leis, 1994) and the South China Sea (Ozawa and Matsui, 1979). In the Indian Ocean they have been recorded from the Laccadive Archipelago (Jones and Kumaran, 1964) and Nosy-Be (Madagascar) (Sardou, 1974). The latter is the nearest record of Schindler's fish to southern Africa, a distance of some 2,500 km. This paper reports on a first record of Schindleria in southern African waters from ichthyoplankton samples taken at a site adjacent to a small reef inside the mouth of the Kosi Estuary, KwaZulu-Natal, South Africa. Seasonality and de- velopmental stages are examined.

METHODS AND MATERIALS

Study Sile.-The Kosi system is situated in the subtropical region of the northern KwaZulu-Natal coast of South Africa (26°47'S; 32°47'E; Fig. 1). It is a clear water system consisting of a series of four lakes linked by narrow channels, that drains into the sea through the northern estuary (Fig. I). The estuary mouth is generally open (20-50 m wide) throughout the year and is subject to regular and strong tidal movements (Begg, 1980). A rocky outcrop approximately 200m from the mouth of the estuary forms a small reef (approximately 50 by 20 m) upon which a diverse fish fauna exists (Blaber and Cyrus, 1981). NOTES 229

27°10'5

Southern Africa

•

o 33°53'E km

Figure I. Location of sampling site at the reef in the Kosi Estuary on the northern KwaZulu-Natal coast of South Africa.

1

Jan May July Sept Dec Mar I summer 1 f autumn II winter II spnng II summer II autumn I MONTH

Figure 2. Mean density (::!: 1 SE) of Schindleria praematura for each sampling period. 230 BULLETIN OF MARINE SCIENCE. VOL. 59. NO. I. 1996

Sampling Regime.-The sampling site was located in the main mouth channel adjacent to the rocky reef. Sampling took place in January, May, July, September, December 1988 and March 1989, with samples being taken over three consecutive spring flood tides at night on each occasion. The ebb tide was only sampled on the first night of each occasion. A ichthyoplankton net (500-/.Lm mesh, 57-COl diameter mouth), with a flow meter (General Oceanic's) was deployed in the flood tidal currcnt behind an anchored boat. Four pairs of surface and bottom samples were taken at approximately hourly intervals depending on the flood tidal period and the strength of the tidal current. Samples were preserved in the field with 4% buffered formalin and in thc laboratory all Schindler's fishes were extracted and measured (standard length) then staged according to Kendall el al. (1984).

Treatment of Data.-The total number of Schindler's fishes collected was recorded and converted to a density (number of individuals per 100 m3). Mean values (Fig. 2) represent the total value divided by the number of samples taken that month. To test significant differences bctween top and bottom samples of fish density, density values were log transformed then analysed using a one-way ANOYA with 95% confidence limits.

RESULTS No significant differences in top and bottom measurements of fish density were found (P > 0.05) and so top and bottom values were combined. All ]20 specimens of Schindleria were taken on flood tides, Only five specimens of S. pietschmanni were recorded in the March sample, with a size range of7.0-12.5 mm (mean 8.7 mm). The remaining 115 specimens, all S. praematura. were recorded in 4 of the 6 months sampled with mean densities being greatest in May (3.5 individuals· 100 m-3) and March (2.2 individuals· 100 m-3) and minimal in January (0.35 individuals· 100 m-3) and September (0.27 individuals· 100 m-3) (Fig. 2). Mean sizes were smaller in January and March than in May and September (Fig. 3): January-mean 8.1 mm (range 5.4-14.0 mm); March-mean 9.0 mm (range 4.0- 16.0 mm); May-mean 11.5 mm (range 5.5-23.5 mm); September-mean 10.6 mm (range 4.5-17.2 mm). Specimens were predominantly postflexion, with no young larvae (preflexion or flexion) but with juveniles and adults being present. In autumn (May and March) postflexion (55% and 78%, respectively), juvenile (36% and 19%, re- spectively) and ripe adults (9% and 3%, respectively) were found. In summer (January) the specimens were predominantly postflexion (83%) but with some juveniles (17%) also present. Mainly adults (60%) and a few postflexion (40%) individuals were present in spring (September).

DISCUSSION Distribution.-Schindleriids are endemic to neritic surface waters of subtropical and tropical Indo-Pacific regions (Watson et a!., 1984; Watson, 1989). The first specimens were collected in the Pacific Ocean, most notably the Hawaiian Islands (Schindler, 1932; Giltay, 1934; Bruun, 1940). Subsequently, Jones and Kumaran (1964) recorded the occurrence of schindleriids in the Indian Ocean from the Laccadive Archipelago off the south-west coast of India. More recently, schin- dleriids have been recorded in coral atoll lagoons of the Coral Sea (Great Barrier Reef) and French Polynesia (Dufour and Galzin, ]993; Leis, ]994). Sardou (1974) and the present study have recorded schindleriids in the Indian Ocean at Nosy- Be (Madagascar) and at Kosi (South Africa), respectively. Both S. praematura and S. pietschmanni were found at all three Indian Ocean sites but only S. prae- matura was found at the Pacific Ocean sites, with the exception of the Hawaiian Islands (Fig. 4). The southernmost distribution of schindleriids at Kosi may be attributable to the Agulhas Current, the prominent western boundary current which flows from the tropical and subtropical Indo-Pacific region (Schumann, ]988) since it trans- NOTES 231

Jan n 6 (summer) = 40

20

May n = 47 (autumn) 40

20

>- () :.:-:-:.:~.: t: :.:~.:.:.:.: eI) ::J e- Sept n = 6 •...el) (spring) -~ 40

20

March n = 56 (autumn) 40

20

2 4 6 B 10 12 14 16 1B 20 22 24 size (mm)

Figure 3. Monthly size frequency of Schindleria praematura for each sampling period. 232 BULLETIN OF MARINE SCIENCE, VOL. 59, NO. I, 1996

I X - S.praematura 0 - S.pietschmanni I

PACIFIC OCEAN

1II.'h/T.b~l.man.I•••

""'!Ne"'OLYNIII,l, X I •• tot,

Figure 4. Geographic distribution of Schindleria. ports many larvae of species from this region (McClurg, 1988). North of St Lucia (Fig. 1) maximum speeds of 1.5·ms-1 have been recorded in the Agulhas Current (Schumann, 1988). Similarly, the occurrence of Schindleria off the east coast of Australia more than likely is a result of transport from the north in the East Australian Current (Miskiewicz, pers. comm.). Two factors facilitate the inshore movement of larval fish being transported in the Agulhas Current off the KwaZulu-Natal coast: 1) the continental shelf north of 28°30'S is very narrow (2-7 km wide, Martin and Flemming, 1988) with the result that the Agulhas Current flow is felt within a few kilometers of the coast (Schumann, 1988), and 2) shoreward intrusions of Agulhas Current surface water have been consistantly recorded along the South African Coast (Beckley and Van Ballegooyen, 1992). A question to ask is whether the population in the Kosi Estuary is closed or whether the population is replenished by larvae being carried south in the Agulhas Current. If one assumes that the larvae hatch at 2mm and grow at say 0.25mm . day-I, the average size of individuals arriving at Kosi from a northern spawning ground (e.g., Nosy-Be, 2,500 km away) would be 9 mm (29 days) if transported l in the Agulhas Current at a speed of l·ms- . The average size of specimens in the present study ranged from 8.1 mm in January to 11.5 in May, i.e., postflexion stages (Fig. 3) which suggests that larval supply is occurring from some northern spawning ground. Once these larvae are transported into suitable nearshore hab- itats such as Kosi, they settle out. Leis et al. (1989) suggested that Schindleria become strongly epibenthic in the postflexion stage. The presence of ripe adults at Kosi also indicates local spawning activity. Larval assemblages of the Agulhas Current was recently investigated by Beck- ley and Coetzee (in prep.) but no Schindleria were found in those samples, prob- ably because the northernmost station was approximately 10 km offshore (Beckley and Van Ballegooyen, 1992). Eight postflexion specimens were found close in- shore (up to 1 km) off the St Lucia Estuary mouth (Harris and Cyrus, in prep.), approximately 150 km south from Kosi Bay (Fig. 1), and two S. praematura (11 mm and 15 mm) were found in ichthyoplankton samples taken from Durban NOTES 233

Harbour (Harris and Cyrus, in prep.), approximately 225 Ian south of St Lucia (Fig. 1). This indicates that schindleriids may range at least as far south as Durban Harbour and that they only occur inshore. The types of habitat these fish occur in are coral atoll lagoons and sheltered areas close to islands in tropical and subtropical regions (Jones and Kumaran, 1964; Sardou, 1974; Leis and Goldman, 1987; Dufour and Galzin, 1993; Leis, 1994). The adults and juveniles are epibenthic during the day and move up into the water column at night (Watson, 1989) with specimens being taken at night at the surface (Gosline and Brock, 1960; Jones and Kumaran, 1964; Sardou, 1974; Leis, 1994). It is, therefore, not surprising that schindleriids have been found at the sample site of the present study since the environmental conditions are suitable for these fish to inhabit. Life-cycle Characteristics.-Schindleriidae are one of the few families which use atoll lagoons throughout their larval stage (Leis, 1991) and are therefore called "lagoon completers" (Leis, 1994). Small fish species occurring in retention areas (coral atoll lagoons and estuaries) of tropical and warm temperate near-shore regions are characterised by small adult size, limited number of adult guilds, non- specialised larvae and non-pelagic eggs (Whitfield, 1990; Leis, 1994). The schin- dleriidae display these characteristics. Although no young larvae were found in this study, S. praematura is a lagoon completer elsewhere (Leis, 1994) and most likely does complete its life cycle at Kosi. From the literature the spawning period of schindleriids is not very clear. In the northern hemisphere it appears that they spawn between December and May (Schindler, 1932; Giltay, 1934) and in the southern hemisphere from October to December (Bruun, ]940; Jones and Kumarun, 1964; Sardou, 1974). Watson and Leis (1974) tentatively identified eggs collected in March, April and July in Ha- waii and showed that mature adults of both species were present from at least May through to September. The present study indicates that they spawned in May and March since postflexion, juvenile and ripe adults were found (Fig. 3). It, therefore, seems that this species spawns in most months of the year. It should be noted, however, that these previous studies (with the exception of Watson and Leis, 1974) and the present study did not sample throughout the year and more research is needed to further clarify the breeding period of these fish.

CONCLUSION To conclude, the reef habitat in the Kosi Bay estuary is essentially a subtropicaL lagoon habitat similar to coral atoll lagoons and is therefore suitable for schin·· dleriids to inhabit. S. praematura possibly has a closed population with sporadic: replenishment of larvae in the oceanic currents along the east coast of Africa. It, therefore, is very important that the Kosi system be maintained in a conservation area.

ACKNOWLEDGMENTS The authors acknowledge KwaZulu Bureau of Natural Resources to work in the area and Professor A. T. Forbes for involvement in sampling program. Financial assistance was provided by Shell South Africa (Pty) Ltd and the University of Zululand Research Committee under project S640/8. This paper forms part of the Estuaries Special Programme (Natal Section) of the Foundation for Research De- velopment.

LITERATURE CITED Beckley, L. E. and R. C. van Ballegooyen. 1992. Oceanographic conditions during three ichthyo- plankton surveys of the Agulhas Current in 1990/91. S. Afr. J. Mar. Sci. 12: 83-93. 234 BULLETINOFMARINESCIENCE.VOL.59. NO.I. 1996

Begg, G. W. 1980. The Kosi system: aspects of its biology, management and research. Pages 358- 373 in M. N. Bruton and K. H. Cooper, eds. The ecology of Maputaland. Rhodes University, Grahamstown. 560 p. Blaber, S. J. M. and D. P. Cyrus. 1981. A revised checklist and further notes on the fishes of the Kosi system. Lammergeyer. 31: 5-14. Bruun, A. F. 1940. A study of a collection of the fish Schindleria from south Pacific waters. Dana Rept. Carlsberg Found 21: 1-12. Dufour, V. and R. Galzin. 1993. Colonization patterns of reef fish larvae to the lagoon at Moorea Island, French Polynesia. Mar. Ecol. Prog. Ser. 102: 143-152. Giltay, L. 1934. Notes ichthyo]ogies. Vlli. Les larvaes de Schindler sont-elles des Hemirhamphidae? Mus. Roy. d'Hist. Nat. Belgique, Bull. 10 no. 13: ]-10. Gos]ine, W. A. and V. E. Brock. 1960. Handbook of Hawaiian fishes. University of Hawaii Press, Honolulu. 372 p. Jones, S. and M. Kumaran. 1964. On the fishes of the genus Schindleria Giltay from the Indian Ocean. J. Mar. BioI. Assoc. India 6: 257-264. Johnson, G. D. and E. B. Brothers. 1994. Schindleria: a paedomorphic (Teleostei: Gobioidei). Bull. Mar. Sci. 52: 441-471. Kendall. A. W. Jr.. E. H. Ahlstrom and H. G. Moser. 1984. Early life history stages of fishes and their characters. Pages 11-22 in H. G. Moser, W. J. Richards, D. M. Cohen, M. P. Fahay, A. W. Kendall Jr. and S. L. Richardson, eds. Ontogeny and systematics of fishes. Amer. Soc. Ich. and Herp .. Spec. Publ. 1. 759 p. Leis, J. M. 1991. Larval and juvenile ecology. Pages 183-230 in P. F. Sale, ed. The ecology of fishes on cora] reefs. Academic Press, London. 754 p. ---. 1994. Cora] atoll lagoons: closed nurseries for the larvae of a few coral reef fishes. Bu]l. Mar. Sci. 54: 206-227. --- and B. Goldman. 1987. Composition and distribution of larval fish assemblages in the Great Barrier Reef lagoon, near Lizard Island, Australia. Aust. J. Mar. Freshw. Res. 38: 211-223. ---, --- and S. E. Reader. 1989. Epibenthic fish larvae in the Great Barrier Reef Lagoon near Lizard Island, Australia. Japan. J. Ichthol. 35: 423-433. Martin, A. K. and B. W. Flemming. 1988. Physiography, structure and geological evolution of the Natal continental shelf. Pages 11-46 in E. H. Schumann, ed. Coastal ocean studies off Natal, South Africa. Springer-Verlag, New York. 271 p. McClurg, T. P. 1988. Benthos of the Natal continental shelf. Pages 178-208 in E. H. Schumann, ed. Coastal ocean studies off Natal, South Africa. Springer-Verlag, New York. 271 p. Ozawa, T. and S. Matsui. 1979. First record of the schindlerid fish, Schindleria praematura, from southern Japan and the South China Sea. Japan. J. lehthyol. 25: 283-285. Sardou, J. 1974. Contribution a la connaissance de la faune ichthyologique Malagache: decourverte de poisson de la famille des Schindleriidae dans Ie canal de Mozambique, a Nosy-Be et etude d'une collection de Schindleria. Cah. O.R.S.T.O.M .., Oceanogr. 12: 3-15. Schindler, O. 1932. Sexually mature larval Hemiramphidae from the Hawaiian Islands. Bull. Bernice P. Bishop Mus. 197: 1-28. Schumann, E. H. 1988. Physical oceanography off Natal. Pages 101-130 in E. H. Schumann, ed. Coastal ocean studies off Natal, South Africa. Springer-Verlag, New York. 271 p. Watson, W. 1989. Schindleriidae-Schindlers fishes. Pages 270-273 in J. M. Leis and T. Tmski. The larvae of Indo-Pacific shorefishes. Univ. of Hawaii Press, Honolulu. 371 p. --- and J. M. Leis. 1974. Ichthyoplankton of Kaneohe Bay, Hawaii: a one year study of the fish eggs and larvae. University of Hawaii Sea Grant Program, Honolulu Tech. Rep. UNIHJSEA- GRANT-TR-75-01. Watson, W., E. G. Stevens and A. C. Matarese. 1984. Schindleroidei: development and relationships. Pages 552-554 in H. G. Moser, W. J. Richards, D. M. Cohen, M. P. Fahay, A. W. Kendall Jr. and S. L. Richardson, eds. Ontogeny and systematics of fishes. Amer. Soc. leh. and Herp., Spec. Publ. 1. 759 p. Whitfield, A. K. 1990. Life-history styles of fishes in southern African estuaries. Environ. BioI. Fishes. 28: 295-308.

DATEACCEPTED: May 25, 1995.

ADDRESS: Coastal Research Unit Zulu land, University of Zulu land, Private Bag Xl 001, Kwa- Dlangezwa 3886, South Africa.