Abstract
The sympatric echinoids Diadema savignyi and D. setosum coexist in shallow reef lagoons throughout East Africa. The reproductive strategies of these echinoids were studied to investigate reproductive isolation as a possible mechanism for maintaining the coexistence of these closely related species. The annual reproductive cycle and lunar periodicity were determined by gonad index measurements, histological examination of gametogenesis, and induction of spawning with injections of KCl. The peak reproductive period of D. savignyi coincided with the north-east monsoon period (when light and temperatures are high) as gonad indices were high (>8%) beginning in February and peaked at 9.7% in May. Gonad indices subsequently rapidly decreased (by 26%) in June at the beginning of the cooler south-east monsoon period. However, the presence of sperm and ova in most months of the year indicates continuous gametogenesis with reduced reproductive effort during the cooler months. The annual cycle for D. setosum showed less of a seasonal trend as gonad indices remained above 7% throughout much of the year but tended to be highest when temperatures were lower. This is the first confirmation of continuous reproduction in these two species at the equator. The reproductive patterns of both species remained consistent over 2 years of sampling. Both species exhibited a synchronized lunar spawning periodicity during the 3 months sampled, with D. setosum spawning on lunar days 8–10 and D. savignyi spawning after the full moon (lunar days 17–18). Whereas spawning in D. savignyi was very tightly synchronized, 20% of D. setosum individuals still spawned after the peak spawning period. The coexistence of these closely related species appears to be maintained by temporal reproductive isolation during the lunar spawning period reinforced by seasonal differences in reproductive effort.
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References
Bauer JC (1976) Growth, aggregation and maturation in the echinoid, Diadema antillarum. Bull Mar Sci 26:273–277
Birkeland C, Neudecker S (1981) Foraging behavior of two Caribbean chaetodontids: Chaetodontid capistratus and C. aculeatus. Copeia 1981:169–178
Bryceson I (1982) Seasonality of oceanographic conditions and phytoplankton in Dar-es-salaam waters. Univ Sci J (University of Dar-es-salaam) 8:66–76
Bwathondi POJ (1973) The biology and fishery potential of Palanurid lobsters in Tanzania. MSc thesis, University of Dar-es-salaam
Clark AM, Rowe FWE (1971) Monograph of the shallow-water Indo-West Pacific echinoderms. Pitman Press, Bath, England
Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310
Drummond AE (1995) Reproduction of the sea urchins Echinometra mathaei and Diadema savignyi on the South African eastern coast. Mar Freshw Res 46:751−757
Fox HM (1924) Lunar periodicity in reproduction. Proc R Soc Lond B 95:523–550
Giese AC, Pearse JS (1974) Introduction: general principles. In: Giese AC, Pearse J (eds) Reproduction of marine invertebrates, vol I. Academic Press, New York, pp 1–49
Hattori A (1995) Coexistence of two anemonefishes, Amphiprion clarkii and A. perideraion, which utilize the same anemone. Environ Biol Fish 42:345–353
Hendler G (1991) Echinodermata: Ophiuroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates, vol VI. Echinoderms and Lophophorates. Boxwood Press, Pacific Grove, Calif., pp 355–511
Herring PJ (1972) Observations on the distribution and feeding habits of some littoral echinoids from Zanzibar. J Nat Hist 6:169–175
Hori R, Phang V, Lam T (1987) Preliminary study on the pattern of gonadal development of the sea urchin Diadema setosum off the coast of Singapore. Zool Sci (Tokyo) 4:665–673
IIiffe TM, Pearse JS (1982) Annual and lunar reproductive rhythms of the sea urchin Diadema antillarum (Philippi) in Bermuda. Int J Invert Reprod 5:139–148
Kennedy B, Pearse JS (1975) Lunar synchronization of the monthly reproductive rhythm in the sea urchin Centrostephanus coronatus Verrill. J Exp Mar Biol Ecol 17:323–331
Kobayashi N, Nakamura K (1967) Spawning periodicity of the sea urchins at Seto 11. Diadema setosum. Publ Seto Mar Biol Lab 15:173–184
Korringa RP (1947) Relations between the moon and periodicity in the breeding of marine animals. Ecol Monogr 17(3):347–381
Lawrence JL, Lawrence AL, Holland ND (1965) Annual cycle in the size of the gut of the purple sea urchin Strongylocentrotus purpuratus (Stimpson). Nature 205:1238–1239
Lessios HA (1981) Reproductive periodicity of the echinoids Diadema and Echinometra on the two coasts of Panama. J Exp Mar Biol Ecol 50:47–61
Lessios HA (1984) Possible prezygotic reproductive isolation in sea urchins separated by the isthmus of Panama. Evolution 38:1144–1148
Lessios HA (1991) Presence and absence of monthly reproductive rhythms among eight Caribbean echinoids off the coast of Panama. J Exp Mar Biol Ecol 153:27–47
Lessios HA, Pearse JS (1996) Hybridization and introgression between Indo-Pacific species of Diadema. Mar Biol 126:715–723
Levitan DR (1991) Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate. Biol Bull 181:261–268
McClanahan TR (1988a) Coexistence in a sea urchin guild and its implications to coral reef diversity and degradation. Oecologia 77:210–218
McClanahan TR (1988b) Seasonality in East Africa's coastal waters. Mar Ecol Prog Ser 44:191–199
McClanahan TR (1998) Predation and the distribution and abundance of tropical sea urchin populations. J Exp Mar Biol Ecol 221:231–255
McClanahan TR, Kurtis JD (1991) Population regulation of the rock-boring sea urchin Echinometra mathaei (de Blainville). J Exp Mar Biol Ecol 147:121–146
Mortensen T (1937) Contributions to the study of the development and larval forms of echinoderms III. K Dansk Vidensk Selsk Skr Naturv Math (Ser 9) 7(3):1–65
Mortensen T (1940) A monograph of the Echinoidea III. Aulodonta. With additions to Vol. II (Lepidocentroida and Stirodonta). Reitzel, Copenhagen
Muthiga NA (1996) The role of early life history strategies on the population dynamics of the sea urchin Echinometra mathaei (de Blainville) on reefs in Kenya. PhD dissertation, University of Nairobi
Ntiba MJ, Jaccarini V (1990) Gonad maturation and spawning times of Siganus sutor off the Kenyan coast: evidence for definite spawning seasons in a tropical fish. J Fish Biol 14:315–325
Nzioka RM (1979) Observations on the spawning seasons of East African reef fishes. J Fish Biol 14:329–342
Pearse JS (1968) Patterns of reproductive periodicities in four species of Indo-Pacific echinoderms. Proc Indian Acad Sci B 67:247–279
Pearse JS (1970) Reproductive periodicities of Indo-Pacific invertebrates in the gulf of Suez III. The echinoid Diadema setosum (Leske). Bull Mar Sci 20:697–720
Pearse JS (1972) A monthly reproductive rhythm in the diadematid sea urchin Centrostephanus coronatus Verrill. J Exp Mar Biol Ecol 8:167–186
Pearse JS (1990) Synchrony of monthly gametogenic cycles and possible reproductive isolation among Indo-Pacific populations of Diadema. Bull Mar Sci 47:259
Robertson DR, Polunin NVC (1981) Coexistence: symbiotic sharing of feeding territories and algal food by some coral reef fishes from the western Indian Ocean. Mar Biol 62:185–195
Ruwa RK, Polk P (1994) Patterns of spat settlement recorded for the tropical oyster Crassostrea cucullata (Born 1778) and the barnacle, Balanus amphitrite (Darwin 1854) in a mangrove creek. Trop Zool 7:121–130
Sale PF (1977) Maintenance of high diversity in coral reef fish communities. Am Nat 111:337–359
Sale PF (1980) The ecology of fishes on coral reefs. Oceanogr Mar Biol Annu Rev 18:367–421
Shpigel M, Fishelson L (1986) Behavior and physiology of coexistence in two species of Dascyllus (Pomacentridae, Teleostei). Environ Biol Fish 17:253–265
Stephenson A (1934) The breeding of reef animals, Part 11. Invertebrates other than corals. Sci Rep Great Barrier Reef Exped 3(9):247–272
Thorson G (1946) Reproduction and larval development of Danish marine bottom invertebrates with special reference to the planktonic larvae in the Sound (Oresund). Medd Komm Dan Fisk-og Havunders Plankton 4:1–518
Tuason AY, Gomez ED (1979) The reproductive biology of Tripneustes gratilla Linnaeus (Echinodermata: Echinoidea), with some notes on Diadema setosum Leske. Proc Int Symp Mar Biogeogr Evol South Hemisphere 2:707–716
Tyler A (1949) A simple non-injurious method for inducing repeated spawning of sea urchins and sand-dollars. Collect Net 19:19–20
Waldner RE, Robertson DR (1980) Patterns of habitat partitioning by eight species of territorial Caribbean damselfishes (Pisces: Pomacentridae). Bull Mar Sci 30:171–186
Yoshida M (1952) Some observations on the maturation of the sea urchin Diadema setosum. Annotnes Zool Jpn 25:265–271
Acknowledgements
My sincere thanks go to James Gonda for his field and laboratory assistance, and the Kenya Marine & Fisheries Research Institute and Coral Reef Conservation Project (CRCP) for logistical assistance. I am also grateful for the critical reviews of Dr. T.R. McClanahan and Prof. V. Jaccarini. This work was supported by a research grant from the East African Wildlife Society and the Wildlife Conservation Society through CRCP.
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Communicated by O. Kinne, Oldendorf/Luhe
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Muthiga, N.A. Coexistence and reproductive isolation of the sympatric echinoids Diadema savignyi Michelin and Diadema setosum (Leske) on Kenyan coral reefs. Marine Biology 143, 669–677 (2003). https://doi.org/10.1007/s00227-003-1095-7
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DOI: https://doi.org/10.1007/s00227-003-1095-7