Abstract
Feeding specialisation is a typical feature of adaptive animal radiations. Different kinds of feeding specialisations have evolved in the endemic sailfin silversides species flock in Lake Matano (Central Sulawesi, Indonesia), including egg-feeding. The present study focuses on Telmatherina sarasinorum, a sailfin silverside species feeding on the eggs of related Telmatherina antoniae. Stomach content analyses supported T. antoniae eggs to be the dominant food item, independent of daytime. We hypothesized that the egg-feeders use alternative tactics for maximising egg consumption under varying densities of both, spawning T. antoniae pairs and competing conspecific egg-feeders. Focal behavioural observations were applied to describe different feeding tactics and to analyse feeding success and the related costs in terms of competitive interactions. Egg-feeders followed single courting pairs of T. antoniae or, alternatively, they switched between different spawning pairs. Following-behaviour, covering one or more spawning events of the host species, was positively related to enhanced egg consumption. Compared to feeding by switching frequently among different spawning pairs, the following tactic came at the cost of likewise increased competition. Behavioural observations suggest that some males monopolize courting pairs of T. antoniae and gain increased amounts of eggs compared to others avoiding competition by switching among pairs. The present results confirm that egg-feeding is a distinct trophic specialisation in T. sarasinorum and increase the scale of behavioural specialisation in Lake Matano’s evolving Telmatherina radiation.
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Bloxam, Q. M. C., J. L. Behler, E. R. Rakatovao, H. J. A. R. Randriamahazo, K. T. Hayes, S. J. Tonge & J. U. Ganzhorn, 1996. Résumé: influences de l’exploration du bois sur la faune des reptiles de la forêt de Kirindy, en considérant particulièrement la Tortue à queue plate (Pyxis planicauda). Primate Report 46: 189–202.
Bramburger, A. J., G. D. Haffner & P. B. Hamilton, 2004. Examining the distributional patterns of the diatom flora of the Malili Lakes, Sulawesi, Indonesia. Proceedings of the 17th International Diatom Symposium, Ottawa, Canada: 11–25.
Bramburger, A. J., P. B. Hamilton, P. E. Hehanussa & G. D. Haffner, 2008. Processes regulating the community composition and relative abundance of taxa in the diatom communities of the Malili Lakes, Sulawesi Island, Indonesia. Hydrobiologia 615: 215–224.
Brooks, J. L., 1950. Speciation in ancient lakes. The Quarterly Review of Biology 25: 131–176.
Coyne, J. A. & H. A. Orr, 2004. Speciation. Sinauer Associates, Sunderland.
Crespi, B. J., 2004. Vicious circles: positive feedback in major evolutionary and ecological transitions. Trends in Ecology & Evolution 19: 627–633.
Cristescu, M., S. J. Adamowicz, J. J. Vaillant & D. G. Haffner, 2010. Ancient lakes revisited: from the ecology to the genetics of speciation. Molecular Ecology 19: 4837–4851.
Daan, R., 1987. Impact of egg predation by Noctiluca miliaris on the summer development of copepod populations in the southern North Sea. Marine Ecology Progress Series 37: 9–17.
Dieckmann, U., M. Doebeli, J. A. J. Metz & D. Tautz, 2004. Adaptive Speciation. University Press, Cambridge.
FitzGerald, J. G., 1992. Egg cannibalism by sticklebacks: spite or selfishness? Behavioural Ecology and Sociobiology 30: 201–206.
Glaubrecht, M. & T. von Rintelen, 2008. The species flocks of lacustrine gastropods: Tylomelania on Sulawesi as models in speciation and adaptive radiation. Hydrobiologia 615: 181–199.
Gray, S. M. & J. S. McKinnon, 2006. A comparative description of mating behaviour in the endemic telmatherinid fishes of Sulawesi’s Malili Lakes. Environmental Biology of Fishes 75: 471–482.
Gray, S. M., L. M. Dill & J. S. McKinnon, 2007. Cuckoldry incites cannibalism: male fish turn to cannibalism when perceived certainty of paternity decreases. The American Naturalist 169: 258–263.
Gray, S. M., J. S. McKinnon & L. M. Dill, 2008a. Sneaky egg-eating in Telmatherina sarasinorum, an endemic fish from Sulawesi. Journal of Fish Biology 73: 728–731.
Gray, S. M., L. M. Dill, F. Y. Tantu, E. R. Loew, F. Herder & J. S. McKinnon, 2008b. Environment-contingent sexual selection in a colour polymorphic fish. Proceedings of the Royal Society of London B 275: 1785–1791.
Haffner, G. D., P. E. Hehanussa & D. Hartoto, 2001. The biology and physical processes of large lakes of Indonesia: lakes Matano and Towuti. In Munawar, M. & R. E. Hecky (eds), The Great Lakes of the World (GLOW) Food Web, Health and Integrity. Backhuis, Leiden: 182–192.
Hammer, Ø., D. A. T. Harper & P. D. Ryan, 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4 [available on internet at http://palaeo-electronica.org/2001_1/past/issue1_01.htm].
Herder, F. & J. Freyhof, 2006. Resource partitioning in a tropical stream fish assemblage. Journal of Fish Biology 69: 571–589.
Herder, F. & U. Schliewen, 2010. Beyond sympatric speciation: radiation of sailfin silverside fishes in the Malili Lakes (Sulawesi). In Glaubrecht, M. & H. Schneider (eds), Evolution in Action – Adaptive Radiations and the Origins of Biodiversity. Springer, Heidelberg: 465–483.
Herder, F., A. Nolte, J. Pfaender, J. Schwarzer, R. K. Hadiaty & U. K. Schliewen, 2006a. Adaptive radiation and hybridization in Wallace’s Dreamponds: evidence from sailfin silversides in the Malili Lakes of Sulawesi. Proceedings of the Royal Society of London B 273: 2209–2217.
Herder, F., J. Schwarzer, J. Pfaender, R. K. Hadiaty & U. K. Schliewen, 2006b. Preliminary checklist of sailfin silversides (Teleostei: Telmatherinidae) in the Malili Lakes of Sulawesi (Indonesia), with a synopsis of systematics and threats. Verhandlungen der Gesellschaft für Ichthyologie 5: 139–163.
Herder, F., J. Pfaender & U. K. Schliewen, 2008. Adaptive sympatric speciation of polychromatic “roundfin” sailfin silverside fish in Lake Matano (Sulawesi). Evolution 62: 2178–2195.
Hernandez, L. P., L. A. Ferry-Graham & A. C. Gibb, 2008. Morphology of a picky eater: a novel mechanism underlies premaxillary protrusion and retraction within cyprinodontiformes. Zoology 111: 442–454.
Hirayama, S., T. Shiiba, Y. Sakai, H. Hashimoto & K. Gushima, 2005. Fish-egg predation by the small clingfish Pherallodichthys meshimaensis (Gobisocidae) on the shallow reefs of Kuchierabu-jima Island, southern Japan. Environmental Biology of Fishes 73: 237–242.
Järnegren, J., C. R. Tobias, S. A. Macko & C. M. Young, 2005. Egg predation fuels unique species association at deep-sea hydrocarbon seeps. Biological Bulletin 209: 87–93.
Kottelat, M., 1990a. Sailfin silversides (Pisces: Telmatherinidae) of Lakes Towuti, Mahalona and Wawontoa (Sulawesi, Indonesia) with descriptions of two new genera and two new species. Ichthyological Exploration of Freshwaters 1: 227–246.
Kottelat, M., 1990b. The ricefishes (Oryziidae) of the Malili Lakes, Sulawesi, Indonesia, with description of a new species. Ichthyological Exploration of Freshwaters 1: 151–166.
Kottelat, M., 1991. Sailfin silversides (Pisces: Telmatherinidae) of Lake Matano, Sulawesi, Indonesia, with descriptions of six new species. Ichthyological Exploration of Freshwaters 1: 321–344.
Kottelat, M., T. Whitten, S. N. Kartikasari & S. Wirjoatmodjo, 1993. Freshwater Fishes of Western Indonesia and Sulawesi. Periplus Editions, Hong Kong.
Light, J. E., F. C. Anthony & B. A. Porter, 2005. Egg-feeding in the freshwater pisciolid leech Cystobranchus virginicus (Annelida, Hirudinea). Invertebrate Biology 124: 50–56.
McKaye, K. R. & T. Kocher, 1983. Head ramming behaviour by three paedophagous cichlids in Lake Malawi, Africa. Animal Behaviour 31: 206–210.
McKaye, K. R. & E. P. van den Berghe, 1997. Specialized egg feeding behavior by African and Central American cichlids. Ichthyological Explorations of Freshwaters 7: 143–148.
Mehlis, M. & C. M. Bakker, 2009. Nutritional benefits of filial cannibalism in three-spined sticklebacks (Gasterosteus aculeatus). Naturwissenschaften 96: 399–403.
Norusis, M. J., 1986. SPSS/PC+ Advanced Statistics. SPSS Inc., Chicago.
Ochi, H., Y. Sato & Y. Yanagisawa, 1999. Obligate feeding of cichlid eggs by Caecomastacembelus zebratus in Lake Tanganyika. Journal of Fish Biology 54: 450–459.
Pfaender, J., U. K. Schliewen & F. Herder, 2010. Phenotypic traits meet patterns of resource use in the radiation of “sharpfin” sailfin silverside fish in Lake Matano. Evolutionary Ecology 24: 957–974.
Pfaender, J., F. W. Miesen, R. K. Hadiaty & F. Herder, 2011. Adaptive speciation and sexual dimorphism contribute to form and functional diversity in Lake Matano’s roundfin sailfin silversides adaptive radiation. Journal of Evolutionary Biology 24: 2329–2345.
Randall, J. E., 1967. Food habits of reef fishes of the West Indies. Studies in Tropical Oceanography 5: 665–847.
Ribbink, A. J. & D. S. C. Lewis, 1981. A cichlid from Lake Malawi which feeds on ectoparasites and catfish eggs. Netherlands Journal of Zoology 32: 72–87.
Ribbink, A. J. & A. C. Ribbink, 1997. Paedophagia among cichlid fishes of Lake Victoria and Lake Malawi-Nyasa. South African Journal of Science 93: 509–512.
Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford.
Schubart, C. D. & P. K. L. Ng, 2008. A new molluscivore crab from Lake Poso confirms multiple colonization of ancient lakes in Sulawesi by freshwater crabs (Decapoda: Brachyura). Zoological Journal of the Linnean Society 154: 211–221.
Schubart, C. D., T. Santl & P. Koller, 2008. Mitochondrial patterns of intra- and interspecific differentiation among endemic freshwater crabs of ancient lakes in Sulawesi. Contributions to Zoology 77: 83–90.
Schwarzer, J., F. Herder, B. Misof, R. K. Hadiaty & U. K. Schliewen, 2008. Gene flow at the margin of Lake Matano’s adaptive sailfin silverside radiation: Telmatherinidae of River Petea in Sulawesi. Hydrobiologia 615: 201–213.
Shine, R., X. Bonnet, M. J. Elphick & E. G. Barrott, 2004. A novel foraging mode in snakes: browsing by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae). Functional Ecology 18: 16–24.
Shiogaki, M. & Y. Dotsu, 1983. Two new genera and two new species of clingfishes from Japan, with comments on head sensory canals of the Gobiesocidae. Japanese Journal of Ichthyology 30: 111–121.
von Rintelen, K. & Y. Cai, 2009. Radiation of endemic species flocks in ancient lakes: systematic revision of the freshwater shrimp Caridina H. Milne Edwards, 1837 (Crustacea: Decapoda: Atyidae) from the ancient lakes of Sulawesi, Indonesia, with the description of eight new species. Raffles Bulletin of Zoology 57: 343–452.
von Rintelen, T., A. B. Wilson, A. Meyer & M. Glaubrecht, 2004. Escalation and trophic specialization drive adaptive radiation of freshwater gastropods in ancient lakes on Sulawesi, Indonesia. Proceedings of the Royal Society of London B 271: 2541–2549.
von Rintelen, T., P. Bouchet & M. Glaubrecht, 2007. Ancient lakes as hotspots of diversity: a morphological review of an endemic species flock of Tylomelania (Gastropoda: Cerithioidea: Pachychilidae) in the Malili lake system on Sulawesi, Indonesia. Hydrobiologia 592: 11–94.
von Rintelen, K., M. Glaubrecht, C. D. Schubart, A. Wessel & T. von Rintelen, 2010. Adaptive radiation and ecological diversification of Sulawesi’s ancient lake shrimps. Evolution 64: 3287–3299.
von Rintelen, T. & K. von Rintelen, M. Glaubrecht, C. D. Schubart & F. Herder, in press. Aquatic biodiversity hotspots in Wallacea – the species flocks in the ancient lakes of Sulawesi, Indonesia. In Gower, D. J., K. G. Johnson, J. E. Richardson, B. R. Rosen, L. Rüber & S. T. Williams (eds), Biotic Evolution and Environmental Change in Southeast Asia. Cambridge University Press, Cambridge.
Walter, R. P., G. D. Haffner & D. D. Heath, 2009a. Dispersal and population genetic structure of Telmatherina antoniae, an endemic freshwater sailfin silverside from Sulawesi, Indonesia. Journal of Evolutionary Biology 22: 314–323.
Walter, R. P., G. D. Haffner & D. D. Heath, 2009b. No barriers to gene flow among sympatric polychromatic ‘small’ Telmatherina antoniae from Lake Matano, Indonesia. Journal of Fish Biology 74: 1804–1815.
Whoriskey, F. G. & J. G. FitzGerald, 1985. Sex, cannibalism and sticklebacks. Behavioural Ecology and Sociobiology 18: 15–18.
Wilhelm, W., 1980. The disputed feeding behaviour of paedophagous Haplochromine cichlid (Pisces) observed and discussed. Behaviour 74: 310–323.
Acknowledgments
We thank the Indonesian Institute of Sciences (LIPI) for the permit to conduct research in Indonesia. PT. INCO provided outstanding logistic support in Sulawesi. J. Pfaender helped with stomach analyses, determination of contents and insightful discussions. Analyses and manuscript preparation benefited from critical comments and suggestions by J. Pfaender, N. Straube, A. Dunz, J. G. Frommen, S. M. Gray, E. Mussard-Forster, M. Geiger, K. Lindner and four anonymous referees. This study was funded by a research grant to U.K.S. from the Deutsche Forschungsgemeinschaft (DFG SCHL 567/3).
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Cerwenka, A.F., Wedekind, J.D., Hadiaty, R.K. et al. Alternative egg-feeding tactics in Telmatherina sarasinorum, a trophic specialist of Lake Matano’s evolving sailfin silversides fish radiation. Hydrobiologia 693, 131–139 (2012). https://doi.org/10.1007/s10750-012-1099-8
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DOI: https://doi.org/10.1007/s10750-012-1099-8