Alternative reproductive tactics (ARTs) are found in several Lake Tanganyika shell-brooding cichlids. Field studies were conducted in the Wonzye population to examine reproductive ecology and ARTs in the Lake Tanganyika shell-brooding cichlid Neolamprologus brevis. We discovered that this fish occurred in both rocky- and sandy-bottom habitats, but in rocky habitats, brood-caring females exclusively occurred in shell-patches that another cichlid species created. All N. brevis of both sexes in the patches were sexually mature, whereas immature males and females with unripe eggs were found frequently in sandy-bottom habitats. Males in sandy-bottom habitats were smaller, but fed more frequently and were in better somatic condition than males in the patches. Similar tendency was found in females. This indicates that N. brevis uses different habitats depending on the stage of its life history, with migration from sandy-bottom habitats to the shell-patches for reproduction. Males in the patches exhibited different behavior patterns: floating above the patches and lying in the patches. The former was larger, more aggressive, and invested less in gonads (relative to body size) than the latter. These results accord with those of other shell-brooding Lake Tanganyika cichlids with ARTs, and they therefore suggest the presence of ARTs in N. brevis. 1. Introduction In species where males hold the resources required for breeding, reproductive behavior is often associated with “bourgeois” territorial tactics that involve defense of resources in an attempt to monopolize mating opportunities [1–4]. Bourgeois tactics are usually adopted by males who achieve competitive superiority (and also attractiveness) thorough behavioral (e.g., antagonistic behaviors) and morphological investments (e.g., large body size). These exclude less competitive males from reproduction. Such intrasexual competition for mating may lead to the evolution of alternative reproductive tactics (ARTs) [5, 6]. Competitively inferior, less attractive, and smaller subordinate males are unlikely to monopolize opportunities for mating, but they may evade monopolization by bourgeois males by using reproductively “parasitic” tactics that often involve “sneaky” behavior and the theft of reproductive efforts by bourgeois males [1, 3, 4, 6]. ARTs inherently give rise to sperm competition, that is, a competition among sperm from different males for the fertilization of ova [7]. Subordinate males exhibiting “sneaky” mating behavior (i.e., sneakers) face a high probability that their sperm will encounter sperm
References
[1]
M. Taborsky, “Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction,” Advances in the Study of Behavior, vol. 23, pp. 1–100, 1994.
[2]
M. Taborsky, “Bourgeois and parasitic tactics: do we need collective, functional terms for alternative reproductive behaviours?” Behavioral Ecology and Sociobiology, vol. 41, no. 5, pp. 361–362, 1997.
[3]
M. Taborsky, “The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes,” Journal of Heredity, vol. 92, no. 2, pp. 100–110, 2001.
[4]
M. R. Gross, “Alternative reproductive strategies and tactics: diversity within sexes,” Trends in Ecology and Evolution, vol. 11, no. 2, pp. 92–98, 1996.
[5]
S. M. Shuster and M. J. Wade, Mating Systems and Strategies, Princeton University Press, Princeton, NJ, USA, 2003.
[6]
R. F. Oliveira, M. Taborsky, and H. J. Brockmann, Alternative Reproductive Tactics: An Integrative Approach, Cambridge University Press, Cambridge, UK, 2008.
[7]
G. A. Parker, “Sperm competition and the evolution of ejaculates: towards a theory base,” in Sperm Competition and Sexual Selection, T. R. Birkhead and A. P. M？ller, Eds., pp. 3–54, Academic Press, Cambridge, UK, 1998.
[8]
G. A. Parker, “Sperm competition games: sneaks and extra-pair copulations,” Proceedings of the Royal Society B, vol. 242, no. 1304, pp. 127–133, 1990.
[9]
M. J. Gage, P. Stockley, and G. A. Parker, “Effects of alternative male mating strategies on characteristics of sperm production in the Atlantic salmon (Salmo salar): theoretical and empirical investigations,” Philosophical Transactions of the Royal Society B, vol. 350, no. 1334, pp. 391–399, 1995.
[10]
L. W. Simmons, J. L. Tomkins, and J. Hunt, “Sperm competition games played by dimorphic male beetles,” Proceedings of the Royal Society B, vol. 266, no. 1415, pp. 145–150, 1999.
[11]
B. Leach and R. Montgomerie, “Sperm characteristics associated with different male reproductive tactics in bluegills (Lepomis macrochirus),” Behavioral Ecology and Sociobiology, vol. 49, no. 1, pp. 31–37, 2000.
[12]
I. Uglem, G. Rosenqvist, and H. S. Wasslavik, “Phenotypic variation between dimorphic males in corkwing wrasse,” Journal of Fish Biology, vol. 57, no. 1, pp. 1–14, 2000.
[13]
T. V. Vladi？ and T. J？rvi, “Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism,” Proceedings of the Royal Society B, vol. 268, no. 1483, pp. 2375–2381, 2001.
[14]
B. D. Neff, P. Fu, and M. R. Gross, “Sperm investment and alternative mating tactics in bluegill sunfish (Lepomis macrochirus),” Behavioral Ecology, vol. 14, no. 5, pp. 634–641, 2003.
[15]
C. C. Drilling and M. S. Grober, “An initial description of alternative male reproductive phenotypes in the bluebanded goby, Lythrypnus dalli (Teleostei, Gobiidae),” Environmental Biology of Fishes, vol. 72, no. 4, pp. 361–372, 2005.
[16]
M. Taborsky, “Alternative reproductive tactics in fish,” in Alternative Reproductive Tactics, R. F. Oliveira, M. Taborsky, and H. J. Brockmann, Eds., Cambridge University Press, Cambridge, UK, 2008.
[17]
J. L. Tomkins and L. W. Simmons, “Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics,” Animal Behaviour, vol. 63, no. 5, pp. 1009–1016, 2002.
[18]
K. Ota, M. Kohda, M. Hori, and T. Sato, “Parker’s sneak-guard model revisited: why do reproductively parasitic males heavily invest in testes?” Naturwissenschaften, vol. 98, pp. 837–843, 2011.
[19]
K. M. Sefc, “Mating and parental care in lake tanganyika's cichlids,” International Journal of Evolutionary Biology, vol. 2011, pp. 470–875, 2011.
[20]
M. P. Haesler, C. M. Lindeyer, and M. Taborsky, “Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth-brooding cichlid Ophthalmotilapia ventralis,” Journal of Fish Biology, vol. 75, no. 7, pp. 1845–1856, 2009.
[21]
S. Awata, D. Heg, H. Munehara, and M. Kohda, “Testis size depends on social status and the presence of male helpers in the cooperatively breeding cichlid Julidochromis ornatus,” Behavioral Ecology, vol. 17, no. 3, pp. 372–379, 2006.
[22]
S. Awata, T. Takeyama, Y. Makino, Y. Kitamura, and M. Kohda, “Cooperatively breeding cichlid fish adjust their testis size but not sperm traits in relation to sperm competition risk,” Behavioral Ecology and Sociobiology, vol. 62, no. 11, pp. 1701–1710, 2008.
[23]
M. Kohda, D. Heg, Y. Makino et al., “Living on the wedge: female control of paternity in a cooperatively polyandrous cichlid,” Proceedings of the Royal Society B, vol. 276, no. 1676, pp. 4207–4214, 2009.
[24]
P. Dierkes, M. Taborsky, and R. Achmann, “Multiple paternity in the cooperatively breeding fish Neolamprologus pulcher,” Behavioral Ecology and Sociobiology, vol. 62, no. 10, pp. 1581–1589, 2008.
[25]
T. Sato and M. M. Gashagaza, “Shell-brooding cichlid fishes of Lake Tanganyika: their habitats and mating systems,” in Fish communities in Lake Tanganyika, H. Kawanabe, M. Hori, and M. Nagoshi, Eds., pp. 219–240, Kyoto University Press, Kyoto, Japan, 1997.
[26]
D. Schütz, G. Pachler, E. Ripmeester, O. Goffinet, and M. Taborsky, “Reproductive investment of giants and dwarfs: specialized tactics in a cichlid fish with alternative male morphs,” Functional Ecology, vol. 24, no. 1, pp. 131–140, 2010.
[27]
K. Ota, M. Kohda, and T. Sato, “Why are reproductively parasitic fish males so small?-influence of tactic-specific selection,” Naturwissenschaften, vol. 97, no. 12, pp. 1113–1116, 2010.
[28]
R. Katoh, H. Munehara, and M. Kohda, “Alternative male mating tactics of the substrate brooding cichlid Telmatochromis temporalis in Lake Tanganyika,” Zoological Science, vol. 22, no. 5, pp. 555–561, 2005.
[29]
S. K. Mboko and M. Kohda, “Piracy mating by large males in a monogamous substrate-breeding cichlid in Lake Tanganyika,” Journal of Ethology, vol. 17, no. 1, pp. 51–55, 1999.
[30]
K. Ota and M. Kohda, “Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika,” Journal of Ethology, vol. 24, no. 1, pp. 9–15, 2006.
[31]
K. Ota, M. Hori, and M. Kohda, “Changes in reproductive life-history strategies in response to nest density in a shell-brooding cichlid, Telmatochromis vittatus,” Naturwissenschaften, vol. 9, pp. 23–31, 2012.
[32]
T. Sunobe and H. Munehara, “Mating system and kin relationship between adults and young in the shell-brooding cichlid fish Neolamprologus meeli in Lake Tanganyika,” Journal of Ethology, vol. 21, no. 2, pp. 87–92, 2003.
[33]
K. M. Sefc, K. Mattersdorfer, C. Sturmbauer, and S. Koblmüller, “High frequency of multiple paternity in broods of a socially monogamous cichlid fish with biparental nest defence,” Molecular Ecology, vol. 17, no. 10, pp. 2531–2543, 2008.
[34]
M. Aibara, Biology and taxonomy of Neolamprologus brevis species complex from LakeTanganyika (Perciformes: Cichlidae) [Ph.D. thesis], Hokkaido University, 2005.
[35]
A. Konings, Tanganyika Cichlids in Their Natural Habitats, Cichlid Press, St. Leon-Rot, Germany, 1998.
[36]
T. Sato, “Active accumulation of spawning substrate: a determinant of extreme polygyny in a shell-brooding cichlid fish,” Animal Behaviour, vol. 48, no. 3, pp. 669–678, 1994.
[37]
T. Sato, M. Hirose, M. Taborsky, and S. Kimura, “Size-dependent male alternative reproductive tactics in the shell-brooding cichlid fish Lamprologus callipterus in Lake Tanganyika,” Ethology, vol. 110, no. 1, pp. 49–62, 2004.
[38]
M. R. Gross, “Sneakers, satellites and parentals: polymorphic mating strategies in North American sunfishes,” Zeitschrift fur Tierpsychologie, vol. 60, no. 1, pp. 1–26, 1982.
[39]
K. Nakai, Y. Yanagisawa, T. Sato, Y. Niimura, and M. M. Gashagaza, “Lunar synchronization of spawning in cichlid fishes of the tribe Lamprologini in Lake Tanganyika,” Journal of Fish Biology, vol. 37, no. 4, pp. 589–598, 1990.
[40]
Y. Takeuchi, H. Ochi, M. Kohda, D. Sinyinza, and M. Hori, “A 20-year census of a rocky littoral fish community in Lake Tanganyika,” Ecology of Freshwater Fish, vol. 19, no. 2, pp. 239–248, 2010.
[41]
T. Hidaka and S. Takahashi, “Reproductive strategy and interspecific competition in the Lake-living gobiid fish isaza, Chaenogobius isaza,” Journal of Ethology, vol. 5, no. 2, pp. 185–196, 1987.
[42]
E. E. Werner and D. J. Hall, “Ontogenetic habitat shifts in bluegill: the foraging rate-predation risk trade-off,” Ecology, vol. 69, no. 5, pp. 1352–1366, 1988.
[43]
M. R. Gross, “Evolution of diadromy in fishes,” American Fisheries Society Symposium, vol. 1, pp. 14–25, 1987.
[44]
R. M. McDowall, “The evolution of diadromy in fishes (revisited) and its place in phylogenetic analysis,” Reviews in Fish Biology and Fisheries, vol. 7, no. 4, pp. 443–462, 1997.
[45]
S. J. Pittman and C. A. McAlpine, “Movements of marine fish and decapod crustaceans: process, theory and application,” Advances in Marine Biology, vol. 44, pp. 205–294, 2003.
[46]
C. E. Johnston, “Nest association in fishes: evidence for mutualism,” Behavioral Ecology and Sociobiology, vol. 35, no. 6, pp. 379–383, 1994.
[47]
J. L. Fitzpatrick, J. K. Desjardins, K. A. Stiver, R. Montgomerie, and S. Balshine, “Male reproductive suppression in the cooperatively breeding fish Neolamprologus pulcher,” Behavioral Ecology, vol. 17, no. 1, pp. 25–33, 2006.
[48]
T. H. Clutton-Brock, “Mammalian mating systems,” Proceedings of the Royal Society of London, Series B, vol. 236, no. 1285, pp. 339–372, 1989.
[49]
D. Schütz, G. A. Parker, M. Taborsky, and T. Sato, “An optimality approach to male and female body sizes in an extremely size-dimorphic cichlid fish,” Evolutionary Ecology Research, vol. 8, no. 8, pp. 1393–1408, 2006.
[50]
D. Schütz and M. Taborsky, “The influence of sexual selection and ecological constraints on an extreme sexual size dimorphism in a cichlid,” Animal Behaviour, vol. 70, no. 3, pp. 539–549, 2005.
[51]
K. Ota, M. Kohda, and T. Sato, “Unusual allometry for sexual size dimorphism in a cichlid where males are extremely larger than females,” Journal of Biosciences, vol. 35, no. 2, pp. 257–265, 2010.
