Abstract
Males of many species display conspicuous colors to attract mates and deter rivals, although this benefit can incur an increased predation risk. In the African cichlid fish, Astatotilapia burtoni, males can change both their social status (dominant, DOM, or subordinate, SUB) and primary body color (yellow or blue). We hypothesized that these phenotypes vary in conspicuousness to predators and conspecifics, thus establishing a trade-off between intraspecific signaling and predation. We quantified the spectral reflectance of yellow and blue DOM and SUB males. We then constructed avian and conspecific visual receiver models to determine the relative conspicuousness of each phenotype. We show that there are significant differences in conspicuousness to predators and conspecifics, with the flanks of the yellow DOM males exhibiting more spectral contrast to both avian predators and conspecifics than the flanks of blue DOM males. Our measurements of escape behavior revealed that each morph exhibits distinct anti-predatory responses, with SUB males shoaling for protection, and the more conspicuous yellow DOM males executing more escape responses, potentially compensating for their increased conspicuousness. Our results suggest a novel mechanism for the maintenance of alternative male phenotypes in this species, where dynamically enhanced conspicuousness is offset by plastic changes in behavior.
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References
Adams, C. F., N. R. Liley & B. B. Gorzalka, 1996. PCPA increases aggression in male firemouth cichlids. Pharmacology 53: 328–330.
Barlow, G. W., W. Rogers & N. Fraley, 1986. Do Midas cichlids win through prowess or daring? It depends. Behavioral Ecology and Sociobiology 19: 1–8.
Border, S. E., T. J. Piefke, R. J. Fialkowski, M. R. Tryc, T. R. Funnell, G. M. DeOliveira & P. D. Dijkstra, 2019. Color change and pigmentation in a color polymorphic cichlid fish. Hydrobiologia 832: 175–191.
Casagrand, J. L., A. L. Guzik & R. C. Eaton, 1999. Mauthner and reticulospinal responses to the onset of acoustic pressure and acceleration stimuli. Journal of Neurophysiology 82: 1422–1437.
Chiao, C. C., J. K. Wickiser, J. J. Allen, B. Genter & R. T. Hanlon, 2011. Hyperspectral imaging of cuttlefish camouflage indicates good color match in the eyes of fish predators. Proceedings of the National Academy of Sciences USA 108: 9148–9153.
Claes, J. M. & J. Mallefet, 2010. The lantern shark’s light switch: turning shallow water crypsis into midwater camouflage. Biology Letters 6: 685–687.
Coulter, G. W., 1992. Lake Tanganyika and its life. Oxford University Press, Oxford.
Crothers, L. R. & M. E. Cummings, 2013. Warning signal brightness variation: sexual selection may work under the radar of natural selection in populations of a polytypic poison frog. American Naturalist 181: E116–E124.
Cummings, M. E., 2004. Modelling divergence in luminance and chromatic detection performance across measured divergence in surfperch (Embiotocidae) habitats. Vision Research 44: 1127–1145.
Cummings, M. E., 2007. Sensory trade-offs predict signal divergence in surfperch. Evolution. 61: 530–545.
Cummings, M. E. & J. C. Partridge, 2001. Visual pigments and optical habitats of surfperch (Embiotocidae) in the California kelp forest. Journal of Comparative Physiology A 187: 875–889.
Cummings, M. E., X. E. Bernal, R. Reynaga, A. S. Rand & M. J. Ryan, 2008. Visual sensitivity to a conspicuous male cue varies by reproductive state in Physalaemus pustulosus females. Journal of Experimental Biology 211: 1203–1210.
Dalton, B. E., T. W. Cronin, N. J. Marshall & K. L. Carleton, 2010. The fish eye view: are cichlids conspicuous? Journal of Experimental Biology 213: 2243–2255.
Dijkstra, P. D., R. Hekman, R. Schulz & T. G. Groothuis, 2007. Social stimulation, nuptial colouration, androgens and immunocompetence in a sexual dimorphic cichlid fish. Behavioral Ecolology & Sociobiology 61: 599–609.
Dijkstra, P. D., C. Hemelrijk, O. Seehausen & T. G. G. Groothuis, 2009. Color polymorphism and intrasexual competition in assemblages of cichlid fish. Behavioral Ecolology 20: 138–144.
Dijkstra, P. D., S. M. Maguire, R. M. Harris, A. A. Rodriguez, R. S. DeAngelis, S. A. Flores & H. A. Hofmann, 2017. The melanocortin system regulates body pigmentation and social behaviour in the cichlid fish Astatotilapia burtoni. Proceedigs of the Royal Society B 284: 20162838.
Endler, J., 1978. A predator’s view of animal color patterns. Evolutionary Biology 11: 319–364.
Endler, J., 1991. Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. Vision Research 31: 587–608.
Endler, J., 1992. Signals, signal conditions, and the direction of evolution. American Naturalist 139(Supplement): S125–S153.
Escobar-Camacho, D., J. Marshall & K. L. Carleton, 2017. Behavioral color vision in a cichlid fish: Metriaclima benetos. Journal of Experimental Biology 220: 2887–2899.
Escobar-Camacho, D., M. A. Taylor, K. L. Cheney, N. F. Green, N. J. Marshall & K. L. Carleton, 2019. Color discrimination thresholds in a cichlid fish Metriaclima benetos. Journal of Experimental Biology 222: jeb201160.
Faber, D. S. & H. Korn, 1978. Neurobiology of the Mauthner Cell. Raven Press, New York.
Fernald, R. D., 1977. Quantitative behavioural observations of Haplochromis burtoni under semi-natural conditions. Animal Behaviour 25: 643–653.
Fernald, R. D. & N. R. Hirata, 1977. Field study of Haplochromis burtoni: quantitative behavioural observations. Animal Behaviour 25: 964–975.
Fernald, R. D. & P. A. Liebman, 1980. Visual receptor pigments in the African cichlid fish, Haplochromis burtoni. Vision Research 20: 857–864.
Godin, J.-G. J. & K. A. V. Clark, 1997. Risk-taking in stickleback fishes faced with different predatory threats. Ecoscience 4: 246–251.
Goldsmith, T. H. & B. K. Butler, 2003. The roles of receptor noise and cone oil droplets in the photopic spectral sensitivity of the budgerigar, Melopsittacus undulatus. Journal of Comparative Physiology A 189: 135–142.
Handegard, N. O., K. M. Boswell, C. C. Ioannou, S. P. Leblanc, D. B. Tjøstheim & I. D. Couzin, 2012. The dynamics of coordinated group hunting and collective information transfer among schooling prey. Current Biology 22: 1213–1217.
Hawryshyn, C. W., 1991. Light-adaptation properties of the ultraviolet-sensitive cone mechanism in comparison to the other receptor mechanisms of goldfish. Visual Neuroscience 6: 293–301.
Heiligenberg, W., U. Kramer & V. Schulz, 1972. The angular orientation of the black eye-bar in Haplochromis burtoni (Cichlidae, Pisces) and its relevance to aggressivity. Zeitschrift für Vergleichende Physiology 76: 168–176.
Hofmann, H. A., 2003. Functional genomics of neural and behavioral plasticity. Journal of Neurobiology 54: 272–282.
Hofmann, H. A., M. E. Benson & R. E. Fernald, 1999. Social status regulates growth rate: consequences for life-history strategies. Proceedings of the National Academy of Sciences USA 96: 14171–14176.
Huffman, L. S., M. M. Mitchell, L. A. O’Connell & H. A. Hofmann, 2012. Rising StARs: behavioral, hormonal, and molecular responses to social challenge and opportunity. Hormones and Behavior 61: 631–641.
Husak, J. F., J. M. Macedonia, S. F. Fox & R. C. Sauceda, 2006. Predation cost of conspicuous male coloration in collared lizards (Crotaphytus collaris): an experimental test using clay-covered model lizards. Ethology 112: 572–580.
Jeschke, J. M. & R. Tollrian, 2007. Prey swarming: which predators become confused and why? Animal Behavior 74: 387–393.
Korn, H. & D. S. Faber, 2005. The Mauthner cell half a century later: a neurobiological model for decision-making? Neuron 47: 13–28.
Korzan, W. J. & R. D. Fernald, 2007. Territorial male color predicts agonistic behavior of conspecifics in a color polymorphic species. Behavioral Ecology 18: 318–323.
Korzan, W. J., R. R. Robison, S. Zhao & R. D. Fernald, 2008. Color change as a potential behavioral strategy. Hormones & Behavior 54: 463–470.
Leong, C.-Y., 1969. The quantitative effect of releasers on the attack readiness of the fish Haplochromis burtoni (Cichlidae, Pisces). Zeitschrift für Vergleichende Physiologie 65: 29–50.
Loveland, J. L., N. Uy, K. P. Maruska, R. E. Carpenter & R. D. Fernald, 2014. Social status differences regulate the serotonergic system of a cichlid fish, Astatotilapia burtoni. Journal of Experimental Biology 217: 2680–2690.
Maan, M. E. & M. E. Cummings, 2012. Poison frog colors are honest signals of toxicity, particularly for bird predators. American Naturalist 179: E1–E14.
Maan, M. E., B. Eshuis, M. P. Haesler, M. V. Schneider, J. J. M. van Alphen & O. Seehausen, 2008. Color polymorphism and Predation in a Lake Victoria Cichlid fish. Copeia 2008: 621–629.
Miczek, K. A., R. M. de Almeida, E. A. Kravitz, E. F. Rissman, S. F. de Boer & A. Raine, 2007. Neurobiology of escalated aggression and violence. Journal of Neuroscience 27: 11803–11806.
Munro, A. D., 1986. Effects of melatonin, serotonin, and naloxone on aggression in isolated cichlid fish (Aequidens pulcher). Journal of Pineal Research 3: 257–262.
Muske, L. E. & R. D. Fernald, 1987. Control of a teleost social signal. I. Neural basis for differential expression of a color pattern. Journal of Comparative Physiology A 160: 99–107.
Neumeister, H., K. W. Whitaker, H. A. Hofmann & T. Preuss, 2010. Social and ecological regulation of a decision-making circuit. Journal of Neurophysiology 104: 3180–3188.
O’Connell, L. A. & H. A. Hofmann, 2012. Social status predicts how sex steroid receptors regulate complex behavior across levels of biological organization. Endocrinology 153: 1341–1351.
Ödeen, A. & O. Håstad, 2003. Complex distribution of avian colour vision systems revealed by sequencing the SWS1 opsin from total DNA. Molecular Biology & Evolution 20: 855–861.
Preuss, T. & D. S. Faber, 2003. Central cellular mechanisms underlying temperature-dependent changes in the goldfish startle-escape behavior. Journal of Neuroscience 23: 5617–5626.
Preuss, T., P. E. Osei-Bonsu, S. A. Weiss, C. Wang & D. S. Faber, 2006. Neural representation of object approach in a decision-making motor circuit. Journal of Neuroscience 26: 3454–3464.
Pryke, S. R. & S. C. Griffith, 2006. Red dominates black: agonistic signalling among head morphs in the colour polymorphic Gouldian finch. Proceedings of the Royal Society B 273: 949–957.
Pryke, S. R. & S. C. Griffith, 2009. Socially mediated trade-offs between aggression and parental effort in competing color morphs. American Naturalist 174: 455–464.
Renn, S. C. P., N. Aubin-Horth & H. A. Hofmann, 2008. Fish & chips: functional genomics of social plasticity in an African cichlid fish. Journal of Experimental Biology 211: 3041–3056.
Reyer, H.-U., 1980. Flexible helper structure as an ecological adaptation in the pied kingfisher. Behavioral Ecology & Sociobiology 6: 219–227.
Reyer, H.-U., W. Migongo-Bake & L. Schmidt, 1988. Field studies and experiments on distribution and foraging of pied and malachite kingfishers at Lake Nakuru (Kenya). Journal of Animal Ecology 57: 595–610.
Ryan, M. J. & M. E. Cummings, 2013. Perceptual biases and mate choice. Annual Reviews in Ecology Evolution & Systematics 44: 437–459.
Sanchez-Guillen, R. A., H. Van Gossum & A. Cordero Rivera, 2005. Hybridization and the inheritance of female colour polymorphism in two ischnurid damselflies (Odonata: Coenagrionidae). Biological Journal of the Linnean Society 85: 471–481.
Shuster, S. M. & M. J. Wade, 2003. Mating systems and strategies. In Krebs, J. R. & T. H. Clutton-Brock (eds), Monographs in Behavior and Ecology. Princeton University Press, Princeton.
Sinervo, B. & C. M. Lively, 1996. The rock-paper-scissors game and the evolution of alternative male strategies. Nature 380: 240–243.
Stobbe, N. & H. M. Schaefer, 2008. Enhancement of chromatic contrast increases predation risk for striped butterflies. Proceedings of the Royal Society B 275: 1535–1541.
Stuart-Fox, D. M., A. Moussalli, N. J. Marshall & I. P. F. Owens, 2003. Conspicuous males suffer higher predation risk: visual modelling and experimental evidence from lizards. Animal Behaviour 66: 541–550.
Torres-Dowdall, J., J. Golcher-Benavides, G. Machado-Schiaffino & A. Meyer, 2017. The role of rare morph advantage and conspicuousness in the stable gold-dark colour polymorphism of a crater lake Midas cichlid fish. Journal of Animal Ecology 86: 1044–1053.
Veenema, A. H., 2009. Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: what can we learn from animal models? Frontiers in Neuroendocrinology 30: 497–518.
Vorobyev, M. & D. Osorio, 1998. Receptor noise as a determinant of colour thresholds. Proceedings of the Royal Society B 265: 351–358.
Vorobyev, M., R. Brandt, D. Peitsch, S. B. Laughlin & R. Menzel, 2001. Colour thresholds and receptor noise: behaviour and physiology compared. Vision Research 41: 639–653.
Wanink, J. H. & K. Goudswaard, 1994. Effects of Nile perch (Lates niloticus) introduction into Lake Victoria, East Africa, on the diet of pied kingfishers (Ceryle rudis). Hydrobiologia 279: 367–376.
Weiss, S. A., S. J. Zottoli, S. C. Do, D. S. Faber & T. Preuss, 2006. Correlation of C-start behaviors with neural activity recorded from the hindbrain in free-swimming goldfish (Carassius auratus). Journal of Experimental Biology 209: 4788–4801.
Whitaker, K. W., H. Neumeister, L. S. Huffman, C. E. Kidd, T. Preuss & H. A. Hofmann, 2011. Serotonergic modulation of startle-escape plasticity in an African cichlid fish: a single-cell molecular and physiological analysis of a vital neural circuit. Journal of Neurophysiology 106: 127–137.
Whitfield, A. K. & S. J. M. Blaber, 1978. Food and feeding ecology of piscivorous fishes at Lake St Lucia, Zululand. Journal of Fish Biology 13: 675–691.
Winberg, S., Y. Winberg & R. D. Fernald, 1997. Effect of social rank on brain monoaminergic activity in a cichlid fish. Brain Behavior & Evolution 49: 230–236.
Zottoli, S. J., B. C. Newman, H. I. Rieff & D. C. Winters, 1999. Decrease in occurrence of fast startle responses after selective Mauthner cell ablation in goldfish (Carassius auratus). Journal of Comparative Physiology A 184: 207–218.
Acknowledgements
We thank Donald Faber for the loan of a high-speed camera and Harold Zakon for generous access to his laboratory. We also thank Kat Ruddick and Kendra Zwonitzer for technical assistance and Laura Crothers, Leslie Whitaker, and Rebecca Young-Brim for critically reading earlier versions of this manuscript. Thanks to all of the members of the Hofmann and Preuss laboratories for discussions. This work was supported by the Department of Defense SMART program (K. W. Whitaker); National Science Foundation (NSF)-IOS Grants IOS 0946637, IOS 11471172, and the Professional Staff Congress (PSC)-CUNY Research Award Program (T. Preuss); and NSF-IOS Grant 0751311, the Alfred P. Sloan Foundation, and the Institute for Cellular and Molecular Biology at The University of Texas at Austin (H. A. Hofmann).
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Whitaker, K.W., Alvarez, M., Preuss, T. et al. Courting danger: socially dominant fish adjust their escape behavior and compensate for increased conspicuousness to avian predators. Hydrobiologia 848, 3667–3681 (2021). https://doi.org/10.1007/s10750-020-04475-9
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DOI: https://doi.org/10.1007/s10750-020-04475-9