Abstract
Carotenoid pigments have myriad functions in fish, including coloration and immunity. The “carotenoid trade-off hypothesis” posits that dietary limitation of carotenoids imposes constraints on animals to allocate to one function at the expense of another. This hypothesis rarely has been tested in fish. We quantified tissue carotenoids in breeding and non-breeding female convict cichlids in Lake Xiloá, Nicaragua. This species is reverse sexually dichromatic such that females possess carotenoid-based coloration that males lack. We also collected algae samples near nest sites to assess carotenoid availability, recorded water depth, and examined cichlids’ behavioral interactions with pair mates, conspecifics, heterospecific competitors, and predators. Each of these, we predicted, would mediate potential carotenoid trade-offs. We found that non-breeding females had significantly higher levels of carotenoids in their integument, liver, and gonads compared to breeding fish. We found that algae and total carotenoids declined with depth across our study transects at 9, 11, 13, and 15 m, but the concentration of carotenoids (ng carotenoid g−1 algae, or algal quality) did not vary with depth. Furthermore, relationships among carotenoid concentrations of the three tissue types did not vary with depth, and female color status (orange or not) was not affected by behavioral interactions with other community members, reproductive status, or water depth. Our results support previous studies showing that carotenoid pigmentation may serve a signal function that facilitates the establishment of non-breeding females within the breeding population. Our study also uncovered no evidence indicating that carotenoids are limiting in the diet of breeding female convict cichlids.
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References
Ahmadi MR, Bazyar AA, Safi S, Ytrestøyl T, Bjerkeng B (2006) Effects of dietary astaxanthin supplementation on reproductive characteristics of rainbow trout (Oncorhynchus mykiss). J Appl Ichthyol 22:388–394. https://doi.org/10.1111/j.1439-0426.2006.00770.x
Allgayer R (2001) Description d’un genre nouveau, Cryptoheros, d’Amerique Centrale et d’une espece nouvelle du Panama (Pisces: Cichlidae). L’An Cichlide 1:13–20
Anderson C, Wong SC, Fuller A, Zigelski K, Earley RL (2015) Carotenoid-based coloration is associated with predation risk, competition, and breeding status in female convict cichlids (Amatitlania siquia) under field conditions. Environ Biol Fish 98:1005–1013. https://doi.org/10.1007/s10641-014-0333-9
Anderson C, Jones R, Moscicki M, Clotfelter ED, Earley RL (2016) Seeing orange: breeding convict cichlids exhibit heightened aggression against more colorful intruders. Behav Ecol Sociobiol 70:647–657. https://doi.org/10.1007/s00265-016-2085-3
Baeta R, Faivre B, Motreuil S, Gaillard M, Moreau J (2008) Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird (Turdus merula). Proc R Soc Lond B 275:427–434. https://doi.org/10.1098/rspb.2007.1383
Bagley JC, Matamoros WA, McMahan CD, Tobler M, Chakrabarty P, Johnson JB (2016) Phylogeography and species delimitation in convict cichlids (Cichlidae: Amatitlania): implications for taxonomy and Plio-Pleistocene evolutionary history in Central America. Biol J Linn Soc 120:155–170. https://doi.org/10.1111/bij.12845
Beeching SC, Gross SH, Bretz HS, Hariatis E (1998) Sexual dichromatism in convict cichlids: the ethological significance of female ventral coloration. Anim Behav 56:1021–1026. https://doi.org/10.1006/anbe.1998.0868
Brown AC, McGraw KJ, Clotfelter ED (2013) Dietary carotenoids increase yellow nonpigment coloration of female convict cichlids (Amantitlania nigrofasciata). Physiol Biochem Zool 86:312–322. https://doi.org/10.1086/670734
Brown AC, Leonard HM, McGraw KJ, Clotfelter ED (2014) Maternal effects of carotenoid supplementation in an ornamented cichlid fish. Funct Ecol 28:612–620. https://doi.org/10.1111/1365-2435.12205
Brown AC, Cahn MD, Choi S, Clotfelter ED (2016) Dietary carotenoids and bacterial infection in wild and domestic convict cichlids (Amatitlania spp.). Environ Biol Fishes 99:439–449. https://doi.org/10.1007/s10641-016-0485-x
Bussing WA (1998) Freshwater fishes of Costa Rica, 2nd edn. Editorial de la Universidad de Costa Rica, San Jose
Cavraro F, Gheno G, Ganzerla R, Zucchetta M, Franzoi P, Malavasi S (2018) Habitat constraints on carotenoid-based coloration in a small euryhaline teleost. Ecol Evol 8:4422–4430. https://doi.org/10.1002/ece3.4003
Clotfelter ED, Ardia DR, McGraw KJ (2007) Red fish, blue fish: trade-offs between pigmentation and immunity in Betta splendens. Behav Ecol 18:1139–1145. https://doi.org/10.1093/beheco/arm090
Constantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370. https://doi.org/10.1111/j.1365-2435.2007.01366.x
de Carvalho CCCR, Caramujo MJ (2017) Carotenoids in aquatic ecosystems and aquaculture: a colorful business with implications for human health. Front Mar Sci 4:93. https://doi.org/10.3389/fmars.2017.00093
Deutsch JC (1997) Colour diversification in Malawi cichlids: evidence for adaptation, reinforcement or sexual selection? Biol J Linn Soc 62:1–14. https://doi.org/10.1111/j.1095-8312.1997.tb01614.x
Garner SR, Neff BD, Bernards MA (2010) Dietary carotenoid levels affect carotenoid and retinoid allocation in female Chinook salmon Oncorhynchus tshawytscha. J Fish Biol 76:1474–1490. https://doi.org/10.1111/j.1095-8649.2010.02579.x
Grether GF, Hudon J, Millie DF (1999) Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc R Soc Lond B 266:1317–1322. https://doi.org/10.1098/rspb.1999.0781
Grether GF, Hudon J, Endler JA (2001) Carotenoid scarcity, synthetic pteridine pigments and the evolution of sexual coloration in guppies (Poecilia reticulata). Proc R Soc Lond B 268:1245–1253. https://doi.org/10.1098/rspb.2001.1624
Grether GF, Kolluru GR, Lin K, Quiroz MA, Robertson G, Snyder AJ (2008) Maternal effects of carotenoid consumption in guppies (Poecilia reticulata). Funct Ecol 22:294–302. https://doi.org/10.1111/j.1365-2435.2007.01365.x
Hill GE (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14:625–634. https://doi.org/10.1111/j.1461-0248.2011.01622.x
Hill GE (2014) Cellular respiration: the nexus of stress, condition, and ornamentation. Integr Comp Biol 54:645–657. https://doi.org/10.1093/icb/icu029
Hill GE, Johnson JD (2012) The vitamin A-redox hypothesis: a biochemical basis for honest signaling via carotenoid pigmentation. Am Nat 180:E127–E150. https://doi.org/10.1086/667861
Itzkowitz M, Santangelo N, Richter M (2001) Parental division of labour and the shift from minimal to maximal role specializations: an examination using a biparental fish. Anim Behav 61:1237–1245. https://doi.org/10.1006/anbe.2000.1724
Janhunen M, Peuhkuri N, Primmer CR, Kolari I, Piironen J (2011) Does breeding ornamentation signal genetic quality in Arctic charr, Salvelinus alpinus? Evol Biol 38:8–78. https://doi.org/10.1007/s11692-010-9100-9
Koch RE, Hill GE (2018) Do carotenoid‐based ornaments entail resource trade‐offs? An evaluation of theory and data. Funct Ecol 32:1908–1920. https://doi.org/10.1111/1365-2435.13122
Koch RE, Kavazis AN, Hasselquist D, Hood WR, Zhang Y, Toomey MB, Hill GE (2018) No evidence that carotenoid pigments boost either immune or antioxidant defenses in a songbird. Nat Commun 9:491. https://doi.org/10.1038/s41467-018-02974-x
Kolluru GR, Grether GF, South SH, Dunlop E, Cardinali A, Liu L, Carapiet A (2006) The effects of carotenoid and food availability on resistance to a naturally occurring parasite (Gyrodactylus turnbulli) in guppies (Poecilia reticulata). Biol J Linn Soc 89:301–309. https://doi.org/10.1111/j.1095-8312.2006.00675.x
Lehtonen TK (2019) Aggression towards shared enemies by heterospecifc and conspecifc cichlid fish neighbours. Oecologia 191:359–368. https://doi.org/10.1007/s00442-019-04483-0
Lin SM, Nieves-Puigdoller K, Brown AC, McGraw KJ, Clotfelter ED (2010) Testing the carotenoid trade-off hypothesis in the polychromatic Midas cichlid, Amphilophus citrinellus. Physiol Biochem Zool 83:333–342. https://doi.org/10.1086/649965
Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311. https://doi.org/10.2307/3545643
McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712. https://doi.org/10.1086/378904
McGraw KJ, Nolan PM, Crino OL (2011) Carotenoids bolster immunity during moult in a wild songbird with sexually selected plumage coloration. Biol J Linn Soc 102:560–572. https://doi.org/10.1111/j.1095-8312.2010.01594.x
McNeil GV, Friesen CN, Gray SM, Aldredge A, Chapman LJ (2016) Male colour variation in a eurytopic African cichlid: the role of diet and hypoxia. Biol J Linn Soc 118:551–568. https://doi.org/10.1111/bij.12748
Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514. https://doi.org/10.1016/S0169-5347(98)01484-0
Parolini M, Iacobuzio R, Possenti CD, Bassano B, Pennati R, Saino N (2018) Carotenoid-based skin coloration signals antioxidant defenses in the brown trout (Salmo trutta). Hydrobiologia 815:267–280. https://doi.org/10.1007/s10750-018-3571-6
Perez-Rodriguez L, Mougeot F, Alonso-Alvarez C (2010) Carotenoid-based coloration predicts resistance to oxidative damage during immune challenge. J Exp Biol 213:1685–1690. https://doi.org/10.1242/jeb.039982
Schmitter-Soto JJ (2007) A systematic revision of the genus Archocentrus (Perciformes: Cichlidae), with the description of two new genera and six new species. Zootaxa 1603:1–76. https://doi.org/10.11646/zootaxa.1603.1.1
Sefc KM, Brown AC, Clotfelter ED (2014) Carotenoid-based coloration in cichlid fishes. Comp Biochem Physiol A Mol Integr Physiol 173:42–51. https://doi.org/10.1016/j.cbpa.2014.03.006
Simons M, Cohen AA, Verhulst S (2012) What does carotenoid-dependent coloration tell? Plasma carotenoid level signals immunocompetence and oxidative stress state in birds - a meta-analysis. PLoS One 7:e43088. https://doi.org/10.1371/journal.pone.0043088
Simons MJ, Maia R, Leenknegt B, Verhulst S (2014) Carotenoid-dependent signals and the evolution of plasma carotenoid levels in birds. Am Nat 184:741–751. https://doi.org/10.1086/678402
Svensson PA, Wong BBM (2011) Carotenoid-based signals in behavioural ecology: a review. Behaviour 148:131–189. https://doi.org/10.1163/000579510X548673
Svensson PA, Forsgren E, Amundsen T, Nilsson Sköld H (2005) Chromatic interaction between egg pigmentation and skin chromatophores the nuptial coloration of female two-spotted gobies. J Exp Biol 208:4391–4397. https://doi.org/10.1242/jeb.01925
Takaichi S (2011) Carotenoids in algae: distributions, biosyntheses and functions. Mar Drugs 9:1101–1118. https://doi.org/10.3390/md9061101
Theis A, Roth O, Cortesi F, Ronco F, Salzburger W, Egger B (2017) Variation of anal fin egg-spots along an environmental gradient in a haplochromine cichlid fish. Evolution 71:766–777. https://doi.org/10.1111/evo.13166
Vinkler M, Albrecht T (2010) Carotenoid maintenance handicap and the physiology of carotenoid-based signalization of health. Naturwissenschaften 97:19–28. https://doi.org/10.1007/s00114-009-0595-9
von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B 266:1–12. https://doi.org/10.1098/rspb.1999.0597
Weaver RJ, Wang P, Hill GE, Cobine PA (2018) An in vivo test of the biologically relevant roles of carotenoids as antioxidants in animals. J Exp Biol 221:jeb183665. https://doi.org/10.1242/jeb.183665
Wisenden BD (1995) Reproductive behaviour in free-ranging convict cichlids. Environ Biol Fish 43:121–134
Acknowledgements
The authors are grateful to K. McKaye for the opportunity to use his facilities at Lake Xiloá and to M. McKaye, E. Van den Berghe, and L. Canda for logistical support. The authors also would like to thank the editor and an anonymous reviewer for their helpful comments.
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This work was supported by a National Science Foundation award to RLE (IOS-1051682) and EDC (IOS-1051598). EDC also received funding from Office of the Dean of Faculty at Amherst College, including the Faculty Research Award Program.
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EDC and RLE designed the study, organized the field and laboratory research, secured funding for the project, conducted data collection in the field and laboratory, and collaborated to generate the manuscript. CTA, MKM and BBN assisted with field and laboratory data collection and with organizing the manuscript. ACB participated in organizing the field research and conducted carotenoid assays in the laboratory.
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This research was supported by a permit issued by the Nicaragua Ministry of the Environment and Natural Resources (MARENA) to RLE and was approved by the University of Alabama IACUC (Protocol #10–345) and the Amherst College IACUC (Protocol #2014–3).
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Earley, R.L., Anderson, C.T., Moscicki, M.K. et al. Carotenoid availability and tradeoffs in female convict cichlids, a reverse sexually-dichromatic fish. Environ Biol Fish 103, 1541–1552 (2020). https://doi.org/10.1007/s10641-020-01036-w
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DOI: https://doi.org/10.1007/s10641-020-01036-w