Abstract
Megalobrama pellegrini, a cyprinid endemic to the upper Yangtze River China, has thick keratinized beaks on the jaws and feeds on algae and molluscs. The size of keratinized beaks varies among different individuals. In the present study, two populations, from Longxihe (LXH) and Chishui (CSH) Rivers, were examined in order to explore the morphological variation of keratinized beaks, together with an analysis of intestine length and of stable isotopes. The results showed that the ratio of upper to lower keratinized beaks varied from 0.84 to 2.06. We defined the ratio < 1.25 as equal beak (EB) form, while >1.26 as thicker upper beak (TUB) form. In the LXH population, there were more TUB forms, while EB forms dominated in CSH population. Intestine length showed a negative relationship with the upper to lower beak ratio (Pearson correlation coefficient = −0.697, P < 0.01) indicating the possible adaptation of beak size to food type. In addition, analysis of stable isotope showed that these two populations differed in their food, and there was a positive relationship between trophic niche and size of beaks (R = 0.5530 and 0.4927, respectively). This further supported the suggestion that the beak size was possibly adapted to food type, with the TUB form to a higher trophic niche and the EB form to a lower trophic niche.
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References
Albert CH, Thuiller W, Yoccoz NG, Douzet R, Aubert S, Lavorel S (2010) A multi – trait approach reveals the structure and the relative importance of intra – vs. interspecific variability in plant traits. Funct Ecol 24(6):1192–1201. https://doi.org/10.1111/j.1365-2435.2010.01727.x
Barlow GW (1961) Causes and significance of morphological variation in fishes. Syst Zool 10(3):105–117. https://doi.org/10.2307/2411595
Boag PT, Grant PR (1981) Intense natural selection in a population of Darwin’s finches (Geospizinae) in the Galapagos. Science 214(4516):82–85. https://doi.org/10.1126/science.214.4516.82
Campàs O, Mallarino R, Herrel A, Abzhanov A, Brenner MP (2010) Scaling and shear transformations capture beak shape variation in Darwin’s finches. Proc Natl Acad Sci 107(8):3356–3360. https://doi.org/10.1073/pnas.0911575107
Chen Y (1998) China Fauna (Osteichthyes: Cpriniformes II). Science Press, Beijing, pp 171–175 (In Chinese)
Chilton DE, Beamish RJ (1982) Age determination methods for fishes studied by the groundfish program at the Pacific Biological Station. Department of Fisheries and Oceans, Ottawa
Connell SD, Kingsford MJ (1998) Spatial, temporal and habitat-related variation in the abundance of large predatory fish at one tree reef. Australia Coral Reefs 17(1):49–57. https://doi.org/10.1007/s003380050094
Cote J, Roussel J, Cam SL, Bal G, Evanno G (2012) Population differences in response to hypoxic stress in Atlantic salmon. J Evol Biol 25(12):2596–2606. https://doi.org/10.1111/jeb.12007
Crutsinger GM, Sanders NJ, Classen AT (2009) Comparing intra- and inter-specific effects on litter decomposition in an old-field ecosystem. Basic Appl Ecol 10(6):535–543. https://doi.org/10.1016/j.baae.2008.10.011
Des Roches S, Post DM, Turley NE, Bailey JK, Hendry AP, Kinnison MT, Schweitzer JA, Palkovacs EP (2018) The ecological importance of intraspecific variation. Nat Ecol Evol 2(1):57–64. https://doi.org/10.1038/s41559-017-0402-5
Focken U, Becker K (1998) Metabolic fractionation of stable carbon isotopes: implications of different proximate compositions for studies of the aquatic food webs using δ13C data. Oecologia 115(3):337–343. https://doi.org/10.1007/s004420050525
Foster K, Bower LM, Piller KR (2015) Getting in shape: habitat-based morphological divergence for two sympatric fishes. Biol J Linn Soc 114(1):152–162. https://doi.org/10.1111/bij.12413
Gao X, Tan DQ, Liu HZ, Wang JW (2009) Exploitation status and conservation of a population of Megalobrama pellegrini in Longxi River in the upper Yangtze River basin. Sichuan J Zool. (In Chinese)
Gerry SP, Vogelzang M, Ascher JM, Ellerby DJ (2013) Variation in the diet and feeding morphology of polyphenic Lepomis macrochirus. J Fish Biol 82(1):338–346. https://doi.org/10.1111/j.1095-8649.2012.03471.x
Gibbs HL, Grant PR (1987) Oscillating selection on Darwin’s finches. Nature 327(6122):511. https://doi.org/10.1038/327511a0
Gonda A, Herczeg G, Merila J (2013) Evolutionary ecology of intraspecific brain size variation: a review. Ecol Evol 3(8):2751–2764. https://doi.org/10.1002/ece3.627
Govaert L, Fronhofer EA, Lion S, Eizaguirre C, Bonte D, Egas M, Hendry AP, Martins ADB, Melian CJ, Raeymaekers JAM, Ratikainen II, Saether BE, Schweitzer JA, Matthews B (2019) Eco-evolutionary feedbacks–theoretical models and perspectives. Funct Ecol 33(1):13–30. https://doi.org/10.1111/1365-2435.13241
Grant PR, Grant BR (1995) Predicting microevolutionary responses to directional selection on heritable variation. Evolution 49(2):241–251. https://doi.org/10.1111/j.1558-5646.1995.tb02236.x
Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296(5568):707–711. https://doi.org/10.1126/science.1070315
Grant PR, Grant BR (2006) Evolution of character displacement in Darwin’s finches. Science. 313(5784):224–226. https://doi.org/10.1126/science.1128374
Hanski I, Mononen T (2011) Eco-evolutionary dynamics of dispersal in spatially heterogeneous environments. Ecol Lett 14(10):1025–1034. https://doi.org/10.1111/j.1461-0248.2011.01671.x
He Y, Wang J, Lek-Ang S, Lek S (2010) Predicting assemblages and species richness of endemic fish in the upper Yangtze River. Sci Total Environ 408(19):4211–4220. https://doi.org/10.1016/j.scitotenv.2010.04.052
Hegrenes S (2001) Diet – induced phenotypic plasticity of feeding morphology in the orangespotted sunfish, Lepomis humilis. Ecol Freshw Fish 10(1):35–42. https://doi.org/10.1034/j.1600-0633.2001.100105.x
Hendry AP (2016) Eco-evolutionary dynamics. Princeton university press, New York
Hendry AP, Green DM (2018) Eco-evolutionary dynamics in cold blood. Copeia 105(3):441–450. https://doi.org/10.1643/OT-17-631
Jackrel SL, Wootton JT (2014) Local adaptation of stream communities to intraspecific variation in a terrestrial ecosystem subsidy. Ecology 95(1):37–43. https://doi.org/10.1890/13-0804.1
Jensen H, Kiljunen M, Amundsen PA (2012) Dietary ontogeny and niche shift to piscivory in lacustrine brown trout Salmo trutta revealed by stomach content and stable isotope analyses. J Fish Biol 80(7):2448–2462. https://doi.org/10.1111/j.1095-8649.2012.03294.x
Johannsson OE, Leggett MF, Rudstam LG, Servos MR, Mohammadian MA, Gal G, Dermott RM, Hesslein RH (2001) Diet of Mysis relicta in Lake Ontario as revealed by stable isotope and gut content analysis. Can J Fish Aquat Sci 58(10):1975–1986. https://doi.org/10.1139/f01-118
Jonsson B, Jonsson N (2001) Polymorphism and speciation in Arctic charr. J Fish Biol 58(3):605–638. https://doi.org/10.1111/j.1095-8649.2001.tb00518.x
Karachle PK, Stergiou KI (2010) Gut length for several marine fish: relationships with body length and trophic implications. Mar Biodivers Rec 3:1–10. https://doi.org/10.1017/S1755267210000904
Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI (2006) A revised model for lipid – normalizing δ13C values from aquatic organisms, with implications for isotope mixing models. J Appl Ecol 43(6):1213–1222. https://doi.org/10.1111/j.1365-2664.2006.01224.x
Kramer DL, Bryant MJ (1995) Intestine length in the fishes of a tropical stream: 2. Relationships to diet – the long and short of a convoluted tissue. Environ Biol Fish 42:129–141. https://doi.org/10.1007/BF00001991
Lamichhaney S, Han F, Berglund J, Wang C, Almén MS, Webster MT, Grant BR, Grant PR, Andersson L (2016) A beak size locus in Darwin’s finches facilitated character displacement during a drought. Science. 352(6284):470–474. https://doi.org/10.1126/science.aad8786
Li WJ, Wang JW, Xie CX, Tan DQ (2007a) Age structure and growth characteristics of Megalobrama Pellegrini – an endemic fish living only in upper reaches of Yangtze River. J Fish Sci China 14(2):215–222 (In Chinese)
Li WJ, Wang JW, Xie CX, Tan DQ (2007b) Reproductive biology and spawning habitats of Megalobrama pellegrini, an endemic fish in upper-reaches of Yangtze River basin. Acta Ecol Sin 27(5):1917–1925 (In Chinese)
Li L, Wei QW, Wu JM, Zhang H, Liu Y, Xie X (2015) Diet of Leptobotia elongata revealed by stomach content analysis and inferred from stable isotope signatures. Environ Biol Fish 98(8):1965–1978. https://doi.org/10.1007/s10641-015-0414-4
Liu C, Gao X, Wang H, Liu H, Cao W, Danley PD (2013) Reproductive characteristics of Ancherythroculter nigrocauda, an endemic fish in the upper Yangtze River, China. Fish Sci 79(5):799–806. https://doi.org/10.1007/s12562-013-0656-z
Liu F, Cao W, Wang J (2014) Length – weight relationships of 77 fish species from the Chishui River, China. J Appl Ichthyol 30(1):254–256. https://doi.org/10.1111/jai.12288
Mittelbach GG, Osenberg CW, Wainwright PC, Kellogg WW (1999) Variation in feeding morphology between pumpkinseed populations: phenotypic plasticity or evolution? Evol Ecol Res 1(1):111–128
Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mamm Sci 26(3):509–572. https://doi.org/10.1111/j.1748-7692.2009.00354.x
Parnell A, Jackson A (2013) siar: Stable Isotope Analysis in R. R package version 4.2. Available from: http://CRAN.R-project.org/package=siar. Accessed 23 Apr 2013
Pelletier F, Garant D, Hendry AP (2009) Eco-evolutionary dynamics. Philos Trans R Soc B Biol Sci 364(1523):1483–1489. https://doi.org/10.1098/rstb.2009.0027
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83(3):703–718. https://doi.org/10.1890/00129658(2002)083[0703:USITET]2.0.CO;2
Price TD, Grant PR, Gibbs HL, Boag PT (1984) Recurrent patterns of natural selection in a population of Darwin’s finches. Nature 309(5971):787–789. https://doi.org/10.1038/309787a0
Robinson BW, Wilson DS, Margosian AS, Lotito PT (1993) Ecological and morphological differentiation of pumpkinseed sunfish in lakes without bluegill sunfish. Evol Ecol 7(5):451–464. https://doi.org/10.1007/BF01237641
Roy A (2006) Estimating correlation coefficient between two variables with repeated observations using mixed effects model. Biom J 48(2):286–301. https://doi.org/10.1002/bimj.200510192
Schoener TW (2011) The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science. 331(6016):426–429. https://doi.org/10.1126/science.1193954
Sheppard C, Inger R, Mcdonald RA, Barker S, Jackson AL, Thompson FJ, Marshall HH (2018) Intragroup competition predicts individual foraging specialisation in a group – living mammal. Ecol Lett 21(5):665–673. https://doi.org/10.1111/ele.12933
Shukla R, Bhat A (2017) Morphological divergences and ecological correlates among wild populations of zebrafish (Danio rerio). Environ Biol Fish 100(3):251–264. https://doi.org/10.1007/s10641-017-0576-3
Siwertsson A, Knudsen R, Adams CE, Præbel K, Amundsen PA (2013) Parallel and non-parallel morphological divergence among foraging specialists in European whitefish (Coregonus lavaretus). Ecol Evol 3(6):1590–1602. https://doi.org/10.1002/ece3.562
Smith TB, Skúlason S (1996) Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annu Rev Ecol Evol Syst 27(1):111–133. https://doi.org/10.1146/annurev.ecolsys.27.1.111
Van Benthem KJ, Bruijning M, Bonnet T, Jongejans E, Postma E, Ozgul A (2017) Disentangling evolutionary, plastic and demographic processes underlying trait dynamics: a review of four frameworks. Methods Ecol Evol 8(1):75–85. https://doi.org/10.1111/2041-210X.12627
Violle C, Enquist BJ, McGill BJ, Jiang LIN, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27(4):244–252. https://doi.org/10.1016/j.tree.2011.11.014
Wagner CE, Mcintyre PB, Buels KS, Gilbert DM, Michel E (2009) Diet predicts intestine length in Lake Tanganyika’s cichlid fishes. Funct Ecol 23(6):1122–1131. https://doi.org/10.1111/j.1365-2435.2009.01589.x
Wang H (2016) Genetic diversity, speciation of the genus Megalobrama in the Yangtze River and the ecological adaptation of Megalobrama pellegrini. Dissertation, Beijing, University of Chinese Academy of Sciences. (In Chinese)
Wang J, Liu F, Zhang X, Cao WX, Li HZ, Gao X (2014) Reproductive biology of Chinese minnow Hemiculterella sauvagei Warpachowski, 1888 in the Chishui River, China. J Appl Ichthyol 30(2):314–321. https://doi.org/10.1111/jai.12353
Wang H, Wang T, Li W, Liu H (2019) The genetic diversity, individual relatedness and possible mating system of an isolated population of the cyprinid species Megalobrama pellgrini in upper reaches of the Changjiang (Yangtze) river, China. J Oceanol Limnol 37(3): 1042-1050. https://doi.org/10.1007/s00343-019-8152-7
Wintzer AP, Motta PJ (2005) Diet-induced phenotypic plasticity in the skull morphology of hatchery-reared Florida largemouth bass, Micropterus salmoides floridanus. Ecol Freshw Fish 14(4):311–318. https://doi.org/10.1111/j.1600-0633.2005.00105.x
Wu J, Wang J, He Y, Cao W (2011) Fish assemblage structure in the Chishui River, a protected tributary of the Yangtze River. Knowl Manag Aquat Ecosyst 400:11. https://doi.org/10.1051/kmae/2011023
Zhang F, Liu F, Qin Q, Liu H, Cao W, Gao X (2018) Diet composition and trophic guild structure of fish assemblage in headwaters of the Chishui River, a tributary of the upper Yangtze River, China. Environ Biol Fish 101: 1235-1248. https://doi.org/10.1007/s10641-018-0771-x
Acknowledgements
We thank Zheng Gong, Wenjing Li, Ning Qiu, Chunling Wang, Xue Wang and Fubin Zhang for their kind help in collecting samples, laboratory work and photo capture. This work was supported by grants from the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31040000), the Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment, China (2019HJ2096001006), the Research Project of China Three Gorges Corporation (0799570, 0799574) and the Special Program for Basic of Science and Technology Research (2014FY120200).
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All experimental protocols in this study were approved by the Ethics Committee for Animal Experiments of the Institute of Hydrobiology, Chinese Academy of Sciences. The methods used in this study were conducted in accordance with Laboratory Animal Management Principles of China.
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Zhang, Z., Yu, D., Zhai, D. et al. Morphological trophic variation of the cyprinid Megalobrama pellegrini (Tchang, 1930) with different keratinized beaks from upper reaches of the Yangtze River, China. Environ Biol Fish 103, 115–123 (2020). https://doi.org/10.1007/s10641-019-00937-9
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DOI: https://doi.org/10.1007/s10641-019-00937-9