Abstract
Plasticity of resource use represents an important strategy for fish species living in unstable freshwater environments. Trophic polymorphism (i.e. variation in the morphology of the alimentary tract) has been observed in dozens of vertebrate species in response to diet variation. The digestive tract has been reported as one of the most reactive systems. The Digestion Theory predicts that consumption of food with a high proportion of indigestible material would produce an increase in the length of the digestive tract. This response allows individuals to get energy enough even when consuming a low-quality diet. We evaluated the diet—using classical stomach content analysis and stable isotopes (nitrogen and carbon)—and the length of digestive organs of an abundant and ubiquitous fish species, the La Plata croaker (Pachyurus bonariensis Steindachner, 1879). A total of 95 individuals were captured at three sites of the lower Uruguay River, with different food supply during two sampling campaigns. We found larger digestive organs (stomach and intestine) at the site with higher sediment vegetal matter availability and, consequently, with the highest vegetal matter consumption. However, these differences in food consumption were not observed with the stable isotope analysis, probably due to the different temporal resolution of this technique. The results presented herein support one prediction of the Digestion Theory, confirming digestive flexibility as an intraspecific compensatory mechanism in a freshwater fish species.
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References
Akin S, Turan H, Kaymak N (2016) Does diet variation determine the digestive tract length of Capoeta banarescui Turan, Kottelat, Ekmekci and Imamoglu, 2006? J Appl Ichthyol 32:883–892. https://doi.org/10.1111/jai.13104
Bloom DD, Lovejoy NR (2011) The biogeography of marine incursions in South America. In: Albert JS, Reis RE (eds) Historical Biogeography of Neotropical Freshwater Fishes. University of California Press, London, England, pp 138–164
Boeger WA, Marteleto FM, Zagonel L, Braga MP (2015) Tracking the history of an invasion: the freshwater croakers (Teleostei: Sciaenidae) in South America. Zool Scr 44:250–262. https://doi.org/10.1111/zsc.12098
Bowen SH, Lutz EV, Ahlgren MO (1995) Dietary protein and energy as determinants of food quality: trophic strategies compared. Ecology 76:899–907. https://doi.org/10.2307/1939355
Bunn SE, Leigh C, Jardine TD (2013) Diet-tissue fractionation of δ15N by consumers from streams and rivers. Limnol Oceanogr 58:765–773. https://doi.org/10.4319/lo.2013.58.3.0765
Cant JP, McBide BW, Croom WJ (1996) The regulation of intestinal metabolism and its impact on whole animal energetics. J Anim Sci 74:2541–2553. https://doi.org/10.2527/1996.74102541x
Chambers JM, Freeny A, Heiberger RM (1992) Analysis of variance; designed experiments. Chapter 5 of Statistical Models in S eds J. M. Chambers and T. J. Hastie, Wadsworth & Brooks/Cole.
D’Anatro A, Vidal N, González-Bergonzoni I, Teixeira de Mello F, Tana J, Naya DE (2013) Geographic and sasonal variation analysis of digestive morphology in the catfish Iheringichthys labrosus along lower Rio Uruguay. Open Access Anim Physiol 5:9–13. https://doi.org/10.2147/OAAP.S47193
Dufech APS, Fialho CB (2007) Biologia populacional de Pachyurus bonariensis Steindachner, 1879 (Perciformes, Sciaenidae), uma espécie alóctone no sistema hidrográfico da laguna dos patos, Brasil. Biota Neotrop 7 0-0. https://doi.org/10.1590/S1676-06032007000100015
Fagan KA, Koops MA, Arts MT, Power M (2011) Assessing the utility of C: N ratios for predicting lipid content in fishes. Can J Fish Aquat Sci 68:374–385. https://doi.org/10.1139/F10-119
Felden J, González-Bergonzoni I, Rauber AM, da Luz SM, ViniciusMassaro M, Bastian R, Reynalte-Tataje (2021) Riparian forest subsidises the biomass of fish in a recently formed subtropical reservoir. Ecol Freshw Fish 30:197–210. https://doi.org/10.1111/eff.12575
Flores SA, Hirt LM (2002) Ciclo reproductivo y fecundidad de Pachyurus bonariensis (Steindachner, 1879), Pisces, Scianidae. Bol Inst Pesca 28:25–31
Fry B (2013) Alternative approaches for solving underdetermined iso-tope mixing problems. Mar Ecol Prog Ser 472:1–13. https://doi.org/10.3354/meps10168
Fugi R, Hahn NS, Novakowski GC, Balassa GC (2007) Ecologia alimentar da corvina, Pachyurus bonariensis (Perciformes, Sciaenidae) em duas baías do Pantanal, Mato Grosso, Brasil. Iheringia Ser Zool 97:343–347. https://doi.org/10.1590/S0073-47212007000300020
Gaucher L, Vidal N, D’Anatro A, Naya DE (2012) Digestive flexibility during fasting in the characid fish Hyphessobrycon luetkenii. J Morphol 273:49–56. https://doi.org/10.1002/jmor.11005
González-Bergonzoni I, D’Anatro A, Vidal N, Stebniki S, Tesitore G, Silva I, Teixeira de Mello F (2019) Origin of fish biomass in a diverse subtropical river: an allochthonic-supported biomass in-crease following flood pulses. Ecosystems 22:1736–1753. https://doi.org/10.1007/s10021-019-00370-0
Horn MH (1989) Biology of marine herbivorous fishes. Oceanogr Mar Biol 27:167–272
Hume ID (2005) Concepts of digestive efficiency. Physiological and ecological adaptations to feeding in vertebrates (eds J M Starck T Wang), pp. 43–58. Science Publishers, Enfield.
Hyslop EJ (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17:411–429. https://doi.org/10.1111/j.1095-8649.1980.tb02775.x
Jackson K, Perry G (2000) Changes in intestinal morphology following feeding in the brown tree snake, Boiga irregularis. J Herpetol 34:459–462. https://doi.org/10.2307/1565371
Karasov WH, Martinez del Rio C, Caviedes-Vidal E (2011) Ecological physiology of diet and digestive systems. Annu Rev Physiol 73:69–93. https://doi.org/10.1146/annurev-physiol-012110-142152
Lagemann GI (2009) Biologia alimentar e reprodutiva de Pachyurus bonariensis Steindachner, 1879 (Perciformes, Sciaenidae) na fase pré-represamento do arroio Taquarembó, sul do Brasil. http://hdl.handle.net/10183/17313. Accessed Sep 2020
LATU (2015) Informe sobre caracterización biológica en el tramo inferior del Río Uruguay, febrero-noviembre 2015. Laboratorio Tecnológico del Uruguay, Montevideo, Uruguay, p 81
López-Rodríguez A, Silva I, de Ávila-Simas S, Stebniki S, Bastian R, Massaro MV, González-Bergonzoni I (2019) Diets and trophic structure of fish assemblages in a large and unexplored subtropical river: the Uruguay River. Water 11:1374. https://doi.org/10.3390/w11071374
Loureiro M, Montenegro F, Bessonart J, Díaz D, Paullier S (2020) Presencia de tres especies de peces nativas de la cuenca del Plata en la cuenca de la Laguna Merín en Uruguay. Bol Soc zool Urug 29:13–16. https://doi.org/10.26462/29.1.2
Masdeu M, Mello FTD, Loureiro M, Arim M (2011) Feeding habits and morphometry of Iheringichthys labrosus (Lütken, 1874) in the Uruguay River (Uruguay). Neotrop Ichthyol 9:657–664. https://doi.org/10.1590/S1679-62252011005000034
McKinney CR, McCrea JM, Epstein S, Allen HA, Urey HC (1950) Improvements in mass spectrometers for the measurement of small differences in isotope abundance ratios. Rev Sci Instrum 21:724–730. https://doi.org/10.1063/1.1745698
Naya DE, Veloso C, Bozinovic F (2009) Gut size variation among Bufo spinulosus populations along an altitudinal (and dietary) gradient. Ann Zool Fenn 46:16–20. https://doi.org/10.5735/086.046.0102
Olsson J, Quevedo M, Colson C, Svanbäck R (2007) Gut length plasticity in perch: into the bowels of resource polymorphisms. Biol J Linn Soc 90:517–523. https://doi.org/10.1111/j.1095-8312.2007.00742.x
Penry DL, Jumars PA (1987) Modeling animal guts as chemical reactors. Am Nat 129:69–96. https://doi.org/10.1086/284623
Piersma T, Lindström Å (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol Evol 12:134–138. https://doi.org/10.1016/S0169-5347(97)01003-3
Post DM (2002) Using stable isotopes to estimate trophic position: models methods and assumptions. Ecology 83:703–718. https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Evol Syst 2:369–404. https://doi.org/10.1146/annurev.es.02.110171.002101
Secor SM (2001) Regulation of digestive performance: a proposed adaptive response. Comp Biochem Physiol Part A Mol Integr Physiol 128:563–575
Secor SM (2005a) Evolutionary and cellular mechanisms regulating intestinal performance of amphibians and reptiles. Integr Comp Biol 45:282–294. https://doi.org/10.1016/S1095-6433(00)00325-1
Secor SM (2005b) Physiological responses to feeding, fasting and estivation for anurans. J Exp Biol 208:2595–2609. https://doi.org/10.1242/jeb.01659
Sibly RM (1981) Strategies of digestion and defecation. In:Townsend CR, Calow P, eds. Physiological ecology: an evo-lutionary approach to resource use. Sunderland, MA: Sin-auer Associates 109–139.
Starck JM, Beese K (2002) Structural flexibility of the small intestine and liver of garter snakes in response to feeding and fasting. J Exp Biol 205:1377–1388. https://doi.org/10.1242/jeb.205.10.1377
Teixeira de Mello F, Iglesias C, Borthagaray AI, Mazzeo N, Vilches J, Larrea D, Ballabio R (2006) Ontogenetic allometric coefficient changes: implications of diet shift and morphometric traits in Hoplias malabaricus (Bloch) (Characiforme, Erythrinidae). J Fish Biol 69:1770–1778. https://doi.org/10.1111/j.1095-8649.2006.01245.x
Teixeira de Mello F, Gonzalez-Bergonzoni I, Loureiro M (2011) Peces de agua dulce de Uruguay. PPR-MGAP. Available at: http://www.academia.edu/16690482/Peces_de_agua_dulce_de_Uruguay. Accessed Sep 2020
Thorp JH, Thoms MC, Delong MD (2010) The riverine ecosystem synthesis: toward conceptual cohesiveness in river science. Elsevier, London, UK
Tieszen LL, Boutton TW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–37
Vegh SL, Lozano IE, Dománico AA (2013) Dieta de Pachyurus bonariensis (Steindachner, 1879)(Perciformes, Sciaenidae) en Mocoretá río Uruguay, Argentina. Lat Am J Aquat Res 41:992–995. https://doi.org/10.3856/vol41-issue5-fulltext-18
Vidal N, Zaldúa N, D’Anatro A, Naya DE (2014) Are the most plastic species the most abundant ones? An assessment using a fish assemblage. Plosone 9:e92446. https://doi.org/10.1371/journal.pone.0092446
Vidal N, González-Bergonzoni I, Naya DE (2019) The effect of fasting on nutritional status, organs size and isotopic composition in a Neotropical fish species (Jenynsia multidentata). Hydrobiologia 828:73–82. https://doi.org/10.1007/s10750-018-3803-9
Vidal N, Teixeira de Mello F, González-Bergonzoni I, López-Rodríguez A, Tesitore G, Pais J, Stebniki S, Silva I, D’Anatro A (2020) Long-term study of the reproductive timing of the Neotropical catfish Iheringichthys labrosus (Lütken, 1874): influence of temperature and river discharge. Ecol Freshw Fish 29:334–345. https://doi.org/10.1111/eff.12518
Wagner CE, McIntyre PB, Buels KS, Gilbert DM, Michel E (2009) Diet predicts intestine length in Lake Tanganyika’s cichlid fishes. Funct Ecol 23:1122–1131. https://doi.org/10.1111/j.1365-2435.2009.01589.x
Wang T, Hung CC, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 68:223–251. https://doi.org/10.1146/annurev.physiol.68.040104.105739
Zaldúa N, Naya DE (2014) Digestive flexibility during fasting in fish: a review. Comp Biochem Physiol Part A Mol Integr Physiol 169:7–14. https://doi.org/10.1016/j.cbpa.2013.12.006
Zhang P, van Leeuwen CH, Bogers D, Poelman M, Xu J, Bakker ES (2020) Ectothermic omnivores increase herbivory in response to rising temperature. Oikos 129:1028–1039. https://doi.org/10.1111/oik.07082
Acknowledgements
We want to thank the URI personnel for field assistance in sampling and data collection. We also acknowledge Gervasio González from UPM for his collaboration and the food availability data from the three sites. The information used in this work was collected during the monitory program and funded by UPM pulp mill.
Funding
NV, IG-B, AD, DEN, and FTM were funded by SNI-ANII and PEDECIBA (Uruguay). This study was partially funded by Agencia Nacional de Investigación e Innovación. Project Number: ANII‐FCE_2_2016_1_126780.
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Conceived and designed the investigation: NV. Performed field and/or laboratory work: NV, NV, AD, IG-B, FTM, and DEN. Data analysis: NV and DEN. Manuscript preparation: NV, AD, IG-B, FTM, and DEN.
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Fish collections were done following the CHEA protocol “Fishing for fish with multi-mesh nets” (form number 1185) approved in the context of the project: “Fish monitoring of the Río Uruguay and Río Negro”approved by the CEUA of the CURE (Centro Universitario Regional Este).
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Vidal, N., D’Anatro, A., González-Bergonzoni, I. et al. Morphological variation of the digestive tract: a feeding behaviour response in a freshwater fish species. Environ Biol Fish 105, 717–727 (2022). https://doi.org/10.1007/s10641-022-01283-z
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DOI: https://doi.org/10.1007/s10641-022-01283-z