Abstract
Since the Asian golden mussel, Limnoperna fortunei, was first reported in the Río de la Plata in the 90’s, its invasion has continuously expanded throughout South America, promoting several negative ecosystem consequences. Several fish species consume and assimilate large fractions of L. fortunei in their biomass, partially controlling the abundance of this invader, but potential fish dietary and trophic niche modifications caused by the invasion have not been studied in deep. Through gut content, stable isotopes and gut morphometry analysis of field-collected and historical museum samples, the potential dietary, trophic niche and physiological consequences of the invasion for two predatory fish of the golden mussel were surveyed. The analysis of historical samples of some of the most frequent and abundant L. fortunei consumers, such as Megaleporinus obtusidens and Pimelodus maculatus, revealed changes in trophic niche when fish started to incorporate L. fortunei. Specifically, an increase in trophic position and a reduction in diet diversity was observed for both predators. Also, a reduction in dietary generalism occurred for M. obtusidens. Furthermore, the digestive tract mass of this species decreased after the invasion, that is, in parallel to a markedly increase in the consumption of animal material. This research raised several questions about the potential effect of L. fortunei on growth rates and abundances of M. obtusidens and P. maculatus, two of the most important species in commercial fisheries in the Uruguay river. Also, it may assist in predicting food web changes to be expected in newly invaded areas.
Similar content being viewed by others
References
Amaral QDF, Rosa E, Wronski JG, Zuravski L, Querol MVM, Anjos B, Andrade CFF, Machado MM, Oliveira LFS (2019) Golden mussel (Limnoperna fortunei) as a bioindicator in aquatic environments contaminated with mercury: cytotoxic and genotoxic aspects. Sci Total Env 675:343–353. https://doi.org/10.1016/j.scitotenv.2019.04.108
Andrade PDB, Razzolini E, Baggio RA (2021) I see Golden Mussel! They are everywhere! Environmental DNA supports widespread dissemination of Limnoperna fortunei in hydrographic basins in the Paraná State, Brazil. Braz Arch Biol Technol. https://doi.org/10.1590/1678-4324-75years-2021210149
Barbosa NPU, Silva FA, de Oliveira MD, Neto MADS, de Carvalho MD, Cardoso AV (2016) Limnoperna fortunei (Dunker, 1857) (Mollusca, Bivalvia, Mytilidae): first record in the São Francisco River basin, Brazil. Check List. https://doi.org/10.15560/12.1.1846
Boltovskoy D, Correa N (2015) Ecosystem impacts of the invasive bivalve Limnoperna fortunei (golden mussel) in South America. Hydrobiol 746:81–95. https://doi.org/10.1007/s10750-014-1882-9
Boltovskoy D, Correa N, Cataldo D, Sylvester F (2006) Dispersion and ecological impact of the invasive freshwater bivalve Limnoperna fortunei in the Río de la Plata watershed and beyond. Biol Invasions 8:947–963. https://doi.org/10.1007/s10530-005-5107-z
Boltovskoy D, Paolucci E, MacIsaac HJ, Zhan A, Xia Z, Correa N (2022) What we know and don’t know about the invasive golden mussel Limnoperna fortunei. Hydrobiologia. https://doi.org/10.1007/s10750-022-04988-5
Brugnoli E, Clemente JM, Boccardi L, Borthagaray A, Scarabino F (2005) Golden mussel Limnoperna fortunei (Bivalvia: Mytilidae) distribution in the main hydrographical basins of Uruguay: update and predictions. An Acad Bras Ciênc 77:235–244
Cataldo D (2015) Trophic relationships of Limnoperna fortunei with adult fishes. In: Boltovskoy D (ed) Limnoperna fortunei: the ecology, distribution and control of a swiftly spreading invasive fouling mussel. Springer International Publishing, Cham, pp 231–248
Clemente JM, Brugnoli E (2002) First record of Limnoperna fortunei (Dunker 1857) (Bivalvia: Mytilidae) in continental waters of Uruguay (Río Negro and Río Yí Rivers). Bol Soc Zool Uruguay 13:29–33
Darrigran G, Pastorino G (1995) The recent introduction of a freshwater asiatic bivalve, Limnoperna fortunei (Mytilidae) into South America. Veliger 38:171–175
Darrigran G (1994) Limnoperna fortunei (Dunker 1857) en el balneario Bagliardi, Río de la Plata. Alteración en la composición de la malacofauna litoral. I Congreso y III Reunión Argentina de Limnología, vol. 1, Tankay, pp 164–166
Delong MD, Thoms MC (2016) Changes in the trophic status of fish feeding guilds in response to flow modification. J Geophys Res: Biogeo 121(3):949–964. https://doi.org/10.1002/2015JG003249
Domínguez E, Fernández HR (2009) Macroinvertebrados bentónicos sudamericanos—sistemática y biología (in Spanish) Eduardo Domínguez and Hugo R. Fernández (eds.) Fundación Miguel Lillo, Tucumán, Argentina, p 656. ISBN 978-950-668-015-2
Edwards MS, Turner TF, Sharp ZD, Montgomery WL (2002) Short and long term effects of fixation and preservation on stable isotope values (δ13C, δ15N, δ34S) of fluid-preserved museum specimens. Copeia 2002:1106–1112. https://doi.org/10.1643/0045-8511(2002)002[1106:SALTEO]2.0.CO;2
Flaherty EA, Ben-David M (2010) Overlap and partitioning of the ecological and isotopic niches. Oikos 119(9):1409–1416
García ML, Protogino LC (2005) Invasive freshwater molluscs are consumed by native fishes in South America. J App Ichthyol 21:34–38. https://doi.org/10.1111/j.1439-0426.2004.00570.x
Gkenas C, Martelo J, Cucherousset J, Ribeiro F, Gago J, Alves MJ, Ribeiro D, Cheoo G, Magalhães MF(2022) Historical food-web changes in invaded fish communities in the lower Guadiana basin. Biol Life Sci Forum 13: 2
González-Bergonzoni I et al (2020) Evaluating the role of predatory fish controlling the invasion of the Asian golden mussel Limnoperna fortunei in a subtropical river. J Appl Ecol 57(4):717–728. https://doi.org/10.1111/1365-2664.13573
González-Bergonzoni I, Vidal N, Wang B, Ning D, Liu Z, Jeppesen E, Meerhoff M (2015) General validation of formalin-preserved fish samples in foodweb studies using stable isotopes. Met Ecol Evol 6:3017–3314. https://doi.org/10.1111/2041-210X.12313
González-BergonzoniTeixeira de MelloVidalD’Anatro IFNA, Masdeu M (2010) Reappearance and diet of juvenile armado catfish (Pterodoras granulosus) in Lower Uruguay River, (Rio Negro, Uruguay). Bol Sociedad Zool Uruguay 19:42–46
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 AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER – stable isotope Bayesian ellipses in R. J Animal Ecol 80:595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Kishe-Machumu MA, van Rijssel JC, Poste A, Hecky RE, Witte F (2017) Stable isotope evidence from formalin–ethanol-preserved specimens indicates dietary shifts and increasing diet overlap in Lake Victoria cichlids. Hydrobiol 791(1):155–173. https://doi.org/10.1007/s10750-016-2925-1
Langone JA (2005) Notas sobre el Mejillón dorado Limnoperna fortunei (Dunker, 1857) (Bivalvia, Mytilidae) en Uruguay. Publicación extra del Museo Nacional de Historia Natural y Antropología on line
Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotopes ratios provide for community-wide measures of trophic structure? Ecology 88:42–48. https://doi.org/10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2
Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer MS, Harrison E, Jud ZR et al (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87:545–562. https://doi.org/10.1111/j.1469185X.2011.00208.x
Lazzaro X, Lacroix G, Gauzens B, Gignoux J, Legendre S (2009) Predator foraging behaviour drives food-web topological structure. J Anim Ecol 78:1307–1317. https://doi.org/10.1111/j.1365-2656.2009.01588.x
Levin LA, Currin C (2012) Stable isotope protocols: sampling and sample processing
López-Rodríguez A, Silva I, de Ávila-Simas S, Stebniki S, Bastian R, Massaro MV, País J, Tesitore G, Teixeira de Mello F, D’Anatro A, Vidal N, Meerhoff M, Reynalte-Tataje D, Zaniboni-Filho E, González-Bergonzoni I (2019) Diets and trophic structure of fish assemblages in a large and unexplored subtropical river: The Uruguay River. Water 11(7):1374. https://doi.org/10.3390/w11071374
Martín SM., Darrigran, GA (1994) Limnoperna fortunei (Dunker, 1857) en el balneario Bagliardi, Río de la Plata: alteración en la composición de la malacofauna litoral (No. DOC 0063)
McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798
Muniz P, Clemente JM, Brugnoli E (2005) Benthic invasive pests in Uruguay: a new problem or an old one recently perceived? Mar Poll Bull 50:993–1018
Mwijage A, Lyasenga TJ, Shilla DJ, Mahugija JAM, Gaspare L, Mfilinge PL, Shilla DA (2021) Diet and isotopic niche dimensions of predatory fish in two estuaries with different degrees of anthropogenic disturbances: a case study of Wami and Pangani Tanzanian coastal estuaries. Adv Oceanogr Limnol. https://doi.org/10.4081/aiol.2021.9987
Nielsen JM, Clare EL, Hayden B, Brett MT, Kratina P (2017) Diet tracing in ecology: method comparison and selection. Methods Ecol Evol 9:278–291
Oliveira CR, Fugi R, Brancalhaõ KP (2010) Fish as potential controllers of invasive mollusks in a neotropical reservoir. Natureza Conservaçaõ 8:140–144
Paolucci E, Thuesen E, Cataldo D, Boltovskoy D (2010) Veligers of an introduced bivalve (Limnoperna fortunei) are a new food resource that enhances growth of larval fish in the Parana ́ river (South America). Fresh Biol 55:1831–1844. https://doi.org/10.1111/j.1365-2427.2010.02418.x
Pastorino G, Darrigran G, Martin S, Lunaschi G (1993) Limnoperna fortunei (Dunker 1857) (Mytilidae), nuevo bivalvo invasor en aguas del Río de la Plata. Neotrópica 39:34
Pazos RS, Spaccesi F, Gómez N (2020) First record of microplastics in the mussel Limnoperna fortunei. Reg Stud Mar Sci 38:101360. https://doi.org/10.1016/j.rsma.2020.101360
Penchaszadeh PE, Darrigran G, Angulo C, Averbuj A, Brogger M, Dogliotti A, Pirez N (2000) Predation of the invasive freshwater mussel Limnoperna fortunei (Dunker 1857) (Mytilidae) by the fish Leporinus obtusidens Valenciennes, 1846 (Anostomidae) in the Rio de la Plata, Argentina. J Shellfish Res 19:229–231
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
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. https://doi.org/10.1007/s00442-006-0630-x
Quezada-Romegialli C, Jackson AL, Hayden B, Kahilainen KK, Lopes C, Harrod C (2018) tRophicPosition, an R package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol Evol 9:1592–1599
Rabuffetti AP, Espínola LA, Abrial E, Amsler ML, Eurich MF, Blettler MC (2021) The influence of hydro-climatic and anthropogenic effects on the long-term variation of commercial fisheries in a large floodplain river. River Res Appl 37(1):78–90. https://doi.org/10.1002/rra.3741
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Riggi LGA, Bommarco R (2019) Subsidy type and quality determine direction and strength of trophic cascades in arthropod food web in agroecosystems. J Appl Ecol 56:1982–1991. https://doi.org/10.1111/1365-2664.13444
Sacramento PA, Manetta GI, Benedito E (2016) Diet-tissue discrimination factors (Δ 13C and Δ 15N) and turnover rate in somatic tissues of a neotropical detritivorous fish on C3 and C4 diets. J Fish Biol 89(1):213–219. https://doi.org/10.1111/jfb.12859
Sarakinos HC, Johnson ML, Zanden MJV (2002) A synthesis of tissue-preservation effects on carbon and nitrogen stable isotope signatures. Can J Zool 80(2):381–387. https://doi.org/10.1139/z02-007
Scarabino F, Verde M (1995) Limnoperna fortunei (Dunker1857) en la costa Uruguaya del Río de la Plata (Bivalvia: Mytilidae). Comunicaciones De La Sociedad Malacológica Del Uruguay 7:374–375
Scarabotti PA, Lucifora LO, Espínola LA, Rabuffetti AP, Liotta J, Mantinian JE, Sánchez S (2021) Long-term trends of fishery landings and target fish populations in the lower La Plata basin. Neotrop Ichthyol. https://doi.org/10.1590/1982-0224-2021-0013
Schoener TW (1989) Food webs from the small to the large: the Robert H MacArthur award lecture. Ecology 70:1559–1589. https://doi.org/10.2307/1938088
Silva Z, Nascimento PEC, Vitule JRS, Frehse FA, Oliveira MS, Mourgués-Schurter LR (2019) Diet and resource sharing by two Pimelodidae species in a Southeastern Brazilian reservoir. Biota Neotrop 19(3):e20180675. https://doi.org/10.1590/1676-0611-BN-2018-0675
Silva I, Naya DE, Teixeira de Mello F, D’Anatro A, Tesitore G, Clavijo C, González-Bergonzoni I (2020) Fish vs. Aliens: predatory fish regulate populations of Limnoperna fortunei mitigating impacts on native macroinvertebrate communities. Hydrobiologia 848(9):2281–2301. https://doi.org/10.1007/s10750-020-04421-9
Silva I et al (2021) Interacciones entre el mejillón dorado y macroinvertebrados bentónicos nativos del Río Uruguay. INNOTEC e573-e573. https://doi.org/10.26461/22.04
Souza Campos MC et al (2014) Modelling of the potential distribution of Limnoperna fortunei (Dunker, 1857) on a global scale. Aquat Invasions 9(3):253–265. https://doi.org/10.3391/ai.2014.9.3.03
Spaccesi FG, Rodrigues-Capítulo A (2012) Benthic communities on hard substrates covered by Limnoperna fortunei Dunker (Bivalvia, Mytilidae) at an estuarine beach (Río de la Plata, Argentina). J Limnol. https://doi.org/10.4081/jlimnol.2012.e15
Stevens CE, Hume ID (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78(2):393–427. https://doi.org/10.1152/physrev.1998.78.2.393
Sylvester F, Boltovskoy D, Cataldo DH (2007) Fast response of freshwater consumers to a new trophic resource: predation on the recently introduced Asian bivalve Limnoperna fortunei in the lower Paraná river, South America. Austral Ecol 32:403–415. https://doi.org/10.1111/j.1442-9993.2007.01707.x
Teixeira de Mello F, González-Bergonzoni I, Loureiro M. (2011). Peces de agua dulce del Uruguay. PPR-MGAP (Montevideo, Uruguay)
Thompson RM et al (2012) Food webs: reconciling the structure and function of biodiversity. Trends Ecol Evol 27:689–697. https://doi.org/10.1016/j.tree.2012.08.005
Turner TF, Krabbenhoft TJ, Collyer ML, Krabbenhoft CA, Edwards MS, Sharp ZD (2015) Retrospective stable isotope analysis reveals ecosystem responses to river regulation over the last century. Ecology 96(12):3213–3226. https://doi.org/10.1890/14-1666.1
Vander Zanden MJ, Chandra S, Allen BC, Reuter JE, Goldman CR (2003) Historical food web structure and restoration of native aquatic communities in the Lake Tahoe (California–Nevada) Basin. Ecosystems 6:274–288. https://doi.org/10.1007/s10021-002-0204-7
Vander Zanden MJ, Clayton MK, Moody EK, Solomon CT, Weidel BC (2015) Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLoS one 10:e0116182. https://doi.org/10.1371/journal.pone.0116182
Vidal N, D'Anatro A, López-Rodríguez A, Teixeira de Mello F (2020) Monitoreo de la pesca artesanal en el Río Uruguay a través de información generada por pescadores de la zona de Nuevo Berlín, Fray Bentos y Las Cañas (Período 2007–2020). Technical report, UPM S.A. https://www.upm.uy/siteassets/documents/medioambiente/informe-pescadores-2020.pdf
Vidal N, D’Anatro A, González-Bergonzoni I, de Mello FT, Naya D (2022) Morphological variation of the digestive tract: a feeding behaviour response in a freshwater fish species. Environ Biol Fish 105:717–727. https://doi.org/10.1007/s10641-022-01283-z
Woodward G, Thompson R, Townsend CR, Hildrew AG (2005) Pattern and process in food webs: evidence from running waters. In: Belgrano A, Scharler UM, Dunne J, Ulanowicz RE (eds) Aquatic food webs an ecosystem approach. Oxford University Press, New York, USA, pp 51–66
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
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, NY
Acknowledgements
We firstly gratefully thank Dr. Marcelo Loureiro, curator of the fish collections of Facultad de Ciencias, UDELAR, and Museo Nacional de Historia Natural in Montevideo, Uruguay. We also thank Giancarlo Tesitore, Samanta Stebniki and Juan Manuel Martínez for helping in sampling campaigns, and to Enrique Lessa for his support to this project. We also thank two anonymous reviewers whose comments contributed greatly to the quality of this manuscript. This research project was funded by the National Agency for Innovation and Research (ANII) project ANII FCE_2_2016_1_126780 and scholarship ANII PD_NAC_2015_1_108121 and partly by the Scientific Research Sectorial Commission (Uruguay) project CSIC I+D_2016_577-348. I.G.-B., D.E.N., A.D., N.V. and F.T.M. received financial support by ANII and PEDECIBA and IS from a scholarship from the Comisión Académica de Posgrado (CAP).
Funding
This research project was funded by the Agencia Nacional de Investigación e Innovación (ANII) project ANII FCE_2_2016_1_126780 and scholarship ANII PD_NAC_2015_1_108121 and partly by the Comisión Sectorial de Investigación Científica (Uruguay) project CSIC I + D_2016_577-348. IGB, NV, AD, FTM and DN received financial support from the Sistema Nacional de Investigadores (SNI) of the ANII and IS from a scholarship from the Comisión Académica de Posgrado (CAP). All authors recived support from the national Programa de Desarrollo de las Ciencias Básicas (PEDECIBA).
Author information
Authors and Affiliations
Contributions
IGB and DEN participated in the conception and design of the study. All authors carried out the fieldwork. IG, NV and DEN carried out the lab work. IGB analysed the data and drafted the manuscript with the help of all authors. All authors gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interests.
Availability of data and material
The datasets generated during and/or analysed during the current study are available from the corresponding author upon request.
Code availability
Does not apply.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
González-Bergonzoni, I., Vidal, N., D’Anatro, A. et al. Historical analysis reveals ecological shifts in two omnivorous fish after the invasion of Limnoperna fortunei in the Uruguay river. Biol Invasions 25, 1935–1954 (2023). https://doi.org/10.1007/s10530-023-03020-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-023-03020-8