Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T04:07:43.126Z Has data issue: false hasContentIssue false
  • English
  • Français

Temporal effects and changes in the parasitic community of Prochilodus lineatus (Valenciennes, 1837) (Characiformes: Prochilodontidae) in a floodplain

Published online by Cambridge University Press:  07 January 2022

Atsler Luana Lehun ,
Lidiany Doreto Cavalcanti Open the ORCID record for Lidiany Doreto Cavalcanti [Opens in a new window] ,
Maria de los Angeles Perez Lizama ,
João Otávio Santos Silva ,
Guilherme Pomaro Casali  and
Ricardo Massato Takemoto
Atsler Luana Lehun
Affiliation:
Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais – PEA, Universidade Estadual de Maringá – UEM, Avenida Colombo, 5790, Maringá, Paraná, Brazil
Lidiany Doreto Cavalcanti*
Affiliation:
Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais – PEA, Universidade Estadual de Maringá – UEM, Avenida Colombo, 5790, Maringá, Paraná, Brazil
Maria de los Angeles Perez Lizama
Affiliation:
Programa de Pós-graduação de Tecnologias Limpas – PPGTL, UNICESUMAR, Avenida Guedner, 1610, Jardim Aclimação, Maringá, Paraná, Brazil
João Otávio Santos Silva
Affiliation:
Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais – PEA, Universidade Estadual de Maringá – UEM, Avenida Colombo, 5790, Maringá, Paraná, Brazil
Guilherme Pomaro Casali
Affiliation:
Programa de Pós-graduação em Biologia Comparada – PGB, Universidade Estadual de Maringá – UEM, Avenida Colombo, 5790, Maringá, Paraná, Brazil
Ricardo Massato Takemoto
Affiliation:
Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais – PEA, Universidade Estadual de Maringá – UEM, Avenida Colombo, 5790, Maringá, Paraná, Brazil Programa de Pós-graduação em Biologia Comparada – PGB, Universidade Estadual de Maringá – UEM, Avenida Colombo, 5790, Maringá, Paraná, Brazil
*
Author for correspondence: Lidiany Doreto Cavalcanti, E-mail: lidianydoretto@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The construction of dams causes several impacts on aquatic environments, altering the flow of rivers, environmental variables, and all biota present, including parasites. Little is known about how the parasitic community can be influenced in the long term by environmental changes. In this study, it was expected that the impacts caused by environmental disturbances will be directly reflected by the composition of the parasite populations. We evaluated the change in the structure of the Prochilodus lineatus endoparasite community between two periods sampled 15 years apart in the upper Paraná River floodplain. There was a significant difference in the weight–length relationship of P. lineatus between these periods and a total of 15 species of parasites were found: 11 species in Period 1 and nine species in Period 2 and five species occurred in both periods. The species richness and diversity were higher in Period 1, and we observed that the correlation of descriptors (richness, diversity and evenness) increased with fish length in this period. In both periods, digeneans numerically dominated the parasitic community, and we verified changes in the composition of parasites between periods. Both the host and the parasites were possibly affected by the environmental impacts resulting from the construction of dams over time, and it is noteworthy that complex life cycle parasites such as Digenea and Acanthocephala require intermediate hosts to complete their life cycle, and the population responds to fluctuations in the face of modified environments.

Keywords

Damsanthropogenic effectsdigeneansacanthocephalansichthyofauna
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e4
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abati, S, Minciardi, MR, Ciadamidaro, S, Fattorini, S and Ceschin, S (2016) Response of macrophyte communities to flow regulation in mountain streams. Environmental Monitoring and Assessment 188(7), 1–12.CrossRefGoogle ScholarPubMed
Agostinho, AA, Gomes, LC, Veríssimo, S and Okada, EK (2004a) Flood regime, dam regulation and fish in the upper Paraná River: Effects on assemblage attributes, reproduction and recruitment. Reviews in Fish Biology and Fisheries 14(1), 11–19.CrossRefGoogle Scholar
Agostinho, AA, Thomaz, SM and Gomes, LC (2004b) Threats for biodiversity in the floodplain of the upper Paraná River: effects of hydrological regulation by dams. Ecohydrology & Hydrobiology 4(3), 255–256.Google Scholar
Agostinho, AA, Bonecker, CC and Gomes, LC (2009) Effects of water quantity on connectivity: the case of the upper Paraná River floodplain. Ecohydrology & Hydrobiology 9(1), 99–113.CrossRefGoogle Scholar
Al-Jahdali, MO and Hassanine, RES (2012) The life cycle of Gyliauchen volubilis Nagaty, 1956 (Digenea: Gyliauchenidae) from the Red Sea. Journal of Helminthology 86(2), 165–172.CrossRefGoogle ScholarPubMed
Anderson, M (2005) Permutational multivariate analysis of variance: A computer program. Auckland, New Zealand, Department of Statistics, University of Auckland.Google Scholar
Anderson, RM and Gordon, DM (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85(2), 373–398.CrossRefGoogle ScholarPubMed
Arantes, CC, Fitzgerald, DB, Hoeinghaus, DJ and Winemiller, KO (2019) Impacts of hydroelectric dams on fishes and fisheries in tropical rivers through the lens of functional traits. Current Opinion in Environmental Sustainability 37, 28–40.10.1016/j.cosust.2019.04.009CrossRefGoogle Scholar
Braghin, LDSM, Almeida, BDA, Amaral, DC, Canella, TF, Gimenez, BCG and Bonecker, CC (2018) Effects of dam's decrease zooplankton functional β-diversity in river-associated lakes. Freshwater Biology 63(7), 721–730.CrossRefGoogle Scholar
Brooks, TM, Mittermeier, RA, da Fonseca, GA, Gerlach, J, Hoffmann, M, Lamoreux, JF, Mittermeier, CG, Pilgrim, JD and Rodrigues, AS (2006) Global biodiversity conservation priorities. Science 313(5783), 58–61.CrossRefGoogle ScholarPubMed
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83(4), 575–583.CrossRefGoogle Scholar
Ceschin, S, Tombolini, I, Abati, S and Zuccarello, V (2015) The effect of river damming on vegetation: Is it always unfavourable? A case study from the River Tiber (Italy). Environmental Monitoring and Assessment 187(5), 1–12.CrossRefGoogle Scholar
Duarte, GSC, Lehun, AL, Leite, LAR, Consolin-Filho, N, Bellay, S and Takemoto, RM (2020) Acanthocephalans parasites of two Characiformes fishes as bioindicators of cadmium contamination in two neotropical rivers in Brazil. Science of the Total Environment 738, 140339.CrossRefGoogle ScholarPubMed
Dufrêne, M and Legendre, P (1997) Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecological Monographs 67(3), 345–366.Google Scholar
Eiras, JC, Takemoto, RM and Pavanelli, GC (2006) Métodos de estudo e técnicas laboratoriais em parasitologia de peixes [Study methods and laboratory techniques in fish parasitology]. Maringá, Brazil, Eduem. [In Portuguese.]Google Scholar
Fallon, SM, Bermingham, E and Ricklefs, RE (2003) Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57(3), 606–615.CrossRefGoogle ScholarPubMed
Fugi, R, Hahn, NS and Agostinho, AA (1996) Estilos alimentares de cinco espécies de peixes que se alimentam de fundo do alto rio Paraná [Food styles of five species of fish that feed on the upper Paraná River]. Environmental Biology of Fishes 46, 297–307. [In Portuguese.]CrossRefGoogle Scholar
Fugi, R, Agostinho, AA and Hahn, NS (2001) Trophic morphology of five benthic-feeding fish species of a tropical floodplain. Brazilian Journal of Biology 61(1), 27–33.Google ScholarPubMed
Gallegos-Navarro, Y, Violante-González, J, Monks, S, García-Ibáñez, S, Rojas-Herrera, AA, Pulido-Flores, G and Rosas-Acevedo, JL (2018) Factors linked to temporal and spatial variation in the metazoan parasite communities of green jack Caranx caballus (Günther 1868) (Pisces: Carangidae) from the Pacific coast of Mexico. Journal of Natural History 52(39–40), 2573–2590.CrossRefGoogle Scholar
García-Berthou, E and Moreno-Amich, R (1993) Multivariate analysis of covariance in morphometric studies of the reproductive cycle. Canadian Journal of Fisheries and Aquatic Sciences 50(7), 1394–1399.CrossRefGoogle Scholar
Garcia-Prieto, L, Mendoza-Garfias, B and Perez-Ponce de Leon, G (2014) Biodiversity of parasitic Platyhelminthes in Mexico. Revista Mexicana de Biodiversidade 85(Suppl), 164–170.CrossRefGoogle Scholar
Gomes, LC and Agostinho, AA (1997) Influence of the flooding regime on the nutritional state and juvenile recruitment of the curimba, Prochilodus scrofa, Steindachner, in upper Paraná River, Brazil. Fisheries Management and Ecology 4(4), 263–274.CrossRefGoogle Scholar
Gubiani, EA, Gomes, LC, Agostinho, AA and Okada, EK (2007) Persistence of fish populations in the upper Paraná River: effects of water regulation by dams. Ecology of Freshwater Fish 16(2), 191–197.Google Scholar
Hechinger, RF and Lafferty, KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B: Biological Sciences 272(1567), 1059–1066.CrossRefGoogle ScholarPubMed
Hsieh, TC, Ma, KH and Chao, A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution 7(12), 1451–1456.CrossRefGoogle Scholar
Iskov, MP (1976) The influence of training the river Dnieper, construction of water stops and hydroelectric plants on the parasitofauna of fish. Wiadomości Parazytologiczne 22(4–5), 451–453.Google Scholar
Izyumova, NA (1979) The fish parasite fauna of the Volga. Monographiae Biologicae (The Volga and its Life) 33, 340–345.Google Scholar
Junk, WJ, Bayley, PB and Sparks, RE (1989) The flood pulse concept in river-floodplain systems. Canadian Journal of Fisheries and Aquatic Sciences 106, 110–127.Google Scholar
Karling, LC, Isaac, A, Affonso, IP, Takemoto, RM and Pavanelli, GC (2013) The impact of a dam on the helminth fauna and health of a neotropical fish species Salminus brasiliensis (Cuvier 1816) from the upper Paraná River, Brazil. Journal of Helminthology 87(2), 245–251.CrossRefGoogle ScholarPubMed
Kohn, A, Fernandes, BM and Cohen, SC (2007) South American trematodes parasites of fishes. Rio de Janeiro, Brazil, Imprinta Express Ltda.Google Scholar
Lafferty, KD and Kuris, AM (1999) How environmental stress affects the impacts of parasites. Limnology and Oceanography 44(3), 925–931.CrossRefGoogle Scholar
Landsberg, JH, Blakesley, BA, Reese, RO, Mcrae, G and Forstchen, PR (1998) Parasites of fish as indicators of environmental stress. Environmental Monitoring and Assessment 51(1–2), 211–232.CrossRefGoogle Scholar
Le Cren, ED (1951) The length–weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). The Journal of Animal Ecology 20(2), 201–219.CrossRefGoogle Scholar
Lehun, AL, Hasuike, WT, Silva, JOS, et al. (2020) Checklist of parasites in fish from the upper Paraná River floodplain: An update. Brazilian Journal of Veterinary Parasitology 29(3), 1–20.Google ScholarPubMed
Leite, LAR, Pelegrini, LS, Agostinho, BN, Azevedo, RKD and Abdallah, VD (2018) Biodiversity of the metazoan parasites of Prochilodus lineatus (Valenciennes, 1837) (Characiformes: Prochilodontidae) in anthropized environments from the Batalha River, São Paulo State, Brazil. Biota Neotropica 18(3), 1–10.CrossRefGoogle Scholar
Lizama, MAP, Takemoto, RM and Pavanelli, GC (2005) Influence of host sex and age on infracommunities of metazoan parasites of Prochilodus lineatus (Valenciennes, 1836) (Prochilodontidae) of the upper Paraná River floodplain, Brazil. Parasite 12(4), 299–304.CrossRefGoogle Scholar
Lopes, CA, Benedito-Cecilio, E and Martinelli, LA (2007) Variability in the carbon isotope signature of Prochilodus lineatus (Prochilodontidae, Characiformes) a bottom-feeding fish of the neotropical region. Journal of Fish Biology 70(6), 1649–1659.CrossRefGoogle Scholar
Lopes, TM, Peláez, O, Dias, RM, Oliveira, AG, Rauber, RG, Gomes, LC and Agostinho, AA (2020) Temporal changes in migratory fish body size in a neotropical floodplain. Oecologia Australis 24(2), 489–504.CrossRefGoogle Scholar
Luque, JL and Poulin, R (2008) Linking ecology with parasite diversity in Neotropical fishes. Journal of Fish Biology 72(1), 189–204.CrossRefGoogle Scholar
Luque, JL, Mouillot, D and Poulin, R (2004) Parasite biodiversity and its determinants in coastal marine teleost fishes of Brazil. Parasitology 128(6), 671–682.CrossRefGoogle ScholarPubMed
Mackenzie, K (1999) Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Pollution Bulletin 381(1), 955–959.CrossRefGoogle Scholar
Marcogliese, DJ and Cone, DK (1997) Food webs: a plea for parasites. Trends in Ecology & Evolution 12(8), 320–325.CrossRefGoogle ScholarPubMed
Marcogliese, DJ, Locke, SA, Gélinas, M and Gendron, AD (2016) Variation in parasite communities in spottail shiners (Notropis hudsonius) linked with precipitation. Journal of Parasitology 102(1), 27–36.CrossRefGoogle ScholarPubMed
Markevich, AP, Iskov, MP, Koval, VP and Chernogorenko, MI (1976) Effect of hydraulic works on the parasite fauna of the Dnieper river. Hydrobiological Journal 2, 1–6.Google Scholar
Martins, ML, Moraes, FR, Fujimoto, RY, Onaka, EM and Quintana, CL (2001) Prevalence and histopathology of Neoechinorhynchus curemai Noranha, 1973 (Acanthocephala: Neoechinorhynchidae) in Prochilodus lineatus Valenciennes, 1836 from Volta Grande reservoir, MG, Brazil. Brazilian Journal of Biology 61(3), 517–522.CrossRefGoogle Scholar
Minchella, DJ (1985) Host life-history variation in response to parasitism. Parasitology 90(1), 205–216.CrossRefGoogle Scholar
Moravec, F (1998) Nematodes of freshwater fishes of the neotropical region. Czech Republic, Academia Praha, Academy of Sciences of the Czech Republic.Google Scholar
Morley, NJ (2007) Anthropogenic effects of reservoir construction on the parasite fauna of aquatic wildlife. EcoHealth 4(4), 374–383.CrossRefGoogle Scholar
Muniz, CM, García-Berthou, E, Ganassin, MJM, Agostinho, AA and Gomes, LC (2021) Alien fish in Neotropical reservoirs: assessing multiple hypotheses in invasion biology. Ecological Indicators 121, 107034.CrossRefGoogle Scholar
Nagel, L, Robb, T and Forbes, MR (2009) Parasite mediated selection amidst marked inter-annual variation in mite parasitism and damselfly life history traits. Ecoscience 16(2), 265–270.CrossRefGoogle Scholar
Neiff, JJ (1990) Aspects of primary productivity in the lower Paraná and Paraguay riverine system. Acta Limnologica Brasiliensia 3(1), 77–113.Google Scholar
Oyakawa, OT, Menezes, NA, Shibatta, OA, Lima, FCT, Langeani, F, Pavanelli, CS, Nielsen, DTB and Hilsdorf, AWS (2009) Peixes de água doce [Freshwater fish]. pp. 349–424 In Bressan, PM, Kierulff, MCM and Sugieda, AM (Eds) Fauna ameaçada de extinção no Estado de São Paulo [Fauna threatened with extinction in the state of São Paulo]. Fundação Parque Zoológico de São Paulo. São Paulo, Brazil, Ministério do Meio Ambiente. [In Portuguese.]Google Scholar
Pavanelli, GC, Machado, MH, Takemoto, RM, Guidelli, GM and Lizama, MAP (2004) Helminth fauna of the fishes: diversity and ecological aspects. pp. 309–329 In Thomaz, SM, Agostinho, AA and Hahn, NS (Eds) The upper Paraná River and its floodplain: Physical aspects, ecology and conservation. Leiden, Brazil, Backhuys Publishers.Google Scholar
Petsch, DK (2016) Causes and consequences of biotic homogenization in freshwater ecosystems. International Review of Hydrobiology 101(3–4), 113–122.CrossRefGoogle Scholar
Piana, PA, Cardoso, BF, Dias, J, Gomes, LC, Agostinho, AA and Miranda, LE (2017) Using long-term data to predict fish abundance: the case of Prochilodus lineatus (Characiformes, Prochilodontidae) in the intensely regulated upper Paraná River. Neotropical Ichthyology 15(3), e160029.CrossRefGoogle Scholar
Pinha, GD, Aviz, D, Lopes Filho, DR, Petsch, DK, Marchese, MR and Takeda, AM (2013) Longitudinal distribution of Chironomidae (Diptera) downstream from a dam in a neotropical river. Brazilian Journal of Biology 73(3), 549–558.CrossRefGoogle Scholar
Poulin, R (2007) Are there general laws in parasite ecology? Parasitology 134(6), 763–776.CrossRefGoogle ScholarPubMed
Poulin, R, Guilhaumon, F, Randhawa, HS, Luque, JL and Mouillot, D (2011) Identifying hotspots of parasite diversity from species–area relationships: host phylogeny versus host ecology. Oikos 120(5), 740–747.CrossRefGoogle Scholar
R Core Team (2017) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Reid, MA and Ogden, RW (2006) Trend, variability or extreme event? The importance of long-term perspectives in river ecology. River Research and Applications 22(1), 167–177.CrossRefGoogle Scholar
Rosa, RS and Lima, FCT (2008) Os peixes Brasileiros ameaçados de extinção [The Brazilian fishes threatened with extinction]. pp. 9–275 In Bressan, PM, Kierulff, MCM, Sugieda, AMS (Eds) Fauna ameaçada de extinção no Estado de São Paulo [Fauna threatened with extinction in the state of São Paulo]. Fundação Parque Zoológico de São Paulo. São Paulo, Brazil, Secretaria do Meio Ambiente. [In Portuguese.]Google Scholar
Santos, NCL, Santana, HS, Ortega, JCG, et al. (2017) Environmental filters predict the trait composition of fish communities in reservoir cascades. Hydrobiologia 802(5), 245–253.CrossRefGoogle Scholar
Simões, NR, Nunes, AH, Dias, JD, Lansac-Tôha, FA, Velho, LFM and Bonecker, CC (2015) Impact of reservoirs on zooplankton diversity and implications for the conservation of natural aquatic environments. Hydrobiologia 758(1), 3–17.CrossRefGoogle Scholar
Song, Z and Proctor, H (2020) Parasite prevalence in intermediate hosts increases with waterbody age and abundance of final hosts. Oecologia 192, 311–321.CrossRefGoogle ScholarPubMed
Takemoto, RM, Amato, JFR and Luque, JL (1996) Comparative analysis of the metazoan parasite communities of leatherjackets, Oligoplites palometa, O. saurus, and O. saliens (Osteichthyes: Carangidae) from Sepetiba Bay, Rio de Janeiro. Brazilian Journal of Biology 56(4), 639–650.Google ScholarPubMed
Thatcher, VE (2006) Aquatic biodiversity in Latin America. Vol 1. Amazon fish parasites. Sofia, Bulgaria, Pensoft Publishers.Google Scholar
Tombolini, I, Caneva, G, Cancellieri, L, Abati, S and Ceschin, S (2014) Damming effects on upstream riparian and aquatic vegetation: the case study of Nazzano (Tiber River, Central Italy). Knowledge and Management of Aquatic Ecosystems 412(1), 1–15.Google Scholar
Tompkins, DM, Dobson, AP, Arneberg, P, et al. (2002) Parasites and host population dynamics. pp. 45–62 In Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H, Dobson, PJ (Eds) The ecology of wildlife diseases. Oxford, Oxford University Press.Google Scholar
Torchin, ME and Mitchell, CE (2004) Parasites, pathogens, and invasions by plants and animals. Frontiers in Ecology and the Environment 2(4), 183–190.CrossRefGoogle Scholar
Vidal-Martínez, VM (2000) Metazoan parasites in the neotropics: A systematic and ecological perspective. México, Universidad Nacional Autonoma de Mexico.Google Scholar
Violante-González, J, Aguirre-Macedo, ML and Vidal-Martinez, VM (2008) Temporal variation in the helminth parasite communities of the Pacific fat sleeper, Dormitator latifrons, from Tres Palos Lagoon, Guerrero, Mexico. Journal of Parasitology 94(2), 326–334.CrossRefGoogle ScholarPubMed
Vital, JF, Varella, AMB, Porto, DB and Malta, JCO (2011) Seasonality of the metazoan fauna of Pygocentrus nattereri (Kner, 1858) in Piranha Lake (Amazonas, Brazil) and evaluation of its potential as an indicator of environmental health. Biota Neotropica 11(1), 199–204.CrossRefGoogle Scholar
Winemiller, KO, McIntyre, PB, Castello, L, et al. (2016) Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong. Science 351(6269), 128–129.CrossRefGoogle ScholarPubMed
Yamada, FH, Bongiovani, MF, Yamada, PO and Silva, RJ (2017) Parasite infracommunities of Leporinus friderici: a comparison of three tributaries of the Jurumirim Reservoir in southeastern Brazil. Anais da Academia Brasileira de Ciências 89(2), 953–963.CrossRefGoogle ScholarPubMed