Acta Limnologica Brasiliensia
https://actalb.org/article/doi/10.1590/S2179-975X7922
Acta Limnologica Brasiliensia
Original Article

Isotopic signature of the caridean shrimp Potimirim brasiliana Villalobos, 1960 in different points of a pristine area in southeastern Brazil

Assinatura isotópica do camarão carídeo Potimirim brasiliana Villalobos, 1960 em diferentes pontos de uma área preservada no sudeste do Brasil

Jeniffer Natalia Teles; Nielson Felix Caetano França; João Alberto Farinelli Pantaleão; Rafael Carvalho Santos; Luis Miguel Pardo; Fernando Luis Mantelatto

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Abstract

Abstract:

Aim: The aim of this study was to investigate the isotopic signature of P. brasiliana captured in three different points along the river flow toward the sea of the Prumirim River, northern coast of the state of São Paulo/Brazil in order to test the hypothesis of similarity between isotopic signature of individuals living in separated areas of the river.

Methods: We used stable isotope analyses (δ13C and δ15N) at three points of the river and ANOVA and Bayesian Ellipses analyses were performed.

Results: Our results showed that are a differential isotopic enrichment along the river course in 13C, providing important results on the environmental condition and anthropogenic impacts in the region. In addition, the food biology of P. brasiliana was characterized as a primary consumer corroborating with the detritivores feeding habit observed in previous studies of stomach content analysis.

Conclusions: Our research, limited to a single area along the northern coast of the state of São Paulo, uncovers intriguing findings that merit replication in other areas within the region. This is particularly crucial given the rising number of anthropogenic influences resulting from urban development, underscoring the need for improved monitoring of these areas.
 

Keywords

amphidromous species, Atyidae, freshwater shrimp, conservation, stable isotopes

Resumo

Resumo:

Objetivo: O objetivo deste estudo foi investigar a assinatura isotópica de P. brasiliana capturada em três diferentes pontos ao longo do fluxo fluvial em direção ao mar do rio Prumirim com a finalidade de testar a hipótese de similaridade entre a assinatura isotópica de indivíduos que vivem em areas diferentes do rio.

Métodos: Foram utilizadas análises de isótopos estáveis (δ13C e δ15N) em três pontos do rio e foram realizadas análises de Stable Isotope Mixing Models e Bayesian Ellipses.

Resultados: Nossos resultados mostraram que há um enriquecimento isotópico diferencial ao longo do curso do rio em 13C, fornecendo resultados importantes sobre as condições ambientais e os impactos antropogênicos na região. Além disso, a biologia alimentar de P. brasiliana foi caracterizada como um consumidor primário, corroborando com o hábito alimentar de detritívoros observado em estudos anteriores de análise de conteúdo estomacal.

Conclusões: Nossa pesquisa, limitada a uma única área ao longo da costa norte do estado de São Paulo, revela descobertas intrigantes que merecem ser replicadas em outras áreas dentro da região. Isso é especialmente crucial dada a crescente quantidade de influências antropogênicas resultantes do desenvolvimento urbano, ressaltando a necessidade de um monitoramento aprimorado dessas áreas.
 

Palavras-chave

espécies anfídromas, Atyidae, camarão de água doce, conservação, isótopos estáveis

Referencias

Abele, L.G. & Blum, N., 1977. Ecological aspects of the freshwater decapod crustaceans of the Perlas Archipelago, Panamá. Biotropica, 9(4), 239-252. http://dx.doi.org/10.2307/2388141.

Andrade, T.M.B., Camargo, P.B., Silva, D.M.L., Piccolo, M.C., Vieira, S.A., Alves, L.F., Joly, C.A. & Martinelli, L.A., 2011. Dynamics of dissolved forms of carbon and inorganic nitrogen in small watersheds of the coastal atlantic forest in southeast Brazil. Water Air Soil Pollut., 214(1-4), 393-408. http://dx.doi.org/10.1007/s11270-010-0431-z.

Andrade, T.M.B.D., 2008. Dinâmica das formas dissolvidas de nitrogênio e carbono em microbacias da Mata Atlântica no município de Ubatuba (SP) [Doctoral dissertation]. Piracicaba: Universidade de São Paulo.

Antonio, E. & Richoux, N., 2014. Trophodynamics of three decapod crustaceans in a temperate estuary using stable isotope and fatty acid analyses. Mar. Ecol. Prog. Ser., 504, 193-205. http://dx.doi.org/10.3354/meps10761.

Barros, M. & Fontoura, N., 1996. Crescimento de Potimirim glabra (Kingsley, 1878) (Crustacea, Decapoda, Atydae), na Praia da Vigia, Garopaba, Santa Catarina, Brasil. Nauplius, 4, 11-28.

Bauer, R.T., 2011. Amphidromy and migrations of freshwater shrimps. II. Delivery of hatching larvae to the sea, return juvenile upstream migration, and human impacts. In: Asakura, A., ed. New frontiers in crustacean biology. Leiden: Brill, 157-168. http://dx.doi.org/10.1163/ej.9789004174252.i-354.115.

Bauer, R.T., 2013. Amphidromy in shrimps: a life cycle between rivers and the sea. Lat. Am. J. Aquat. Res. 41(4), 633-650. http://dx.doi.org/10.3856/vol41-issue4-fulltext-2.

Bauer, R.T., 2023. Shrimps: their diversity, intriguing adaptations and variety lifestyles Cham: Springer. Life histories, 443-514, Fish & Fisheries Series, vol. 42. http://dx.doi.org/10.1007/978-3-031-20966-6_9.

Bearhop, S., Adams, C.E., Waldron, S., Fuller, R.A. & Macleod, H., 2004. Determining trophic niche width: a novel approach using stable isotope analysis. J. Anim. Ecol., 73(5), 1007-1012. http://dx.doi.org/10.1111/j.0021-8790.2004.00861.x.

Benzie, J.A.H., 1982. The complete larval development of Caridina mccullochi Roux, 1926 (Decapoda, Atyidae) reared in the laboratory. J. Crustac. Biol., 2(4), 493-513. http://dx.doi.org/10.2307/1548091.

Burress, E.D., Gangloff, M.M. & Siefferman, L., 2013. Trophic analysis of two subtropical South American freshwater crabs using stable isotope ratios. Hydrobiologia, 702(1), 5-13. http://dx.doi.org/10.1007/s10750-012-1290-y.

Comissão Temática de Biodiversidade e Áreas Protegidas – CTBio, 2020. Plano de manejo: área de proteção ambiental marinha do litoral norte. São Paulo: CTBio. Retrieved in 2023, June 1, from https://sigam.ambiente.sp.gov.br/sigam3/Repositorio/511/Documentos/APAM_LN/APAMLN_Plano_de_manejo_CTBio.pdf

Covich, A.P., Crowl, T.A., Hein, C.L., Townsend, M.J. & McDowell, W.H., 2009. Predator-prey interactions in river networks: comparing shrimp spatial refugia in two drainage basins. Freshw. Biol., 54(3), 450-465. http://dx.doi.org/10.1111/j.1365-2427.2008.02121.x.

Cross, W.F., Covich, A.P., Crowl, T.A., Benstead, J.P. & Ramírez, A., 2008. Secondary production, longevity and resource consumption rates of freshwater shrimps in two tropical streams with contrasting geomorphology and food web structure. Freshw. Biol., 53(12), 2504-2519. http://dx.doi.org/10.1111/j.1365-2427.2008.02078.x.

Davis, A.M., Blanchette, M.L., Pusey, B.J., Jardine, T.D. & Pearson, R.G., 2012. Gut content and stable isotope analyses provide complementary understanding of ontogenetic dietary shifts and trophic relationships among fishes in a tropical river. Freshw. Biol., 57(10), 2156-2172. http://dx.doi.org/10.1111/j.1365-2427.2012.02858.x.

Denadai, A.C., Costa, V.E., Wolf, M.R., Gonçalves, G.R.L. & Castilho, A.L., 2022. Isotopic signature and the trophic interactions of Aegla castro Schmitt, 1942 (Crustacea: Anomura: Aeglidae). Nauplius, 30, e2022024. http://dx.doi.org/10.1590/2358-2936e2022024.

Ducatti, C., Martins, C.L., Arrigoni, M.B., Martins, M.B., Vieira Júnior, L.C. & Denadai, J.C., 2011. Utilização de isótopos estáveis em ruminantes. Rev. Bras. Zootec., 40, 68-75.

Ebner, B.C., Donaldson, J.A., Murphy, H., Thuesen, P., Ford, A., Schaffer, J. & Keith, P., 2021. Waterfalls mediate the longitudinal distribution of diadromous predatory fishes structuring communities in tropical, short, steep coastal streams. Freshw. Biol., 66(6), 1225-1241. http://dx.doi.org/10.1111/fwb.13712.

Felgenhauer, B.E. & Abele, L.G., 1985. Feeding structures of two atyid shrimps, with comments on caridean phylogeny. J. Crustac. Biol., 5(3), 397-419. http://dx.doi.org/10.2307/1547911.

Fry, B., 1981. Natural stable carbon isotope tag traces Texas shrimp migrations. Fish Bull., 79, 337-345.

Fry, B., 2006. Stable isotope ecology. New York: Springer. http://dx.doi.org/10.1007/0-387-33745-8.

Fry, B., Mumford, P.L. & Robblee, M.B., 1999. Stable isotope studies of pink shrimp (Farfantepenaeus duorarum Burkenroad) migrations on the southwestern Florida shelf. Mar. Sci. Bull., 65, 419-430.

Graves, S., Piepho, H. & Dorai-Raj, S., 2019. multcompView: visualizations of paired comparisons. R package version 0.1-8 [online]. Vienna: The R Project for Statistical Computing. Retrieved in 2023, June 1, from https://CRAN.R-project.org/package=multcompView

Greathouse, E.A. & Pringle, C.M., 2006. Does the river continuum concept apply on a tropical island? Longitudinal variation in a Puerto Rican stream. Can. J. Fish. Aquat. Sci., 63(1), 134-152. http://dx.doi.org/10.1139/f05-201.

Grilli, N.M., Terossi, M. & Mantelatto, F.L., 2014. Sexual system of the freshwater shrimps of the genus Potimirim Holthuis (Decapoda: Caridea: Atyidae): is there a pattern in this genus? Mar. Freshw. Res., 65(9), 759-765. http://dx.doi.org/10.1071/MF13238.

Hanski, I., 1994. A practical model of metapopulation dynamics. J. Anim. Ecol., 63(1), 151-162. http://dx.doi.org/10.2307/5591.

Hein, C.L., Pike, A.S., Blanco, J.F., Covich, A., Scatena, F., Hawkins, C. & Crowl, T.A., 2011. Effects of coupled natural and anthropogenic factors on the community structure of diadromous fish and shrimp species in tropical island streams. Freshw. Biol., 56(5), 1002-1015. http://dx.doi.org/10.1111/j.1365-2427.2010.02537.x.

Hesslein, R.H., Capel, M.J., Fox, D.E. & Hallard, K.A., 1991. Stable isotopes of sulfur, carbon, and nitrogen as indicators of trophic level and fish migration in the lower Mackenzie River Basin, Canada. Can. J. Fish. Aquat. Sci., 48(11), 2258-2265. http://dx.doi.org/10.1139/f91-265.

Hoffmann, P. & Negreiros-Fransozo, M.L., 2010. Reproductive cycle and fecundity of Potimirim glabra (Kingsley, 1954) (Caridea, Atyidae) from a littoral stream. Invertebr. Reprod. Dev., 54(3), 133-141. http://dx.doi.org/10.1080/07924259.2010.9652325.

Hongjamrassilp, W., Maiphrom, W. & Blumstein, D.T., 2021. Why do shrimps leave the water? Mechanisms and functions of parading behaviour in freshwater shrimps. J. Zool., 313(2), 87-98. http://dx.doi.org/10.1111/jzo.12841.

Jackson, A.L., Inger, R., Parnell, A.C. & Bearhop, S., 2011. Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. J. Anim. Ecol., 80(3), 595-602. PMid:21401589. http://dx.doi.org/10.1111/j.1365-2656.2011.01806.x.

Jönck, C.R. & Aranha, J.M.R., 2010. Influence of a waterfall over richness and similarity in adjoining pools of an Atlantic Rainforest stream. Acta Limnol. Bras., 22(4), 378-383. http://dx.doi.org/10.4322/actalb.2011.003.

Kikkert, D.A., Crowl, T.A. & Covich, A.P., 2009. Upstream migration of amphidromous shrimps in the Luquillo Experimental Forest, Puerto Rico: temporal patterns and environmental cues. J. N. Am. Benthol. Soc., 28(1), 233-246. http://dx.doi.org/10.1899/08-019.1.

Layman, C.A., Winemiller, K.O. & Arrington, D.A., 2005. Describing the structure and function of a Neotropical river food web using stable isotopes, stomach contents, and functional experiments. In: Ruiter, P.C., Wolters, V. & Moore, J.C., eds. Dynamic food webs: multispecies assemblages, ecosystem development and environmental change. Amsterdam: Elsevier, 395-406. http://dx.doi.org/10.1016/B978-012088458-2/50037-0.

Lima, G.V. & Oshiro, L.M.Y., 2002. Partição ambiental de Potimirim glabra (Kingsley) e Potimirim potimirim (Müller) (Crustacea, Decapoda, Atyidae) no rio Sahy, Mangaratiba, Rio de Janeiro, Brasil. Rev. Bras. Zool., 19(Suppl. 2), 175-179. http://dx.doi.org/10.1590/S0101-81752002000600017.

Lima, G.V., Silveira, C.M. & Oshiro, L.M.Y., 2006. Estrutura populacional dos camarões simpátricos Potimirim glabra e Potimirim potimirim (Crustacea, Decapoda, Atyidae) no rio Sahy, Rio de Janeiro, Brasil. Iheringia Ser. Zool., 96(1), 81-87. http://dx.doi.org/10.1590/S0073-47212006000100015.

Lugendo, B.R., Nagelkerken, I., Van Der Velde, G. & Mgaya, Y.D., 2006. The importance of mangroves, mud and sand flats, and seagrass beds as feeding areas for juvenile fishes in Chwaka Bay, Zanzibar: gut content and stable isotope analyses. J. Fish Biol., 69(6), 1639-1661. http://dx.doi.org/10.1111/j.1095-8649.2006.01231.x.

Mantelatto, F.L., Torati, L.S., Pileggi, L.G., Mossolin, E.C., Terossi, M., Carvalho, F.L., Rocha, S.S. & Magalhães, C., 2016. Avaliação dos camarões atiídeos (Decapoda: Atyidae). In: Pinheiro, M. & Boos, H., eds. Livro vermelho dos crustáceos do Brasil: avaliação 2010-2014. Porto Alegre: Sociedade Brasileira de Carcinologia, 92-102.

Mantelatto, F.L., Vera-Silva, A.L., Prado, B.M. & Pileggi, L.G., 2021. Phylogenomic analyses reveals gene flow between populations of the freshwater shrimp Potimirim brasiliana (Caridea, Atyidae) along its wide distribution. An. Acad. Bras. Cienc., 93(2), e20190384. PMid:33729377. http://dx.doi.org/10.1590/0001-3765202120190384.

Mao, Z., Gu, X. & Zeng, Q., 2016. Food sources and trophic relationships of three decapod crustaceans: insights from gut contents and stable isotope analyses. Aquacult. Res., 47(9), 2888-2898. http://dx.doi.org/10.1111/are.12739.

Mazzoni, R., Fenerich-Verani, N., Caramaschi, É.P. & Iglesias-Rios, R., 2006. Stream-dwelling fish communities from an Atlantic rain forest drainage. Braz. Arch. Biol. Technol., 49(2), 249-256. http://dx.doi.org/10.1590/S1516-89132006000300010.

Minagawa, M. & Wada, E., 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim. Cosmochim. Acta, 48(5), 1135-1140. http://dx.doi.org/10.1016/0016-7037(84)90204-7.

Peterson, B.J. & Fry, B., 1987. Stable isotopes in ecosystem studies. Annu. Rev. Ecol. Syst., 18(1), 293-320. http://dx.doi.org/10.1146/annurev.es.18.110187.001453.

Post, D.M., 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83(3), 703-718. http://dx.doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2.

Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J. & Montaña, C.G., 2007. Getting to the fat of the matter: Models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia, 152(1), 179-189. PMid:17225157. http://dx.doi.org/10.1007/s00442-006-0630-x.

Reznick, D.N. & Ghalambor, C.K., 2005. Selection in nature: experimental manipulations of natural populations. Integr. Comp. Biol., 45(3), 456-462. PMid:21676790. http://dx.doi.org/10.1093/icb/45.3.456.

Rocha, S.S., Bueno, S.L.S., Shimizu, R.M. & Mantelatto, F.L., 2013. Reproductive biology and population structure of Potimirim brasiliana Villalobos, 1959 (Decapoda, Atyidae) from a littoral fast-flowing stream, São Paulo State, Brazil. Crustaceana, 86(1), 67-83. http://dx.doi.org/10.1163/15685403-00003151.

Santos, R.C., Pantaleão, J.A.F., Teles, J.N., França, N.F.C., Costa, J.R.P., Cabral, H., Pardo, L.M. & Mantelatto, F.L., 2022. The influence of natural barriers on the amphidromous shrimp Potimirim brasiliana (Caridea, Atyidae) from two rivers in Southeastern Brazil. Biol. Bull., 242(1), 27-39. PMid:35245163. http://dx.doi.org/10.1086/718590.

Selleslagh, J., Blanchet, H., Bachelet, G. & Lobry, J., 2015. Feeding habitats, connectivity and origin of organic matter supporting fish populations in an estuary with a reduced intertidal area assessed by stable isotope analysis. Estuaries Coasts, 38(5), 1431-1447. http://dx.doi.org/10.1007/s12237-014-9911-5.

Souza, M.L. & Moulton, T.P., 2005. The effects of shrimps on benthic material in a Brazilian island stream. Freshw. Biol., 50(4), 592-602. http://dx.doi.org/10.1111/j.1365-2427.2005.01348.x.

Taylor, M.D., Fry, B., Becker, A. & Moltschaniwskyj, N., 2017. Recruitment and connectivity influence the role of seagrass as a penaeid nursery habitat in a wave dominated estuary. Sci. Total Environ., 584-585, 622-630. PMid:28131456. http://dx.doi.org/10.1016/j.scitotenv.2017.01.087.

Terui, A., Miyazaki, Y., Yoshioka, A., Kaifu, K., Matsuzaki, S.S. & Washitani, I., 2014. Asymmetric dispersal structures a riverine metapopulation of the freshwater pearl mussel Margaritifera laevis. Ecol. Evol., 4(15), 3004-3014. PMid:25247058. http://dx.doi.org/10.1002/ece3.1135.

Torati, L.S. & Mantelatto, F.L., 2012. Ontogenetic and evolutionary change of external morphology of the neotropical shrimp Potimirim (Holthuis, 1954) explained by a molecular phylogeny of the genus. J. Crustac. Biol., 32(4), 625-640. http://dx.doi.org/10.1163/193724012X635322.

Vasconcellos, A.N. & Sanches, F.O., 2009. Análise e espacialização dos manguezais no município de Ubatuba (SP) utilizando-se recursos do sensoriamento remoto. Encicl. Biosf., 5(8), 1-21.

Villalobos, A., 1959. Contribución al conocimiento de los Atyidae de México. II (Crustacea, Decapoda). Estudio de algunas especies del género Potimirim (Ortmannia), con descripción de una especie nueva en Brasil. An. Inst. Biol., 30, 269-330.

Viozzi, M.F., Del Rio, C.M. & Williner, V., 2021. Tissue-specific isotopic incorporation turnover rates and trophic discrimination factors in the freshwater shrimp Macrobrachium borellii (Crustacea: Decapoda: Palaemonidae). Zool. Stud., 60, e32. PMid:34963785. https://doi.org/10.6620/ZS.2021.60-32.

Wickham, H., 2016. ggplot2: elegant graphics for data analysis [online]. New York: Springer-Verlag. Retrieved in 2023, June 1, from https://ggplot2.tidyverse.org

Wickham, H., François, R., Henry, L., Müller, K. & Vaughan, D., 2023. dplyr: a grammar of data manipulation. R package version 1.1.0 [online]. Vienna: The R Project for Statistical Computing. Retrieved in 2023, June 1, from https://CRAN.R-project.org/package=dplyr

World Register of Marine Species – WoRMS, 2023. Decapoda [online]. Oostende: WoRMS. Retrieved in 2023, June 19, from https://www.marinespecies.org/aphia.php?p=taxdetails&id=1130
 


Submitted date:
25/11/2022

Accepted date:
01/06/2023

Publication date:
19/07/2023

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