Skip to main content
Log in

Environmental factors modulated the fatty acid profile of the shrimp Xiphopenaeus spp. in Cananéia and Ubatuba southeast Brazilian coast

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Environmental characteristics influence the fatty acids (FAs) of aquatic organisms. Environmental factors and anthropic actions such as water pollution can impact FA composition. This directly affects the trophic network, especially when low-quality FA is provided to other trophic levels. The omnivore Penaeoidea shrimp is rich in proteins and polyunsaturated fatty acids (PUFA), representing an important node in the trophic web. We compared the FA composition of the commercially exploited seabob shrimp Xiphopenaeus spp. in two distinct coastal sites, Cananéia and Ubatuba, on the southeast Brazilian coast. Cananéia has a low human population density and is a preserved area with nearby mangroves, while Ubatuba is highly urbanised and influenced by tourism (increasing the domestic sewage), with diverse microhabitats but without mangrove influence. We found a total of 29 different FAs in seabob shrimp samples. Saturated FAs and PUFAS were the most representatives. For sex or age (juvenile and adult), deviations were found in the monosaturated FA, ω6, and ω3/ω6. However, FA composition was significantly different between sites, with Ubatuba presenting a lower abundance of FAs than Cananéia. The fatty acid composition of Xiphopenaeus spp. was influenced by environmental quality factors such as dissolved oxygen, chlorophyll, organic matter, and size gradient. The presence of high amounts of organic matter (especially sewage) during decomposition can decrease dissolved oxygen levels, reducing the quality of the first producers and limiting the availability of FAs for other trophic levels. The study suggests that water pollution and mangrove forests can impact the FAs of Xiphopenaeus spp., potentially reducing their nutritional value and causing an imbalance in the transference of FAs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

Gonçalves GRL, De Troch M. Zoology Department, Institute of Biosciences of Botucatu — São Paulo State University (UNESP), Brazil; Marine Biology Research Group; Ghent University (UGent-MARBIOL), Belgium (2020); fatty acids analysis of shrimp in São Paulo, Brazil; and Marine Data Archive: https://doi.org/10.14284/392.

References

  • Abarca-Arenas LG, Franco-López J, Peterson MS, Brown-Peterson NJ, Valero-Pacheco E (2007) Sociometric analysis of the role of penaeids in the continental shelf food web off Veracruz, Mexico based on by-catch. Fish Res 87(1):46–57

    Article  Google Scholar 

  • Ackman RG, Sipos JC (1964) Application of specific response factors in the gas chromatographic analysis of methyl esters of fatty acids with flame ionization detectors. J Am Oil Chem Soc 41(5):377–378

    Article  CAS  Google Scholar 

  • Alfaro AC, Thomas F, Sergent L, Duxbury M (2006) Identification of trophic interactions within an estuarine food web (northern New Zealand) using fatty acid biomarkers and stable isotopes. Estuar Coast Shelf Sci 70(1–2):271–286

    Article  Google Scholar 

  • Batista SS, Harari J (2017) Modelagem da dispersão de coliformes termotolerantes e enterococos em duas enseadas na região costeira de Ubatuba (SP), Brasil. Eng Sanit e Ambient 22(2):403–413. https://doi.org/10.1590/S1413-41522016158594

    Article  CAS  Google Scholar 

  • Becegato JL (2007) Impacto ambiental antrópico na APA (Área de Proteção Ambiental) da Ilha Comprida (SP), da Pré–História à atualidade. Dissertação de Mestrado em Análise Geoambiental. Universidade de Guarulhos

  • Bejaoui S, Boussoufa D, Telahigue K, Chetoui I, Ghribi F, Rabeh I, El Cafsi M (2019) Geographic variation in fatty acid composition and food source of the commercial clam (Venerupis decussata, Linnaeus, 1758), from the Tunisian Coast: trophic links. Grasas Aceites 70(1):289. https://doi.org/10.3989/gya.0580181

    Article  CAS  Google Scholar 

  • Bolton PW, Currie JC, Tervey DJ, Welsh WT (1978) An index to improve water quality classification. Wat Pollut Control 12(2):271–280

    Google Scholar 

  • Boos H, Costa RC, Santos RAF, Dias-Neto J, Severino-Rodrigues E, Rodrigues LF, D’incao F, Ivo CTC, Coelho PA (2016) Avaliação dos camarões peneídeos (Decapoda: Penaeidae). In: Pinheiro M, Boos H (eds.) Livro Vermelho Dos Crustáceos Do Brasil: Avaliação 2010–2014. Sociedade Brasileira de Carcinologia – SBC, Porto Alegre, RS, pp 300–317

  • Boyen J, Fink P, Mensens C, Hablützel PI, De Troch M (2020) Fatty acid bioconversion in harpacticoid copepods in a changing environment: a transcriptomic approach. Philos Trans R Soc B 375:20190645. https://doi.org/10.1098/rstb.2019.0645

    Article  CAS  Google Scholar 

  • Brett MT, Müller-Navarra DC (1997) The role of fatty acids in aquatic foodweb processes. Freshw Biol 38:483−499

  • Burbano-Rosero EM, Ueda-Ito M, Kisielius JJ, Nagasse-Sugahara TK, Almeida BC, Souza CP, Markman C, Martins GG, Albertini L, Rivera ING (2011) Diversity of somatic coliphages in coastal regions with different levels of anthropogenic activity in Sao Paulo State, Brazil. Appl Environ Microbiol 77(12):4208–4216

    Article  CAS  Google Scholar 

  • Canuel EA (2001) Relations between river flow, primary production and fatty acid composition of particulate organic matter in San Francisco and Chesapeake Bays: a multivariate approach. Org Geochem 32(4):563–583

    Article  CAS  Google Scholar 

  • Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Kinzig AP (2012) Biodiversity loss and its impact on humanity. Nature 486(7401):59–67

    Article  CAS  Google Scholar 

  • Carvalho-Batista A, Terossi M, Zara FJ, Mantelatto FL, Costa RC (2019) A multigene and morphological analysis expands the diversity of the seabod shrimp Xiphopenaeus Smith, 1869 (Decapoda: Penaeidae), with descriptions of two new species. Sci Rep 9(1):1–19. https://doi.org/10.1038/s41598-019-51484-3

    Article  CAS  Google Scholar 

  • CETESB (2018) Relatório de qualidade das águas costeiras no estado de São Paulo. Disponible in https://cetesb.sp.gov.br/aguas-costeiras/wp-content/uploads/sites/2/2019/10/Relat%C3%B3rio-de-Qualidade-das-%C3%81guas-Costeiras-no-Estado-de-S%C3%A3o-Paulo-2018.pdf. Accessed 12 July 2020

  • Costa RC, Heckler GS, Simões SM, Lopes M, Castilho AL (2011) Seasonal variation and environmental influences on abundance of juveniles of the seabob shrimp Xiphopenaeus kroyeri (Heller, 1862) in southeastern Brazil. In: Pessani D, Tirelli T, Froglia C (eds), IX Colloquium Crustacea Mediterranea – Behaviour, Ecology, Fishery. Torino, Italy: Monografie del Museo Regionale di Scienze Naturali, pp 47−58

  • Dall W, Hill BJ, Rothlisberg PC, Sharples DJ (1990) The biology of the Penaeidae. In: Blaxter JHS, Southward AJ (eds) Advances in marine biology. Academic Press, London, pp 1–489

    Google Scholar 

  • Dalsgaard J, John MS, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:226–340

    Google Scholar 

  • De Laender F, Rohr JR, Ashauer R, Baird DJ, Berger U, Eisenhauer N, Grimm V, Hommen U, Maltby L, Meliàn CJ, Pomati F, Roessink I, Radchuk V, Van den Brink PJ (2016) Reintroducing environmental change drivers in biodiversity–ecosystem functioning research. Trends Ecol Evol 31(12):905–915. https://doi.org/10.1016/j.tree.2016.09.007

    Article  Google Scholar 

  • De Troch M, Boeckx P, Cnudde C, Van Gansbeke D, Vanreusel A, Vincx M, Caramujo MJ (2012) Bioconversion of fatty acids at the basis of marine food webs: insights from a compound-specific stable isotope analysis. Mar Ecol Prog Ser 465:53–67. https://doi.org/10.3354/meps09920

    Article  CAS  Google Scholar 

  • Diegues ACS (1987) Conservação e desenvolvimento sustentado de ecossistemas litorâneos no Brasil. In: Simpósio sobre Ecossistemas da Costa Sul e Sudeste Brasileira, Academia de Ciências do Estado de São Paulo, Cananéia, São Paulo, pp 196−213

  • Di Salvatore P, Calcagno JA, Ortíz N, de Molina MDCR, Sabatini SE (2013) Effect of seasonality on oxidative stress responses and metal accumulation in soft tissues of Aulacomya atra, a mussel from the South Atlantic Patagonian coast. Mar Environ Res 92:244–252. https://doi.org/10.1016/j.marenvres.2013.10.004

    Article  CAS  Google Scholar 

  • Djuricic I, Calder PC (2021) Beneficial outcomes of omega-6 and omega-3 polyunsaturated fatty acids on human health: an update for 2021. Nutrients 13(7):2421. https://doi.org/10.3390/nu13072421

    Article  CAS  Google Scholar 

  • Fransozo V, Carvalho dos Santos D, López-Greco LS, Júnior EAB (2011) Development of secondary sexual characters in the seabob shrimp Xiphopenaeus kroyeri (Heller 1862) (Crustacea, Decapoda, Penaeidae): a scanning electron microscope study. Invertebr Reprod Dev 55(1):6–15

    Article  Google Scholar 

  • Galloway AWE, Winder M (2015) Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids. PLoS ONE 10(6):1–23. https://doi.org/10.1371/journal.pone.0130053

    Article  CAS  Google Scholar 

  • Garcia JR, Lopes AEB, Silvestre AKC, Grabowski RC, Barioto JG, Costa RC, Castilho AL (2018) Environmental characterization of the Cananéia coastal area and its associated estuarine system (São Paulo state, Brazil): considerations for three Penaeoidean shrimp species. Reg Stud Mar Sci 19:9–16. https://doi.org/10.1016/j.rsma.2018.02.010

    Article  Google Scholar 

  • Gatune WC, Vanreusel A, Ruwa R, Bossier P, De Troch M (2014) Fatty acid profiling reveals a trophic link between mangrove leaf litter biofilms and the post-larvae of giant tiger shrimp Penaeus monodon. Aquacult Environ Interact 6(1):1–10. https://doi.org/10.3354/aei00117

    Article  Google Scholar 

  • Gonçalves GRL, Denadai AC, Sousa AN, Castilho AL, De Troch M (2021) Fatty acid profiles of three commercial shrimp from southeastern Brazil. Reg Stud Mar Sci 48:102032. https://doi.org/10.1016/j.rsma.2021.102032

    Article  Google Scholar 

  • Gonçalves Loureiro T, Anastácio PM, de Siqueira Bueno SL, Wood CT, Araujo PB (2019) Food matters: trophodynamics and the role of diet in the invasion success of Procambarus clarkii in an Atlantic Forest conservation area. Limnologica 79:125717. https://doi.org/10.1016/j.limno.2019.125717

    Article  Google Scholar 

  • Grabowski RC, Negreiros-Fransozo ML, Castilho AL (2016) Reproductive ecology of the seabob shrimp Xiphopenaeus kroyeri (Heller, 1862) in a coastal area of southern Brazil. Chin J Oceanol Limnol 34(1):125–135. https://doi.org/10.1007/s00343-015-4279-3

    Article  Google Scholar 

  • Guckert JB, Antworth CP, Nichols PD, White DC (1985) Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Ecol 1(3):147–158

    Article  Google Scholar 

  • Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319(5865):948–952

    Article  CAS  Google Scholar 

  • IBGE (2019) Brazilian Institute for Geography and Statistics. Disponible in http://www.sidra.ibge.gov.br (in Portuguese). Accessed 03 Febuary 2020

  • Instituto de Pesca do Estado de São Paulo (2019) Secretaria de Agricultura e Abastecimento. http://www.propesq.pesca.sp.gov.br/relatorio/30. Accessed April 2019

  • Iverson SJ (2009) Tracing aquatic food webs using fatty acids: from qualitative indicators to quantitative determination. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, Dordrecht, pp 281–307

    Chapter  Google Scholar 

  • Jannathulla R, Chitra V, Vasanthakumar D, Nagavel A, Ambasankar K, Muralidhar M, Dayal JS (2019) Effect of dietary lipid/essential fatty acid level on Pacific whiteleg shrimp, Litopenaeus vannamei (Boone, 1931) reared at three different water salinities–emphasis on growth, hemolymph indices and body composition. Aquaculture 513:734405. https://doi.org/10.1016/j.aquaculture.2019.734405

    Article  CAS  Google Scholar 

  • Jari O, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szoecs E, Wagner H (2019) vegan: Community ecology package. R package version 2.5–6. https://CRAN.R-project.org/package=vegan

  • Kaneda T (1991) Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomical significance. Microbiol Rev 55:288–302

    Article  CAS  Google Scholar 

  • Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22. https://doi.org/10.3354/meps09559

    Article  CAS  Google Scholar 

  • Kerkhove TR, Boyen J, De Backer A, Mol JH, Volckaert FA, Leliaert F, De Troch M (2019b) Multilocus data reveal cryptic species in the Atlantic seabob shrimp Xiphopenaeus kroyeri (Crustacea: Decapoda). Biol J Linn Soc Lond 127(4):847–862. https://doi.org/10.1093/biolinnean/blz065

    Article  Google Scholar 

  • Kerkhove TR, Hellemans B, De Troch M, De Backer A, Volckaert FA (2019a) Isolation and characterisation of 14 novel microsatellite markers through next generation sequencing for the commercial Atlantic seabob shrimp Xiphopenaeus kroyeri. Mol Biol Rep 46(6):6565–6569. https://doi.org/10.1007/s11033-019-05026-9

    Article  CAS  Google Scholar 

  • Kharlamenko VI, Kiyashko SI, Imbs AB, Vyshkvartzev DI (2001) Identification of food sources of invertebrates from the seagrass Zostera marina community using carbon and sulfur stable isotope ratio and fatty acid analyses. Mar Ecol Prog Ser 220:103–117

    Article  CAS  Google Scholar 

  • Kunlasak K, Chitmanat C, Whangchai N, Promya J, Lebel L (2013) Relationships of dissolved oxygen with chlorophyll-a and phytoplankton composition in tilapia ponds. Int J Geosci 4(05):46. https://doi.org/10.4236/ijg.2013.45B008

    Article  CAS  Google Scholar 

  • Li M, Xie GQ, Dai CR, Yu LX, Li FR, Yang SP (2009) A study of the relationship between the water body chlorophyll and water quality factors of the off coast of Dianchi Lake. Yunnan Geographic Environ Res 21(2):102–106

    Google Scholar 

  • Lowe AT, Galloway AWE, Yeung JS, Dethier MN, Duggins DO (2014) Broad sampling and diverse biomarkers allow characterization of nearshore particulate organic matter. Oikos 123(11):1341–1354. https://doi.org/10.1111/oik.01392

    Article  CAS  Google Scholar 

  • Maia ML, Almeida A, Soares C, Silva LM, Delerue-Matos C, Calhau C, Domingues VF (2022) Minerals and fatty acids profile of Northwest Portuguese coast shrimps. J Food Compos Anal 112:104652. https://doi.org/10.1016/j.jfca.2022.104652

    Article  CAS  Google Scholar 

  • Mantelatto FLM, Corrêa EK (1996) Composition and seasonal variations of the brachyuran crabs (Crustacea, Decapoda) living on Sargassum cymosum in Ubatuba region, São Paulo, Brazil. Bioikos 9(1):22–31

    Google Scholar 

  • Mantelatto FLM, Avelar WEP, Silva DML, Tomazelli AC, Lopez JLC, Shuhama T (1999) Heavy metals in the shrimp Xiphopenaeus kroyeri (Heller, 1862) (crustacea, penaeidae) from Ubatuba Bay, Sao Paulo, Brazil. Bull Environ Contam Toxicol 62(2):152–159

    Article  CAS  Google Scholar 

  • Mantelatto FLM, Bernardo CH, Silva TE, Bernardes VP, Fransozo A (2016) Composição e distribuição de crustáceos decápodes associados à pesca do camarão-sete-barbas Xiphopenaeus kroyeri (Heller, 1862) no litoral norte do estado de São Paulo. Bol Inst Pesca 42(2):307–326. https://doi.org/10.20950/1678-2305.2016v42n2p307

    Article  Google Scholar 

  • Mariamenatu AH, Abdu EM (2021) Overconsumption of omega-6 polyunsaturated fatty acids (PUFAs) versus deficiency of omega-3 PUFAs in modern-day diets: the disturbing factor for their “balanced antagonistic metabolic functions” in the human body. J Lipids 2021:1–15. https://doi.org/10.1155/2021/8848161

    Article  CAS  Google Scholar 

  • Melo KC, Furlan SÂ (2017) Diferentes paisagens do município de Ubatuba-SP: um estudo geográfico. GEOUSP Espaço E Tempo 21(3):650–666. https://doi.org/10.11606/issn.2179-0892.geousp.2017.116478

    Article  Google Scholar 

  • Mendonça JT, Katsuragawa M (2001) Caracterização da pesca artesanal no complexo estuarino-lagunar de Cananéia-Iguape, Estado de São Paulo, Brasil (1995–1996). Acta Sci Biol Sci 23:535–547

    Google Scholar 

  • Mendonça JT, Verani JR, Nordi N (2010) Evaluation and management of blue crab Callinectes sapidus (Rathbun, 1896) (Decapoda-Portunidae) fishery in the estuary of Cananéia, Iguape and Ilha Comprida, São Paulo, Brazil. Braz J Biol 70(1):37–45. https://doi.org/10.1590/S1519-69842010000100007

    Article  Google Scholar 

  • Mensens C, De Laender F, Janssen CR, Rivera FC, Sabbe K, De Troch M (2018) Selective and context-dependent effects of chemical stress across trophic levels at the basis of marine food webs. Ecol Appl 28(5):1342–1353. https://doi.org/10.1002/eap.1737

    Article  Google Scholar 

  • Müller-Navarra DC, Brett MT, Park S, Chandra S, Ballantyne AP, Zorita E, Goldman CR (2004) Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes. Nature 427(69):72

    Google Scholar 

  • Nagata RM, Moreira MZ, Pimentel CR, Morandini AC (2015) Food web characterization based on δ15N and δ13C reveals isotopic niche partitioning between fish and jellyfish in a relatively pristine ecosystem. Mar Ecol Prog Ser 519:13–27. https://doi.org/10.3354/meps11071

    Article  CAS  Google Scholar 

  • Nakagaki JM, Negreiros-Fransozo ML (1998) Population biology of Xiphopenaeus kroyeri (Heller 1986) (Decapoda: Penaeidae) from Ubatuba bay, São Paulo Brazil. J Shellfish Res 17(4):931–935

    Google Scholar 

  • Negreiros-Fransozo ML, Fransozo A, Hebling NJ (1991) Estrutura populacional e determinação do tamanho da concha em 4 espécies de ermitões (Crustacea, Decapoda, Anomura) do litoral paulista. Biotemas 4(2):135–148

    Google Scholar 

  • Parrish CC (2009) Essential fatty acids in aquatic food webs. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 309–326

    Chapter  Google Scholar 

  • Parrish CC, Abrajano TA, Budge SM, Helleur RJ, Hudson ED, Pulchan K, Ramos C (2000) Lipid and phenolic biomarkers in marine ecosystems: analysis and applications. In: Wangersky PJ (ed) Marine chemistry. Springer, Heidelberg, pp 193–223

    Chapter  Google Scholar 

  • Pinto KC, Lauretto MS, Gonzalez MIJN, Sato MIZ, Nardocci AC, Razzolini MTP (2020) Assessment of health risks from recreational exposure to Giardia and Cryptosporidium in coastal bathing waters. Environ Sci Pollut Res Int 1–12. https://doi.org/10.1007/s11356-020-08650-2

  • Pires DR, De Morais ACN, Coelho CCS, Marinho AF, Góes LCDSA, Augusta IM, Ferreira FS, Saldanha T (2018) Nutritional composition, fatty acids and cholesterol levels in Atlantic white shrimp (Litopenaeus schimitti). Int Food Res J 25(1):151–157

    CAS  Google Scholar 

  • Powell N, Chaudhary S, Zaidi A (2021) It is time for an oil change: polyunsaturated fatty acids and human health. Mo Med 118(5):426

    Google Scholar 

  • R Core Team (2020) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna (Austria). https://www.r-project.org.atstical

  • Rocchetta I, Mazzuca M, Conforti V, Balzaretti V, Molina MDCR (2012) Chromium induced stress conditions in heterotrophic and auxotrophic strains of Euglena gracilis. Ecotoxicol Environ Saf 84:147–154. https://doi.org/10.1016/j.ecoenv.2012.07.020

    Article  CAS  Google Scholar 

  • Rocchetta I, Pasquevich MY, Heras H, Molina MDCR, Luquet CM (2014) Effects of sewage discharges on lipid and fatty acid composition of the Patagonian bivalve Diplodon chilensis. Mar Pollut Bull 79(1–2):211–219. https://doi.org/10.1016/j.marpolbul.2013.12.011

    Article  CAS  Google Scholar 

  • Rodrigues VF, Rivera IN, Lim KY, Jiang SC (2016) Detection and risk assessment of diarrheagenic E. coli in recreational beaches of Brazil. Mar Pollut Bull 109(1):163–170. https://doi.org/10.1016/j.marpolbul.2016.06.007

    Article  CAS  Google Scholar 

  • Ruan XH, Shi XD, Zhao ZH, Ni LX, Wu Y, Jiao T (2008) Correlation between chlorophyll a concentration and environmental factors in shallow lakes in plain river network areas of Suzhou. J Lake Sci 20(5):556–562

    Article  CAS  Google Scholar 

  • Sabatini SE, Rocchetta I, Luquet CM, Guido MI, De Molina MDCR (2011) Effects of sewage pollution and bacterial load on growth and oxidative balance in the freshwater mussel Diplodon chilensis. Limnologica 41(4):356–362. https://doi.org/10.1016/j.limno.2011.04.004

    Article  CAS  Google Scholar 

  • Sato MIZ, Di Bari M, Lamparelli CC, Truzzi AC, Coelho MCLS, Hachich EM (2005) Sanitary quality of sands from marine recreational beaches of São Paulo, Brazil. Braz J Microbiol 36(4):321–326

    Article  Google Scholar 

  • Segura R (1988) Preparation of fatty acid methyl esters by direct transesterification of lipids with aluminium chloride methanol. J Chromatogr 441:99–118

    Article  CAS  Google Scholar 

  • SNIS (2014) Diagnóstico dos Serviços de Água e Esgotos – 2104 (Diagnoses of water and wastewater services – 2014). Ministério das Cidades (Ministery of Cities), Brasília. Accessed 04 Febuary 2020. http://www.snis.gov.br/diagnostico-anual-agua-e-esgotos/diagnostico-ae-2014

  • Sokal RR, Rohlf FJ (1987) Introduction to biostatistics, 2nd edn. Freeman, New York

    Google Scholar 

  • UNESCO (1999) World Heritage Nomination - IUCN Technical Evaluation Atlantic Forests (southeast) (Brazil). UNESCO, pp 8

  • UNESCO (2005) World Network of Biosphere Reserves – SC/EES – June 2005. The MAB Program. UNESCO, pp 19

  • William JA, Sharma A, Morris JL, Holman RT (1960) Fatty acid composition of feces and fecaliths. Proc Soc Exp Biol Med 105:192–195

    Article  Google Scholar 

  • Willems T, De Backer A, Kerkhove T, Dakriet NN, De Troch M, Vincx M, Hostens K (2016) Trophic ecology of Atlantic seabob shrimp Xiphopenaeus kroyeri: intertidal benthic microalgae support the subtidal food web off Suriname. Estuar Coas Shelf Sci 182:146–157. https://doi.org/10.1016/j.ecss.2016.09.015

    Article  CAS  Google Scholar 

  • Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, De Vos P, Heylen K, Verstraete W, Boon N (2009) Initial community evenness favours functionality under selective stress. Nature 458:623–626. https://doi.org/10.1038/nature07840

    Article  CAS  Google Scholar 

  • Wolff RL, Bayard CC, Fabien RJ (1995) Evaluation of sequential methods for the determination of butterfat fatty acid composition with emphasis ontrans-18: 1 acids. Application to the study of seasonal variations in French butters. J Am Oil Chem Soc 72(12):1471–1483

    Article  CAS  Google Scholar 

  • Zang C, Huang S, Wu M, Du S, Scholz M, Gao F, Lin C, Guo Y, Dong Y (2011) Comparison of relationships between pH, dissolved oxygen and chlorophyll a for aquaculture and non-aquaculture waters. Water Air Soil Pollut 219(1–4):157–174. https://doi.org/10.1007/s11270-010-0695-3

    Article  CAS  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1(1):3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x

    Article  Google Scholar 

Download references

Acknowledgements

We thank the PhD Camila T. Woody and the Ma. Alexander Wilkes for the English corrections. We also thank “Instituto Chico Mendes de Conservação da Biodiversidade” (ICMBio) and the “Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis” (IBAMA) for granting permission to collect the samples. The research leading to the results presented in this publication was carried out with infrastructure funded by EMBRC Belgium — FWO International Research Infrastructure I001621N.

Funding

This work was supported by the following: Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP: 2016/20177-0, 2018/01659-0, 2019/00105-3), “Conselho Nacional de Desenvolvimento Científico e Tecnológico — CNPq” (311034/2018-7 to ALC), European Union’s Horizon 2020 research and innovation programme under grant agreement no. 730984, and ASSEMBLE Plus project. The FA analyses were supported by Special Research Fund of Ghent University (BOF-UGent) in the form of the starting grant “Energy transfer at the basis of marine food webs in a changing world” awarded to the last author.

Author information

Authors and Affiliations

Authors

Contributions

GRLG, conceptualization, methodology, investigation, formal analysis, funding acquisition, and writing — original draft; PVMS, investigation and formal analysis; MLNF, conceptualization, methodology, investigation, and writing — review and editing; ALC, investigation, funding acquisition, supervision, and writing — review and editing; and MDT, conceptualization, methodology, investigation, funding acquisition, formal analysis, supervision, and writing — review and editing.

Corresponding author

Correspondence to Geslaine Rafaela Lemos Gonçalves.

Ethics declarations

Ethics approval and consent to participate

Not applicable. Animals used in this assay are from an invertebrate species, which do not require previous ethics approval.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Bruno Nunes

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 26 KB)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gonçalves, G.R.L., dos Santos, P.V.M., Negreiros-Fransozo, M.L. et al. Environmental factors modulated the fatty acid profile of the shrimp Xiphopenaeus spp. in Cananéia and Ubatuba southeast Brazilian coast. Environ Sci Pollut Res 30, 76936–76949 (2023). https://doi.org/10.1007/s11356-023-27846-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-27846-w

Keywords

Navigation