Phylogenetic and environmental components of inter-specific variability in the antioxidant defense system in freshwater anomurans Aegla (Crustacea, Decapoda)

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Faria, Samuel Coelho ^a,c   Klein, Roberta Daniele ^a   Costa, Patrícia Gomes ^a   Crivellaro, Marcelo Schüler ^b   Santos, Sandro ^b   Bueno, Sérgio Luiz De Siqueira ^c   Bianchini, Adalto ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE   (Brazil)

^b FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ARTHROPOD PROTEIN; FRESH WATER; METAL;

ANIMAL; CHEMISTRY; CLASSIFICATION; DECAPODA (CRUSTACEA); ECOSYSTEM; FEMALE; GENETICS; HEPATOPANCREAS; MALE; METABOLISM; OXIDATIVE STRESS; PH; PHYLOGENY; SPECIES DIFFERENCE; WATER POLLUTANT;

ANIMALS; ARTHROPOD PROTEINS; DECAPODA (CRUSTACEA); ECOSYSTEM; FEMALE; FRESH WATER; HEPATOPANCREAS; HYDROGEN-ION CONCENTRATION; MALE; METALS; OXIDATIVE STRESS; PHYLOGENY; SPECIES SPECIFICITY; WATER POLLUTANTS, CHEMICAL;

EID: 85042022817     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-21188-1     Document Type: Article

References (83)

1. Monosson, E. Evolution in a toxic world. (Island Press., Washington, DC, 2006).
2. Falkowski, P. Tracing oxygen's imprint on earth's metabolic evolution. Science. 311, 1724-1725 (2006).
3. Costantini, D., Rowe, M., Butler, M. W., Kevin, J. &McGraw, K. J. From molecules to living systems: historical and contemporary issues in oxidative stress and antioxidant ecology. Funct. Ecol. 24, 950-959 (2010).
4. Abell, R. Conservation biology for the biodiversity crisis: a freshwater follow-up. Conserv. Biol. 16, 1435-1437 (2002).
5. Hochachka, P. W. &Somero, G. N. Biochemical adaptation: mechanism and process in physiological evolution. (Oxford University Press., New York., 2002).
6. Bond-Buckup, G., Jara, C. J., Pérez-Losada, M., Buckup, L. &Crandall, K. A. Global diversity of crabs (Aeglidae: Anomura: Decapoda) in freshwater. Hydrobiologia. 595, 267-273 (2008).
7. McNamara, J. C. &Faria, S. C. Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. J. Comp. Physiol. B. 182, 997-1014 (2012).
8. Tumini, G., Giri, F., Williner, V. &Collins, P. A. The importance of biogeographical history and extant environmental conditions as drivers of freshwater decapod distribution in southern South America. Freshwater Biol. 61, 715-728 (2016).
9. Lane, N. Oxygen: the molecule that made the world. (Oxford University Press, U.K., 2004).
10. Stearns, S. C. The evolution of life histories. (Oxford University Press, UK, 1992).
11. Wikelski, M. &Ricklefs, R. E. The physiology of life-histories. Trends Ecol. Evol. 16, 479-481 (2001).
12. Baldauf, S. L. The deep roots of eukaryotes. Science. 300, 1703-1706 (2003).
13. Wiersma, P., Muñoz-Garcia, A., Walker, A. &Williams, J. B. Tropical birds have a slow pace of life. Proc. Natl. Acad. Sci. 104, 9340-9345 (2007).
14. Bradshaw, W. E. &Holzapfel, C. M. Genetic response to rapid climate change: it's seasonal timing that matters. Mol. Ecol. 17, 157-166 (2008).
15. Trevisan, A., Hepp, L. U. &Santos, S. Abundância e distribuição de Aeglidae (Crustacea: Anomura) em função do uso da terra na bacia hidrográfica do Rio Jacutinga, Rio Grande do Sul, Brasil. Zoologia (Curitiba, Impr.). 26, 419-426 (2009).
16. Giam, X., Ng, T. H., Lok, A. F. &Ng, H. H. Local geographic range predicts freshwater fish extinctions in Singapore. J. Appl. Ecol. 48, 356-363 (2011).
17. Moraes, J. C. et al. Morphological and molecular data reveal the cryptic diversity among populations of Aegla paulensis (Decapoda, Anomura, Aeglidae), with descriptions of four new species and comments on dispersal routes and conservation status. Zootaxa. 4193, https://doi.org/10.11646/zootaxa.4193.1.1 (2016).
18. Bueno, S. L. D. S., Camargo, A. L. &Moraes, J. C. B. A new species of stygobitic aeglid from lentic subterranean waters in southeastern Brazil, with an unusual morphological trait: short pleopods in adult males. Nauplius 25, https://doi.org/10.1590/2358-2936e2017021 (2017).
19. Santos, S. et al. Diversity and conservation status of Aegla spp. (Anomura, Aeglidae): an update. Nauplius 25, https://doi. org/10.1590/2358-2936e2017011 (2017).
20. Pérez-Losada, M., Bond-Buckup, G., Jara, C. G. &Crandall, K. A. Molecular systematics and biogeography of the southern South American freshwater "crabs" Aegla (Decapoda: Anomura: Aeglidae) using multiple heuristic tree search approaches. Syst. Biol. 53, 767-780 (2004).
21. Bueno, S. L. S., Shimizu, R. M. &Moraes, J. C. B. A Remarkable Anomuran: The Taxon Aegla Leach, 1820. Taxonomic Remarks, Distribution, Biology, Diversity and Conservation. In A Global Overview of the Conservation of Freshwater Decapod Crustaceans (eds Kawai, T. &Cumberlidge, N.)23-64 (Springer International Publishing, 2016).
22. Pérez-Losada, M., Bond-Buckup, G., Jara, C. G. &Crandall, K. A. Conservation assessment of southern South American freshwater ecoregions on the basis of the distribution and genetic diversity of crabs from the genus Aegla. Conserv. Biol. 23, 692-702 (2009).
23. Bond-Buckup, G. &Buckup, L. A família Aeglidae (Crustacea, Decapoda, Anomura). Arq. Zool. 32, 159-347 (1994).
24. Bond-Buckup, G. Família Aeglidae, In Manual de identificação dos Crustacea Decapoda de água doce do Brasil (ed. Melo, G. A. S.) 429 (Editora Loyola, São Paulo, 2003).
25. Jara, C. Taxonomía, Sistemática Y Zoogeografía de Las Especies Chilenas Del Género Aegla Leach (Crustacea, Decapoda, Anomura, Aeglidae). Ph.D. Thesis (University of Concepción, Concepción, CL, 1996).
26. Bahamonde, N. et al. Categorías de conservación de Decápodos nativos de aguas continentales de Chile. Bol. Mus. Nac. Hist. Nat. 47, 91-100 (1998).
27. Oliveira, G. T., Fernandes, F. A., Bueno, A. A. P. &Bond-Buckup, G. Seasonal variations in the intermediate metabolism of Aegla platensis (Crustacea, Aeglidae). Comp. Biochem. Physiol. A. 147, 600-606 (2006).
28. Dalosto, M. &Santos, S. Differences in oxygen consumption and diel activity as adaptations related to microhabitat in Neotropical freshwater decapods (Crustacea). Comp. Biochem. Physiol. A. 160, 461-466 (2011).
29. Freire, C. A. et al. Muscle water control in crustaceans and fishes as a function of habitat, osmoregulatory capacity, and degree of euryhalinity. Comp. Biochem. Physiol. A. 149, 435-446 (2008).
30. Freire, C. A., Souza-Bastos, L. R., Amado, E. M., Prodocimo, V. &Souza, M. M. Regulation of muscle hydration upon hypo-or hyper-osmotic shocks: differences related to invasion of the freshwater habitat by decapod crustaceans. J. Exp. Zool. A. Ecol. Genet. Physiol. 319, 297-309 (2013).
31. Faria, S. C., Augusto, A. S. &McNamara, J. C. Intra-and extracellular osmotic regulation in the hololimnetic Caridea and Anomura: a phylogenetic perspective on the conquest of fresh water by the decapod Crustacea. J. Comp. Physiol. B. 181, 175-186 (2011).
32. Zall, D. M., Fisher, D. &Gamer, M. Q. Photometric determination of chlorides in water. Anal. Chem. 28, 1665-1668 (1956).
33. Tabatabai, M. A. A rapid method for determination of sulfate in water sample. Environ. Lett. 7, 237-243 (1974).
34. APHA. Standard Methods for the Examination of Water and Wastewater. (American Public Health Association, Washington D.C, 1989).
35. Zimmermann, C. F., Keefe, C. W., Bashe, J. Method 440.0. Determination of carbon and nitrogen in sediments and particulates of estuarine/coastal waters using elemental analysis. U.S. Environmental Protection Agency, Washington, DC, EPA/600/R-15/009, (1997).
36. Mantel, L. H. &Farmer, L. L. Osmotic and ionic regulation. In The Biology of Crustacea, Vol. 5 Internal Anatomy and Physiological Regulation (ed. Bliss, D. E.) 53-159 (Academic Press, 1983).
37. Winston, G. W., Regoli, F., Dugas, A. J., Fong, J. H. &Blanchard, K. A. A rapid gas chromatographic assay for determining oxyradical scavenging capacity of antioxidants and biological fluids. Free Rad. Biol. Med. 24, 480-493 (1998).
38. Regoli, F. &Winston, G. W. Quantification of total oxidant scavenging capacity of antioxidants for peroxynitrite, peroxyl radicals, and hydroxyl radicals. Toxicol. Appl. Pharmacol. 156, 96-105 (1999).
39. Amado, L. L. et al. A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: Application to evaluate microcystins toxicity. Sci. Total Environ. 407, 2115-2123 (2009).
40. Regoli, F. Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: a predictive biomarker of oxidative stress. Aquat. Toxicol. 50, 351-361 (2000).
41. Zaroogian, G. &Jackim, E. In vivo metallothionein and glutathione status in an acute response to cadmium in Mercenaria mercenaria brown cells. Comp. Biochem. Physiol. C. 127, 251-261 (2000).
42. Amiard, J. C., Amiard-Triquet, C., Barka, S., Pellerin, J. &Rainbow, P. S. Metallothioneins in aquatic invertebrates: Their role in metal detoxification and their use as biomarkers. Aquat. Toxicol. 76, 160-202 (2006).
43. Viarengo, A. et al. Role of metallothionein against oxidative stress in the mussel Mytilus galloprovincialis. Am. J. Physiol. 277, 1612-1619 (1999).
44. Cavaletto, M. et al. Effect of hydrogen peroxide on antioxidant enzymes and metallothionein level in the digestive gland of Mytilus galloprovincialis. Comp. Biochem. Physiol. 131, 447-455 (2002).
45. Correia, A. D., Livingstone, D. R. &Costa, M. H. Effects of water-borne copper on metallothionein and lipid peroxidation in the marine amphipod Gammarus locusta. Mar. Environ. Res. 54, 357-360 (2002).
46. Viarengo, A., Ponzano, E., Dondero, F. &Fabbri, R. A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Mar. Environ. Res. 44, 69-84 (1997).
47. Deneke, S. M. &Fanburg, B. L. Regulation of cellular glutathione. Am. J. Physiol-Lung. C. 257, L163-L173 (1989).
48. Oktyabrsky, O. N. &Smirnova, G. V. Redox regulation of cellular functions. Biochemistry (Mosc). 72, 132-145 (2007).
49. Hermes-Lima, M. Oxygen in biology and biochemistry: role of free radicals. In Functional Metabolism: Regulation and Adaptation (ed. Storey, K. B.) 319-368 (John Wiley &Sons, New Jersey, 2004).
50. Sies, H. Glutathione and its role in cellular functions. Free Radic. Biol. Med. 27, 916-921 (1999).
51. Felsenstein, J. Phylogenies and the comparative method. Am. Nat. 125, 1-15 (1985).
52. Grafen, A. The phylogenetic regression. Philos. T. Roy. Soc. B. 326, 119-157 (1989).
53. Blomberg, S. P. &Garland, T. Jr. Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J. Evol. Biol. 15, 899-910 (2002).
54. Garland, T., Bennett, A. F. &Rezende, E. L. Phylogenetic approaches in comparative physiology. J. Exp. Biol. 208, 3015-3035 (2005).
55. Harvey, P. H. &Pagel, M. D. The comparative method in evolutionary biology (Oxford University Press, Oxford, U.K., 1991).
56. Rezende, E. L. &Diniz-Filho, J. A. F. Phylogenetic analyses: comparing species to infer adaptations and physiological mechanisms. Compr Physiol. 2, 639-674 (2012).
57. Faria, S. C., Provete, D. B., Thurman, C. L. &McNamara, J. C. Phylogenetic patterns and the adaptive evolution of osmoregulation in fiddler crabs (Brachyura, Uca). PloS one. 12, e0171870 (2017).
58. Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics. 26, 1463-1464 (2010).
59. Diniz-Filho, J. A. F. Métodos filogenéticos comparativos. (Holos, Ribeirão Preto, Brazil., 2000).
60. Gittleman, J. L. &Kot, M. Adaptation: statistics and a null model for estimating phylogenetic effects. Syst Biol. 39, 227-241 (1990).
61. Rangel, T. F. et al. Phylogenetic uncertainty revisited: Implications for ecological analyses. Evolution. 69, 1301-1312 (2015).
62. Revell, L. J. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223 (2012).
63. Jombart, T., Balloux, F. &Dray, S. Adephylo: new tools for investigating the phylogenetic signal in biological traits. Bioinformatics. 26, 1907-1909 (2010).
64. Garland, T. Jr &Ives, A. R. Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am. Nat. 155, 346-364 (2000).
65. Pinheiro, J. D., Bates, S., DebRoy, D., Sarkar &R Core Team. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1 ± 122, http://CRAN.R-project.org/package=nlme (2015).
66. Paradis, E., Claude, J. &Strimmer, K. Ape: analyses of phylogenetics and evolution in R language. Bioinformatics. 20, (289-290 (2004).
67. R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Austria (2009).
68. CONAMA. Conselho Nacional do Meio Ambiente. Resolução N 344 de 25 de março de, http://www.mma.gov.br/port/conama/ legiabre.cfm?codlegi=445 (2004).
69. USEPA. A Guidance Manual to Support the Assessment of Contaminated Sediments in Freshwater Ecosystems. Volume III Interpretation of the results of sediment quality investigations. EPA-905-B02-001-C. US Environmental Protection Agency, Washington, DC (2002).
70. Noro, C. K. &Buckup, L. Biologia reprodutiva e ecologia de Aegla leptodactyla Buckup &Rossi (Crustacea, Anomura, Aeglidae). Revta. Bras. Zool. 19, 1063-1074 (2002).
71. Anger, K., Spivak, E., Bas, C., Ismael, D. &Luppi, T. Hatching rhythms and dispersion of decapods crustacean larvae in a brackish coastal lagoon in Argentina. Helgolander. meeresun. 48, 445-466 (1994).
72. Miserendino, M. L. Macroinvertebrate assemblages in Andean Patagonian Rivers and streams: environmental relationships. Hydrobiologia. 444, 147-158 (2001).
73. Gonçalves, R. S., Castiglioni, D. S. &Bond-Buckup, G. Ecologia populacional de Aegla franciscana (Crustacea, Decapoda, Anomura) em São Francisco de Paula, RS, Brasil. Iheringia, Sér. Zool. 96, 109-114 (2006).
74. Dallinger, R. &Rainbow, P. S. Ecotoxicology of metals in invertebrates (CRC Press., 1993).
75. Poteat, M. D., Garland, T. Jr, Fisher, N. S., Wang, W. X. &Buchwalter, D. B. Evolutionary patterns in trace metal (Cd and Zn) efflux capacity in aquatic organisms. Environ. Sci. Technol. 47, 7989-7995 (2013).
76. Rainbow, P. S. Phylogeny of trace metal accumulation in crustaceans. In Metal Metabolism in Aquatic Environments (ed. Langston, W. J. &Bebianno, M.) 285-319 (Chapman and Hall, London., 1998).
77. Lushchak, V. I. Enviromentally induced oxidative stress in aquatic animals. Aquat. Toxicol. 101, 13-30 (2011).
78. Gamble, S. C., Goldfarb, P. S., Porte, C. &Livingstone, D. R. Glutathione peroxidase and other antioxidant enzyme function in marine invertebrates (Mytilus edulis, Pecten maximus, Carcinus maenas and Asterias rubens). Mar. Environ. Res. 39, 191-195 (1995).
79. Abele, D. &Puntarulo, S. Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp. Biochem. Physiol. A. 138, 405-415 (2004).
80. Monserrat, J. M. et al. Pollution biomarkers in estuarine animals: Critical review and new perspectives. Comp. Biochem. Physiol. C. 46, 221-234 (2207).
81. Teodósio, E. A. O. &Masunari, S. Estrutura populacional de Aegla schmitti (Crustacea: Anomura: Aeglidae) nos reservatórios dos Mananciais da Serra, Piraquara, Paraná, Brasil. Zoologia (Curitiba, Impr.). 26, 19-24 (2009).
82. Junior, H. B. Crustáceos límnicos e aspectos da biologia de Aegla jarai Bond-Buckup &Buckup e Aegla sp. (Decapoda, Aeglidae) no Parque Natural Municipal das Nascentes do Ribeirão Garcia, Blumenau, SC. Ph.D. Thesis (Universidade Federal do Rio Grande do Sul, Porto Alegre, BR, 2003).
83. Rocha, S. S. Biologia reprodutiva, estrutura e dinâmica populacional e avaliação do grau de risco de extinção de Aegla strinatii Türkay, 1972 (Crustacea, Decapoda, Aeglidae). Ph.D. Thesis (Universidade de São Paulo, São Paulo, BR). https://doi. org/10.11606/T.41.2007.tde-17102007-095635 (2007).