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Biological Invasions

, Volume 17, Issue 12, pp 3503–3515 | Cite as

One step ahead of the enemy: investigating aggressive interactions between invasive and native crayfish before the contact in nature

  • Marcelo M. Dalosto
  • Alexandre V. Palaoro
  • Catherine Souty-Grosset
  • Sérgio Luiz de Siqueira Bueno
  • Tainã Gonçalves Loureiro
  • Maurício Pereira Almerão
  • Paula Beatriz de Araujo
  • Sandro Santos
Original Paper

Abstract

Biological invasions are a major cause of biodiversity loss, and early action in these cases is more cost-effective than dealing with widespread invasions. Thus, understanding possible consequences of invasions is essential for control and management actions. Given the early stage of invasion of South America by Procambarus clarkii, a potentially harmful crayfish, we investigated aggressive interactions between this invasive crayfish and the native Parastacus brasiliensis to understand potential impacts of the invader on native species before they encounter each other in nature. We paired size-matched crayfish for two experiments: one with Pr. clarkii males and females against Pa. brasiliensis; and another with Pr. clarkii intraspecific interactions. We starved the crayfish then allowed to interact in the presence of food. In interspecific fights we compared the number of attacks, time with the resource, frequency of won interactions of each species and the first species to reach the resource. Regarding the interspecific fights, Pr. clarkii attacked more often, spent more time with the resource, won more interactions and reached the resource first more often than Pa. brasiliensis. Interspecific fights escalated faster than intraspecific fights. The invasive crayfish’s ability to win might be enhanced due to ownership effects, and its impact is likely to be severe because of its life-history traits. We conclude that Pr. clarkii is definitely a threat for native crayfish, requiring that immediate actions be taken, such as dam construction and manual removal of Pr. clarkii.

Keywords

Aggressive behavior Interspecific interactions Invasion prevention Invasive species Parastacus brasiliensis Procambarus clarkii 

Notes

Acknowledgments

We thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the scholarship for A.V.P. and T.G.L., CAPES/FAPERGS (Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul) for the scholarship to M.M.D. and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for the productivity grant to S.S (Process No: 311142/2014-1) and P.B.A (Process No: 302274/2011-1). This work was also supported by CAPES/COFECUB (international consortium Brazil - France) (Project: Freshwater limnetic ecosystems and conservation of freshwater crayfish of the genus Parastacus in southern Brazil - 8209/2012), We thank Mr. Alderi Baggio, Mrs. Lúcia Baggio, and Mr. Charles Zarantonello for allowing us to collect Pa. brasiliensis on their properties, and the staff from the Alfredo Volpi Park for allowing us to collect Pr. clarkii. We thank Nilton Carlos Cáceres, Thomas Heinrich Breithaupt, Gabriel Costa, Ana Beatriz Barros de Morais and two anonymous reviewers for their valuable comments that improved the manuscript. Lastly, we thank our colleagues from the Núcleo de Estudos em Biodiversidade Aquática for their help in collecting, transporting and maintaining the crayfish, and also during the execution of the experiments.

Compliance with ethical standards

Conflicts of interest

None.

Supplementary material

10530_2015_974_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 16 kb)

References

  1. Alexander ME, Dick JTA, Weyl OLF, Robinson TB, Richardson DM (2014) Existing and emerging high impact invasive species are characterized by higher functional responses than natives. Biol Lett 10:20130946. doi: 10.1098/rsbl.2013.0946 PubMedCentralCrossRefPubMedGoogle Scholar
  2. Almeida AO, Buckup L (2000) Occurence of protandric hermaphroditism in a population of the neotropical crayfish Parastacus brasiliensis (Parastacidae). J Crust Biol 20(2):224–230. doi: 10.1163/20021975-99990034 CrossRefGoogle Scholar
  3. Almerão MP, Rudolph EH, Souty-Grosset C, Crandall K, Buckup L, Amouret J, Verdi A, Santos S, Araújo PB (2014) The native South American crayfishes (Crustacea, Parastacidae): state of knowledge and conservation status. Aquat Conserv 25(2):288–301. doi: 10.1002/aqc.2488 CrossRefGoogle Scholar
  4. Balshine S, Verma A, Chant V, Thaysmeyer T (2005) Competitive interactions between round gobies and logperch. J Great Lakes Res 31:67–77. doi: 10.1016/S0380-1330(05)70238-0 CrossRefGoogle Scholar
  5. Barbaresi S, Santini G, Tricarico E, Gherardi F (2004) Ranging behaviour of the invasive crayfish, Procambarus clarkii (Girard). J Nat Hist 38:2821–2832. doi: 10.1080/00222930410001663308 CrossRefGoogle Scholar
  6. Bergman D, Moore PA (2003) Field observations of intraspecific agonistic behavior of two crayfish species, Orconectes rusticus and Orconectes virilis, in different habitats. Biol Bull 205:26–35CrossRefPubMedGoogle Scholar
  7. Breinholt J, Pérez-Losada M, Crandall KA (2009) The timing of the diversification of freshwater crayfishes. In: Crandall KA, Felder DR (eds) Decapod Crustacean Phylogenetics. CRC Press, Boca Raton, pp 434–456Google Scholar
  8. Bubb DH, Thom TJ, Lucas MC (2006) Movement, dispersal and refuge use of co-occurring introduced and native crayfish. Freshwater Biol 51:1359–1368. doi: 10.1111/j.1365-2427.2006.01578.x CrossRefGoogle Scholar
  9. Buckup L (2003) Família Parastacidae. In: Melo GAS (ed) Manual de identificação dos Crustacea Decapoda de água doce do Brasil. Editora Loyola, São Paulo, pp 117–141Google Scholar
  10. Chamorro-Florescano IA, Favila ME, Macías-Ordoñez R (2011) Ownership, size and reproductive status affect the outcome of food ball contests in a dung roller beetle: when do enemies share? Evol Ecol 25:277–289. doi: 10.1007/s10682-010-9428-8 CrossRefGoogle Scholar
  11. Chang AL, Grossman JD, Spezio TS, Weiskel HW, Blum JC, Burt JW, Muir AA, Piovia-Scott J, Veblen KE, Grosholz ED (2009) Tackling aquatic invasions: risks and opportunities for the aquarium fish industry. Biol Inv 11:773–785. doi: 10.1007/s10530-008-9292-4 CrossRefGoogle Scholar
  12. Chucholl C (2013) Invaders for sale: trade and determinants of introduction of ornamental freshwater crayfish. Biol Inv 15:125–141. doi: 10.1007/s10530-012-0273-2 CrossRefGoogle Scholar
  13. Collins PA, Giri F, Williner V (2011) Biogeography of the freshwater decapods in the La Plata Basin. South America. J Crust Biol 31(1):179–191. doi: 10.1651/10-3306.1 CrossRefGoogle Scholar
  14. Correia AM, Ferreira O (1995) Burrowing behavior of the introduced red swamp crayfish Procambarus clarkii (Decapoda: Cambaridae) in Portugal. J Crust Biol 15(2):248–257CrossRefGoogle Scholar
  15. Dalosto MM, Palaoro AV, Santos S (2012) Mother-offspring relationship in the Neotropical burrowing crayfish, Parastacus pilimanus (von Martens, 1869) (Decapoda: Parastacidae). Crustaceana 85(11):1305–1315. doi: 10.1163/156854012X651367 CrossRefGoogle Scholar
  16. Dalosto MM, Palaoro AV, Costa JR, Santos S (2013) Aggression and life underground: the case of burrowing crayfish. Behaviour 150:3–22. doi: 10.1163/1568539X-00003034 CrossRefGoogle Scholar
  17. Dana ED, García-de-Lomas J, González R, Ortega F (2011) Effectiveness of dam construction to contain the invasive crayfish Procambarus clarkii in a Mediterranean mountain stream. Ecol Eng 37:1607–1613. doi: 10.1016/j.ecoleng.2011.06.014 CrossRefGoogle Scholar
  18. Diéguez-Uribeondo J, Söderhäll K (1993) Procambarus clarkii Girard as a vector for the crayfish plague fungus, Aphanomyces astaci Schikora. Aquacult Fish Manage 24:761–765. doi: 10.1111/j.1365-2109.1993.tb00655.x Google Scholar
  19. Duggan IC, Rixon CAM, MacIsaac HJ (2006) Popularity and propagule pressure: determinants of introduction and establishment of aquarium fish. Biol Inv 8:377–382. doi: 10.1007/s10530-004-2310-2 CrossRefGoogle Scholar
  20. Elvey W, Richardson AMM, Barmuta L (1996) Interactions between the introduced yabby, Cherax destructor, and the endemic crayfish, Astacopsis franklinii, in Tasmanian Streams. Freshwater Crayfish 11:349–363Google Scholar
  21. Fero K, Moore PA (2008) Social spacing of crayfish in natural habitats: what role does dominance play? Behav Ecol Sociobiol 62:1119–1125. doi: 10.1007/s00265-007-0540-x CrossRefGoogle Scholar
  22. Ficetola GF, Siesa ME, Manenti R, Bottoni L, De Bernardi F, Padoa-Schioppa E (2011) Early assessment of the impact of alien species: differential consequences of an invasive crayfish on adult and larval amphibians. Div Distr 17:1141–1151. doi: 10.1111/j.1472-4642.2011.00797.x CrossRefGoogle Scholar
  23. Fontoura NF, Buckup L (1989a) O crescimento de Parastacus brasiliensis (von Martens, 1869) (Crustacea, Decapoda, Parastacidae). Rev Bras Biol 49(4):897–909Google Scholar
  24. Fontoura NF, Buckup L (1989b) Dinâmica populacional e reprodução em Parastacus brasiliensis (von Martens, 1869) (Crustacea, Decapoda, Parastacidae). Rev Bras Biol 49(4):911–921Google Scholar
  25. Genovesi P (2011) Are we turning the tide? Eradications in times of crisis: how the global community is responding to biological invasions. In: Veitch CR et al (eds) Island Invasives: Eradication and Management. IUCN, Gland, Switzerland, pp 5–8Google Scholar
  26. Gherardi F (2002) Behaviour. In: Holdich DM (ed) Biology of freshwater crayfish, 1st edn. Blackwell Science, Oxford, pp 258–290Google Scholar
  27. Gherardi F (2006) Crayfish invading Europe: the case study of Procambarus clarkii. Mar Fresh Beh Physiol 39(3):175–191. doi: 10.1080/10236240600869702 CrossRefGoogle Scholar
  28. Gherardi F, Cioni A (2004) Agonism and interference competition in freshwater decapods. Behaviour 141(10):1297–1324CrossRefGoogle Scholar
  29. Gherardi F, Daniels WH (2004) Agonism and shelter competition between invasive and indigenous crayfish species. Can J Zool 82:1923–1932. doi: 10.1139/z04-185 CrossRefGoogle Scholar
  30. Gherardi F, Aquiloni L, Diéguez-Uribeondo J, Tricarico E (2011) Managing invasive crayfish, is there a hope? Aq Sciences 73:185–200. doi: 10.1007/s00027-011-0181-z CrossRefGoogle Scholar
  31. Gherardi F, Coignet A, Souty-Grosset C, Spigoli D, Aquiloni L (2013) Global warming and the agonistic behaviour of invasive crayfishes in Europe. Freshw Biol 58:1958–1967. doi: 10.1111/fwb.12183 CrossRefGoogle Scholar
  32. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological Statistics Software Package for education and data analysis. Palaeontologia Electronica 4:1–9Google Scholar
  33. Hazlett BA, Lawler S, Edney G (2007) Agonistic behavior of the crayfish Euastacus armatus and Cherax destructor. Mar Freshw Beh Physiol 40(4):257–266. doi: 10.1080/10236240701562412 CrossRefGoogle Scholar
  34. Herberholz J, McCurdy C, Edwards DH (2007) Direct benefits of social dominance in juvenile crayfish. Biol Bull 213:21–27CrossRefPubMedGoogle Scholar
  35. Holway DA, Suarez AV (1999) Animal behavior: an essential component of invasion biology. Trends Ecol Evol 14(8):328–330. doi: 10.1016/S0169-5347(99)01636-5 CrossRefPubMedGoogle Scholar
  36. Huner JV (2002) Procambarus. In: Holdich DM (ed) Biology of freshwater crayfish, 1st edn. Blackwell Science, Oxford, pp 541–584Google Scholar
  37. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA). Resolution no 5, January 28th, 2008Google Scholar
  38. Jimenes SA, Faulkes Z (2011) Can the parthenogenetic marbled crayfish Marmorkrebs compete with other crayfish species in fights? J Ethol 29:115–120. doi: 10.1007/s10164-010-0232-2 CrossRefGoogle Scholar
  39. Kerby JL, Riley SPD, Kats LB, Wilson P (2005) Barriers and flow as limiting factors in the spread of an invasive crayfish (Procambarus clarkii) in southern California streams. Biol Cons 126:402–409. doi: 10.1016/j.biocon.2005.06.020 CrossRefGoogle Scholar
  40. López P, Martín J (2011) Male Iberian rock lizards may reduce the costs of fighting by scent matching of the resource holders. Behav Ecol Sociobiol 65:1891–1898. doi: 10.1007/s00265-011-1198-y CrossRefGoogle Scholar
  41. Loureiro TG, Anastácio PM, Bueno SLS, Araújo PB, Souty-Grosset C, Almerão MP (2015a) Distribution, introduction pathway and invasion risk analysis of the North American crayfish Procambarus clarkii (Crustacea, Decapoda, Cambaridae) in Southeast Brazil. J Crust Biol 35(1):88–96. doi: 10.1163/1937240X-00002307 CrossRefGoogle Scholar
  42. Loureiro TG, Anastácio PMSG, Araujo PB, Souty-Grosset C, Almerão MP (2015b) Red swamp crayfish: biology, ecology and invasion—an overview. Nauplius 23(1):1–19. doi: 10.1590/S0104-64972014002214 CrossRefGoogle Scholar
  43. Lynch BR, Rochette R (2009) Spatial overlap and interaction between sub-adult American lobsters, Homarus americanus, and the invasive European green crab Carcinus maenas. J Exp Mar Ecol Biol 369:127–135. doi: 10.1016/j.jembe.2008.11.002 CrossRefGoogle Scholar
  44. MacNeil C, Dick JTA, Platvoet D, Briffa M (2011) Direct and indirect effects of species displacements: an invading freshwater amphipod can disrupt leaf-litter processing and shredder efficiency. J N Am Benthol Soc 30(1):38–48. doi: 10.1899/10-056.1 CrossRefGoogle Scholar
  45. Macom TE, Porter SD (1996) Comparison of polygyne and monogyne imported red fire ant (Hymenoptera: Formicidae) population densities. Annals of the Entomol Soc Amer 89:535–543CrossRefGoogle Scholar
  46. Magalhães C, Bueno SLS, Bond-Buckup G, Valenti WC, Silva HLM, Kiyohara F, Mossolin EC, Rocha SS (2005) Exotic species of freshwater decapod crustaceans in the state of São Paulo, Brazil: records and possible causes of their introduction. Biodivers Cons 14:1929–1945. doi: 10.1007/s10531-004-2123-8 CrossRefGoogle Scholar
  47. Maynard-Smith J, Parker PA (1976) The logic of asymmetric contests. Anim Behav 4:159–175CrossRefGoogle Scholar
  48. Meinesz A (2001) Killer Algae, University of Chicago Press, Chicago, p 360Google Scholar
  49. Mohamad R, Monge J, Goubault M (2012) Do resource value and ownership status affect intensity and resolution of contests in a parasitoid wasp? Entomol Exp Appl 147:99–109. doi: 10.1111/eea.12049 CrossRefGoogle Scholar
  50. Moore PA (2007) Agonistic behavior in freshwater crayfish: the influence of intrinsic and extrinsic factors on aggressive encounters and dominance. In: Duffy JE, Thiel M (eds) Evolutionary Ecology of Social and Sexual Systems - Crustaceans as Model Organisms. Oxford University Press, Oxford, pp 90–114CrossRefGoogle Scholar
  51. Moorhouse TP, Macdonald DW (2011) The effect of removal by trapping on body condition in populations of signal crayfish. Biol Cons 144:1826–1831. doi: 10.1016/j.biocon.2011.03.017 CrossRefGoogle Scholar
  52. Mrugała A, Kozubíková-Balcarová E, Chucholl C, Cabanillas Resino S, Viljamaa-Dirks S, Vukić J, Petrusek A (2014) Trade of ornamental crayfish in Europe as a possible introduction pathway for important crustacean diseases: crayfish plague and white spot syndrome. Biol Inv 12:1313–1326. doi: 10.1007/s10530-014-0795-x Google Scholar
  53. Oluoch AO (1990) Breeding biology of the Louisiana red swamp crayfish Procambarus clarkii Girard in Lake Naivasha, Kenya. Hydrobiologia 208:85–92. doi: 10.1007/BF00008447 CrossRefGoogle Scholar
  54. Palaoro AV, Dalosto MM, Costa GC, Santos S (2013a) Niche conservatism and the potential for the crayfish Procambarus clarkii to invade South America. Freshwater Biol 58:1379–1391. doi: 10.1111/fwb.12134 CrossRefGoogle Scholar
  55. Palaoro AV, Dalosto MM, Coutinho C, Santos S (2013b) Assessing the importance of burrows through behavioral observations of Parastacus brasiliensis, a Neotropical burrowing crayfish (Crustacea), in laboratory conditions. Zool Stud 52:4. doi: 10.1186/1810-522X-52-4 CrossRefGoogle Scholar
  56. Panzacchi M, Bertolino S, Cocchi R, Genovesi P (2007) Population control of coypu Myocastor coypus in Italy compared to eradication in UK: a cost-benefit analysis. Wildl Biol 13(2):159–171. doi: 10.2981/0909-6396(2007)13[159:PCOCMC]2.0.CO;2 CrossRefGoogle Scholar
  57. Penn GH (1943) A study of the life history of the Louisiana red-crawfish. Cambarus clarkii Girard. Ecology 24(1):1–18CrossRefGoogle Scholar
  58. Pintor LM, Sih A, Bauer M (2008) Differences in aggression, activity and boldness between native introduced populations of an invasive crayfish. Oikos 117:1629–1636. doi: 10.1111/j.1600-0706.2008.16578.x CrossRefGoogle Scholar
  59. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  60. Rejmánek M, Pitcairn MJ (2002) When is eradication of exotic pest plants a realistic goal? In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species, IUCN SSC invasive species specialist group, pp 249–253Google Scholar
  61. Reynolds J, Souty-Grosset C (2012) Management of freshwater biodiversity: crayfish as bioindicators. Cambridge University Press, Cambridge, p 384Google Scholar
  62. Rudolph EH, Almeida AO (2000) On the sexuality of South American Parastacidae (Crustacea, Decapoda). Invertebr Reprod Dev 37(3):249–257. doi: 10.1080/07924259.2000.9652425 CrossRefGoogle Scholar
  63. Scalici M, Chiesa S, Scuderi S, Celauro D, Gilbertini D (2010) Population structure and dynamics of Procambarus clarkii (Girard, 1852) in a Mediterranean brackish wetland (Central Italy). Biol Inv 12:1415–1425. doi: 10.1007/s10530-009-9557-6 CrossRefGoogle Scholar
  64. Schrimpf A, Maiwald T, Vrålstad T, Schulz HK, Śmietana P, Schulz R (2013) Absence of the crayfish plague pathogen (Aphanomyces astaci) facilitates coexistence of European and American crayfish in central Europe. Freshwater Biol 58:1116–1125. doi: 10.1111/fwb.12112 CrossRefGoogle Scholar
  65. Shine R (2014) A review of ecological interactions between native frogs and invasive cane toads in Australia. Austral Ecol 39:1–16. doi: 10.1111/aec.12066 CrossRefGoogle Scholar
  66. Silva HLM, Bueno SLS (2005) Population size estimation of the exotic crayfish Procambarus clarkii (Girard) (Crustacea, Decapoda, Cambaridae) in the Alfredo Volpi City Park, São Paulo. Brazil. Rev Bras Zool 22(1):93–98. doi: 10.1590/S0101-81752005000100012 CrossRefGoogle Scholar
  67. Simberloff D (2013) Biological invasions: what’s worth fighting and what can be won? Ecol Eng 65:112–121. doi: 10.1016/j.ecoleng.2013.08.004 CrossRefGoogle Scholar
  68. Simberloff D, Martin J, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vilà M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28(1):58–66. doi: 10.1016/j.tree.2012.07.013 CrossRefPubMedGoogle Scholar
  69. Sousa R, Freitas FEP, Mota M, Nogueira AJA, Antunes C (2013) Invasive dynamics of the crayfish Procambarus clarkii (Girard, 1852) in the international section of the River Minho (NW of the Iberian Peninsula). Aquatic Conserv Mar Freshw Ecosyst 23:656–666. doi: 10.1002/aqc.2323 Google Scholar
  70. Souty-Grosset C, Holdich DM, Noël PY, Reynolds JD, Haffner P (2006) Atlas of Crayfish in Europe. Museum national d’Histoire naturelle, Paris, 187 pp (Patrimoines naturels, 64)Google Scholar
  71. Souty-Grosset C, Reynolds J, Gherardi F, Aquiloni L, Coignet A, Pinet F, Del Mar Mancha Cisneros M (2014) Burrowing activity of the invasive red swamp crayfish, Procambarus clarkii, in fishponds of La Brenne (France). Ecol Ethol Evol 26(2–3):263–276. doi: 10.1080/03949370.2014.892538 CrossRefGoogle Scholar
  72. Unestam T (1975) Defence reactions in and susceptibility of Australian and New Guinean freshwater crayfish to European-crayfish-plague fungus. Australian J Exp Biol Med 53:349–359CrossRefGoogle Scholar
  73. Vander Zanden MJ, Hansen GJA, Higgins SN, Kornis MS (2010) A pound of prevention, plus a pound of cure: early detection and eradication of invasive species in the Laurentian Great Lakes. J Great Lakes Res 36:199–205. doi: 10.1016/j.jglr.2009.11.002 CrossRefGoogle Scholar
  74. Vandermeer RK, Obin MS, Morel L (1991) Nestmate recognition in fire ants: monogyne and polygyne populations. In: Jaffe K, Cedeno A (eds) Vandermeer RK. A World Perspective, Westview Press, Applied Myrmecology, pp 322–328Google Scholar
  75. Vorburger C, Ribi G (1999) Aggression and competition for shelter between a native and an introduced crayfish in Europe. Freshw Biol 42(1):111–119. doi: 10.1046/j.1365-2427.1999.00465.x CrossRefGoogle Scholar
  76. Wang W, Gu W, Ding Z, Ren Y, Chen J, Hou Y (2005) A novel Spiroplasma pathogen causing systemic infection in the crayfish Procambarus clarkii (Crustacea: Decapod), in China. FEMS Micriobiol Lett 249:131–137. doi: 10.1016/j.femsle.2005.06.005 CrossRefGoogle Scholar
  77. Westermann FL, Suckling DM, Lester PJ (2014) Disruption of foraging by a dominant invasive species to decrease its competitive ability. PLoS ONE 9(3):e90173. doi: 10.1371/journal.pone.0090173 PubMedCentralCrossRefPubMedGoogle Scholar
  78. Williams PJ, Floyd TA, Rossong MA (2006) Agonistic interactions between invasive green crabs, Carcinus maenas (Linnaeus), and sub-adult American lobsters, Homarus americanus (Milne Edwards). J Exp Mar Ecol Biol 329:66–74. doi: 10.1016/j.jembe.2005.08.008 CrossRefGoogle Scholar
  79. Woodfield R, Mooney R (2002) Field Response to infestations of Caulerpa taxifolia in Southern California. California and the World Ocean 2002 ProceedingsGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Marcelo M. Dalosto
    • 1
  • Alexandre V. Palaoro
    • 1
  • Catherine Souty-Grosset
    • 2
  • Sérgio Luiz de Siqueira Bueno
    • 3
  • Tainã Gonçalves Loureiro
    • 4
  • Maurício Pereira Almerão
    • 4
  • Paula Beatriz de Araujo
    • 4
  • Sandro Santos
    • 1
  1. 1.Núcleo de Estudos em Biodiversidade Aquática, Programa de Pós-Graduação em Biodiversidade AnimalUniversidade Federal de Santa MariaSanta MariaBrazil
  2. 2.Laboratoire Ecologie et Biologie des Interactions, Equipe Ecologie Evolution Symbiose, UMR CNRS 7267Université de PoitiersCedex 9, PoitiersFrance
  3. 3.Departamento de Zoologia, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil
  4. 4.Laboratório de Carcinologia, PPG em Biologia Animal, Departamento de Zoologia, Instituto de BiociênciasUniversidade Federal do Rio Grande do SulPorto AlegreBrazil

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