, Volume 773, Issue 1, pp 241–252 | Cite as

Does retention or exportation occur in the larvae of the mud shrimp Upogebia vasquezi (Decapoda, Gebiidea)? Implications for the reproductive strategy of the species on the Amazon coast

  • Danielly Brito de OliveiraEmail author
  • Jussara Moretto Martinelli-Lemos
  • Adelson Silva de Souza
  • Jossianne Rodrigues da Costa
  • Fernando Araújo Abrunhosa
Primary Research Paper


We investigated the effects of eight different levels of salinity (0–35) on the larval development of Upogebia vasquezi, while the abundance of the larvae within the Marapanim estuary on the Amazon Coast was verified through the monthly collection of specimens between August 2006 and July 2007. This species reproduces year-round on the Amazon Coast, which is subjected to strong seasonal fluctuations in salinity due to the local precipitation regime. Upogebia vasquezi larvae developed optimally in salinity close to that of seawater (20–35), while low salinities (0, 5, and 10) did not support the survival of the larvae. Only zoeal stages I, II, and III were captured in the field and were more abundant at the higher end of the salinity gradient, in the areas closest to the adjacent coastal waters. Data from both the laboratory and the field data emphasized the low survival potential of the larvae in low salinities, and increased survival and improved development in more saline water. These results support the hypothesis that U. vasquezi undergo development on the shelf, and also suggest the possibility of an ontogenetic migration toward to adjacent coastal areas during early larval stages, as observed in other decapod species around the world.


Estuary Life cycle Macrotide Megalopa Mud shrimp Zoea 



We thank our colleagues Danielle Arruda, Darlan Simith, Luiz Paulo Melo, Orlando Galli, Rubem Pessoa, and Wellington Trindade for the collection of seawater samples in the field, and Rory Oliveira for helping to collect ovigerous females. We also appreciate the valuable suggestions of Dr. Cristiana Maciel, Dr. Eduardo Martinelli, Dr. Marcelo Petracco, Dr. Ralf Schwamborn, and Dr. Sandra Shumway, which greatly improved the paper. This study is part of the Ph.D thesis of the first author (DBO) and was funded by the Brazilian National Research Council (CNPq) through the CT-AMAZÔNIA project (Grant 553106/2005-8 to JMML), the Brazilian Higher Education Training Program (CAPES), and the Brazilian Carcinology Society (Grant SBC 01/2012). We also thank PROPESP/FADESP (PAPQ Program) for sponsoring the translation of the original manuscript by Stephen Ferrari. All experiments conducted in this study complied with current Brazilian federal legislation (environmental authorization MMA/ICMBIO/SISBIO Number 29434-5) and Pará state laws.


  1. Anger, K., 1991. Effects of temperature and salinity on the larval development of the Chinese mitten crab Eriocheir sinensis (Decapoda: Grapsidae). Marine Ecology Progress Series 72: 103–110.CrossRefGoogle Scholar
  2. Anger, K., 1996. Salinity tolerance of the larvae and first juveniles of a semiterrestrial grapsid crab, Armases miersii (Rathbun). Journal of Experimental Marine Biology and Ecology 202: 205–223.CrossRefGoogle Scholar
  3. Anger, K., 2001. The biology of decapod crustacean larvae, Vol. 14., Crustacean Issues A. A. Balkema Publishers, Lisse.Google Scholar
  4. Anger, K., 2003. Salinity as a key parameter in the larval biology of decapods crustaceans. Invertebrate Reproduction and Development 43(1): 29–45.CrossRefGoogle Scholar
  5. Anger, K., E. Spivak, C. Bas, D. Ismael & T. Luppi, 1994. Hatching rhythms and dispersion of decapod crustacean larvae in a brackish coastal lagoon in Argentina. Helgolander Meeresuntersuchungen 48: 445–466.CrossRefGoogle Scholar
  6. Anger, K., E. Spivak, T. Luppi, C. Bas & D. Ismael, 2008. Larval salinity tolerance of the South American salt-marsh crab, Neohelice (Chasmagnathus) granulata: physiological constraints to estuarine retention, export and reimmigration. Helgoland Marine Research 62: 93–102.CrossRefGoogle Scholar
  7. Ayres, M., M. Ayres Jr, D. L. Ayres & A. S. Santos, 2007. BioEstat 5.0 Aplicações estatísticas nas áreas das ciências biológicas e médicas. Instituto do desenvolvimento sustentável Mamirauá – IDSM/MCT/CNPq, Pará.Google Scholar
  8. Berrêdo, J. F., M. L. Costa & M. P. S. Progene, 2008. Efeitos das variações sazonais do clima tropical úmido sobre as águas e sedimentos de manguezais do estuário do rio Marapanim, costa nordeste do Estado do Pará. Acta Amazonica 38(3): 473–482.CrossRefGoogle Scholar
  9. Boschi, E. E., 1981. Larvas de Crustacea Decapoda. In Boltovskoy, D. (ed.), Atlas del zooplancton del Atlántico sudoccidental y métodos de trabajo con el zooplancton marino. Inedep, Mar del Plata.Google Scholar
  10. Charmantier, G., 1998. Ontogeny of osmoregulation in crustaceans: a review. Invertebrate Reproduction and Development 33: 177–190.CrossRefGoogle Scholar
  11. Charmantier, G., L. Giménez, M. Charmantier-Daures & K. Anger, 2002. Ontogeny of osmoregulation, physiological plasticity and larval export strategy in the grapsid crab Chasmagnathus granulata (Crustacea, Decapoda). Marine Ecology Progress Series 229: 185–194.CrossRefGoogle Scholar
  12. Christy, J. H. & S. G. Morgan, 1998. Estuarine immigration by crab postlarvae: mechanisms, reliability and adaptive significance. Marine Ecology Progress Series 174: 51–65.CrossRefGoogle Scholar
  13. Costlow, J. D., C. G. Bookhout & R. Monroe, 1960. The effect of salinity and temperature on larval development of Sesarma cinereum (Bosc) reared in the laboratory. Biological Bulletin 118(2): 183–202.CrossRefGoogle Scholar
  14. Diele, K. & D. J. B. Simith, 2006. Salinity tolerance of northern Brazilian mangrove crab larvae, Ucides cordatus (Ocypodidae): necessity for larval export? Estuarine, Coastal and Shelf Science 68: 600–608.CrossRefGoogle Scholar
  15. Dworschak, P. C., 1988. The biology of Upogebia pusilla (Petagna) (Decapoda, Thalassinidea) III. Growth and production. Marine Ecology 9(1): 51–77.CrossRefGoogle Scholar
  16. Dworschak, P. C., 2005. Global diversity in the Thalassinidea (Decapoda): an update (1998–2004). Nauplius 13(1): 57–63.Google Scholar
  17. Dworschak, P. C., D. L. Felder & C. C. Tudge, 2012. Infraorders Axiidea De Saint Laurent, 1979 and Gebiidea De Saint Laurent, 1979 (formerly known collectively as Thalassinidea). In Schran, F. R. & J. C. Vaupel Klein (eds), The Crustacea - Treatise on Zoology: anatomy, taxonomy, biology. Koninklijke Brill NV, Boston: 109–219.CrossRefGoogle Scholar
  18. Esser, L. J. & N. Cumberlidge, 2011. Evidence that salt water may not be a barrier to the dispersal of Asian freshwater crabs (Decapoda: Brachyura: Gecarcinucidae and Potamidae). Raffles Bulletin of Zoology 59(2): 259–268.Google Scholar
  19. Faleiro, F., J. Paula & L. Narciso, 2012. Hot and salty: the temperature and salinity preferences of a temperate estuarine shrimp larva, Upogebia pusilla (Decapoda: Thalassinidea). Hydrobiologia 691: 89–95.CrossRefGoogle Scholar
  20. Fowler, A. E., N. V. Gerner & M. A. Sewell, 2011. Temperature and salinity tolerances of Stage 1 zoeae predict possible range expansion of an introduced portunid crab, Charybdis japonica, in New Zealand. Biological Invasions 13: 691–699.CrossRefGoogle Scholar
  21. Johnson, G. E. & J. J. Gonor, 1982. The tidal exchange of Callianassa californiensis (Crustacea, Decapoda) larvae between the Ocean and the Salmon River estuary, Oregon. Estuarine, Coastal and Shelf Science 14: 501–516.CrossRefGoogle Scholar
  22. Melo Jr, M., R. Schwamborn, S. Neumann-Leitão & M. Paranaguá, 2012. Abundance and instantaneous transport of Petrolisthes armatus (Gibbes, 1850) planktonic larvae in the Catuama inlet, Northeast Brazil. Anais da Academia Brasileira de Ciências 84(1): 95–102.CrossRefGoogle Scholar
  23. Moraes, B. C., J. M. N. Costa, A. C. L. Costa & M. H. Costa, 2005. Variação espacial e temporal da precipitação no estado do Pará. Acta Amazonica 35(2): 207–214.CrossRefGoogle Scholar
  24. Nóbrega, P. S. V., B. Bentes & J. M. Martinelli-Lemos, 2013. Composition of shrimp populations (Crustacea: Decapoda) in non-vegetated areas of two river islands in a Brazilian Amazon estuary. Zoologia 30(6): 652–660.CrossRefGoogle Scholar
  25. O’Connor, N. J. & C. E. Epifanio, 1985. The effect of salinity on the dispersal and recruitment of fiddler Crab Larvae. Journal of Crustacean Biology 5(1): 137–145.CrossRefGoogle Scholar
  26. Oliveira, D. B., D. C. Silva & J. M. Martinelli-Lemos, 2012. Density of larval and adult forms of the burrowing crustaceans Lepidophthalmus siriboia (Callianassidae) and Upogebia vasquezi (Upogebiidae) in an Amazon estuary, northern Brazil. Journal of the Marine Biological Association of the United Kingdom 92(2): 295–303.CrossRefGoogle Scholar
  27. Oliveira, D. B., D. C. Silva & J. M. Martinelli-Lemos, 2013. Larval and adult density of the porcellanid crab Petrolisthes armatus (Anomura: Porcellanidae) in an Amazon estuary, northern Brazil. Zoologia 30(6): 592–600.CrossRefGoogle Scholar
  28. Oliveira, D. B., J. M. Martinelli-Lemos & F. A. Abrunhosa, 2014. The complete larval development of the mud shrimp Upogebia vasquezi (Gebiidea: Upogebiidae) reared in the laboratory. Zootaxa 3826(3): 517–543.CrossRefPubMedGoogle Scholar
  29. Paula, J., R. N. Mendes, S. Paci, P. McLaughlin, F. Gherardi & W. Emmerson, 2001. Combined effects of temperature and salinity on the larval development of the estuarine mud prawn Upogebia africana (Crustacea, Thalassinidea). Hydrobiologia 449: 141–148.CrossRefGoogle Scholar
  30. Pires, R. F. T., M. Pan, M. P. Santos, A. Peliz, D. Boutov & A. Santos, 2013. Modelling the variation in larval dispersal of estuarine and coastal ghost shrimp: Upogebia congeners in the Gulf of Cadiz. Marine Ecology Progress Series 492: 153–168.CrossRefGoogle Scholar
  31. Sakai, K. & M. Turkay, 2014. A review of the collections of the infraorders Thalassinidea Latreille, 1831 and Callianassidea Dana, 1852 (Decapoda, Pleocyemata) lodged in three German museums, with revised keys to the genera and species. Crustaceana 87(2): 129–211.CrossRefGoogle Scholar
  32. Santos, A., A. M. P. Santos, D. V. P. Conwa, C. Bartilotti, P. Lourenço & H. Queiroga, 2008. Diel vertical migration of decapod larvae in the Portuguese coastal upwelling ecosystem: implications for offshore transport. Marine Ecology Progress Series 359: 171–183.CrossRefGoogle Scholar
  33. Silva, D. C. & J. M. Martinelli-Lemos, 2012. Species composition and abundance of the benthic community of Axiidea and Gebiidea (Crustacea: Decapoda) in the Marapanim Bay, Amazon estuary, northern Brazil. Zoologia 29(2): 144–158.Google Scholar
  34. Simith, D. J. B. & K. Diele, 2008. O efeito da salinidade no desenvolvimento larval do caranguejo-uçá, Ucides cordatus (Linnaeus, 1763) (Decapoda: Ocypodidae) no Norte do Brasil. Acta Amazonica 38(2): 345–350.CrossRefGoogle Scholar
  35. Simith, D. J. B., A. S. Souza, C. R. Maciel, F. A. Abrunhosa & K. Diele, 2012. Influence of salinity on the larval development of the fiddler crab Uca vocator (Ocypodidae) as an indicator of ontogenetic migration towards offshore waters. Helgoland Marine Research 66: 77–85.CrossRefGoogle Scholar
  36. Simith, D. J. B., M. A. B. Pires, F. A. Abrunhosa, C. R. Maciel & K. Diele, 2014. Is larval dispersal a necessity for decapod crabs from the Amazon mangroves? Response of Uca rapax zoeae to different salinities and comparison with sympatric species. Journal of Experimental Marine Biology and Ecology 457: 22–30.CrossRefGoogle Scholar
  37. Souza Filho, P. W. M., 2005. Costa de manguezais de macromaré da Amazônia: cenários morfológicos, mapeamento e quantificação de áreas usando dados de sensores remotos. Revista Brasileira de Geofísica 23(4): 427–435.CrossRefGoogle Scholar
  38. Statsoft Inc., 2004. STATISTICA data analysis software system, version 7,
  39. Thessalou-Legaki, M., 1990. Advanced larval development of Callianassa tyrrhena (Decapoda: Thalassinidea) and the effect of environmental factors. Journal of Crustacean Biology 10(4): 659–666.CrossRefGoogle Scholar
  40. Thompson, L. C. & A. W. Pritchard, 1969. Osmoregulatory capacities of Callianassa and Upogebia (Crustacea: Thalassinidea). Biological Bulletin 136(1): 114–129.CrossRefGoogle Scholar
  41. Torres, G., L. Giménez & K. Anger, 2011. Growth, tolerance to low salinity, and osmoregulation in decapod crustacean larvae. Aquatic Biology 12: 249–260.CrossRefGoogle Scholar
  42. Vuichard, G. S., N. Farías & T. Luppi, 2013. Hatching and larval export of the intertidal crab Neohelice granulata in Mar Chiquita coastal lagoon, Argentina. Iheringia Série Zoologia 103(2): 124–133.CrossRefGoogle Scholar
  43. Wooldridge, T. H. & H. Loubser, 1996. Larval release rhythms and tidal exchange in the estuarine mudprawn, Upogebia africana. Hydrobiologia 337: 113–121.CrossRefGoogle Scholar
  44. Yannicelli, B., L. R. Castro, A. Valle-Levinson, L. Atkinson & D. Figueroa, 2006. Vertical distribution of decapod larvae in the entrance of an equatorward facing bay of central Chile: implications for transport. Journal of Plankton Research 28(1): 19–37.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Danielly Brito de Oliveira
    • 1
    • 2
    Email author
  • Jussara Moretto Martinelli-Lemos
    • 1
  • Adelson Silva de Souza
    • 2
  • Jossianne Rodrigues da Costa
    • 2
  • Fernando Araújo Abrunhosa
    • 2
  1. 1.Laboratory for Fishery Biology and Management of Aquatic Resources, Ecology of Amazonian Crustaceans Research Group (GPECA)Universidade Federal do ParáBelémBrazil
  2. 2.Carcinology LaboratoryUniversidade Federal do ParáBragançaBrazil

Personalised recommendations