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RESEARCH ARTICLE
Contents Vol 70(10)

Reproductive biology of Macrobrachium amazonicum (Heller, 1862) populations with distinct phenotypes in Neotropical reservoirs during the ‘El Niño’ event

Lucas R. P. Paschoal https://orcid.org/0000-0003-2461-4675 A E , Leo J. F. de Oliveira D , Guilherme C. Andrioli B and Fernando J. Zara A B C
+ Author Affiliations
- Author Affiliations

A Universidade Estadual Paulista (UNESP), 13506-900, Rio Claro, São Paulo, Brazil.

B Universidade Estadual Paulista (UNESP), Centro de Aquicultura (CAUNESP), 14884-900, Jaboticabal, São Paulo, Brazil.

C Invertebrate Morphology Laboratory (IML), Departamento de Biologia Aplicada, CAUNESP and IEAMar, Universidade Estadual Paulista (UNESP), 14884-900, Jaboticabal, São Paulo, Brazil.

D Deceased, 21 February 2019. Formerly at UNESP, CAUNESP, 14884-900, Jaboticabal, São Paulo, Brazil.

E Corresponding author. Email: lucasrezende20@gmail.com

Marine and Freshwater Research 70(10) 1465-1479 https://doi.org/10.1071/MF18228
Submitted: 23 June 2018  Accepted: 30 January 2019   Published: 16 April 2019

Abstract

Here, we investigated the reproductive biology (frequency and distribution patterns of ovigerous females, fecundity, reproductive output and egg size and volume) of Macrobrachium amazonicum in four populations living in Neotropical reservoirs, so as to verify whether this process was affected by the 2014–2016 ‘El Niño’ event. The following two phenotypes were identified: in two populations, small-size (SS) females (CL: 9.05 and 10.06 mm) carried few eggs (X: 141 and 219) with a larger volume (X: 0.188 and 0.212 mm3), whereas, in the other two populations, large-size (LS) females (CL: 15.89 and 14.51 mm) carried many eggs (X: 814 and 846) with a smaller volume (X: 0.130 and 0.143 mm3). All populations showed continuous reproduction and similar reproductive output. ‘El Niño’ did not directly affect both phenotypes, which is a reflection of the reproductive plasticity observed in this species. This phenomenon acted as a stressing factor, modifying the reproductive patterns of the species in a space–temporal scale. Ovigerous females showed specificity in habitat use, with SS females being associated with macrophytes in deeper environments (refuges), and LS females being associated with shallow sandy areas (shelter and nursery). The high variability of reproductive aspects is better explained by intrinsic factors and could be implying an incipient speciation.

Additional keywords: Amazon River prawn, Caridea, ENSO, water-column levels.


References

Abdennour, C. (1997). Copper, zinc and haemocyanin concentrations in four caridean decapods (Crustacea): size relationships. Hydrobiologia 346, 1–9.
| Copper, zinc and haemocyanin concentrations in four caridean decapods (Crustacea): size relationships.Crossref | GoogleScholarGoogle Scholar |

Agostinho, A. A., Júlio, H. F., and Borghetti, J. R. (1992). Considerações sobre os impactos dos represamentos na ictiofauna e medidas para sua atenuação. um estudo de caso: reservatório de Itaipu. Revista Unimar 14, 89–107.

American Public Health Association (1999). ‘Standard Methods for the Examination of Water and Wastewater’, 20th edn. (APHA: Washington, DC, USA.)

Anger, K. (1995). The conquest of freshwater and land by marine crabs: adaptations in life-history patterns and larval bioenergetics. Journal of Experimental Marine Biology and Ecology 193, 119–145.
| The conquest of freshwater and land by marine crabs: adaptations in life-history patterns and larval bioenergetics.Crossref | GoogleScholarGoogle Scholar |

Anger, K. (2013). Neotropical Macrobrachium (Caridea: Palaemonidae): on the biology, origin, and radiation of freshwater-invading shrimp. Journal of Crustacean Biology 33, 151–183.
| Neotropical Macrobrachium (Caridea: Palaemonidae): on the biology, origin, and radiation of freshwater-invading shrimp.Crossref | GoogleScholarGoogle Scholar |

Anger, K., and Hayd, L. (2009). From lecithotrophy to planktotrophy: ontogeny of larval feeding in the Amazon River prawn Macrobrachium amazonicum. Aquatic Biology 7, 19–30.
| From lecithotrophy to planktotrophy: ontogeny of larval feeding in the Amazon River prawn Macrobrachium amazonicum.Crossref | GoogleScholarGoogle Scholar |

Anger, K., and Hayd, L. (2010). Feeding and growth in early larval shrimp Macrobrachium amazonicum from the Pantanal, southwestern Brazil. Aquatic Biology 9, 251–261.
| Feeding and growth in early larval shrimp Macrobrachium amazonicum from the Pantanal, southwestern Brazil.Crossref | GoogleScholarGoogle Scholar |

Anger, K., and Moreira, G. S. (1998). Morphometric and reproductive traits of tropical caridean shrimps. Journal of Crustacean Biology 18, 823–838.
| Morphometric and reproductive traits of tropical caridean shrimps.Crossref | GoogleScholarGoogle Scholar |

Ashelby, C. W., Page, T. J., De Grave, S., Hughes, J. M., and Johnson, M. (2012). Regional scale speciation reveals multiple invasions of freshwater in Palaemoninae (Decapoda). Zoologica Scripta 41, 293–306.
| Regional scale speciation reveals multiple invasions of freshwater in Palaemoninae (Decapoda).Crossref | GoogleScholarGoogle Scholar |

Augusto, A., and Valenti, W. C. (2016). Are there any physiological differences between the male morphotypes of the freshwater shrimp Macrobrachium amazonicum (Heller, 1862) (Caridea: Palaemonidae)? Journal of Crustacean Biology 36, 716–723.
| Are there any physiological differences between the male morphotypes of the freshwater shrimp Macrobrachium amazonicum (Heller, 1862) (Caridea: Palaemonidae)?Crossref | GoogleScholarGoogle Scholar |

Bauer, R. T. (2004). ‘Remarkable Shrimps. Adaptations and Natural History of the Carideans’, 1st edn. (University of Oklahoma Press: Oklahoma, OK, USA.)

Bialetzki, A., Nakatani, K., Baumgartner, G., and Bond-Buckup, G. (1997). Occurrence of Macrobrachium amazonicum (Heller) (Decapoda, Palaemonidae) in Leopoldo’s inlet (Ressaco do Leopoldo), upper Paraná River, Porto Rico, Paraná, Brazil. Revista brasileira de Zoologia = Zoologia 14, 379–390.
| Occurrence of Macrobrachium amazonicum (Heller) (Decapoda, Palaemonidae) in Leopoldo’s inlet (Ressaco do Leopoldo), upper Paraná River, Porto Rico, Paraná, Brazil. Revista brasileira de Zoologia =Crossref | GoogleScholarGoogle Scholar |

Boubonari, T., Kevrekidis, T., and Malea, P. (2009). Metal (Fe, Zn, Cu, Pb and Cd) concentration patterns in components of a macrophyte-based coastal lagoon ecosystem. Hydrobiologia 635, 27–36.
| Metal (Fe, Zn, Cu, Pb and Cd) concentration patterns in components of a macrophyte-based coastal lagoon ecosystem.Crossref | GoogleScholarGoogle Scholar |

Bouvy, M., Falcão, D., Marinho, M., Pagano, M., and Moura, A. (2000). Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquatic Microbial Ecology 23, 13–27.
| Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought.Crossref | GoogleScholarGoogle Scholar |

Bouvy, M., Nascimento, S. M., Molica, R. J., Ferreira, A., Huszar, V., and Azevedo, S. M. (2003). Limnological features in Tapacurá reservoir (northeast Brazil) during a severe drought. Hydrobiologia 493, 115–130.
| Limnological features in Tapacurá reservoir (northeast Brazil) during a severe drought.Crossref | GoogleScholarGoogle Scholar |

Correa, C., and Thiel, M. (2003). Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology. Revista Chilena de Historia Natural 76, 187–203.
| Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology.Crossref | GoogleScholarGoogle Scholar |

Evtimova, V. V., and Donohue, I. (2016). Water-level fluctuations regulate the structure and functioning of natural lakes. Freshwater Biology 61, 251–264.
| Water-level fluctuations regulate the structure and functioning of natural lakes.Crossref | GoogleScholarGoogle Scholar |

Golterman, H. L., Clymo, R. S., and Ohnstad, M. A. M. (1978). ‘Methods for Physical and Chemical Analysis of Freshwaters’, 2nd edn. (Blackwell Scientific Publications: Oxford, UK.)

Grimm, A. M. (2003). The El Niño impact on the summer monsoon in Brazil: regional processes versus remote influences. Journal of Climate 16, 263–280.
| The El Niño impact on the summer monsoon in Brazil: regional processes versus remote influences.Crossref | GoogleScholarGoogle Scholar |

Hayd, L., and Anger, K. (2013). Reproductive and morphometric traits of Macrobrachium amazonicum (Decapoda: Palaemonidae) from the Pantanal, Brazil, suggests initial speciation. Revista de Biología Tropical 61, 39–57.
| Reproductive and morphometric traits of Macrobrachium amazonicum (Decapoda: Palaemonidae) from the Pantanal, Brazil, suggests initial speciation.Crossref | GoogleScholarGoogle Scholar | 23894962PubMed |

Henry, R. (1999). ‘Ecologia de Reservatórios: Estrutura, Função e Aspectos Sociais’, 1st edn. (Fapesp/Fundibio: Botucatu, Brazil.)

Herring, P. J. (1974). Observations on the embryonic development of some deep-living decapod crustaceans, with particular reference to species of Acanthephyra. Marine Biology 25, 25–33.
| Observations on the embryonic development of some deep-living decapod crustaceans, with particular reference to species of Acanthephyra.Crossref | GoogleScholarGoogle Scholar |

Hotelling, H. (1951). A generalized T test and measure of multivariate dispersion. In ‘Proceedings of the Second Berkeley Symposium on Mathematical Statistics and Probability’, 31 July–12 August 1950, Berkeley, CA, USA. (Ed. J. Neyman.) pp. 23–41. (University of California Press: Berkeley, CA, USA.)

Jalihal, D. R., Sankolli, K. N., and Shenoy, S. (1993). Evolution of larval developmental patterns and the process of freshwaterization in the prawn genus Macrobrachium Bate, 1868 (Decapoda, Palaemonidae). Crustaceana 65, 365–376.
| Evolution of larval developmental patterns and the process of freshwaterization in the prawn genus Macrobrachium Bate, 1868 (Decapoda, Palaemonidae).Crossref | GoogleScholarGoogle Scholar |

Kaster, J. L., and Jacobi, G. Z. (1978). Benthic macroinvertebrates of a fluctuating reservoir. Freshwater Biology 8, 283–290.
| Benthic macroinvertebrates of a fluctuating reservoir.Crossref | GoogleScholarGoogle Scholar |

Keitel, J., Zak, D., and Hupfer, M. (2016). Water level fluctuations in a tropical reservoir: the impact of sediment drying, aquatic macrophyte dieback, and oxygen availability on phosphorus mobilization. Environmental Science and Pollution Research International 23, 6883–6894.
| Water level fluctuations in a tropical reservoir: the impact of sediment drying, aquatic macrophyte dieback, and oxygen availability on phosphorus mobilization.Crossref | GoogleScholarGoogle Scholar | 26670030PubMed |

Maciel, C. R., and Valenti, W. C. (2009). Biology, fisheries, and aquaculture of the Amazon River prawn Macrobrachium amazonicum: a review. Nauplius 17, 61–79.

Mashiko, K. (1990). Diversified egg and clutch sizes among local populations of the fresh-water prawn Macrobrachium nipponense (de Haan). Journal of Crustacean Biology 10, 306–314.
| Diversified egg and clutch sizes among local populations of the fresh-water prawn Macrobrachium nipponense (de Haan).Crossref | GoogleScholarGoogle Scholar |

Mashiko, K. (1992). Genetic egg and clutch size variations in freshwater prawn populations. Oikos 63, 454–458.
| Genetic egg and clutch size variations in freshwater prawn populations.Crossref | GoogleScholarGoogle Scholar |

Mashiko, K., and Numachi, K. (2000). Derivation of populations with different-sized eggs in the palaemonid prawn Macrobrachium nipponense. Journal of Crustacean Biology 20, 118–127.
| Derivation of populations with different-sized eggs in the palaemonid prawn Macrobrachium nipponense.Crossref | GoogleScholarGoogle Scholar |

Meireles, A. L., Valenti, W. C., and Mantelatto, F. L. (2013). Reproductive variability of the Amazon River prawn, Macrobrachium amazonicum (Caridea, Palaemonidae): influence of life cycle on egg production. Latin American Journal of Aquatic Research 41, 718–731.
| Reproductive variability of the Amazon River prawn, Macrobrachium amazonicum (Caridea, Palaemonidae): influence of life cycle on egg production.Crossref | GoogleScholarGoogle Scholar |

Moraes-Riodades, P. M. C., and Valenti, W. C. (2004). Morphotypes in male Amazon River prawns, Macrobrachium amazonicum. Aquaculture 236, 297–307.
| Morphotypes in male Amazon River prawns, Macrobrachium amazonicum.Crossref | GoogleScholarGoogle Scholar |

Moraes-Valenti, P. M., and Valenti, W. C. (2010). Culture of the Amazon River Prawn Macrobrachium amazonicum. In ‘Freshwater Prawns: Biology and Farming’. (Eds M. B. New, W. C. Valenti, J. H. Tidwell, L.R. D'ABramo, and M. N. Kutty.) pp. 485–501. (Wiley-Blackwell: Oxford, UK.)

National Weather Service and National Oceanic and Atmospheric Administration (2017). Cold & warm episodes by season. In ‘Historical El Niño/La Niña episodes (1950–present)’. (NWS/NOAA.) Available at http://www.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ensoyears.shtml [Verified 12 March 2019].

Nazari, E. M., Simões-Costa, M. S., Muller, Y. M. R., Ammar, D., and Dias, M. (2003). Comparisons of fecundity, egg size and egg mass volume of the freshwater prawns Macrobrachium potiuna and Macrobrachium olfersii (Decapoda, Palaemonidae). Journal of Crustacean Biology 23, 862–868.
| Comparisons of fecundity, egg size and egg mass volume of the freshwater prawns Macrobrachium potiuna and Macrobrachium olfersii (Decapoda, Palaemonidae).Crossref | GoogleScholarGoogle Scholar |

Nusch, E. A. (1980). Comparison of different methods for chlorophyll and phaeopigments determination. Archiv für Hydrobiologie – Beiheft Ergebnisse der Limnologie 14, 14–36.

Odinetz Collart, O. (1991). Strategie de reproduction de Macrobrachium amazonicum en Amazonie Centrale (Decapoda, Caridea, Palaemonidae). Crustaceana 61, 253–270.
| Strategie de reproduction de Macrobrachium amazonicum en Amazonie Centrale (Decapoda, Caridea, Palaemonidae).Crossref | GoogleScholarGoogle Scholar |

Odinetz Collart, O., and Rabelo, H. (1996). Variation in egg size of the freshwater prawn Macrobrachium amazonicum (Decapoda, Palaemonidae). Journal of Crustacean Biology 16, 684–688.
| Variation in egg size of the freshwater prawn Macrobrachium amazonicum (Decapoda, Palaemonidae).Crossref | GoogleScholarGoogle Scholar |

Operador Nacional do Sistema Elétrico (2017). Dados Hidrológicos / Níveis. In ‘Histórico da Operação’. (ONS.) Available at http://www.ons.org.br/Paginas/resultados-da-operacao/historico-da-operacao/dados_hidrologicos_ niveis.aspx [Verified 1 February 2017].

Pantaleão, J. A. F., Hirose, G. L., and Costa, R. C. (2012). Relative growth, morphological sexual maturity, and size of Macrobrachium amazonicum (Heller 1862) (Crustacea, Decapoda, Palaemonidae) in a population with an entirely freshwater life cycle. Invertebrate Reproduction & Development 56, 180–190.
| Relative growth, morphological sexual maturity, and size of Macrobrachium amazonicum (Heller 1862) (Crustacea, Decapoda, Palaemonidae) in a population with an entirely freshwater life cycle.Crossref | GoogleScholarGoogle Scholar |

Pantaleão, J. A. F., Hirose, G. L., and Costa, R. C. (2014). Ocurrence of male morphotypes of Macrobrachium amazonicum (Caridea, Palaemonidae) in a population with an entirely freshwater life cycle. Brazilian Journal of Biology 74, S223–S232.
| Ocurrence of male morphotypes of Macrobrachium amazonicum (Caridea, Palaemonidae) in a population with an entirely freshwater life cycle.Crossref | GoogleScholarGoogle Scholar |

Pantaleão, J. A. F., Carvalho-Batista, A., Teodoro, S. S. A., and Costa, R. C. (2018). The influence of environmental variables in the reproductive performance of Macrobrachium amazonicum (Heller, 1862) (Caridea: Palaemonidae) females in a continental population. Anais da Academia Brasileira de Ciências 90, 1445–1458.
| The influence of environmental variables in the reproductive performance of Macrobrachium amazonicum (Heller, 1862) (Caridea: Palaemonidae) females in a continental population.Crossref | GoogleScholarGoogle Scholar |

Paschoal, L. R. P., and Rigolin-Sá, O. (2011). Análise da qualidade da água das UHE Marechal Mascarenhas de Morais e Luiz Carlos Barreto de Carvalho da Bacia hidrográfica do médio rio Grande (MG) utilizando o índice do estado trófico (IET) e o índice da qualidade da água (IQA). Ciência et Praxis 7, 13–20.

Paschoal, L. R. P., and Zara, F. J. (2017). First record of intersexuality in the Amazon River shrimp Macrobrachium amazonicum (Heller, 1862) (Caridea: Palaemonidae). Journal of Crustacean Biology 37, 507–511.
| First record of intersexuality in the Amazon River shrimp Macrobrachium amazonicum (Heller, 1862) (Caridea: Palaemonidae).Crossref | GoogleScholarGoogle Scholar |

Paschoal, L. R. P., and Zara, F. J. (2018). Sperm count of Macrobrachium amazonicum (Heller, 1862) populations with distinct life histories, with introduction of a simple counting method. Aquaculture 491, 368–374.
| Sperm count of Macrobrachium amazonicum (Heller, 1862) populations with distinct life histories, with introduction of a simple counting method.Crossref | GoogleScholarGoogle Scholar |

Paschoal, L. R. P., and Zara, F. J. (in press). Size at onset of sexual maturity in Macrobrachium amazonicum (Heller, 1862) phenotypes: an integrative approach. Anais da Academia Brasileira de Ciências , .

Paschoal, L. R. P., Souza, R. M., Guimarães, F. J., and Couto, E. C. G. (2013). Phytophilous caridean shrimps (Atyidae and Palaemonidae) in Salsa river (Canavieiras, Bahia, Brazil). Nauplius 21, 123–126.
| Phytophilous caridean shrimps (Atyidae and Palaemonidae) in Salsa river (Canavieiras, Bahia, Brazil).Crossref | GoogleScholarGoogle Scholar |

Paschoal, L. R. P., Andrade, D. P., and Darrigran, G. (2015). How the fluctuations of water levels affect populations of invasive bivalve Corbicula fluminea (Müller, 1774) in a Neotropical reservoir? Brazilian Journal of Biology 75, 135–143.
| How the fluctuations of water levels affect populations of invasive bivalve Corbicula fluminea (Müller, 1774) in a Neotropical reservoir?Crossref | GoogleScholarGoogle Scholar |

Paschoal, L. R. P., Guimarães, F. J., and Couto, E. C. G. (2016). Growth and reproductive biology of the amphidromous shrimp Palaemon pandaliformis (Decapoda, Caridea) in a Neotropical river from northeastern Brazil. Zoologia 33, 1–14.
| Growth and reproductive biology of the amphidromous shrimp Palaemon pandaliformis (Decapoda, Caridea) in a Neotropical river from northeastern Brazil.Crossref | GoogleScholarGoogle Scholar |

Pileggi, L. G., and Mantelatto, F. L. (2010). Molecular phylogeny of the freshwater prawn genus Macrobrachium (Decapoda, Palaemonidae), with emphasis on the relationships among selected American species. Invertebrate Systematics 24, 194–208.
| Molecular phylogeny of the freshwater prawn genus Macrobrachium (Decapoda, Palaemonidae), with emphasis on the relationships among selected American species.Crossref | GoogleScholarGoogle Scholar |

Relyea, C. D., Minshall, G. W., and Danehy, R. J. (2000). Stream insects as bioindicators of fine sediment. In ‘Proceedings of the ASCE Watershed Management 2000 Conference’. (Eds M. Flug, D. Frevert, and D. W. Watkins Jr.) pp. 1–19. (American Society of Civil Engineers: Fort Collins, CO, USA.)

Strickland, J. D. H., and Parsons, T. R. (1960). A manual of seawater analysis. Bulletin – Fisheries Research Board of Canada 125, 1–185.

Torres, M. V., Giri, F., and Collins, P. A. (2017). ‘La Niña’ phenomenon and the relationship between decapod populations and fishes in temporarily isolated shallow lakes. Marine and Freshwater Research 68, 1010–1022.
| ‘La Niña’ phenomenon and the relationship between decapod populations and fishes in temporarily isolated shallow lakes.Crossref | GoogleScholarGoogle Scholar |

Trenberth, K. E. (1997). The definition of El Niño. Bulletin of the American Meteorological Society 78, 2771–2777.
| The definition of El Niño.Crossref | GoogleScholarGoogle Scholar |

Valderrama, J. C. (1981). The simultaneous analysis of total nitrogen and phosphorus in natural waters. Marine Chemistry 10, 109–122.
| The simultaneous analysis of total nitrogen and phosphorus in natural waters.Crossref | GoogleScholarGoogle Scholar |

Van Raij, B., Andrade, J. C., Cantarella, H., and Quaggio, J. A. (2001). ‘Análise Química para Avaliação da Fertilidade de Solos Tropicais’, 1 edn. (Instituto Agronômico: Campinas, Brazil.)

Vergamini, F. G., Pileggi, L. G., and Mantelatto, F. L. (2011). Genetic variability of the Amazon River prawn Macrobrachium amazonicum (Decapoda, Caridea, Palaemonidae). Contributions to Zoology (Amsterdam, Netherlands) 80, 67–83.

Zimmermann, U., Carvalho, F. L., and Mantelatto, F. L. (2015). The reproductive performance of the red-algae shrimp Leander paulensis (Ortmann, 1897) (Decapoda, Palaemonidae) and the effect of post-spawning female weight gain on weight-dependent parameters. Brazilian Journal of Oceanography 63, 207–216.
| The reproductive performance of the red-algae shrimp Leander paulensis (Ortmann, 1897) (Decapoda, Palaemonidae) and the effect of post-spawning female weight gain on weight-dependent parameters.Crossref | GoogleScholarGoogle Scholar |