Population dynamics and reproductive features of the Amazon River prawn Macrobrachium amazonicum (Heller, 1862) in Neotropical reservoirs under drought events

Lucas Rezende Penido Paschoal; Fernando José Zara

doi:10.26496/bjz.2024.193

Authors

Lucas Rezende Penido Paschoal Invertebrate Morphology Laboratory (IML), Department of Biology, Agricultural and Veterinary School of Jaboticabal and Aquaculture Center of UNESP (CAUNESP), São Paulo State University (UNESP). 14884-900, Jaboticabal, São Paulo, Brazil
Fernando José Zara Invertebrate Morphology Laboratory (IML), Department of Biology, Agricultural and Veterinary School of Jaboticabal and Aquaculture Center of UNESP (CAUNESP), São Paulo State University (UNESP). 14884-900, Jaboticabal, São Paulo, Brazil

DOI:

https://doi.org/10.26496/bjz.2024.193

Keywords:

Caridea, drought, phenotypes, reproduction, synergistic events

Abstract

Here, we describe population and reproductive dynamics of four populations of Macrobrachium amazonicum in reservoirs during drought events. Additionally, we analyze possible phenotypic changes in this species promoted by fish predation. Two populations had a large-size phenotype (with large body proportions and morphotypes in males) while a small-size phenotype (with reduced sizes and no morphotypes) was found in the two other populations. Overall, females were larger than males and there were varying sex ratios among the four studied populations. All populations had bimodal or polymodal patterns in their monthly size-class frequency, suggesting a seasonal influence and a potentially great capacity of these populations to adapt to adverse environmental conditions. No major changes were found in the patterns of sex ratio, recruitment, frequency of (larger) male morphotypes and female ovarian development stages during drought events. Macrobrachium amazonicum is a resilient species and undergoes continuous reproduction. Females with immature ovaries were predominant in all populations, performing multiple spawns and exhibiting rapid ovarian development cycles. In males, the initial morphotype (TC - translucent claw) was predominant in populations with a social hierarchy. Males of dominant morphotypes (GC1 and GC2 - green claw 1 and 2) use more energy to carry out and maintain metabolic processes, which could probably one of the explanations why their number in populations are limited. We did not find any clear evidence that fish predation affected phenotypes, suggesting that phenotypic plasticity could be more related to intrinsic factors, which would have to be further investigated.

References

Abdi H. & Valentin D. (2007). Multiple Correspondence Analysis. In: Salkind N. (ed.) Encyclopedia of Measurement and Statistics: 1–13. Thousand Oaks, California.

Agência nacional de águas - ANA. (2017). Sistema Nacional de Informações sobre Recursos Hídricos. Available from https://www.snirh.gov.br [accessed 1 February 2017].

Andrade D.P., Paschoal L.R.P., Rigolin-Sá O. & França N. (2012). Water quality assessment of fifth-order tributaries of the reservoir at the Marechal Mascarenhas de Morais Hydroelectric Power Station in the Rio Grande watershed (State of Minas Gerais, Brazil). Acta Limnologica Brasiliensia 24: 326–337. https://doi.org/10.1590/S2179-975X2013005000002

Anger K. & Moreira G.S. (1998). Morphometric and reproductive traits of tropical caridean shrimps. Journal of Crustacean Biology 18: 823–838. https://doi.org/10.1163/193724098X00674

Augusto A. & 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 6: 716–723. https://doi.org/10.1163/1937240X-00002467

Bentes B.S., Martinelli J.M., Souza L.S., Cavalcante D.V., Almeida M.C. & Isaac V.J. (2011). Spatial distribution of the Amazon River prawn Macrobrachium amazonicum (Heller, 1862) (Decapoda, Caridea, Palaemonidae) in two perennial creeks of an estuary on the northern coast of Brazil (Guajará Bay, Belém, Pará). Brazilian Journal of Biology 71: 925–935. https://doi.org/10.1590/S1519-69842011000500013

Bouvy M., Nascimento S.M., Molica R.J., Ferreira A., Huszar V. & Azevedo S.M. (2003). Limnological features in Tapacurá reservoir (northeast Brazil) during a severe drought. Hydrobiologia 493: 115–130. https://doi.org/10.1023/A:1025405817350

Costa T.V., Mattos L.A. & Machado N.D.J.B. (2016). Estrutura populacional de Macrobrachium amazonicum em dois lagos de várzea da Amazônia. Boletim do Instituto de Pesca 42: 281–293. https://doi.org/10.20950/1678-2305.2016v42n2p281

Cohen D., Raanan Z. & Brody T. (1981). Population profile development and morphotypic differentiation in the giant freshwater prawn Macrobrachium rosenbergii (de Man). Journal of the World Mariculture Society 12: 231–243. https://doi.org/10.1111/j.1749-7345.1981.tb00298.x

De Grave S. & Mantelatto F. (2013). Macrobrachium denticulatum. Available from www.iucnredlist.org [accessed 1 February 2017].

Díaz H. & Conde J.E. (1989). Population dynamics and life history of the mangrove crab Aratus pisonii (Brachyura, Grapsidae) in a marine environment. Bulletin of Marine Science 45: 148–163.

Fisher R.A. (1930). The Genetical Theory of Natural Selection. Claredon Press, New York.

Freire J.L., Bentes B., Fontes V.B. & Silva EM. (2017). Morphometric discrimination among three stocks of Macrobrachium amazonicum in the Brazilian Amazon. Limnologica 64: 1–10. https://doi.org/10.1016/j.limno.2017.01.007

Goodbody H. (1965). Continuous breeding in populations of two tropical crustaceans, Mysidium columbiae (Zimmer) and Emerita portoricensis Schmidt. Ecology 46: 195–197. https://doi.org/10.2307/1935274

Gotelli N.J. & Ellison A.M. (2004). A Primer of Ecological Statistics. Sinauer Associates, Inc. Sunderland, Massachusetts.

Habashy M.M., Sharshar K.M. & Hassan M.M. (2012). Morphological and histological studies on the embryonic development of the freshwater prawn, Macrobrachium rosenbergii (Crustacea, Decapoda). The Journal of Basic & Applied Zoology 65: 157–165. https://doi.org/10.1016/j.jobaz.2012.01.002

Hayd L. & 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.

Henry R. (1999). Ecologia de reservatórios: estrutura, função e aspectos sociais. Fapesp/ FundibioBrazil, Botucatu.

Iketani G., Aviz M.A.B., Maciel C., Valenti W.C., Schneider H. & Sampaio I. (2016). Successful invasion of the Amazon Coast by the giant river prawn, Macrobrachium rosenbergii: evidence of a reproductively viable population. Aquatic Invasions 11: 277–286. https://doi.org/10.3391/ai.2016.11.3.06

Keitel J., Zak D. & Hupfer M. (2015). 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 23: 6883–6894. https://doi.org/10.1007/s11356-015-5915-3

Lima J.D.F., Silva L.M.A., Silva T.C., Garcia J.S., Pereira I.L. & Amaral K.D.S. (2014). Reproductive aspects of Macrobrachium amazonicum (Decapoda: Palaemonidae) in the State of Amapá, Amazon River mouth. Acta Amazonica 44: 245–254. https://doi.org/10.1590/S0044-59672014000200010

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

Magalhães C., Bueno S.L.S., Bond-Buckup G., Valenti W.C., Silva H.M., Kiyohara F., Mossolin E.C. & Rocha S.S. (2005). Exotic species of freshwater decapod crustaceans in the state of São Paulo, Brazil: records and possible causes of their introduction. Biodiversity and Conservation 14: 1929–1945. https://doi.org/10.1007/s10531-004-2123-8

Melo D.C.D., Scanlon B.R., Zhang Z., Wendland E. & Yin L. (2016). Reservoir storage and hydrologic responses to droughts in the Paraná River basin, south-eastern Brazil. Hydrology and Earth System Sciences 20: 4673. https://doi.org/10.5194/hess-20-4673-2016

Moraes-Riodades P.M.C. & Valenti W.C. (2004). Morphotypes in male Amazon River prawns, Macrobrachium amazonicum. Aquaculture 236: 297–307. https://doi.org/10.1016/j.aquaculture.2004.02.015

Mossolin E.C. & Bueno S.L.S. (2002). Reproductive biology of Macrobrachium olfersi (Decapoda, Palaemonidae) in São Sebastião, Brazil. Journal of Crustacean Biology 22: 367–376. https://doi.org/10.1651/0278-0372(2002)022[0367:RBOMOD]2.0.CO;2

National Weather Service/National Oceanic and Atmospheric Administration - NWS/NOAA. (2017). El Niño/La Niña Home - Climate Prediction Center. Available from http://www.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ensoyears.shtml [accessed 1 February 2017].

Nobre C.A., Marengo J.A., Seluchi M.E., Cuartas L.A. & Alves L.M. (2016). Some characteristics and impacts of the drought and water crisis in southeastern Brazil during 2014 and 2015. Journal of Water Resource and Protection 8: 252–262. https://doi.org/10.4236/jwarp.2016.82022

Ocasio-Torres M.E., Crowl T.A. & Sabat A.M. (2014). Long rostrum in an amphidromous shrimp induced by chemical signals from a predatory fish. Freshwater Science 33: 451–458. https://doi.org/10.1086/675500

Ocasio-Torres M.E., Crowl T.A. & Sabat A.M. (2015a). Allometric differences between two phenotypes of the amphidromous shrimp Xiphocaris elongata. Journal of Crustacean Biology 35: 747–752. https://doi.org/10.1163/1937240X-00002372

Ocasio-Torres M.E., Giray T., Crowl T.A. & Sabat A.M. (2015b). Antipredator defense mechanism in the amphidromous shrimp Xiphocaris elongata (Decapoda: Xiphocarididae): rostrum length. Journal of Natural History 35: 747–752. https://doi.org/10.1080/00222933.2015.1005716

Odinetz-Collart O. (1991a). Strategie de reproduction de Macrobrachium amazonicum en Amazonie Centrale (Decapoda, Caridea, Palaemonidae). Crustaceana 61: 253–270.

Odinetz-Collart O. (1991b). Tucurui dam and the population of the prawn Macrobrachium amazonicum in the Lower Tocantins (PA-Brazil): a four year study. Archiv für Hydrobiologie 122: 213–227. https://doi.org/10.1127/archiv-hydrobiol/122/1991/213

Operador Nacional Do Sistema Elétrico – ONS. (2017). Histórico da Operação. Available from https://www.ons.org.br/Paginas/resultados-da-operacao/historico-da-operacao/dados_hidrologicos_volumes.aspx [accessed 1 February 2017].

Ota R.R., Deprá G.C., Graça W.J. & Pavanelli C.S. (2018). Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotropical Ichthyology 16: e170094. https://doi.org/10.1590/1982-0224-20170094

Pantaleão J.A.F., Hirose G.L. & 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: 80–190. https://doi.org/10.1080/07924259.2011.587276

Pantaleão J.A.F., Hirose G.L. & Costa R.C. (2014). Occurrence of male morphotypes of Macrobrachium amazonicum (Caridea, Palaemonidae) in a population with an entirely freshwater life cycle. Brazilian Journal of Biology 74: 223–232. https://doi.org/10.1590/1519-6984.03713

Paschoal L.R.P. & Zara F.J. (2020). Size at onset of sexual maturity in Macrobrachium amazonicum (Heller, 1862) phenotypes: an integrative approach. Anais da Academia Brasileira de Ciências 92: e20180560. https://doi.org/10.1590/0001-3675202020180560

Paschoal L.R.P. & Zara F.J. (2022). Is there a trade-off between sperm production and sexual weaponry in the Amazon River prawn Macrobrachium amazonicum (Heller, 1862)? Zoology 153: e26029. https://doi.org/10.1016/j.zool.2022.126029

Paschoal L.R.P. & Zara F.J. (2023). Assessing the ovarian development of Macrobrachium amazonicum (Heller, 1862) phenotypes by means of an integrative analysis. Tissue and Cell 84: e102166. https://doi.org/10.1016/j.tice.2023.102166

Paschoal L.R.P., Souza R.M., Guimarães F.J. & Couto E.C.G. (2013). Phytophilous caridean shrimps (Atyidae and Palaemonidae) in Salsa river (Canavieiras, Bahia, Brazil). Nauplius 21: 123-126. https://doi.org/10.1590/S0104-64972013000100011

Paschoal L.R.P., Andrade D.P. & 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. https://doi.org/10.1590/1519-6984.09113

Paschoal L.R.P., Oliveira L.J.F., Andreoli G.C. & Zara F.J. (2019a). Reproductive biology of Macrobrachium amazonicum (Heller, 1862) populations with distinct phenotypes in Neotropical reservoirs during the “El Niño” event. Marine and Freshwater Research 70: 1465–1479. https://doi.org/10.1071/MF18228

Paschoal L.R.P., Oliveira L.J.F., Andreoli G.C. & Zara F.J. (2019b). Dry or wet? What is the best choice to determine gonadosomatic and hepatosomatic indexes in females of Macrobrachium amazonicum? Aquaculture Research 50: 3589–3596. https://doi.org/10.1111/are.14314

Paschoal L.R.P., Andrade D.P., Pimpão D.M., Torres S. & Darrigran G. (2020). Massive mortality of the giant freshwater mussel Anodontites trapesialis (Lamarck, 1819) (Bivalvia: Mycetopodidae) during a severe drought in a Neotropical reservoir. Anais da Academia Brasileira de Ciências 92: e20180811. https://doi.org/10.1590/0001-3765202020180811

Pileggi L.A.G. (2009). Sistemática filogenética dos camarões do gênero Macrobrachium Bate, 1868 do Brasil: análises morfológicas e moleculares. PhD Thesis, Universidade de São Paulo – USP, São Paulo.

R Core Team. R (The R Project for Statistical Computing). Software version 3.3.1. 2017. Available from www.r-project.org [accessed 1 February 2017].

Ragonese S. & Bianchini M.L. (1996). Growth, mortality and yield-per-recruit of the deep-water shrimp Aristeus antennatus (Crustacea-Aristeidae) of the Strait of Sicily (Mediterranean Sea). Fisheries Research 26: 125–137. https://doi.org/10.1016/0165-7836(95)00394-0

Rocha S.S., Silva R.L.S, Santos J.L. & Oliveira G. (2015). Length-weight relationship and condition factor of Macrobrachium amazonicum (Heller, 1862) (Decapoda, Palaemonidae) from a reservoir in Bahia, Brazil. Nauplius 23: 149–161. https://doi.org/10.1590/S0104-64972015002308

Sampaio C.M.S., Silva RR., Santos JA. & Sales SP. (2007). Reproductive cycle of Macrobrachium amazonicum females (Crustacea, Palaemonidae). Brazilian Journal of Biology 67: 551–559. https://doi.org/10.1590/S1519-69842007000300022

Santos J.A., Sampaio C.M.S & Soares-Filho A.A. (2006). Male population structure of the Amazon River prawn (Macrobrachium amazonicum) in a natural environment. Nauplius 14: 55–63.

Sousa R., Halabowski D., Labecka A.M., Douda K., Aksenova O., Bespalaya Y., Bolotov I., Geist J., Jones H.A., Konopleva E., Klunzinger M.W., Lasso C.A., Lewin I., Liu X., Lopes-Lima M. et al. (2021). The role of anthropogenic habitats in freshwater mussel conservation. Global Change Biology 27: 2298–2314. https://doi.org/10.1111/gcb.15549

Sturges H.A. (1926). The choice of a class interval. Journal of the American Statistical Association 21: 65–66. https://doi.org/10.1080/01621459.1926.10502161

Tsuchida S. & Watanabe S. (1997). Growth and reproduction of the grapsid crab Plagusia dentipes (Deca-poda: Brachyura). Journal of Crustacean Biology 17: 90–97. https://doi.org/10.1163/193724097X00133

Valenti W.C., Mello J.T.C. & Lobão V.L. (1986). Dinâmica da reprodução de Macrobrachium acanthurus (Wiegmann, 1836) e Macrobrachium carcinus (Linnaeus, 1758) do Rio Ribeira de Iguape (Crustacea, Decapoda, Palaemonidae). Ciência e Cultura 38: 1256–1262.

Vergamini F.G., Pileggi L.G. & Mantelatto F.L. (2011). Genetic variability of the Amazon River prawn Macrobrachium amazonicum (Decapoda, Caridea, Palaemonidae). Contributions to Zoology 80: 67–83. https://doi.org/10.1163/18759866-08001003

Wang Y., Ziqiang X. & Wang D. (2012). A transitional region concept for assessing the effects of reservoirs on river habitats: a case of Yangtze River, China. Ecohydrology 5: 28–35. https://doi.org/10.1002/eco.186

Wenner E.L., Conn W.P. III, Sandifer P.A. & Shealy M.H. jr. (1991). A Comparison of Species Composition and Abundance of Decapod Crustaceans and Fishes from the North and South Edisto Rivers in South Carolina. South Carolina Marine Research Center, Technical Report No. 78, Charleston.

Wilson M.F. & Pianka E.R. (1963). Sexual selection, sex ratio and mating system. American Naturalist 97: 405–407.