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Long-term monitoring of the non-native giant river prawn Macrobrachium rosenbergii (De Man, 1879) in the Furnas mega reservoir (southeastern Brazil)

Abstract

In this study, we report six records of the non-native giant river prawn Macrobrachium rosenbergii (De Man, 1879) in the Furnas mega reservoir, state of Minas Gerais (Southeast Brazil), during continuous monitoring conducted from 2006 to 2023. All recorded specimens were males of the blue claw (BC) morphotype and possibly entered interior areas of the reservoir via accidental escapes. There was no occurrence of established populations in the region, nor any evidence of disease in the specimens obtained. However, continuous monitoring is recommended to record new escapes and determine the possibility of establishment of giant river prawn populations in the aquatic environment of the Furnas mega reservoir.

Keywords:
Bio-invasion; Caridea; escapes; Neotropical region; new records

Reservoirs are artificial environments that have unique structural characteristics, such as an upstream lentic portion and a downstream lotic portion. These characteristics promote hydrological and energy flow variations along the reservoir path, allowing humans to use this environment for various purposes (Henry, 1999Henry R 1999. Ecologia de reservatórios: estrutura, função e aspectos sociais. Botucatu, Fapesp/Fundibio, 800p.; Wang et al., 2012Wang Y, Xia Z and Wang D 2012. A transitional region concept for assessing the effects of reservoirs on river habitats: a case of Yangtze River, China. Ecohydrology, 5(1): 28-35. https://doi.org/10.1002/eco.186). Brazil has the largest number of reservoirs in the world (N = 393), which vary in category according to the height of the dam and its storage capacity (FAO, 2016FAO [Food And Agriculture Organization of the United Nations] 2016. AQUASTAT website. Available at http://www.fao.org/nr/water/aquastat/dams/index.stm . Accessed on 14 January 2023.
http://www.fao.org/nr/water/aquastat/dam...
). Therefore, mega reservoirs, structures with heights above 100 meters and storing more than 1 km3 of water (sensu Gupta et al., 2012Gupta H, Kao SJ and Dai M 2012. The role of mega dams in reducing sediment fluxes: A case study of large Asian rivers. Journal of Hydrology, 464: 447-458. https://doi.org/10.1016/j.jhydrol.2012.07.038
https://doi.org/10.1016/j.jhydrol.2012.0...
), are considered the most important and strategic reservoirs in the country (ONS, 2023ONS [Operador Nacional do Sistema Elétrico] 2023. Reservatórios. Available at https://www.ons.org.br/paginas/energia-agora/reservatorios . Accessed on 14 January 2023.
https://www.ons.org.br/paginas/energia-a...
).

Among such reservoirs, the Furnas mega reservoir, located in the southeastern region of the country, stands out. Dammed in 1962, it is formed mainly by the Grande and Sapucaí Rivers, which are part of the Upper Paraná River basin, and other small tributaries (Fig. 1). It has a 127 m high dam and a total volume of 22.95 km3, its flooded area extends for 1,440 km2 and its generation capacity is 1,216 MW. Approximately 40 municipalities in the state of Minas Gerais benefit from the Furnas mega reservoir, using it as a water reservoir, for electricity generation, tourism, leisure and direct exploitation of fishery resources (e.g., fishing, aquaculture and related activities). In addition, the mega reservoir directly and indirectly sustains a great diversity of wild life (Rigolin-Sá, 2012Rigolin-Sá O 2012. Bacia Hidrográfica: Estudos do Rio Grande no Sudoeste de Minas Gerais - Brasil. Passos, Edifesp , 302p.).

The Furnas mega reservoir is of great socioeconomic and environmental importance for the entire region where it is located. However, its implementation was responsible for significantly modifying the environmental landscape in its surroundings (Pereira et al., 2012Pereira VA, Rigolin-Sá O, Ribeiro MM and Nogueira DJ 2012. Impactos ambientais e sociais devido à implantação da usina hidrelétrica de Furnas, nos municípios de Passos e São José da Barra - MG. p. 247-278. In: Rigolin-Sá O (Ed.), Bacia Hidrográfica: Estudos do Rio Grande no Sudoeste de Minas Gerais - Brasil. Passos, Edifesp. 1ed.). Added to this are other environmental changes caused by humans, the main type in this region being bio-invasions. Valéry et al. (2008) defined bio-invasion as “… a species acquiring a competitive advantage following the disappearance of natural obstacles to its proliferation, which allows it to spread rapidly and to conquer novel areas within the recipient ecosystem in which it becomes a dominant population.”

Figure 1.
Occurrence of male Macrobrachium rosenbergii (De Man, 1879) of the blue claw morphotype recorded in the Furnas mega reservoir according to the time of capture (1 to 6) from 2010 to 2022.

Bio-invasions are common and constant in the Furnas mega reservoir and are easily observed among the aquatic fauna of the region, especially in fish (e.g., Nile tilapia Oreochromis niloticus (Linnaeus, 1758), peacock bass Cichla monoculus Agassiz, 1831 (among other species reported in Azevedo-Santos et al., 2010aAzevedo-Santos VM and Lima-Stripari N 2010. Primeiro registro de Dilocarcinus pagei Stimpson, 1861 (Decapoda, Trichodactylidae) no estado de Minas Gerais. Biotemas, 23(2): 199-202. https://doi.org/10.5007/2175-7925.2010v23n2p199
https://doi.org/10.5007/2175-7925.2010v2...
; 2011Azevedo-Santos VM, Rigolin-Sá O and Pelicice FM 2011. Growing, losing or introducing? Cage aquaculture as a vector for the introduction of non-native fish in Furnas Reservoir, Minas Gerais, Brazil. Neotropical Ichthyology, 9: 915-919. https://doi.org/10.1590/S1679-62252011000400024
https://doi.org/10.1590/S1679-6225201100...
), mollusks (e.g., Asian clam Corbicula fluminea (Müller, 1774) analyzed by Paschoal et al., 2015Paschoal LRP, Andrade DP 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. https://doi.org/10.1590/1519-6984.09113
https://doi.org/10.1590/1519-6984.09113...
) and crustaceans (e.g., red freshwater crab Dilocarcinus pagei Stimpson, 1861 and Amazon River prawn Macrobrachium amazonicum (Heller, 1862), analyzed by Azevedo-Santos et al., 2010b Azevedo-Santos VM, Costa NetoEM and Lima-Stripari N 2010. Concepção dos pescadores artesanais que utilizam o reservatório de Furnas, Estado de Minas Gerais, acerca dos recursos pesqueiros: um estudo etnoictiológico. Biotemas, 23(4): 135-145. https://doi.org/10.5007/2175-7925.2010v23n4p135
https://doi.org/10.5007/2175-7925.2010v2...
and Paschoal et al., 2019Paschoal LRP, Oliveira LF, Andrioli GC and Zara FJ 2019. Reproductive biology of Macrobrachium amazonicum (Heller, 1862) populations with distinct phenotypes in Neotropical reservoirs during the “El Niño” event. Marine and Freshwater Research, 70(10): 1465-1479. https://doi.org/10.1071/MF18228
https://doi.org/10.1071/MF18228...
, respectively). Therefore, continuous and long-term monitoring of the aquatic fauna of the Furnas mega reservoir is necessary so that new non-native species are cataloged and possible environmental risks and problems are avoided and/or monitored over time, as is the case for the giant river prawn Macrobrachium rosenbergii (De Man, 1879) (Fig. 1).

Macrobrachium rosenbergii is a species of Asian origin with an amphidromous life cycle (i.e., its larvae depend on brackish water for development) and is currently the most commonly farmed species in freshwater aquaculture worldwide (New et al., 2010New MB, Valenti WC, Tidwell JH, D’Abramo LR and Kutty MN 2010. Freshwater Prawns: Biology and Farming. Oxford, Wiley-Blackwell , 544p.; Oliveira and Santos, 2021Oliveira CDL and Santos LVR 2021. Distribution of the giant river prawn Macrobrachium rosenbergii (De Man, 1879) in Brazil: 43 years after its introduction. Nauplius, 29: e2021007. https://doi.org/10.1590/2358-2936e2021007
https://doi.org/10.1590/2358-2936e202100...
). The giant river prawn exhibits sexual dimorphism and social hierarchy, where large males with hypertrophied chelipeds gain adaptive advantages, such as ease in obtaining resources, in conquering and defending territories and in reproductive success. Males of this species have three distinct morphotypes: blue claw (BC) - dominant males with large bodies that have large blue chelipeds covered by spines, which greatly exceed their body length; orange claw (OC) - subdominant males with intermediate body sizes and orange chelipeds without spines that do not exceed their body length; and small male (SM) - submissive males with small bodies and small translucent and delicate chelipeds (Ra'anan and Sagi, 1985Ra’Anan Z and Sagi A 1985. Alternative mating strategies in male morphotypes of the freshwater prawn Macrobrachium rosenbergii (De Man). The Biological Bulletin, 169(3): 592-601. https://doi.org/10.2307/1541301
https://doi.org/10.2307/1541301...
). In this context, the present report presents some records of the giant river prawn M. rosenbergii in the Furnas mega reservoir over 17 years of continuous monitoring, i.e., without gaps of more than a year. In addition, the possible escape routes and environmental problems caused by this bio-invasion are discussed.

From 2006 to April 2023, bio-invasions have been observed and monitored throughout the flooded area of the Furnas mega reservoir, either through seasonal field collections (monthly, bimonthly or semiannually, i.e., locations were sampled at least twice a year) and/or consensual interviews (at least one interview after encountering the non-native specimen) and reliable photographic documentation (i.e., without evidence of image alteration or manipulation) from professional fisher-people in the region. Animals were verified by active sampling (one collector with a sieve or D-net, which was employed several times along the marginal vegetation and macrophyte banks) and passive collection (traps baited with beef liver or gillnets were placed near the margin, and removed after 24 hr). The first record of M. rosenbergii was documented in 2010 in a stretch of the Grande River portion of the mega reservoir. There was a subsequent gap in records until 2022, when five new occurrences were recorded in the Sapucaí River portion and added to the initial record. All six records of M. rosenbergii in the mega reservoir were of large dominant (BC) males (Fig. 1 and Appendix Appendix Additional information on the occurrence records of Macrobrachium rosenbergii (De Man, 1879) from Furnas mega reservoir between 2010 and 2022. Occurrence Date of capture Section of the reservoir where the specimen was obtained Municipality (district) Coordinates Collector Total length (mm)* Morphotype 1 09.vii.2010 Grande River Formiga (Pontevila district) 20°33’14.4’’S 45°37’36.1”W Raimundo Luiz nm BC 2 10.iii.2022 Sapucaí River Carmo do Rio Claro 20°55’52.0”S 46°08’00.6”W Divino Silva 215.6 BC 3 14.v.2022 Sapucaí River Areado 21°18’57.6”S 46°05’00.6”W Carlos Donizeti nm BC 4 10.vi.2022 Sapucaí River Alfenas 21°23’19.0”S 46°02’30.5”W Nelson Augusto nm BC 5 29.x.2022 Sapucaí River Alfenas (Barranco Alto district) 21°09’27.0”S 45°58’45.5”W Rafael Silva nm BC 6 24.xi.2022 Sapucaí River Carmo do Rio Claro 20°55’06.6”S 46°07’04.1”W Bruno Ribeiro 213.7 BC * : distance between the posterior margin of the ocular orbit to tip of telson BC: blue claw nm: not measured ). These specimens exhibited the key characteristics for the identification of the species (Holthuis and Ng, 2010Holthuis LB and Ng PKL 2010. Nomenclature and Taxonomy. p. 12-17. In: New MB, Valenti WC, Tidwell JH, D’Abramo LR and Kutty MN (Eds.), Freshwater Prawns: Biology and Farming. Oxford, Wiley-Blackwell. ): a long, upward-curving rostrum with a distinct basal crest, chelipeds large and deep bluish in color covered by spines along their length, and a distinct velvety pubescence on the movable finger (Fig. 1). There were no clinical signs of disease caused by viruses or microsporidia in these specimens, as was previously reported in this mega reservoir for other species of the genus (Paschoal et al., 2021Paschoal LRP, Zara FJ, Rocha S, Alves Â, Casal G and Azevedo C. 2021. Ultrastructure of two microsporidians Inodosporus sp. and Myospora sp. co-infecting muscles of the Amazon River prawn Macrobrachium amazonicum (Heller, 1862). Nauplius, 29: e2021046. https://doi.org/10.1590/2358-2936e2021046
https://doi.org/10.1590/2358-2936e202104...
). These animals were captured using gillnets (40 mm), photographed and subsequently were sold or used as bait or consumed by collectors. Due to this, only the BC male observed during the second record of the species in the mega reservoir was deposited in a scientific collection. This prawn was deposited in the Coleção de Crustáceos do Departamento de Biologia (CCDB), da Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, under the catalog number CCDB 7551.

After these occurrence records were obtained, new collections were performed in the same areas to detect the possible establishment of the species. However, no other giant river prawn individuals were found, and only individuals of M. amazonicum were captured at the site, allowing the conclusion that the records described here are accidental escapes. In the Sapucaí River portion, net cage farming is a very frequent activity, and escapes of aquatic organisms in this area are very common (Azevedo-Santos et al., 2011Azevedo-Santos VM, Rigolin-Sá O and Pelicice FM 2011. Growing, losing or introducing? Cage aquaculture as a vector for the introduction of non-native fish in Furnas Reservoir, Minas Gerais, Brazil. Neotropical Ichthyology, 9: 915-919. https://doi.org/10.1590/S1679-62252011000400024
https://doi.org/10.1590/S1679-6225201100...
). In addition, there have been failed and often illegal attempts at combined farming of O. niloticus tilapia and giant river prawn in the Furnas mega reservoir (L.R.P. Paschoal, pers. comm.). It is possible that during pond maintenance and/or harvesting, some individuals of M. rosenbergii escaped to areas far from the original farming area. In addition, the fact that we recorded only BC males in the region reinforces the hypothesis of an escape from an already established, artificial population. As described by New et al. (2000New MB, Valenti WC, Tidwell JH, D’Abramo LR and Kutty MN 2010. Freshwater Prawns: Biology and Farming. Oxford, Wiley-Blackwell , 544p.), BC males are considered the reproducers of the herd and are the most profitable animals for the breeder due to their large bodies when compared to the other morphotypes, which would explain the occurrence of only this morphotype in the mega reservoir.

As suggested by Oliveira and Santos (2021Oliveira CDL and Santos LVR 2021. Distribution of the giant river prawn Macrobrachium rosenbergii (De Man, 1879) in Brazil: 43 years after its introduction. Nauplius, 29: e2021007. https://doi.org/10.1590/2358-2936e2021007
https://doi.org/10.1590/2358-2936e202100...
), monitoring the aquatic environment allows us to understand the status of M. rosenbergii bio-invasions in Brazil. It can be concluded that in the Furnas mega reservoir, the giant river prawn did not present established populations and that accidental escapes of this species occurred without compromising the biota. However, recently, some populations of M. amazonicum was able to colonize several areas of this mega reservoir and the Marechal Mascarenhas de Moraes reservoir below it (Paschoal et al., 2019Paschoal LRP, Oliveira LF, Andrioli GC and Zara FJ 2019. Reproductive biology of Macrobrachium amazonicum (Heller, 1862) populations with distinct phenotypes in Neotropical reservoirs during the “El Niño” event. Marine and Freshwater Research, 70(10): 1465-1479. https://doi.org/10.1071/MF18228
https://doi.org/10.1071/MF18228...
). Thus, we suggest the continuous monitoring of M. rosenbergii in this region, as well as in other areas of recorded occurrence in Brazil. Such action could avoid direct impacts on the aquatic biota, such as the reduction of native populations, local extinctions and transmission of diseases.

ACKNOWLEDGEMENTS

The first author thanks FAPEMIG for the graduate fellowship. FJZ thanks CAPES program [Ciências do Mar II (CIMAR II #1989/2014 proc. 23038.004309/2014-5)], São Paulo Research Foundation (FAPESP) [program #JP 2005/04707-5 and Biota Temático Intercrusta (#2018/13685-5)] and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) [CNPq PQ2# 309298/2020-2]. LRPP was supported by a FAPESP postdoctoral fellowship 2022/09727-0. The helpful comments and suggestions of the anonymous reviewers in reviewing this manuscript are greatly appreciated.

REFERENCES

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    » https://doi.org/10.5007/2175-7925.2010v23n2p199
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    » https://doi.org/10.5007/2175-7925.2010v23n4p135
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    » https://doi.org/10.1590/S1679-62252011000400024
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    » https://doi.org/10.1016/j.jhydrol.2012.07.038
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  • New MB, Valenti WC, Tidwell JH, D’Abramo LR and Kutty MN 2010. Freshwater Prawns: Biology and Farming. Oxford, Wiley-Blackwell , 544p.
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    » https://doi.org/10.1590/2358-2936e2021007
  • ONS [Operador Nacional do Sistema Elétrico] 2023. Reservatórios. Available at https://www.ons.org.br/paginas/energia-agora/reservatorios Accessed on 14 January 2023.
    » https://www.ons.org.br/paginas/energia-agora/reservatorios
  • Paschoal LRP, Andrade DP 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. https://doi.org/10.1590/1519-6984.09113
    » https://doi.org/10.1590/1519-6984.09113
  • Paschoal LRP, Oliveira LF, Andrioli GC and Zara FJ 2019. Reproductive biology of Macrobrachium amazonicum (Heller, 1862) populations with distinct phenotypes in Neotropical reservoirs during the “El Niño” event. Marine and Freshwater Research, 70(10): 1465-1479. https://doi.org/10.1071/MF18228
    » https://doi.org/10.1071/MF18228
  • Paschoal LRP, Zara FJ, Rocha S, Alves Â, Casal G and Azevedo C. 2021. Ultrastructure of two microsporidians Inodosporus sp. and Myospora sp. co-infecting muscles of the Amazon River prawn Macrobrachium amazonicum (Heller, 1862). Nauplius, 29: e2021046. https://doi.org/10.1590/2358-2936e2021046
    » https://doi.org/10.1590/2358-2936e2021046
  • Pereira VA, Rigolin-Sá O, Ribeiro MM and Nogueira DJ 2012. Impactos ambientais e sociais devido à implantação da usina hidrelétrica de Furnas, nos municípios de Passos e São José da Barra - MG. p. 247-278. In: Rigolin-Sá O (Ed.), Bacia Hidrográfica: Estudos do Rio Grande no Sudoeste de Minas Gerais - Brasil. Passos, Edifesp. 1ed.
  • Ra’Anan Z and Sagi A 1985. Alternative mating strategies in male morphotypes of the freshwater prawn Macrobrachium rosenbergii (De Man). The Biological Bulletin, 169(3): 592-601. https://doi.org/10.2307/1541301
    » https://doi.org/10.2307/1541301
  • Rigolin-Sá O 2012. Bacia Hidrográfica: Estudos do Rio Grande no Sudoeste de Minas Gerais - Brasil. Passos, Edifesp , 302p.
  • Wang Y, Xia Z and Wang D 2012. A transitional region concept for assessing the effects of reservoirs on river habitats: a case of Yangtze River, China. Ecohydrology, 5(1): 28-35. https://doi.org/10.1002/eco.186
  • Zoobank:

    http://zoobank.org/urn:lsid:zoobank.org:pub:25C8A5C4-1A63-4765-B976-236ACBAD9C11
  • Consent for publication

    All authors declare that they have reviewed the content of the manuscript and gave their consent to submit the document.
  • Data availability statement

    All data generated and analyzed during this study are presented in this article.
  • Funding and grant disclosures

    São Paulo Research Foundation (FAPESP), Grant/Award Number: #JP 2005/04707-5, Biota Temático Intercrusta #2018/13685-5 and PD fellowship 2022/09727-0; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) program Ciências do Mar II, Grant/Award Number: CIMAR II #1989/2014 proc. 23038.004309/2014-5; Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq, Grant/ Award Number: CNPq PQ2# 309298/2020-2.
  • Study association

    No particular study defined.
  • Study permits

    Field collection and transportation of specimens were made under the SISBIO permit number 87496-1 issued to L.R.P. Paschoal

Appendix

Additional information on the occurrence records of Macrobrachium rosenbergii (De Man, 1879) from Furnas mega reservoir between 2010 and 2022.

Occurrence Date of capture Section of the reservoir where the specimen was obtained Municipality (district) Coordinates Collector Total length (mm)* Morphotype 1 09.vii.2010 Grande River Formiga (Pontevila district) 20°33’14.4’’S 45°37’36.1”W Raimundo Luiz nm BC 2 10.iii.2022 Sapucaí River Carmo do Rio Claro 20°55’52.0”S 46°08’00.6”W Divino Silva 215.6 BC 3 14.v.2022 Sapucaí River Areado 21°18’57.6”S 46°05’00.6”W Carlos Donizeti nm BC 4 10.vi.2022 Sapucaí River Alfenas 21°23’19.0”S 46°02’30.5”W Nelson Augusto nm BC 5 29.x.2022 Sapucaí River Alfenas (Barranco Alto district) 21°09’27.0”S 45°58’45.5”W Rafael Silva nm BC 6 24.xi.2022 Sapucaí River Carmo do Rio Claro 20°55’06.6”S 46°07’04.1”W Bruno Ribeiro 213.7 BC * : distance between the posterior margin of the ocular orbit to tip of telson BC: blue claw nm: not measured

Edited by

Associate Editor:

Fernando Mantelatto

Data availability

All data generated and analyzed during this study are presented in this article.

Publication Dates

  • Publication in this collection
    04 Dec 2023
  • Date of issue
    2023

History

  • Received
    25 Jan 2023
  • Accepted
    23 June 2023
Sociedade Brasileira de Carcinologia Instituto de Biociências, UNESP, Campus Botucatu, Rua Professor Doutor Antônio Celso Wagner Zanin, 250 , Botucatu, SP, 18618-689 - Botucatu - SP - Brazil
E-mail: editor.nauplius@gmail.com