Skip to main content
SpringerLink
Log in

First record of parasitism by Probopyrus pandalicola (Isopoda, Bopyridae) on the freshwater prawn Macrobrachium acanthurus (Decapoda, Palaemonidae) and ecological interactions

  • Original Article
  • Published:
Journal of Parasitic Diseases Aims and scope Submit manuscript

Abstract

In this study, we aimed to record, for the first time, parasitic infestation by the isopod Probopyrus pandalicola on the prawn Macrobrachium acanthurus, as well as to register some ecological interactions. We hypothesized that the parasitic infection is able to negatively affect the prawn’s nutritional condition and that this interaction can modify growth relationships in male individuals. We collected both parasitized (n = 25) and parasite-free (n = 25) individuals in several locations of the Contas River, state of Bahia, Brazil, which had their morphometric characteristics determined, including of the parasites. Relative growth models were constructed for both groups in order to compare slopes and intercepts and determine if the growth patterns are modified by the parasite. We also determined the body condition of the prawns, which was also compared between the two groups. Our results clearly demonstrated that the parasitic infection is able to induce modifications in relative growth patterns in male individuals and that this isopod is capable of reducing the nutritional condition of the prawns. This study indicates that this parasite can induce deleterious effects in the prawn, but individually. Further studies should be conducted to assess the relevance of our findings in conservation and management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abu-Hakima R (1984) Preliminary observations on the effects of Epipenaeon elegans Chopra (Isopoda; Bopyridae) on reproduction of Penaeus semisulcatus de Haan (Decapoda; Penaeidae). Int J Invertebr Reprod Dev 7(1):51–62

    Google Scholar 

  • Anderson G (1990) Postinfection mortality of Palaemonetes spp. (Decapoda: Palaemonidae) following experimental exposure to the bopyrid isopod Probopyrus pandalicola (Packard)(Isopoda: Epicaridea). J Crustacean Biol 10(2):284–292

    Google Scholar 

  • Andrade JM, Estévez-Pérez MG (2014) Statistical comparison of the slopes of two regression lines: a tutorial. Anal Chim Acta 838:1–12

    CAS  PubMed  Google Scholar 

  • Bass CS, Weis JS (1999) Behavioral changes in the grass shrimp, Palaemonetes pugio (Holthuis), induced by the parasitic isopod, Probopyrus pandalicola (Packard). J Exp Mar Biol Ecol 241(2):223–233

    Google Scholar 

  • Beck JT (1980a) The effects of an isopod castrator, Probopyrus pandalicola, on the sex characters of one of its caridean shrimp hosts, Palaemonetes paludosus. Biol Bull 158(1):1–15

    Google Scholar 

  • Beck JT (1980b) Larval and adult habitats of a branchial bopyrid Probopyrus pandalicola on one of its freshwater shrimp hosts Palaemonetes paludosus. Crustaceana 38(3):265–270

    Google Scholar 

  • Becker DJ, Streicker DG, Altizer S (2015) Linking anthropogenic resources to wildlife–pathogen dynamics: a review and meta-analysis. Ecol Lett 18(5):483–495

    PubMed  PubMed Central  Google Scholar 

  • Bertini G, Baeza JA, Perez E (2014) A test of large-scale reproductive migration in females of the amphidromous shrimp Macrobrachium acanthurus (Caridea: Palaemonidae) from south-eastern Brazil. Mar Freshw Res 65(1):81–93

    Google Scholar 

  • Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the Cost of Mounting an Immune Response. Am Nat 161(3):367–379

    PubMed  Google Scholar 

  • Boxshall G, Lester R, Grygier MJ, Hoeg JT, Glenner H, Shields JD, Lützen J (2005) Crustacean parasites. Rohde K.

  • Calado R, Vitorino A, Dinis MT (2006) Bopyrid isopods do not castrate the simultaneously hermaphroditic shrimp Lysmata amboinensis (Decapoda: Hippolytidae). Dis Aquat Org 73(1):73–76

    Google Scholar 

  • Calado R, Bartilotti C, Goy JW, Dinis MT (2008) Parasitic castration of the stenopodid shrimp Stenopus hispidus (Decapoda: Stenopodidae) induced by the bopyrid isopod Argeiopsis inhacae (Isopoda: Bopyridae). J Mar Biol Assoc U K 88(2):307–309

    Google Scholar 

  • Cash CE, Bauer RT (1993) Adaptations of the branchial ectoparasite Probopyrus pandalicola (Isopoda: Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio (Caridea: Palaemonidae). J Crustacean Biol 13(1):111–124

    Google Scholar 

  • Chaplin-Ebanks SA, Curran MC (2007) Prevalence of the bopyrid isopod Probopyrus pandalicola in the grass shrimp, Palaemonetes pugio, in four tidal creeks on the South Carolina-Georgia coast. J of Parasitol 93(1):73–77

    Google Scholar 

  • Choi JH, Jamieson G, Han KH, Hung SY (2004) Parapenaeon consolidatum (Isopoda: Bopyridae) and the relative growth and reproduction of Metapenaeopsis dalei (Decapoda: Penaeidae) in South Korea. J Shellfish Res 23(1):237–243

    Google Scholar 

  • Choudhury PC (1971) Complete larval development of the palaemonid shrimp Macrobrachium carcinus (L.), reared in the laboratory (Decapoda, Palaemonidae). Crustaceana 20(1):51–69

    Google Scholar 

  • Coelho PA (1963) Observações preliminares sobre a biologia e a pesca dos camarões do gênero Macrobrachium Bate, 1868 (Decapoda Palaemonidae) no Estado de Pernambuco. Brasil. Trabs. IO Univ. Recife 3:75–81

    Google Scholar 

  • Coelho PA, Ramos-Porto M (1984) Camarões de água doce do Brasil: distribuição geográfica. Revista brasileira de Zoologia 2(6):405–410

    Google Scholar 

  • Collart OO (1990) Interactions Entre Le Parasite Probopyrus Bithynis (Isopoda, Bopyridae) Et L’Un De Ses Hôtes, La Crevette Macrobrachium Amazonicum (Decapoda, Palaemonidae). Crustaceana 58(3):258–269

    Google Scholar 

  • Conner SL, Bauer RT (2010) Infection of adult migratory river shrimps, Macrobrachium ohione, by the branchial bopyrid isopod Probopyrus pandalicola. Invertebr Biol 129(4):344–352

    Google Scholar 

  • de Barros MSF, dos Santos Calado TC (2020) Plastic ingestion lead to reduced body condition and modified diet patterns in the rocky shore crab Pachygrapsus transversus (Gibbes, 1850)(Brachyura: Grapsidae). Mar Pollut Bull 156:111249

    PubMed  Google Scholar 

  • de Barros MSF, dos Santos Calado TC, dos Santos EV, Silva AS, de Andrade Albuquerque LG (2020) Population biology and sexual dimorphism in the freshwater prawn Atya scabra (Decapoda: Atyidae) in the De Contas River, Bahia. Brazil. Revista de Biología Tropical 68(3):743–751

    Google Scholar 

  • Dumbauld BR, Chapman JW, Torchin ME, Kuris AM (2011) Is the collapse of mud shrimp (Upogebia pugettensis) populations along the Pacific coast of North America caused by outbreaks of a previously unknown bopyrid isopod parasite (Orthione griffenis)? Estuar Coasts 34(2):336–350

    Google Scholar 

  • Eraud C, Duriez O, Chastel O, Faivre B (2005) The energetic cost of humoral immunity in the Collared Dove, Streptopelia decaocto: is the magnitude sufficient to force energy-based trade-offs? Funct Ecol 19(1):110–118

    Google Scholar 

  • Felten V, Guerold F (2001) Hyperventilation and loss of hemolymph Na+ and Cl-in the freshwater amphipod Gammarus fossarum exposed to acid stress: a preliminary study. Dis Aquat Organ 45(1):77–80

    CAS  PubMed  Google Scholar 

  • Fingerman M (1997) Roles of neurotransmitters in regulating reproductive hormone release and gonadal maturation in decapod crustaceans. Invertebr Reprod Dev 31(1–3):47–54

    CAS  Google Scholar 

  • Froese R (2006) Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22(4):241–253

    Google Scholar 

  • Gamba AL (1982) Macrobrachium: its presence in estuaries of the northern Venezuelan coast (Decapoda, Palaemonidae). Caribb J Sci 18(1–4):23–28

    Google Scholar 

  • García-Guerrero M, de los Santos Romero R, Vega-Villasante F, Cortes-Jacinto E (2015) Conservation and aquaculture of native freshwater prawns: the case of the cauque river prawn Macrobrachium americanum (Bate, 1868). Lat Am J Aquat Res 43(5):819–827

    Google Scholar 

  • Ghai RR, Fugere V, Chapman CA, Goldberg TL, Davies TJ (2015) Sickness behaviour associated with non-lethal infections in wild primates. Proc R Soc B Biol Sci 282(1814):20151436

    Google Scholar 

  • Hua J, Wuerthner VP, Jones DK, Mattes B, Cothran RD, Relyea RA, Hoverman JT (2017) Evolved pesticide tolerance influences susceptibility to parasites in amphibians. Evol Appl 10(8):802–812

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lester RJG (2005) Crustacean parasites. Marine parasitology. University of New England, Sidney, pp 123–169

    Google Scholar 

  • Maciel CR, Valenti WC (2009) Biology, fisheries, and aquaculture of the Amazon River prawn Macrobrachium amazonicum: a review. Nauplius 17(2):61–79

    Google Scholar 

  • Markham JC (1985) A review of the bopyrid isopods infesting caridean shrimps in the northwestern Atlantic Ocean, with special reference to those collected during the Hourglass Cruises in the Gulf of Mexico. Florida Department of Natural Resources, Bureau Of Marine Research, St. Petersburg, Florida

    Google Scholar 

  • Morris JA (1948) Studies on the Host-parasite Relationship of Probopyrus Pandalicola (Packard). (No. 8). Catholic University of America Press

  • Neves CA, Santos EA, Bainy ACD (2000) Reduced superoxide dismutase activity in Palaemonetes argentinus (Decapoda, Palemonidae) infected by Probopyrus ringueleti (Isopoda, Bopyridae). Dis Aquat Org 39(2):155–158

    CAS  Google Scholar 

  • New MB, D’Abramo LR, Valenti WC, Singholka S (2000) Sustainability of freshwater prawn culture. Freshwater Prawn Culture: The Farming of Macrobrachium rosenbergii. Blackwell, Oxford, pp 429–434

    Google Scholar 

  • Nilsson J, Granbom M, Råberg L (2007) Does the strength of an immune response reflect its energetic cost? J Avian Biol 38(4):488–494

    Google Scholar 

  • Ninawe AS, Selvin J (2009) Probiotics in shrimp aquaculture: avenues and challenges. Crit Rev Microbiol 35(1):43–66

    CAS  PubMed  Google Scholar 

  • Oliveira E, da Silva Castagini A, Masunari S (2000) The population structure of Probopyrus floridensis (Isopoda, Bopyridae), a parasite of Macrobrachium potiuna (Decapoda, Palaemonidae) from the Perequê River, Paranaguá Basin, southern Brazil. Crustaceana 73(9):1095–1108

    Google Scholar 

  • Ostfeld RS, Glass GE, Keesing F (2005) Spatial epidemiology: an emerging (or re-emerging) discipline. Trends Ecol Evol 20(6):328–336

    PubMed  Google Scholar 

  • Román-Contreras R (1996) A new species of Probopyrus (Isopoda, Bopyridae), parasite of Macrobrachium americanum Bate, 1868 (Decapoda, Palaemonidae). Crustaceana 69(2):204–210

    Google Scholar 

  • Sánchez CA, Becker DJ, Teitelbaum CS, Barriga P, Brown LM, Majewska AA et al (2018) On the relationship between body condition and parasite infection in wildlife: a review and meta-analysis. Ecol Lett 21(12):1869–1884

    PubMed  Google Scholar 

  • Sherman MB, Curran MC (2013) The effect of the bopyrid isopod Probopyrus pandalicola (Packard, 1879)(Isopoda, Bopyridae) on the survival time of the daggerblade grass shrimp Palaemonetes pugio Holthuis, 1949 (Decapoda, Palaemonidae) during starvation at two different temperatures. Crustaceana 86(11):1328–1342

    Google Scholar 

  • Sherman MB, Curran MC (2015) Sexual sterilization of the daggerblade grass shrimp Palaemonetes pugio (Decapoda: Palaemonidae) by the bopyrid isopod Probopyrus pandalicola (Isopoda: Bopyridae). J Parasitol 101(1):1–5

    PubMed  Google Scholar 

  • Smith AE, Chapman JW, Dumbauld BR (2008) Population structure and energetics of the bopyrid isopod parasite Orthione griffenis in mud shrimp Upogebia pugettensis. J Crustacean Biol 28(2):228–233

    Google Scholar 

  • SRH – Secretaria de Recursos Hídricos (2007) Resolução No 20, de 23 de Agosto de 2007. http://www.semarh.ba.gov.br/Legislacao/RESOLUCAOCONERH/CONERHn20prorrogaprazoContas.pdf. Accessed 27 Sep 2020

  • Subramoniam T (2011) Mechanisms and control of vitellogenesis in crustaceans. Fish Sci 77(1):1–21

    CAS  Google Scholar 

  • Swetha CH, Sainath SB, Reddy PR, Reddy PS (2011) Reproductive endocrinology of female crustaceans: perspective and prospective. J Mar Sci Res Dev S 3:1–13

    Google Scholar 

  • Thompson RK (1980) Aquaculture of Macrobrachium rosenbergii in Mauritius commercial production of juveniles. In: Giant Prawn 1980: an international conference on Macrobrachium (Freshwater Prawn) Farming, Bangkok (Thailand), 15–21 Jun 1980

  • Valenti WC, Mello JD, Lobão VL (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(7):1256–1262

    Google Scholar 

  • Van Wyk PM (1982) Inhibition of the growth and reproduction of the porcellanid crab Pachycheles rudis by the bopyrid isopod Aporobopyrus muguensis. Parasitol 85(3):459–473

    Google Scholar 

  • Vargas-Ceballos MA, López-Uriarte E, García-Guerrero MU, Vega-Villasante F, Román-Contreras R, Akintola SL et al (2016) Infestation of Probopyrus pacificensis (Isopoda: Bopyridae) in Macrobrachium tenellum (Caridea: Palaemonidae) in the Ameca River, Jalisco, Mexico: prevalence and effects on growth. Pan-Am J Aquat Sci 11(1):39–46

    Google Scholar 

  • Vinagre AS, Chung JS (2016) Effects of starvation on energy metabolism and crustacean hyperglycemic hormone (CHH) of the Atlantic ghost crab Ocypode quadrata (Fabricius, 1787). Mar Biol 163(1):3

    Google Scholar 

  • Walker SP (1977) Probopyrus pandalicola: discontinuous ingestion of shrimp hemolymph. Exp Parasitol 41(1):198–205

    CAS  PubMed  Google Scholar 

  • Wu L, Dong S, Jiang Z (2004) Research advances in ecophysiological effects of starvation on crustacean. J Appl Ecol 15(4):723

    Google Scholar 

  • Williams JD, Boyko CB (2012) The global diversity of parasitic isopods associated with crustacean hosts (Isopoda: Bopyroidea and Cryptoniscoidea). PLoS One 4:e35350

    Google Scholar 

  • Zar JH (2010) Biostatistical analysis. Pearson Prentice-Hall, Upper Saddle River, NJ

    Google Scholar 

Download references

Funding

This research was not supported by funding.

Author information

Authors and Affiliations

  1. Laboratório de Ecologia de Peixes e Pesca (LAEPP) da Universidade Federal de Alagoas, Instituto de Ciências Biológicas e da Saúde, Maceió, Brazil

    Matheus Souza Ferreira de Barros

  2. Laboratórios Integrados de Ciências do Mar e Naturais da Universidade Federal de Alagoas, Setor de Crustáceos, Maceió, Brazil

    Luiz Soares da Silva Neto & Tereza Cristina dos Santos Calado

Authors
  1. Matheus Souza Ferreira de Barros
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luiz Soares da Silva Neto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tereza Cristina dos Santos Calado
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matheus Souza Ferreira de Barros.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Barros, M.S.F., da Silva Neto, L.S. & Calado, T. First record of parasitism by Probopyrus pandalicola (Isopoda, Bopyridae) on the freshwater prawn Macrobrachium acanthurus (Decapoda, Palaemonidae) and ecological interactions. J Parasit Dis 45, 273–278 (2021). https://doi.org/10.1007/s12639-020-01306-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12639-020-01306-5

Keywords

Search

Navigation