Skip to main content
SpringerLink
Log in

Molecular and morphological evidence of a new species of Crassicutis Manter 1936 (Digenea), a parasite of cichlids in South America

  • Fish Parasitology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

A new species of Crassicutis Manter, 1936 (Digenea: Megaperidae) is described from the intestine of Satanoperca jurupari (Cichlidae) in the Amazon River basin, Brazil. The genus Crassicutis currently contains eight species. Crassicutis manteri n. sp. is morphologically very similar to Crassicutis cichlasomae Manter, 1936, a parasite of cichlids reported from Mexico, the Antilles, and Central and South America. Molecular data revealed that C. cichlasomae represents a species complex in Middle American cichlids. The new species can be readily distinguished from C. cichlasomae sensu lato, and the other congeners, by a combination of morphological traits such as a narrow, elongate mouth opening (versus spherical in other species), the tandem position of testes (symmetrical or oblique in most congeners), narrow body widening towards its posterior end (versus widely oval, leaf-like in other species), and short intestinal caeca ending close to the posterior end of the posterior testis (versus reaching more posteriorly in other species). Six novel sequences of 28S rDNA, ITS1, and cox1 were generated for two isolates of the new species. Sequences of the 28S rRNA gene were used to corroborate that Crassicutis is sister taxa of Homalometron Stafford, 1904. Mitochondrial DNA corroborated the distinction of the new species with previously sequenced congeners in Middle American cichlids; the interspecific divergence between the new species and the genetic lineages of C. cichlasomae was very high, varying between 23.7 and 27.2%. Biogeographical implications of our findings are briefly discussed including questionable validity of records of C. cichlasomae from South America.

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

  • Aguirre-Macedo ML, Scholz T, Gonzáles-Solís D, Vidal-Martinez VM, Posel P, Arjona-Torres G, Dumailo S, Siu-Estrada E (2001) Some adult endohelminths parasitizing freshwater fishes from the Atlantic drainages of Nicaragua. Comp Parasitol 68:190–195

    Google Scholar 

  • Blend CK, Karar YFM, Dronen NO (2017) Revision of Megaperidae Manter, 1934 n. comb. (syn. Apocreadiidae Skrjabin, 1942) including a reorganization of the Schistorchiinae Yamaguti, 1942. Zootaxa 4358:1–44

    Article  PubMed  Google Scholar 

  • Blend CK, Karar YFM, Dronen NO (2019) Case 3775 – Megaperidae Manter, 1934 and Apocreadiinae Skrjabin, 1942 (Platyhelminthes, Digenea): proposed re-establishment of precedence of the older family-group name. Bull Zool Nomencl 76:23–27

    Article  Google Scholar 

  • Bravo-Hollis M, Arroyo G (1962) Trematodes de peces de Costa Rica. I. Sobre dos especies del genero Crassicutis Manter, 1936 (Lepocreadiidae Nicoll, 1914) del intestino de Cichlasoma sp. Rev Biol Trop 10:229–235

    Google Scholar 

  • Bray RA, de Chambrier A, Vaucher C (1996) Crassicutis intermedius (Szidat, 1954) n. comb. and Procaudotestis uruguayensis Szidat, 1954 (Digenea: Homalometridae) from siluriform fishes in Paraguay. Syst Parasitol 35:119–126

    Article  Google Scholar 

  • Bray RA, Waeschenbach A, Cribb TH, Weedall GD, Dyal P, Littlewood DTJ (2009) The phylogeny of the Lepocreadiidae (Platyhelminthes: Digenea) inferred from nuclear and mitochondrial genes: implications for their systematics and evolution. Acta Parasitol 54:310–329

    Article  Google Scholar 

  • Choudhury A, Aguirre-Macedo ML, Curran SS, Ostrowski de Núñez M, Overstreet RM, Pérez-Ponce de León G, Portes Santos C (2016) Trematode diversity in freshwater fishes of the Globe II: ‘New World’. Syst Parasitol 93:271–282

    Article  PubMed  Google Scholar 

  • Cribb T (2005) Family Apocreadiidae Skrjabin, 1942. In: Jones A, Bray R, Gibson DI (eds) Keys to the Trematoda, 2nd edn. CAB International & The Natural History Museum, Wallingford, pp 621–639

    Chapter  Google Scholar 

  • Cribb TH, Bray RA (1999) A review of the Apocreadiidae Skrjabin, 1942 (Trematoda: Digenea) and description of Australian species. Syst Parasitol 44:1–36

    Article  CAS  PubMed  Google Scholar 

  • Curran SS, Tkach VV, Overstreet RM (2013) Molecular evidence for two cryptic species of Homalometron (Digenea: Apocreadiidae) in freshwater fishes of the southeastern United States. Comp Parasitol 80:186–195

    Article  Google Scholar 

  • Cutmore SC, Miller TL, Curran SS, Bennett MB, Cribb TH (2013) Phylogenetic relationships of the Gorgoderidae (Platyhelminthes: Trematoda), including the proposal of a new subfamily (Degeneriinae n. subfam.). Parasitol Res 112:3063–3074

    Article  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dias KG, Müller MI, De Almeida AC, Da Silva RJ, de Azevedo RK, Pérez-Ponce de León G, Abdallah VD (2018) A new species of Wallinia Pearse, 1920 (Digenea: Allocreadiidae) collected from Astyanax fasciatus (Cuvier, 1819) and A. lacustris Lucena and Soares, 2016 (Characiformes: Characidae) in Brazil based on morphology and DNA sequences. Parasitol Res 117:2847–2854

    Article  PubMed  Google Scholar 

  • Dias KA, Pérez-Ponce de León G, Camargo AA, Müller MI, Da Silva RJ, de Azevedo RK, Abdallah VD (2020) A new species of Creptotrematina (Trematoda: Allocreadiidae) from characid fishes of Brazil: morphological and molecular data. J Helminthol 94:E163

    Article  Google Scholar 

  • Dollfus RPH (1950) Trematodes recoltées en Congo belge par le Professeur Paul Brien. Ann Mus Belg Congo 5(1):136

    Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandes BM, Kohn A (2001) On some trematodes parasites of fishes from Paraná River. Braz J Biol 61:461–466

    Article  CAS  PubMed  Google Scholar 

  • Froese R, Pauly D. (Eds) (2020) FishBase. World Wide Web electronic publication. http://www.fishbase.org, version 2019. Accessed 05 Dec 2019

  • Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Guzmán F, Caballero EC (1974) Trematódeos digeneos de peces dulceacuícolas de Nuevo León, México II. Crassicutis bravoae n. sp. de la mojara Cichlasoma cyanoguttatus cyanoguttatus (Baird & Girard). Publ Biol Inst Inv Cient, UANL 1:65–77

    Google Scholar 

  • Kohn A, Fernandes BMM, Cohen SC (2007) South American trematodes parasites of fishes. Fiocruz, Instituto Oswaldo Cruz, Rio de Janeiro, p 318

    Google Scholar 

  • Kullander SO (2003) Family Cichlidae (cichlids). In: Reis RE, Kullander SO, Ferraris C Jr (eds) Check List of the freshwater fishes of South and Central America. Porto Alegre, Edipucrs, pp 605–654

    Google Scholar 

  • Littlewood DT, Rohde K, Clough KA (1997) Parasite speciation within or between host species? – Phylogenetic evidence from site-specific polystome monogeneans. Int J Parasitol 27:1289–1297

    Article  CAS  PubMed  Google Scholar 

  • Littlewood DTJ, Curini-Galletti M, Herniou EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol Phylogenet Evol 16:449–466

    Article  CAS  PubMed  Google Scholar 

  • Luque JL, Pereira FB, Alves PV, Oliva ME, Timi JT (2016) Helminth parasites of South American fishes: current status and characterization as a model for studies of biodiversity. J Helminthol 91:150–164

    Article  PubMed  Google Scholar 

  • Malta JCO (1984) Os peixes de um lago de várzea da Amazônia Central (Lago Janauacá, Rio Solimões) e suas relações com os crustáceos ectoparasitas (Branchiura: Argulidae). Acta Amazon 14:355–372

    Article  Google Scholar 

  • Manter HW (1936) Some trematodes of cenote fish from Yucatan. Carnegie Inst Wash, Pub No 457:33–38

    Google Scholar 

  • Manter HW (1962) Notes on the taxonomy of certain digenetic trematodes of South American freshwater fishes. Proc Helminthol Soc Wash 29:97–102

    Google Scholar 

  • Melo MFC, Santos EGN, Giese EG, Santos JN, Santos CP (2012a) Parasites of Satanoperca jurupari (Osteichthyes: Cichlidae) from Brazil. Parasitol Res 110:389–394

    Article  Google Scholar 

  • Melo MFC, Dos Santos JN, Santos CP (2012b) Sciadicleithrum juruparii n. sp. (Monogenea: Ancyrocephalidae) from the gills of Satanoperca jurupari (Heckel) (Osteichthyes: Cichlidae) in the Guamá River, Amazon Delta, Brazil. Syst Parasitol 82:125–129

    Article  Google Scholar 

  • Moravec F, Baruš V (1972) Studies on parasitic worms from Cuban fishes. Acta Soc Zool Bohemoslov 35:56–74

    Google Scholar 

  • Moszczynska A, Locke SA, McLaughlin JD, Marcogliese DJ, Crease TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Mol Ecol Resour 9:75–82

    Article  CAS  PubMed  Google Scholar 

  • Oliveira MSBD, Gonçalves RA, Neves LR, Ferreira DO, Tavares-Dias M (2017) Ectoparasite community in Satanoperca jurupari (Cichlidae) from the Jari River, a tributary from Amazon River in Northern Brazil. Rev Bras Parasitol Vet 26:136–142

    Article  PubMed  Google Scholar 

  • Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DT (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755

    Article  CAS  PubMed  Google Scholar 

  • Ostrowski de Núñez M, Arredondo NJ, Gil de Pertierra AA (2017) Adult trematodes (Platyhelminthes) of freshwater fishes from Argentina: a checklist. Rev Suisse Zool 124:91–113

    Google Scholar 

  • Overstreet RM (1976) A redescription of Crassicutis archosargi, a digenean exhibiting an unusual tegumental attachment. J Parasitol 62:702–708

    Article  CAS  PubMed  Google Scholar 

  • Pantoja C, Scholz T, Luque JL, Jones A (2018) New genera and species of paramphistomes (Digenea: Paramphistomoidea: Cladorchiidae) parasitic in fishes from the Amazon basin in Peru. Syst Parasitol 95:611–624

    Article  PubMed  Google Scholar 

  • Pantoja C, Scholz T, Luque JL, Jones A (2019) First molecular assessment of the interrelationships of cladorchiid digeneans (Digenea: Paramphistomoidea), parasites of Neotropical fishes, including descriptions of three new species and new host and geographical records. Folia Parasitol 66:011

    Article  CAS  Google Scholar 

  • Parker JH, Curran SS, Overstreet RM, Tkach VV (2010) Examination of Homalometron elongatum Manter, 1947 and description of a new congener from Eucinostomus currani Zahuranec, 1980 in the Pacific Ocean off Costa Rica. Comp Parasitol 77:154–163

    Article  Google Scholar 

  • Paschoal F, Scholz T, Tavares-Dias M, Luque JL (2016) Dactylogyrids (Monogenea) parasitic on cichlids from northern Brazil, with description of two new species of Sciadicleithrum and new host and geographical records. Acta Parasitol 6:158–164

    Google Scholar 

  • Pearse AS (1920) The fishes of Lake Valencia, Venezuela. University of Wisconsin Studies (12) Science 1: 28–51

  • Pérez-Ponce de León G, Hernández-Mena DI (2019) Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ tree of life. J Helminthol 93:260–276

    Article  PubMed  Google Scholar 

  • Pérez-Ponce de León G, García-Prieto L, Mendoza-Garfias B (2007) Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534:1–247

    Article  Google Scholar 

  • Pérez-Ponce de León G, Razo-Mendivil U, Rosas-Valdez R, Mendoza-Garfias B, Mejía-Madrid H (2008) Description of a new species of Crassicutis Manter, 1936, parasite of Cichlasoma beani Jordan (Osteichthyes: Cichlidae) in Mexico, based on morphology and sequences of the ITS1 and 28S ribosomal RNA genes. J Parasitol 94:257–263

    Article  PubMed  Google Scholar 

  • Pérez-Ponce de León G, Razo-Mendivil U, García-Magaña L (2012) Morphological and molecular evidences for the existence of two new species of Homalometron (Digenea: Apocreadiidae), parasites of cichlids (Osteichthyes: Cichlidae). Zootaxa 3407:37–48

    Article  Google Scholar 

  • Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, Sundberg P, Thollesson M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol Phylogenet Evol 48:369–371

    Article  CAS  Google Scholar 

  • Pulis EE, Curran SS, Andres MJ, Overstreet RM (2014) Change in rank of Megaperidae (Trematoda) to Megaperinae within the Apocreadiidae and description of Haintestinum amplum n. g., n. sp. Parasitol Int 63:269–274

    Article  PubMed  Google Scholar 

  • Razo-Mendivil U, Vásquez-Domínguez E, Rosas-Valdez R, Pérez-Ponce de León G, Nadler S (2010) Phylogenetic analysis of nuclear and mitochondrial DNA reveals a complex of cryptic species in Crassicutis cichlasomae (Digenea: Apocreadiidae), a parasite of Middle-American cichlids. Int J Parasitol 40:471–486

    Article  CAS  PubMed  Google Scholar 

  • Razo-Mendivil U, Vázquez-Domínguez E, Pérez-Ponce de León G (2013) Discordant genetic diversity and geographic patterns between Crassicutis cichlasomae (Digenea: Apocreadiidae) and its cichlid host, “Cichlasoma” urophthalmus (Osteichthyes: Cichlidae), in Middle-America. J Parasitol 99:978–988

    Article  CAS  PubMed  Google Scholar 

  • Reis RE, Albert JS, Di Dario F, Mincarone MM, Petry P, Rocha LA (2016) Fish biodiversity and conservation in South America. J Fish Biol 89:12–47

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Ortíz B, García-Prieto L, Herrera-Vázquez J, Pérez-Ponce de León G (2004) Checklist of the helminth parasites of vertebrates in Costa Rica. Rev Biol Trop 52:313–354

    Article  PubMed  Google Scholar 

  • Scholz T, Vargas-Vásquez J, Moravec F, Vivas-Rodríguez C, Mendoza-Franco E (1995a) Cenotes (sinkholes) of the Yucatán Peninsula, Mexico, as habitat of adult trematodes of fish. Folia Parasitol 42:37–47

    CAS  Google Scholar 

  • Scholz T, Pech-Ek MCF, Rodriguez-Canul R (1995b) Biology of Crassicutis cichlasomae, a parasite of cichlid fishes in Mexico and Central America. J Helminthol 69:69–75

    Article  CAS  PubMed  Google Scholar 

  • Snyder SD, Tkach VV (2001) Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). J Parasitol 87:1433–1440

    Article  CAS  PubMed  Google Scholar 

  • Tavares-Dias M, Oliveira MSB, Gonçalves RA, Neves LR (2017) Parasitic diversity of a wild Satanoperca jurupari population, an ornamental cichlid in the Brazilian Amazon. Acta Amazon 47:155–162

    Article  Google Scholar 

  • Van Steenkiste N, Locke SA, Castelin M, Marcogliese DJ, Abbott CL (2015) New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Mol Ecol Resour 15:945–952

    Article  Google Scholar 

  • Vidal-Martínez V, Aguirre-Macedo L, Scholz T, González-Solís D, Mendoza-Franco E (2001) Atlas of the helminth parasites of cichlid fish of Mexico. Academia, Praha, Czech Republic, p 165

    Google Scholar 

  • Vinjoy M, Prieto A, Fajer E, Cartaya E (1985) Presencia de Crassicutis sp. (Trematoda: Allocreadidae) en el tracto intestinal de la biajaca (Cichlasoma tetracanthum) en Cuba. Revista Salud Anim 7:287–290

    Google Scholar 

  • Watson DE (1976) Digenea of fishes from Lake Nicaragua. In Investigations of the Ichthyofauna of Nicaraguan Lakes, Thorson, TR (ed.), School of Life Sciences, University of Nebraska, Lincoln, pp. 251–260

  • Yamada FH, Takemoto RM, Bellay S, Pavanelli GC (2009) Two new species of Sciadicleithrum (Monogenea: Dactylogyridae) parasites of Neotropical cichlid fishes from the Paraná River, Brazil. Acta Parasitol 54:6–9

    Article  Google Scholar 

Download references

Acknowledgements

The authors are indebted to Marcos Sidney Brito Oliveira (UNIFAP) and Marcos Tavares (Embrapa Amapá) for their invaluable help with sampling. We thank Ulises Razo-Mendivil for the design of specific cox1 primers and providing unpublished cox1 sequences of some specimens of Crassicutis from Mexico and Guatemala. We thank Marcelo Knoff, curator of the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC), for sending photos of voucher specimens of Crassicutis cichlasomae from Brazil. We also thank Olena Kudlai (Nature Research Centre, Vilnius, Lithuania) and Tom Cribb (University of Queensland, Brisbane, Australia) for providing us with valuable literature.

Funding

This study was financially supported by the Institute of Parasitology, BC CAS (RVO 60077344), by AGEVAP – Comitê da Bacia Hidrográfica Guandu (n° 09/2015), by Conselho Nacional de Desenvolvimento Científco e Tecnológico, Brazil (CNPq) to José L. Luque, and also partially funded by the Consejo Nacional de Ciencia y Tecnología, México (CONACyT No. A1-S-21694) and the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT-UNAM IN212621) to G.P.P.L.

Author information

Authors and Affiliations

  1. Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Camila Pantoja & Tomás Scholz

  2. Institute of Ecology, Nature Research Centre, Akademijos 2, 08412, Vilnius, Lithuania

    Camila Pantoja

  3. Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil

    José Luis Luque

  4. Escuela Nacional de Estudios Superiores Unidad Mérida (ENES-Mérida), Universidad Nacional Autónoma de México, Km. 4.5 carretera Mérida-Tétiz, Municipio de Ucú, C.P 97357, Yucatán, México

    Gerardo Perez-Ponce deLeón

Authors
  1. Camila Pantoja
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomás Scholz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. José Luis Luque
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gerardo Perez-Ponce deLeón
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gerardo Perez-Ponce deLeón.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Section Editor: Federica Marcer

Publisher’s note

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

Supplementary Information

ESM 1

(DOC 94 kb)

ESM 2

(DOC 82 kb)

ESM 3

(DOC 178 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pantoja, C., Scholz, T., Luque, J.L. et al. Molecular and morphological evidence of a new species of Crassicutis Manter 1936 (Digenea), a parasite of cichlids in South America. Parasitol Res 120, 2429–2443 (2021). https://doi.org/10.1007/s00436-021-07161-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-021-07161-4

Keywords

Search

Navigation