Open-access Redescription of the fish-parasitic isopod Cymothoa ianuarii Schioedte & Meinert, 1884 and further records of C.lexcisa Perty, 1833 and C. oestrum (Linnaeus, 1758) (Isopoda: Cymothoida: Cymothoidae) from Brazil

Abstract

Cymothoa ianuariiSchioedte & Meinert, 1884 is rediscovered almost 136 years after its original description and redescribed from specimens collected in the state of São Paulo. This species is mainly characterized by adult females with cephalon with conspicuous eyes and not deeply immersed in pereonite 1, pereonites 5-6 much wider than 4, pleotelson twice as wide as long and pleopods 1-5 decreasing in size; Cymothoa excisaPerty, 1833 and C. oestrum (Linnaeus, 1758) are recorded from the state of Bahia. Illustrations and an updated distribution map for these species in Brazil are provided.

Keywords.
Distribution; Parasitic crustaceans; Taxonomy; Fishes; Cymothoid

INTRODUCTION

Species of Cymothoidae Leach, 1818 are distributed worldwide, except in polar waters, and are known to be obligate fish parasites (Trilles, 1994; Smit et al., 2014; Hata et al., 2017). Cymothoids are represented by 42 genera and about 366 species and are characterized by the hematophagous life-style and protandry (Boyko et al., 2008; Poore & Bruce, 2012; Smit et al., 2014). The genus CymothoaFabricius, 1793 comprises 51 species usually found infesting the tongue of the host fish (Smit et al., 2014). In Brazil, nine species of Cymothoa have been recorded (Thatcher, 2000; Thatcher et al., 2003; Thatcher & Fonseca, 2005; Thatcher et al., 2007; Luque et al., 2013). In a comparative study, Thatcher et al. (2003) analyzed all these species, providing the redescription of Cymothoa excisaPerty, 1833 and C. oestrum (Linnaeus, 1758). However, for C. ianuariiSchioedte & Meinert, 1884, Thatcher et al. (2003) pointed that no records were found since its original description and the type-material could be apparently lost, but the authors have no evidence as to why they concluded it. Consequently, the redescription of the species was not possible due to the absence of any material. Taxonomic studies of cymothoid isopods can be complicated given past mistake identifications, poor descriptions and redescriptions and lack of type-material. In addition, the intra-specific variation can be confounded with interspecific differences (Smit et al., 2014). In the present contribution, we provide new records of three species of Cymothoa from Brazilian waters and the redescription of C. ianuarii based on material collected in past years. New illustrations and an updated distribution map for these species in Brazil are also provided.

MATERIAL AND METHODS

The material examined is stored in ethanol 70% and deposited in the Carcinological Collection of the Departamento de Zoologia of the Universidade Federal do Rio Grande do Sul (UFRGS) and in the Museu de Ciências e Tecnologia of the Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, state of Rio Grande do Sul, Brazil (MCP). Specimens were examined under a stereomicroscope Nikon SMZ800 and the illustrations were obtained with the aid of a camera lucida. Distribution map in Brazil was elaborated using the software Arcview 9.3 program (ESRI, 2009). Morphological description and terminology follows Thatcher et al. (2003) and Hadfield et al. (2013). For each specimen, we measured the total length and width and the pleotelson length and width. For a complete list of synonyms consult Trilles (1994).

RESULTS

Taxonomy

Order Isopoda Latreille, 1817

Suborder Cymothoida Wägele, 1989

Family Cymothoidae Leach, 1818

Genus Cymothoa Fabricius, 1793

CymothoaFabricius, 1793: 503. Milne Edwards, 1840: 264. Schioedte & Meinert, 1884: 223. Kussakin, 1979: 289. Brusca, 1981: 185. Brusca & Iverson, 1985: 45. Trilles, 1994: 137. Thatcher et al., 2003: 342. Hadfield et al., 2011: 58. Hadfield et al., 2013: 153. Martin et al., 2016: 5.

Type species:Oniscus oestrumFabricius, 1793; by subsequent designation (Kussakin, 1979).

Diagnosis:Hadfield et al. (2011, 2013).

Remarks: In Brazil, this genus encompass nine species distributed along the coast: Cymothoa brasiliensisSchioedte & Meinert, 1884, C. catarinensisThatcher, Loyola e Silva, Jost & Souza-Conceição, 2003, C. excisa, C. exiguaSchioedte & Meinert, 1884, C. gerrisSchioedte & Meinert, 1884, C. ianuarii, C. liannaeSartor & Pires, 1988, C. oestrum and C. spinipalpaThatcher, de Araujo, de Lima & Chellapa, 2007 (Thatcher, 2000; Thatcher et al., 2003; Thatcher & Fonseca, 2005; Thatcher et al., 2007; Luque et al., 2013).

Cymothoa excisa Perty, 1833

(Figs. 1, 6; Table 1)

Figure 1
Cymothoa excisaPerty, 1833 (MCP 2996): (A) habitus dorsal view; (B) habitus ventral view; (C) habitus lateral view; (D) cephalon frontal view. Scale bar: A-C = 5 mm; D = 2.5 mm.

Figure 2
Cymothoa ianuariiSchioedte & Meinert, 1884 (UFRGS 6516): (A) habitus dorsal view (UFRGS 6516); (B) habitus ventral view (UFRGS 6516); (C) habitus lateral view (UFRGS 6516); (D) cephalon frontal view (UFRGS 6516); (E) pleotelson dorsal view (UFRGS 6520). Scale bar: A-C = 5 mm; D = 2.5 mm; E = 1 mm.

Figure 3
Cymothoa ianuariiSchioedte & Meinert, 1884: (A) antennule (UFRGS 6516); (B) apical article of antennule (UFRGS 6516); (C) antenna (UFRGS 6516); (D) mandible (UFRGS 6515); (E) maxilulle (UFRGS 6520); (F) apex of maxillula (UFRGS 6520); (G) maxilla (UFRGS 6515); (H) maxilla distal portion (UFRGS 6515); (I) maxilliped with oostegite (UFRGS 6515); (J) maxilliped articles 2 and 3 (UFRGS 6515). Scale bar: A, C and D = 0.5 mm; E and G = 0.3 mm; B = 0.125 mm; F, H and J = 0.1 mm; I = 1 mm.

Figure 4
Cymothoa ianuariiSchioedte & Meinert, 1884 (UFRGS 6516): (A-G) pereopods 1-7; (H-J) pleopods 1-5 dorsal view; (M) uropod. Scale bar: E-G = 2 mm; A-D, H-J = 1 mm; D = 2.5 mm; M = 0.5 mm.

Figure 5
Cymothoa oestrum (Linnaeus, 1758) (MCP 2999): (A) habitus dorsal view; (B) habitus ventral view; (C) habitus lateral view; (D) cephalon frontal view. Scale bar: A-C = 5 mm; D = 2.5 mm.

Figure 6
Map with the records of Cymothoa excisa (▲), C. ianuarii (▄) and C. oestrum (●) in Brazil. Symbols in dark gray indicate literature records and white indicates new records. Abbreviations: PA = Pará; MA = Maranhão; PE = Pernambuco; SE = Sergipe; BA = Bahia; RJ = Rio de Janeiro; SP = São Paulo; SC = Santa Catarina.

Table 1
Measurements (mm) of analyzed female specimens of Cymothoa spp.

Restricted synonymy:Cymothoa excisaPerty, 1833: 211, tab. 40, fig. 11. Coelho & Koenig, 1972: 1976, table 1. Trilles 1994: 141. Thatcher et al., 2003: 545, figs. 27-51. Luque et al., 2013: 1454.

Material examined: BRAZIL: Bahia: one ovigerous female, Candeias, coll. J. Pezzi da Silva, 11/V/2010 (MCP 2996); two ovigerous females, Candeias, coll. J. Pezzi da Silva, 11/V/2010 (MCP 2997) [illustrated].

Remarks:Cymothoa excisa was most recently diagnosed by Thatcher et al. (2003). The species had already been recorded from northeastern Brazil, in the states of Maranhão, Pernambuco and Sergipe by Coelho & Koenig (1972). These authors also raised the possibility of the occurrence in the states of Piauí, Ceará, Rio Grande do Norte, Paraíba, Alagoas, Bahia and Espírito Santo, the latter in the southeastern Brazil. In addition, the occurrence of this species was also recorded in the states of Pará (Monod, 1969) and Rio de Janeiro (Richardson, 1901). This is the first record for the state of Bahia, particularly in the northern portion (12°44′49″S 38°29′38″W). The southernmost record of C. excisa in western South Atlantic is La Plata (Argentina) (Gerstaecker, 1901). Cymothoa excisa was redescribed by Thatcher et al. (2003) based on material from the Florianopolis Island, state of Santa Catarina, southern Brazil. Females are distinguished mainly by the acute anterolateral angles of pereonite 1 reaching or surpassing the eyes; the truncate cephalon, deeply immersed in pereonite 1; eyes present but inconspicuous; pereonites 4-6 subequal in width; pleon deeply immersed in pereonite 7 (Fig. 1); and pleopods trilaminate (Thatcher et al., 2003). Males are similar to females, but smaller and with pleopod 2 lacking an appendix masculinum (Thatcher et al., 2003).

Hosts: The host of present specimens is unknown. However, C. excisa was already found parasitizing fishes of the families Gerreidae, Haemulidae, Lutjanidae, Priacanthidae, Sciaenidae and Synodontidae (Joca et al., 2015).

Distribution: USA (Massachusetts to Florida), Antilles, Venezuela, Brazil (Pará, Maranhão, Pernambuco, Bahia, Sergipe, Rio de Janeiro and Santa Catarina) and Argentina (Trilles, 1994; Thatcher et al., 2003) (Fig. 6).

Cymothoa ianuarii Schioedte & Meinert, 1884

(Figs. 2-4, 6; Table 1)

Cymothoa IanuariiSchioedte & Meinert, 1884: 246-248, tab. VI (Cym. XXIV), figs. 19-20.

Cymothoa ianuariiTrilles, 1994: Thatcher et al., 2003: 551, fig. 80. Luque et al., 2013: 1454.

Cymothoa januariiSartor & Pires, 1988: 146-156. [erroneus spelling].

Material examined: BRAZIL: São Paulo: three ovigerous females, Enseada de Ubatuba, 03/V/2007 (UFRGS 6515); one ovigerous female, Enseada de Ubatuba, coll. F. Mantelatto, 02/VI/2008 (UFRGS 6516) [illustrated]; one ovigerous female, Enseada de Ubatuba, 15/VI/2003 (UFRGS 6517); one female, Enseada de Ubatuba, 15/VI/2003 (UFRGS 6518); one ovigerous female, Enseada de Ubatuba, X/2002 (UFRGS 6520) [illustrated].

Redescription (based on seven females)

Body 1.8 times as long than wide (Table 1), widest at pereonite 5, narrowest at pereonite 1 (Fig. 2A).

Cephalon: longer than wide, frons transversely truncated, visible in dorsal view, immersed on pereonite 1; eyes visible (Figs. 2A, C, D).

Pereon: Convex. Pereonite 1 with anterolateral angles surpassing eyes; pereonites 1 and 4 largest; pereonites 2 and 3 subequal; pereonites 5 and 6 subequal; pereonite 7 shorter and narrower than pereonite 6. Coxae 2 and 3 morphologically similar and bent downwards; 4-7 morphologically similar to each other and falciform (Fig. 2A, C).

Pleon: Immersed in pereonite 7; pleonites similar in length with posterolateral margins not overlapped by lateral margins of the subsequent pleonite (Figs. 2A, E). Pleotelson sub-rectangular and 0.46 times as long as wide; posterior margin sinuous; dorsal surface smooth; lateral margins convex (Fig. 2A, E).

Antennula: with eight articles, the first two being stouter, distal article with five small apical setae (Figs. 2B, 3A).

Antenna: comprised of nine articles, terminal article without setae; extending to posterior margin of cephalon. Labrum lateral margins concave, without median point (Figs. 2B, 3C).

Mandible: with chitinous and acute incisor and straight molar process. Palp shorter than mandible (Fig. 3D).

Maxillula: bilobed with four apical stout robust setae (Figs. 3E, F).

Maxilla: mesial lobe with four recurved robust setae, partly fused to lateral lobe with two recurved robust setae (Fig. 3G, H).

Maxilliped: Maxilliped article 3 with three recurved robust setae (Figs. 3I, J).

Oostegite: smooth, with marginal setae (not illustrated) (Fig. 2B).

Pereopods: 1-3 smaller than 4-7, which gradually increase in size and with carina on basis. Pereopod 1 basis 1.1 times as long as greatest width; ischium 0.7 times as long as basis; merus proximal margin without bulbous protrusion; carpus with straight proximal margin; propodus 1.6 times as long as wide; dactylus slender, 1.3 as long as propodus, 3.2 times as long as basal width. Pereopod 2 propodus 1.4 times as long as wide; dactylus 1.7 times as long as propodus; Pereopod 3 basis 1.5 times as long as greatest width; ischium 0.5 times as long as basis; propodus 1.2 times as long as wide; dactylus slender, 1.7 as long as propodus, 2.4 times as long as basal width. Pereopod 4 basis 1.67 times as long as greatest width; ischium 0.5 times as long as basis; propodus 1.4 times as long as wide; dactylus slender, 1.43 as long as propodus, 2.1 times as long as basal width. Pereopod 5 basis 1.3 times as long as greatest width; ischium 0.6 times as long as basis; propodus 1.07 times as long as wide; dactylus slender, 2.03 as long as propodus, 2.18 times as long as basal width. Pereopod 6 basis 1.3 times as long as greatest width; ischium 0.6 times as long as basis; propodus 1.6 as long as wide; dactylus 1.2 times as long as propodus. Pereopod 7 basis 1.5 times as long as greatest width; ischium 0.4 times as long as basis, with large proximal bulbous protrusion; merus proximal margin with slight protrusion, 0.3 times as long as ischium, 0.4 times as long as wide; carpus without bulbous protrusion; propodus 0.8 times as long as ischium, 1.6 times as long as wide; dactylus slender, 1.8 times as long as propodus, 2.6 times as long as basal width.

Pleopods: without setae, lobes decreasing in size from pleonites 1 to 5, exopod larger than endopod. Pleopod 1 exopod 1.1 times as long as greatest width, lateral margin straight, distal margin sinuous, mesial margin straight; endopod as long as wide, lateral margin convex, distally narrowly rounded, mesial margin convex; peduncle 2.75 times as wide as long. Pleopods 1-3 endopod proximal borders decreasing in size and increasing in size in pleopods 4-5; with fleshy folds absent and medial lobes present and decreasing in size (Figs. 4H-L).

Uropods: shorter than pleotelson. Peduncle 0.8 times as long as rami; lateral margins without setae. Endopod apically rounded, 2.8 times as long as greatest width, lateral margin weakly convex, mesial margin weakly convex. Exopod 0.9 times as long as endopod, 2.5 times as long as greatest width and without setae (Figs. 2A, C, E; 4M).

Remarks: Adult females of Cymothoa ianuarii can be distinguished mainly by the cephalon with conspicuous eyes and not deeply immersed in pereonite 1, anterolateral angles of pereonites 1 surpassing eyes, pereonites 5-6 much wider than 4, pleotelson twice wide as long and pleopods 1-5 decreasing in size. Males are unknown (Thatcher et al., 2003). This is the first record from the state of São Paulo, particularly in the northern portion of the coast (23°29′38.72″S, 45°05′16.0″W). This new record represents the rediscovery of this species after a hiatus of approximately 136 years since its original description from material collected in Rio de Janeiro in the 1880’s. We provided the redescription of this species based on the analyzed specimens.

Hosts: The host of present specimens is unknown. However, C. ianuarii was already found parasitizing fishes of the families Priacanthidae and Pleuronectidae (Schioedte & Meinert, 1884).

Distribution: Rio de Janeiro (Schioedte & Meinert, 1884) and São Paulo, Brazil (Fig. 6).

Cymothoa oestrum ( Linnaeus, 1758 )

(Figs. 5-6; Table 1)

Oniscus oestrumLinnaeus, 1758: 636.

Asellus oestrumOlivier, 1789: 253.

Cymothoa oestrumFabricius, 1793: 505. Thatcher et al., 2003: 546, figs. 52-76. Luque et al., 2013: 1454.

Material examined: BRAZIL: Bahia: one ovigerous female, Candeias, coll. J. Pezzi da Silva, 11/V/2010 (MCP 2999) [illustrated].

Remarks: This is the first record of this species from Bahia, particularly in the northern portion (12°44′49″S, 38°29′38″W), and it is the second record from Brazil. This species was redescribed by Thatcher et al. (2003) based on material from Camboriú, state of Santa Catarina, southern Brazil. Females can be distinguished by the truncate cephalon deeply immersed in the pereonite 1, eyes absent, anterolateral margins of pereonite 1 blunt and bilaminate pleopods with folding on the fifth endopod (Fig. 5). Males are unknown (Thatcher et al., 2003).

Hosts: The host of the present specimen is unknown. However, C. ianuarii was already found parasitizing fishes of the families Carangidae and Priacanthidae (Trilles, 1994).

Distribution: United States of America (Massachusetts to Florida), Antilles, Venezuela and Brazil (Bahia and Santa Catarina) (Fig. 6) (Thatcher et al., 2003).

CONCLUSION

This study deepen the knowledge on the distribution of three species of Cymothoa from Brazil. The rediscovery of C. ianuarii after a gap of almost 136 years of its original description and its redescription with the inclusion of new illustrations and description of the mouth parts are particularly important once the type material was lost and past descriptions were incomplete. We believe that these new data will help researchers to better identify the species and, therefore, further the understanding of distribution of these species in the southwestern Atlantic.

ACKNOWLEDGMENTS

The authors would like to thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior in the form of a Master’s scholarship to A.F. Huber and a postdoctoral fellowship to F.B. Ribeiro (PNPD process № 88887.470134/2019-00). Professor Gláucia Maria Funk Pontes (MCP-PUCRS) is thanked for the loan of the isopod material for study. This paper has benefited from the valuable comments from two anonymous reviewers.

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Edited by

  • Edited by: Marcos Domingos Siqueira Tavares

Publication Dates

  • Publication in this collection
    12 Feb 2021
  • Date of issue
    2021

History

  • Received
    25 May 2020
  • Accepted
    24 Nov 2020
  • Published
    29 Jan 2021
location_on
Museu de Zoologia da Universidade de São Paulo Av. Nazaré, 481, Ipiranga, 04263-000 São Paulo SP Brasil, Tel.: (55 11) 2065-8133 - São Paulo - SP - Brazil
E-mail: einicker@usp.br
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