Characiformes (sensu Fink and Fink, 1996) represents one of the largest groups of teleost fishes, including 23 families and around 2,247 species (Eschmeyer et al. 2016). They inhabit freshwater environments, and many species are popular aquarium fishes or an important source of human food (Nelson 2006). Characidae Buckup, 1998 is one of the largest families included in this order, with 1,126 described species (Eschmeyer et al. 2016).
Several species of characid fishes are known in Brazil, with those belonging to the genus Astyanax Baird and Girard, 1854 the richest in species (Nelson 2006). Astyanax lacustris (Lütken, 1875) (=Astyanax altiparanae Garutti and Britski, 2000) popularly known as “lambari-do-rabo-amarelo”, is native to Eastern Brazil; while Astyanax fasciatus (Cuvier, 1819) known as “lambari-do-rabo-vermelho”, is distributed in freshwater basins in North, Central and South America (Argentina, Belize, Brazil, Colombia, Costa Rica, Mexico, Panama, Uruguay, and Venezuela) (Reis et al. 2003).
Monogeneans are common fish parasites, and a significant number of new species has been described in the recent years, mainly in the Neotropics (Mendoza-Palmero et al. 2012; Monteiro and Brasil-Sato 2014; Rossin and Timi 2014; Moreira et al. 2016; Acosta et al. 2017; Franceschini et al. 2017; Zago et al. 2017). Dactylogyridae is the most abundant taxon in South America (Cohen et al. 2013), which accommodates the genus Cacatuocotyle, parasites of Characidae fishes in the Neotropical region.
To date, four species have been placed in this genus, two of which were described in Brazil: Cacatuocotyle paranaensis Boeger, Domingues and Kritsky, 1997 (type-species), which was found parasitizing Characidium lanei Travassos, 1967 and Characidium pterostictum Gomes, 1947 in the Cacatu and 2 de Fevereiro Rivers, in the state of Paraná (Boeger et al. 1997); and Cacatuocotyle guaibensis Gallas, Callegaro-Marques and Amato, 2014, originally described parasitizing specimens of Astyanax aff. fasciatus and Astyanax jacuhiensis (Cope, 1894) from Lake Guaíba, in the state of Rio Grande do Sul (Gallas et al. 2014). After that, two species have been described in Mexico: Cacatuocotyle chajuli Mendoza-Franco, Caspeta-Mandujano and Salgado-Maldonado, 2013, and Cacatuocotyle exiguum Mendoza-Franco, Caspeta-Mandujano and Salgado-Maldonado, 2013, parasitizing Astyanax aeneus (Günther, 1860) from the Lacantún River Basin in the Montes Azules Biosphere Reserve in the state of Chiapas (Mendoza-Franco et al. 2013).
The use of molecular techniques has become increasingly common in descriptions of new species or redescriptions, as it is complementary to and supports morphological analysis (Cunningham et al. 2001; Huyse et al. 2004; Řehulková et al. 2013; Franceschini et al. 2017). Thus, the aim of the present study was therefore to describe a new species of Cacatuocotyle from the Sapucaí-Mirim River, in the southeast of Brazil, supported by morphological and molecular characterization. An identification key to the genus Cacatuocotyle is also provided.
Materials and Methods
Collection of host and parasite specimens
Forty specimens of A. lacustris and 40 of A. fasciatus were collected from the Sapucaí-Mirim River, in the state of São Paulo, Brazil (20°26′12.5″S, 47°53′18.59″W) between March 2012 and July 2013 using gillnets. The capture of fish specimens was authorized under a Permanent License for the Collection of Zoological Material (SISBio 13794-1). The fish specimens collected were stored individually in plastic bags in a Styrofoam box with ice, for immediate transportation to the laboratory.
The monogeneans were collected and stored in 70% ethanol solution. Samples of these parasites were stained with Gömöri’s trichrome and mounted in Canada balsam for analysis of the internal organs. Some specimens were mounted in Hoyer’s or in Gray and Wess medium for the study of sclerotized structures (Kritsky et al. 1986).
The morphological and morphometric analysis of the parasites was carried out using a computerized system for image analysis with differential interference contrast (DIC) – LAS V3 (Leica Application Suite V3; Leica Microsystems, Wetzlar, Germany). The illustrations of the sclerotized structures were performed with the aid of a camera lucida mounted on a Leica DMLS microscope with phase contrast optics.
All the measurements were presented in micrometers (μm) and expressed as means, followed by the range and number of specimens measured (n) in parentheses. Measurements of the (a) bar length, (b) bar width, (c) anchor width, (d) anchor length, (e) extern length, (f) intern length and (g) tip length were performed according to the scheme shown in Figure 1. The prevalence and mean intensity of infestation were calculated in accordance with Bush et al. (1997).
Voucher host fish specimens were deposited in the fish collection of the Laboratório de Biologia e Genética de Peixes (the Fish Biology and Genetics Laboratory) (LBP), Universidade Estadual Paulista (São Paulo State University - UNESP), in the municipality of Botucatu, in the state of São Paulo, Brazil (A. lacustris - LBP 18794 and A. fasciatus - LBP 18795). Holotype and the paratypes of the new species proposed were deposited in the Coleção Helmintológica do Instituto Oswaldo Cruz (the Helminthological Collection of the Oswaldo Cruz Institute) (CHIOC), in the state of Rio de Janeiro, Brazil. Voucher specimens were deposited in the zoological collection of the Instituto Nacional de Pesquisas da Amazônia (Amazonas National Research Institute) (INPA), in the state of Amazonas, Brazil, and in the Coleção Helmintológica do Instituto de Biociências (the Helminthological Collection of the Institute of Biosciences of Botucatu) (CHIBB) of the Universidade Estadual Paulista (São Paulo State University - UNESP), in the municipality of Botucatu, in the state of São Paulo, Brazil.
DNA extraction, amplification and sequencing
For separation to be performed correctly and identification confirmed, each parasite specimen subjected to molecular analysis was mounted on a slide with glycerin and photographed. The same specimens were then used for molecular characterization. The total DNA genomic was extracted using the Qiagen Dneasy® Blood and Tissue Kit, according to the manufacturer’s protocol, with a final volume of 30 μl. Conventional PCR amplifications were performed in 25 μl reactions containing 5 μl of DNA extract. A quantity of 0.5 μl of each PCR primer was added using Ready-to-Go PCR beads (Pure Taq™ Ready-to-Go™ beads, GE Healthcare, Chicago, USA), with the solution consisting of stabilizers, BSA, dATP, dCTP, dGTP, dTTP, ~2.5 units of puReTaq DNA polymerase and reaction buffer. The beads were reconstituted to a final volume of 25 μl, and the concentration of each dNTP was 200 μM in 10 mM Tris-HCl, (pH 9.0 at room temperature), 50 mM KCl and 1.5 mM MgCl2. The thermocycling profile employed was: initial denaturation of DNA at 94°C for 3 min, followed by 34 amplification cycles at 94°C for 30 s, 56°C for 30 s and 72°C for 1:30 min, and a final extension at 72°C for 7 min (Mendoza-Palmero et al. 2015). The primers used for amplification and for sequencing were the partial 28S rDNA (LSU) fragments U178 (5’ - GCA CCC GCT GAA YTT AAG - 3’) and L1642 (5’ - CCA GCG CCA TCC ATT TTC A - 3’) (Lockyer et al. 2003), and L1200R (5’ - GCA TAG TTC ACC ATC TTT CGG - 3’) for sequencing (Littlewood et al. 2000).
The PCR products were run on agarose gel using GelRed and loading buffer and purified using the QIAquick PCR Purification Kit (Qiagen®, CA, USA). Automated sequencing was performed directly on the purified PCR products from specimens using BigDye v.3.1 Terminator Cycle Sequencing Ready Reaction kit (Applied Biosystems, Foster City, CA, USA) for cycle sequencing. Sequences were run on an Applied Biosystems ABI 3500 DNA genetic analyzer.
Contiguous sequences were assembled and edited in Sequencher v. 5.2.4 (Gene Codes, Ann Arbor, MI) and subjected to BLAST analysis (http://blast.ncbi.nlm.nih.gov) to confirm their identity. Unambiguous alignment was carried out using the MUSCLE software implemented in Geneious version 7.1.3 (Kearse et al. 2012) with dactylogyrids available in GenBank (Table I). The outgroup chosen was Ancyrocephalus percae (KF499080).
The genetic divergence between the sequences was calculated within the aligned portion using the Kimura-2-parameter distance model (Kimura 1980) in the MEGA6 program (Tamura et al. 2013). The NJ analyzes were performed using the Kimura-2-parameter model and 2000 bootstrap replicates.
Dactylogyridae Bychowsky, 1933
Cacatuocotyle Boeger, Domingues and Kritsky, 1997
Cacatuocotyle papilionis (Fig. 2)
Diagnosis: Based on 14 specimens. Body 728 (383–1,100; n = 11) long; greatest width 178 (113–286; n = 12) near mid-length; tegument smooth. Cephalic lobe well defined and cephalic glands not observed. Two pair of eyes, with the anterior smaller than the posterior pair; one or both members of each pair sometimes absent; numerous accessory granules in cephalic and anterior trunk region. Pharynx spherical, 38 (28–53; n = 12) in diameter; esophagus long: 78 (50–149; n = 8) length, 16 (9–23; n = 8) width; caeca confluent and not sinuous. Haptor 142 (115–203; n = 14) wide, 77 (55–109; n = 14) long, with thickened muscular on anterior margins; one pair of anchors, (d) 38 (34–42; n = 13) long, (c) 28 (23–34; n = 13) wide, (f) 35.5 (30.1–40.1; n = 14) intern length, (e) 34.6 (31.1–37.8; n = 14) extern length, (g) 13.8 (10.8–16.1; n = 14) tip length, robust, with broad superficial root, short deep root, regularly curved shaft and point; presence of protuberances on both superficial and deep root. Bar (a) 10 (8–12; n = 14) long, (b) 24 (21–25; n = 14) wide, with variable opening of its ends and a shape resembling a butterfly; presence of medial enlargement and tapered ends, with one protuberance in the anterior midportion margin; irregular margins and some indents in the posterior midportion, with the presence of several protuberances. Hooks similar, with uniform shank and protruding thumb; hook 17 (14–19; n = 13) long; FH loop nearly one half of shank length. Testis elongated, 34 (21–73; n = 9) long, 11 (8–16; n = 9) wide; ovary elongated, 79 (60–120; n = 10) long, with greatest width 22 (14–32; n = 10) at anterior end. Male copulatory organ (MCO), a coiled tube of 4.5–5.5 counterclockwise rings with a spherical base surrounded by 2 tandem circular flanges; articulation process of the accessory piece present; ring diameter 18 (14–20; n = 14). Accessory piece 21 (17–24; n = 13) long, with greatest width 11 (8–14; n = 13), with distal portion tweezer-shaped. Vaginal aperture sinistral; vagina comprising an elongated, sclerotized and delicate tube. Seminal receptacle observed. Vas deferens looping left intestinal caecum anterior to the ovary. Seminal vesicle pyriform; small prostatic reservoir posterior to the base of the MCO. Oviduct, ootype and uterus not observed. Vitelline follicles coextensive with intestinal caecum and absent near esophagus, pharynx and reproductive organs. An egg without polar filament was observed in one specimen, which was 39 long and 30 wide.
Type host: Astyanax lacustris (Lütken, 1875) (=Astyanax altiparanae Garutti and Britski, 2000) (Characiformes: Characidae).
Other hosts: Astyanax fasciatus (Cuvier, 1819) (Characiformes: Characidae).
Site of infestation: Skin.
Type locality: Sapucaí–Mirim River, Grande River Basin, state of São Paulo, Brazil (20°29′38.38″S, 47°51′33.11″W).
Prevalence and mean intensity of infestation: A. lacustris - 9 fish from 40 examined (22.5%), and 1.8 ± 0.3 (1–4), respectively; and A. fasciatus - 2 fish from 40 examined (5%), and 1, respectively.
Specimens deposited: Holotype CHIOC (39028) and Paratypes CHIOC (39029, 39030); Vouchers INPA (758, 759) and CHIBB (345L).
Specimens examined: Paratypes (CHIOC 37965b and 37965c) of Cacatuocotyle guaibensis Gallas, Callegaro-Marques and Amato, 2014 deposited by Gallas et al. (2014).
Etymology: the specific name is derived from the Latin (papilio = butterfly) and refers to the ventral bar that resembles a butterfly.
Based on the presence of a convex haptor with thickened muscular anterior margins, one anchor-bar complex (ventral), seven pairs of ventral hooks (one pair associated with the anchor shafts; one central pair anterior to the bar; five submarginal bilateral pairs) and a sinistral vaginal aperture (Boeger et al. 1997), the new species proposed in this study is considered a member of Cacatuocotyle.
Cacatuocotyle papilionis n. sp. can be distinguished from most of its congeners mainly by the morphology of the ventral bar (resembling a butterfly) and accessory piece, and the number of rings of the male copulatory organ. The new species resembles C. paranaensis due to the shape of the ventral anchor (robust and with the presence of protuberances on both the superficial and deep root) and the eyes (one or both members of each pair is sometimes absent); but can be differentiated by the shape of the accessory piece (distal portion tweezer-shaped in C. papilionis n. sp.), the number of rings of the MCO (3.5 in C. paranaensis and 4.5–5.5 in C. papilionis n. sp.), body length (400–555 in C. paranaensis and 383–1,100 in C. papilionis n. sp.), bar (U-shaped in C. paranaensis, and with the presence of one protuberance in the anterior midportion margin, irregular margins and some indents in the posterior midportion with the presence of several protuberances, and the shape resembling a butterfly in C. papilionis n. sp.) and the intestinal caecum (sinuous in C. paranaensis and not sinuous in C. papilionis n. sp.).
Cacatuocotyle papilionis n. sp. is similar to C. guaibensis in relation to body length (580–1,010 for C. guaibensis and 383–1,100 for C. papilionis n. sp.), but differs in relation to haptor width (72.5–112.5 in C. guaibensis and 115–203 in C. papilionis n. sp.), protuberances on both superficial and deep root in the ventral anchor (absent in C. guaibensis and present in C. papilionis n. sp.), shaft of the ventral anchor (more robust and short in C. papilionis n. sp. than in C. guaibensis), prominent tips in the inner and outer roots of the ventral anchor (present in C. guaibensis and absent in C. papilionis n. sp.), bar (U-shaped with regular anterior margin and small irregularities in the posterior margin at midportion in C. guaibensis, and with the presence of one protuberance in the anterior midportion margin, irregular margins and some indents in the posterior midportion with the presence of several protuberances, and the shape resembling a butterfly in C. papilionis n. sp.), hooks (smaller in C. papilionis n. sp.: 14–19 μm long than in C. guaibensis: 17.5–25 μm long), the shape of the accessory piece (distal portion tweezer-shaped in C. papilionis n. sp.), and the eyes (one or both members of each pair is sometimes absent only in C. papilionis n. sp.).
The new species differs from C. chajuli and C. exiguum through its body length (270–418 for C. chajuli, 270–275 for C. exiguum, and 383–1,100 for C. papilionis n. sp.), haptor width (54–95 in C. chajuli, 60 in C. exiguum, and 115–203 in C. papilionis n. sp.), bar (V-shaped in C. chajuli, U-shaped in C. exiguum, and with the presence of one protuberance in the anterior midportion margin, irregular margins and some indents in the posterior midportion with the presence of several protuberances, and the shape resembling a butterfly in C. papilionis n. sp.), and the shape of the accessory piece (distal portion tweezer-shaped in C. papilionis n. sp.)
Key to species of Cacatuocotyle
Vagina sclerotized ............................................................ 2
Vagina slightly visible and apparently unsclerotized ....................................................... Cacatuocotyle exiguum
Bar U-shaped ................................................................... 3
Bar not U-shaped ............................................................ 4
Anchor with protuberances on deep root and proximal mar gin of the superficial root; MCO with up to 3.5 counterclockwise rings ........................ Cacatuocotyle paranaensis
Anchor without protuberances on deep root and proximal margin of the superficial root; MCO with 4–5 counterclockwise rings ........................ Cacatuocotyle guaibensis
Bar V-shaped ................................... Cacatuocotyle chajuli
Bar resembling a butterfly, with irregular margins and some indents in the posterior midportion, with the presence of several protuberances; MCO with 4.5–5.5 counterclockwise rings ............ Cacatuocotyle papilionis n. sp.
The 28S ribosomal gene sequence of C. papilionis n. sp. was 1,490bp and was aligned with 20 dactylogyrids retrieved from the GenBank database. The alignment was 883bp long and the data obtained, based on the K2P distance matrix (Table II), identified a lowest nucleotide interspecific distance of 26% with Unilatus unilatus (Mizelle and Kritsky, 1967) and a greatest interspecific distance of 41% with Aphanoblastella sp.3.
Astyanax spp. exhibit a great diversity of parasite fauna, and have been found parasitized by species of Nematoda, Monogenea, Digenea, Trematoda, Acanthocephala, Myxozoa, Branchiura, Isopoda, and Copepoda (Eiras et al. 2010). According to Mendoza-Franco et al. (2013), some reports indicate that species of Astyanax are considered the most diverse suite of monogeneans species in the Neotropics, because of the large number of this parasite group that they can harbor. Until now 13 genera of monogeneans have been reported in Astyanax spp., including: Amphithecium, Anacanthocotyle, Cacatuocotyle, Characithecium, Cyclopectanum, Diaphorocleidus, Gyrodactylus, Jainus, Notozothecium, Palombitrema, Pseudorhabdosynochus, Trinibaculum, and Urocleidoides (Kritsky and Fritts 1970; Kritsky and Leiby 1972; Boeger et al. 1997; Thatcher 2006; Mendoza-Franco et al. 2009; Cohen et al. 2013; Narciso et al. 2014).
Only two fish genera of the family Characidae have been found parasitized by Cacatuocotyle to date: Astyanax and Characidium, demonstrating high specificity for the host or closely related species. According to Buchmann and Lindenstrøm (2002), the selection of a certain host species by an ectoparasitic monogenean must be governed mainly by factors related to the host surface, and it has been suggested that the chemical stimuli emitted from the host attract parasites and even initiate certain behavioral and physiological changes in the parasite. Furthermore, anatomical structures of certain host surfaces are likely to exhibit greater compatibility with some parasite attachment mechanisms (Buchmann and LindenstrØm 2002).
Although only five species of the genus Cacatuocotyle have been described to date (including the new species described in the present study), they exhibit broad, preferably micro-habitats, as they can be found in the gills (C. paranaensis and C. exiguum), skin (C. guaibensis and C. papilionis n. sp.) or external surface of the anal aperture (C. chajuli). According to Euzet and Combes (1998), it is estimated that more than 95% of monogeneans parasite the gills or skin of fish, and these ectoparasitic modes of life are generally supposed to be “ancestral” traits. In the course of evolution, some species or groups have changed their habitat type, and these changes by monogeneans in fish could may represent a tendency to abandon the ectoparasitic mode of life for a meso- or endoparasitic form, in order to avoid competition, or to have access to better resources, or even reduce the pressures exerted by predators of ectoparasites (Euzet and Combes 1998).
The occurrence of C. papilionis n. sp. in A. lacustris and A. fasciatus expands the list of hosts of Cacatuocotyle, as well as presenting a new register of occurrence in the Sapucaí-Mirim River in the southeast of Brazil. In addition, we present for the first time molecular data of a species of the genus Cacatuocotyle, which will contribute to studies on the phylogenetics and diversity of Dactylogyridae in the Neotropical region. As there are few molecular studies regarding monogeneans in Brazil (Fehlauer-Ale et al. 2011; Gasques et al. 2016; Müller et al. 2016; Acosta et al. 2017; Franceschini et al. 2017) it is hoped that this work will encourage others to sequence more data on Cacatuocotyle species and study host associations and interrelationships among monogeneans from the Neotropical region.
This work was supported by FAPESP - Fundação de Amparo á Pesquisa do Estado de São Paulo (São Paulo Research Foundation) (A.C.Z., grant numbers 2011/23588-8, 2015/11542-4, 2016/07829-9; L.F., grant number 2012/07850-7), CAPES - Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (the Coordination for the Improvement of Higher Education Personnel) and CAPES/PNPD (L.F.: 17/2016); AUX-PE-PNPD (M.I.M., grant number 3005/2010), the Young Researcher Program PROPE-UNESP (M. I. M., grant number 02/2016); FUNEP - Fundação de Apoio a Pesquisa, Ensino e Extensão (the Research, Teaching and Extension Support Foundation) (grant number 1.01852/2011); R.J.S. was supported by CNPq (grant number 309125/2017-0) and CNPq-PROTAX (grant number 440496/2015-2) / FAPESP (grant number 2016/50377-1). We are grateful to Edmir Daniel Carvalho (in memoriam), Sandro Geraldo de Castro Britto, Diogo Freitas Souza, Marcos Gomes Nogueira, Duke Energy and CELAN (Central Elétrica Anhanguera) for logistical support during the collections.
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About the article
Published Online: 2018-04-13
Published in Print: 2018-06-26