Cichlidocestus gillesi, Alain de Chambrier & Carlos Daniel Pinacho-Pinacho & Jesus Servando Hernández-Orts & Tomáš Scholz, 2017

Alain de Chambrier, Carlos Daniel Pinacho-Pinacho, Jesus Servando Hernández-Orts & Tomáš Scholz, 2017, A New Genus And Two New Species Of Proteocephalidean Tapeworms (Cestoda) From Cichlid Fish (Perciformes: Cichlidae) In The Neotropics, J. Parasitol. 103 (1), pp. 83-94 : 87-89

Cichlidocestus gillesi n. sp.

(Figs. 1–7, 20–22)

Diagnosis (based on 4 specimens from Cichlasoma amazonarum in Peru including 1 scolex studied using SEM; measurements in micrometers unless otherwise stated; x ‾ = mean, n = number of measurements): Proteocephalidae, Proteocephalinae. Total body length 11–13 mm (n = 2), maximum width up to 760 (n = 3). Strobila acraspedote, anapolytic, consisting of about 35–38 proglottids: 25–30 immature (up to appearance of spermatozoa in vas deferens), 1–2 mature (up to appearance of eggs in uterus), 6–7 pregravid (up to appearance of hooks in oncospheres), 1 gravid proglottid. Immature and mature proglottids wider than long (length:width ratio 0.32–0.66), pregravid and gravid proglottids wider than long to longer than wide (length:width ratio 0.71–2.21).

Scolex 240–245 long and 360–505 wide (n = 3), wider than neck (proliferation zone), 570–590 long and 410–470 wide (Figs. 1, 20, 21). Suckers spherical, 120–140 (n = 8) in diameter, with anterior distal margin lined with circular musculature (Fig. 1). Apical part of scolex with a muscular apical sucker, 75–80 long 3 85–90 wide, and numerous cells with granular content between suckers (Fig. 1). Apex of scolex, sucker cavities, anterior part of scolex, and proliferation zone covered with capilliform filitriches of similar appearance and density; proglottids covered with acicular filitriches (data not shown).

Inner longitudinal musculature well-developed, formed by 1 irregular row of numerous small bundles of muscle fibers (Fig. 7). Eight to 10 anastomosed ventral osmoregulatory canals situated in medulla, just beneath fibers of inner longitudinal musculature 10–20 wide (Fig. 4). Two to 3 dorsal osmoregulatory canals thickwalled, narrow, about 5 in diameter.

Testes ovoid, small, 35–45 long and 25–35 wide, in 3–4 irregular layers, 37–46 in number (x ‾ = 42, n = 5). Testes form 2 wellseparated groups, with some testes dorsal to cirrus-sac and vagina (Fig. 4); aporal group with 17–22 testes, poral group with 19–26 testes. Posteriormost testes approach, but do not reach, posterior margin of proglottids, being posterior to ovary, but not posterior to posteriormost vitelline follicles (Fig. 4). Testes disappear in first pregravid proglottids.

Vas deferens strongly coiled, with loops forming elongate field crossing median line of proglottid (Fig. 4). Cirrus-sac pyriform to elongate, thin-walled, widened towards proximal part (Fig. 2), 125–140 long and 40–70 wide (n = 6), cirrus-sac length:width ratio 1.95–3.5, length of cirrus-sac represents 21–28% (x ‾ = 25%, n = 6) of proglottid width. Internal sperm duct enlarged to form voluminous, spherical internal seminal vesicle occupying proximal 1/3–1/2 of cirrus-sac (Fig. 2). Cirrus short, muscular, reaching up to 40% of cirrus-sac length (n = 6). Common genital atrium narrow, deep (Fig. 2), alternating irregularly, situated near anterior margin of proglottids, at 10–18% (x ‾ = 12, n = 6) of its length from anterior margin (Figs. 3, 4).

Ovary medullary, bilobed, with narrow isthmus situated almost equatorially, and 2 follicular (grape-like) lateral wings (Fig. 4), occupying two-thirds of median space of proglottids. Length of ovary represents 62–70% (x ‾ = 65%, n = 11) of proglottid length, its width representing 45–52% (x ‾= 48%, n = 6) of proglottid width (Fig. 4); ovary may reach laterally up to vitelline follicles. Mehlis’ gland about 65–90 in diameter, representing 11–17% of proglottid width (n = 5). Relative ovarian size, i.e., percentage of ovary surface to total surface of mature or pregravid proglottids (see de Chambrier et al., 2012), about 22%. Ovary disintegrates soon after appearance of first eggs (in fourth to fifth pregravid proglottid).

Vaginal canal slightly sinuous; seminal receptacle ovoid, thickwalled, situated anterior to ovarian isthmus (Fig. 4), full of spermatozoids in mature and first pregravid proglottids; terminal (distal) part of vaginal canal (pars copulathrix vaginae) surrounded by chromophilic cells and large, spherical vaginal sphincter (Fig. 2). Vagina posterior to cirrus-sac (n = 30).

Vitelline follicles medullary, forming 2 long, narrow lateral bands, absent anterior to cirrus-sac on poral side (Figs. 3, 4). Length of bands represents 89–93% (x ‾= 91%, n = 7) and 83–93% (x ‾ = 88%, n = 7) of length of proglottid on poral and aporal side, respectively, width of vitelline bands presents 11–13% of proglottid width. Uteroduct passing dorsal to ovarian isthmus, entering uterus anteriorly, at about 25% of length of proglottid from anterior margin.

Uterus medullary, with development of type 2 (see de Chambrier et al., 2004a), i.e., uterine stem present as elongated longitudinal median concentration of chromophilic cells in immature proglottids, with lumen appearing in last immature proglottids. In mature proglottids, uterine stem thin-walled, with median lumen and almost invisible long and narrow digitate diverticula. In pregravid proglottids, uterine diverticula (lateral uterine branches) thinwalled, digitate, lined with few chromophilic cells. Uterus with 16– 21 lateral diverticula on each side (Fig. 3).

Eggs spherical, with hyaline outer envelope (collapsed in whole mounts); embryophore bilayered, with external layer 30–33 in diameter and internal nucleate envelope 24–25 in diameter; oncosphere 14–15 in diameter, with 6 embryonic hooks 7–8 long (Figs. 5, 6). Ripe eggs released through 4–5 pore-like uterine openings on ventral side (Fig. 3).

Taxonomic summary

Type host: Cichlasoma amazonarum Kullander, 1983 ( Perciformes : Cichlidae ), vernacular name ‘bujurqui.’

Type locality: A private aquarium in Iquitos, Region of Loreto, Peru (3 8 12 ′ S, 52 8 12 ′ W); precise origin of fish is unknown, but they were captured near Iquitos (E. Panduro, pers. comm.).

Site of infection: Anterior intestine.

Infection rate: Three of 11 fish from a private aquarium of Edgard Panduro in Iquitos, Peru, examined by T. Scholz on 1 October 2008, were infected with 4 tapeworms (prevalence 27%; total length of infected fish 9, 12, and 12.5 cm; mean intensity 1.3; range 1–2); the remaining 20 fish from other localities around Iquitos examined by T. Scholz and A. de Chambrier in 2005 and 2009 were negative.

Deposition of specimens: Holotype (MHNG-PLAT 63202; 1 whole mount with a complete specimen from the host of the field number PI 477a), 1 paratype (MHNG-PLAT 63208; whole mount with proglottids of a specimen from the host field number PI 474d), 1 paratype ( IPCAS C-733; whole mount of the anterior part and several proglottids of a complete specimen from the host field numbers PI 470); all specimens were collected on 1 October 2008 by T. Scholz in Iquitos, Peru.

Etymology: Specific name refers to Gilles Roth from the Natural History Museum in Geneva for his excellent illustrations (line drawings) of proteocephalidean cestodes made more than 20 yr ago.

Molecular data: A fragment of 1,085 bp of the 28S rRNA gene of 1 specimen of C. gillesi was amplified. The nucleotide sequence is available in the GenBank database (Accession No. KY403889 ).

Remarks

The new species is designated as the type species of the new genus because its material is of a better quality compared to specimens of the second new species from Costa Rica (see below), and molecular data are available for C. gillesi . The fact that hosts of this species were found in a private aquarium in Iquitos does not enable us to locate their precise origin, but they were captured near Iquitos according to the provider of these fish (E. Panduro, Iquitos, pers. comm.). This species is typified by the morphological characteristics listed in the diagnosis of the new genus (see above) such as the peculiar appearance, size and position of the ovary with follicular, large lateral wings, which occupy middle and posterior thirds of the median region of proglottids (Fig. 4), presence of a voluminous internal seminal vesicle (Fig. 2) and several narrow, thin-walled ventral osmoregulatory canals in the medulla (Fig. 7), morphology of the scolex, which is quadrilobed and bears a muscular apical sucker with a deep cavity (Figs. 1, 20, 21), and the testes disappearing in the first pregravid proglottids. The new species was found only in 3 of 31 cichlids (overall prevalence less than 10%) examined.

A comparative analysis of partial 28S rRNA gene sequences of 1 sample of C. gillesi (a piece of the holotype) with available sequences of proteocephalideans has revealed the closest relationship with another parasite of Neotropical cichlids, S. megalodiscus (Fig. 22). This species appeared at a very basal position compared to all other Neotropical proteocephalideans in a comprehensive molecular phylogenetic analysis of de Chambrier et al. (2015b), but its position was unstable. Interestingly, species of both genera from Neotropical cichlids share some peculiar morphological traits, namely (1) a large-sized ovary that occupies more than one-half of the proglottid lengths, but disappears soon after the eggs appear in the first pregravid proglottids; (2) internal sperm duct is enlarged in the proximal part of the cirrus-sac to form spherical internal seminal vesicle; (3) the anterior rim of suckers comprises a narrow band of circular musculature, thus forming a small sphincter near sucker opening; and (4) a functional apical sucker is present.