Heteropriapulus heterotylioides, Mendoza-Franco & Hern & andez-Gomez & Caspeta-Mandujano, 2023

Mendoza-Franco, Edgar F., Hern, Raúl E., andez-Gomez & Caspeta-Mandujano, Juan M., 2023, New and previously known ectoparasitic monogenoids (Platyhelminthes) on native and non-native fishes from tributaries of the Usumacinta River basin (southern Mexico), a Neotropical transition zone, International Journal for Parasitology: Parasites and Wildlife 22, pp. 92-100 : 96-98

Heteropriapulus heterotylioides n. sp. ( Fig. 3A–M )

Type host: Pterygoplichthys pardalis (Castelnau) (Weber, 1991) ( Loricariidae : Siluriformes ).

Site of infection: Gill lamellae.

Prevalence and intensity of infection: see H. simplexioides n. sp.

Type locality: Palizada river (18 ◦ 5′12.95″N, 92 ◦ 5′27.25″W) (tributary of the Usumacinta River basin) in the state of Campeche (southern Mexico) .

Another host: Pterygoplichthys disyunctivus (Weber, 1991) from the Recreo river (17 ◦ 28′40.05″N; 91 ◦ 25′47.8″W) located in the municipality of Tenosique, in the state of Tabasco (southern Mexico) .

Specimens deposited: Holotype, CNHE (12048); 31 paratypes, CNHE (12049); 7 voucher specimens on P. disyunctivus from the Recreo river in CNHE (12050).

Etymology: The specific name reflects the close morphological resemblance of the new species to H. heterotylus (type species of the genus) parasitizing Hypostomus sp. (type host) introduced to India.

Description (based on 29 specimens mounted unstained in Gray and Wess medium and 3 unstained with LA-GAP mixture; measurements of specimens on P. disyunctivus from the Recreo river are in brackets and those from the type locality are in parentheses): Body 167 (128–190; n = 13) [237 (190–270; n = 6)] long, fusiform; greatest width 62 (50–80; n = 6) [90–120] usually in posterior trunk at level of gonads. Terminal cephalic lobes well developed, containing large head organ; 3 bilateral pairs of head organs lying posterior to cephalic lobes; cephalic glands indistinct, lying posterolateral to pharynx. Accessory (melanistic) granules extending from level of gonads to cephalic lobes. Pharynx subspherical, 18 (14–18; n = 5) in diameter. Testis 15 long, 10 wide, subspherical; seminal vesicle in left side of body near mid-length; prostatic reservoirs pyriform. Copulatory organ 36 (33–40; n = 16) [35 (33–40; n = 7)] long, a delicate tube (usually bent on its midportion) with sigmoid proximal portion and rounded base. Accessory piece 29 (25–33; n = 7) [33 (30–34; n = 3)] long, a complex of 3 subunits: 1 rod-shaped subunit, distally bent and proximally bifurcated; 1 subunit, variable, with submedial spine-like branch; 1 Y-inverted shaped subunit. Germarium ovate, 34 (31–36; n = 5) long, 21 (14–25; n = 5) wide. Vaginal pore mid-ventral; vaginal canal short, poorly sclerotized; seminal receptacle inconspicuous, immediately internal to vaginal pore. Vitelline follicles moderately dense. Peduncle broad to non-existent, slightly tapered posteriorly. Haptor 62 (55–68; n = 13) [70 (55–82; n = 6)] wide, subtrapezoidal. Hooks 12 (11–12; n = 18) long, with upright acute thumb and slender shank. Ventral anchor 38 (35–43; n = 39) [38 (33–42; n = 16)] long, with flattened base, elongate shaft and point with recurved tip; base 9 (8–12; n = 28) [8 (7–9; n = 11)] wide; shaft and point of ventral anchors extending posteroventrally from haptor; anchor filament double, well developed (not illustrated). Dorsal anchor 20 (19–23; n = 31) [22 (20–24; n = 15)] long, variable, with short to non-existent deep root, rounded superficial root, evenly curved shaft and elongate point extending past level of superficial root; base 6 (5–9; n = 13) [6 (5–7; n = 3)] wide. Ventral bar 51 (43–55; n = 22) [53 (47–61; n = 7)] long, variable in shape, straight to bowed, with tapered ends directed posteriorly. Dorsal bar 21 (18–25; n = 18) [22 (20–25; n = 5)] long, narrow, rod-shaped, straight to slightly arched posteriorly.

3.2.1.3. Remarks. In P. pardalis and P. disyunctivus , a simultaneous infection with H. simplexioides n. sp. and H. heterotylioides n. sp. was found. Since all worms could not be properly identified, the data on infection rate relate to both monogenoidean species on each of these hosts. Heteropriapulus heterotylioides n. sp. on P. pardalis most resembles H. heterotylus , this latter originally described on the introduced Hypostomus sp. to India by Jogunoori et al. (2004) and subsequently reported on P. pardalis , P. disyunctivus , H. plecostomus and P. ambrosettii from Mexico, China, Japan and Brazil (see Remarks section for H. simplexioides n. sp. and Acosta et al., 2017). Both monogenoidean species possess anchors/bars of similar size, i.e., ventral (length 35–43 vs 34–41) and dorsal anchors (length 19–23 vs 18–21); and ventral (length 43–55 vs 40–47) and dorsal (length 18–25 vs 18–23) bars. The new species differs from H. heterotylus in having an accessory piece composed of 3 subunits (compare Fig. 3A–C [present study]) (4 subunits in H. heterotylus ), in lacking a patch on ventral anchor base, an asymmetrical thickened wall of the MCO base, a vaginal pore as a transverse slit with thickened anterior and posterior margins (as a short vaginal tube in H. heterotylioides n. sp.) and by size of its hooks (length 11–12 vs

13–15 in H. heterotylus ). The noted shape differences of the subunits of the accessory piece, anchors and bars in H. heterotylioides n. sp. might be considered intraspecific variation. Rodríguez-Santiago et al. (2015, 2016) reported H. heterotylus on P. pardalis and P. disyunctivus from southern Mexico. While no morphometric evidence is available that would suggest that the report was based on specimens representing two distinct species (i.e, H. heterotylioides n. sp. and H. simplexioides n. sp.) (see Remarks section for this latter species), confirmation of the identity of H. heterotylus may depend on examination of newly collected specimens.

Ligictaluridus mirabilis (Mueller 1937; Klassen and Beverley-Burton

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(1985) ( Fig. 4A and B ).

Host: Southern blue catfish Ictalurus meridionalis (Günther, 1864) ( Ictaluridae : Siluriformes ).

Localities: Recreo river (17 ◦ 28′40.05″N; 91 ◦ 25′47.8″W) river, located in the municipality of Tenosique , in the state of Tabasco; and Lacantún river in the Biosphere Reserve Montes Azules ( BRMA), Chiapas, Mexico (19 ◦ 09″96.6″N, 90 ◦ 95″56.8″W) (both tributaries of the Usumacinta River basin, southern Mexico) .

Site of infection: Gill lamellae.

Prevalence and intensity of infection: 15 fish infected of 15 examined (100%); mean intensity of infection 4 parasites per infected fish from the Recreo river; 7 of 7 fish examined from Lacantún river (100%; 8).

Specimens deposited: 12 and 31 voucher specimens in CNHE (12043 and 12044 from Recreo and Lacantún rivers, respectively).

3.2.1.4. Remarks. Ligictaluridus was proposed by Beverley-Burton (1984) for gill and olfactory chamber monogenoids of North American catfishes ( Ictaluridae ). This ictalurid-specific genus was primarily characterized by dactylogyrids having a MCO characterized as a sclerotized curved tube proximally articulated with accessory piece which possess distal limb with one or more terminal projections; a sinistral vaginal opening; dorsal and ventral anchor/bar complexes; and hooks of disimilar shape and size. Klassen and Beverley-Burton (1985) revised diagnosis of Ligictaluridus above mentioned, redescribed and/or transferred to it dactylogyrids previously assigned in Cleidodiscus (sensu Beverley-Burton and Suriano, 1980) as Ligictaluridus pricei (Mueller, 1936) (type species), L. monticellii (Cognetti de Martis, 1924) , L. floridanus (Mueller, 1936) , L. mirabilis and L. bychowskyi (Price and Mura, 1969) (see Klassen and Beverley-Burton, 1985). Ligictaluridus mirabilis was originally described on flathead catfish Pylodictis olivaris (Rafinesque, 1818) from Mississippi River, USA from which other two Ligictaluridus spp. have also been described and/or reported, Ligictaluridus michaelalicea Leis et al. (2018) , L. floridanus and L. pricei . Additionally, Ligictaluridus posthon Klassen and Beverley-Burton, 1985 has been described on Noturus flavus Rafinesque, 1818 from Ontario, being a total of seven currently known Ligictaluridus spp. from North American catfishes (see Cloutman et al., 2018; Klassen and Beverley-Burton, 1985; Leis et al., 2018). Among these Ligictaluridus spp. , L. floridanus , L. pricei and L. mirabilis have been extensively reported on native and/or introduced Ictalurus spp. and cyprinids to Mexico and Japan (see Mendoza-Garfias et al., 2017; Nitta and Nagasawa, 2015; R´abago-Castro et al., 2011, 2014). However, not any taxonomic account is described and/or provided in these reports from Mexico to support identification of these dactylogyrids, overall due to the confusion over the identity of L. mirabilis and L. floridanus . Both monogenoidean species are morphologically closer to each other and differ primarily in the size and shape of the copulatory complex (see Klassen and Beverley-Burton, 1985; Leis et al., 2018). In the present study, drawings and measurements of the morphological features (i.e., copulatory complex) of the specimens identified as L. mirabilis on I. meridionalis from southern Mexico are provided (see Fig. 4 and Table 3). Measurements of these specimens are consistent with those originally used to describe and redescribe this species (on P. olivaris and Ictalurus punctatus , respectively) from North America (see Table 3) and with the most updated taxonomic key

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provided by Leis et al. (2018) for Ligictaluridus spp. , thus separating L. mirabilis from L. floridanus (i.e., accessory piece 70–90 [from the Recreo river], 70–80 [from the Lacantún river] long, with distal tip possessing two recurved points in present specimens (see Fig. 4 ) vs 40–47 long, with single recurved point in L. floridanus (see Table 3, and drawings/measurements of L. floridanus from the key to Leis et al., 2018). While not within the scope of the present study, it is noted urgent need of a formal revision of those dactylogyrids referenced as L. floridanus , L. pricei and L. mirabilis on Ictalurus spp. and cyprinids from Mexico. Ictalurus meridionalis represents a new host record for L. mirabilis in the Recreo river and new host and locality records from Lacantún river.

Aristocleidus mexicanus Mendoza-Franco, Tapia and Caspeta-- Mandujano, 2015

Host: Eugerres mexicanus (Steindachner, 1863) ( Gerreidae : Perciformes ).

Locality: Recreo river (17 ◦ 28′40.05″N; 91 ◦ 25′47.8″W) (tributary of the Usumacinta River basin) located in the municipality of Tenosique, in the state of Tabasco southern Mexico .

Site of infection: Gill lamellae.

Prevalence and intensity of infection: 13 fish infected of 16 examined (81%); mean intensity of infection 3 parasites per infected fish.

Specimens deposited: 5 voucher specimens in CNHE (12061).

Supplemental observations (original measurements of this species by Mendoza-Franco et al. [2015] follow those of the present study in brackets, respectively): Body 577 (505–625; n = 5) [425–630] long; greatest width (excluding haptor) 98 (90–110; n = 4) [85–150]. Haptor 96 (85–102; n = 3) [90–120] wide. Pharynx 33 (30–34; n = 4) [25–45] wide. Copulatory complex 31 (28–38; n = 5) [27–50] long. Ventral anchor 50 (46–52; n = 9) [46–50] long, base 18 (16–22; n = 5) [13–18] wide; dorsal anchor 45 (42–48; n = 7) [43–51] long, base 17 (15–21; n = 5) wide. Ventral bar 28 (24–35; n = 4) [23–30] long; dorsal bar 44 (42–47; n = 4) [42–47] long. Hook 12 (12–13; n = 11) [12–13] long. Egg 55–62 long, 42–58 wide.

3.2.1.5. Remarks. Aristocleidus mexicanus is clearly a member of a group of five species distributed from Neotropical region surveyed on Atlantic coasts from Florida to Brazil, and Pacific coast of Mexico on species of Gerres , Diapterus , Eucinostomus and Eugerres ( Gerreidae ) inhabiting in marine, brackish and freshwater environments (see Kritsky and MendozaFranco, 2008; Mendoza-Franco et al., 2009; Cohen et al., 2022). Aristocleidus mexicanus was originally described on E. mexicanus inhabiting in the freshwater environment of the Lacantun River. This latter species of Aristocleidus and Aristocleidus lacantuni Mendoza-Franco, Tapia and Caspeta-Mandujano, 2015 , on the same host species are the only two known species of Aristocleidus occurring in freshwater waters. The Recreo river in the municipality of Tenosique, Tabasco represents a new locality record for A. mexicanus .

Diplectanocotyla megalopis Rakotofiringa and Oliver (1987) .

Host: tarpon Megalops atlanticus Valenciennes, 1847 ( Megalopidae : Elopiformes ).

Locality: Recreo river (17 ◦ 28′40.05″N; 91 ◦ 25′47.8″W) (tributary of the Usumacinta River basin) located in the municipality of Tenosique, in the state of Tabasco, southern Mexico .

Site of infection site: Gill lamellae.

Prevalence and intensity of infection: 2 fish infected of 2 examined (100%); mean intensity of infection 6 parasites per infected fish.

Specimens deposited: 7 voucher specimens, CNHE (12062).

Supplemental observations (measurements of those specimens used to redescribed this species by Mendoza-Franco et al. [2004] follow those of the present study in brackets, respectively): Body 409 (337–525; n = 6) [387–454] long; greatest width (excluding haptor) 83 (75–90; n = 5) [81–101]. Haptor 116 (100–125; n = 6) [123–138] wide; haptoral sucker 50 (42–60; n = 7) [44–54] width. Pharynx 24 (22–27; n = 6) [22–27] wide. Copulatory complex 22 (19–25; n = 7) [20–33] wide.

Ventral anchor 33 (32–33; n = 6) [33–38] long, base 14 (13–15; n = 3) [12–16] wide; dorsal anchor 35 (33–37; n = 5) [30–37] long, base 12 (11–13; n = 3) [9–14] wide. Ventral bar 47 (42–51; n = 7) [39–51] long; dorsal bar 44 (42–47; n = 7) [36–50] long. Hook 9 (9–10; n = 6) [9–11] long.

3.2.1.6. Remarks. Diplectanocotyla megalopis was originally described on Indo-Pacific tarpon Megalops cyprinoides (Broussonet, 1782) from Madagascar by Rakotofiringa and Oliver (1987). Subsequently, D. megalopis was reported and redescribed from the Atlantic tarpon, Megalops atlanticus Cuvier and Valenciennes, 1847 from the Atlantic coasts of Nicaragua and Mexico (Yalahau Lagoon in the Caribbean State of Quintana Roo) by Mendoza-Franco et al. (2004) who also recognized this monogenoidean species on M. atlanticus from Puerto Rico. Currently, there are four species allocated within Diplectanocotyla Yamaguti, 1953 (as emended by Mendoza-Franco et al., [2004], and Lim and Gibson, [2007]): D. megalopis , D. gracilis Yamaguti, 1953 (type species) on M. cyprinoides (Broussonet, 1782) from Makassar, East Indies and off Peninsular Malaysia; Diplectanocotyla parva Lim and Gibson (2007) ; and Diplectanocotyla langkawiensis Lim and Gibson (2007) on M. cyprinoides from off Peninsular Malaysia. Present specimens of D. megalopis did not differ morphometrically from those originally described and redescribed (see measurements above and Table 1 in Mendoza-Franco et al., 2004). The occurrence of D. megalopis on M. atlanticus from the marine and brackish waters of Nicaragua and off Mexico vs freshwater from the Usumacinta River basin (see Mendoza-- Franco et al., 2004; present study) is noteworthy. It would suggest that salinity variation of the waters might not affect the presence and distribution of this monogenoidean species. A similar factor of salinity gradients has been suggested to restrict distribution of species of Rhabdosynochus ( Diplectanidae ) that parasitize snooks ( Centropomidae ) from which worms show varying tolerances to salinity during diadromous migrations of their hosts (see Kritsky et al., 2010). The Recreo river represents a new geographical and locality record for D. megalopis .

Figures

Fig. 3. Haptoral and copulatory complex sclerites of Heteropriapulus heterotylioides n. sp. on Pterygoplichthys pardalis (Loricariidae) from the Usumacinta river basin (southern Mexico). A, B, and C – copulatory complexes (A and C in dorsal view; B in ventral view); D – ventral anchor; E – hook; F, G and H – dorsal anchors; I and J – ventral bars; K and L – dorsal bars; M – vaginal tube.

Fig. 4. Copulatory complexes of Ligictaluridus mirabilis (Mueller 1937; Klassen and Beverley-Burton (1985) on Southern blue catfish Ictalurus meridionalis (Ictaluridae) from the Usumacinta river basin (southern Mexico). A – copulatory complex in ventral view; B – copulatory complex in dorsal view. Abbreviations: mco – male copulatory organ; ap – accessory piece.