EDP Sciences logo
Submit your paper
Search
Menu
All issues Volume 22 (2015) Parasite, 22 (2015) 33 Full HTML
Open Access
Issue
Parasite
Volume 22, 2015
Article Number 33
Number of page(s) 6
DOI https://doi.org/10.1051/parasite/2015033
Published online 25 November 2015

© E.F. Mendoza-Franco et al., published by EDP Sciences, 2015

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Gerreidae comprises a group of marine and/or brackish water fish commonly known as mojarras distributed along the subtropical and tropical coastal areas of the world. In the Americas, Gerreidae consists of 22 valid species belonging to four genera: Gerres Quoy & Gaimard, Diapterus Ranzani, Eucinostomus Baird & Girard, and Eugerres Jordan & Evermann [2]. Eugerres includes seven species from which only Eugerres mexicanus (Steindachner, 1863) and Eugerres castroaguirrei González-Acosta & Rodiles-Hernández, 2013 are confined to freshwater habitats in southeastern Mexico and northern Guatemala [2–4]. Diapterus auratus Ranzani, 1842, Diapterus peruvianus (Cuvier), Diapterus rhombeus (Cuvier), Eugerres brasilianus (Cuvier), Eugerres plumieri (Cuvier), and Gerres cinereus Jordan & Evermann of the Gulf (coastal areas from the States of Veracruz and Yucatán) and Pacific (a coastal lagoon from the state of Guerrero) of Mexico and Panama are known to be parasitized by species of Aristocleidus Mueller, 1936 (Dactylogyridae), i.e., A. hastatus (type species of the genus), Aristocleidus lamothei Kritsky & Mendoza-Franco, 2008, and Aristocleidus sp. of Mendoza-Franco et al. [8, 11]. On the other hand, only A. hastatus has been described from the gills of the striped bass, Roccus lineatus (Bloch) [now Morone saxatilis (Walbaum)] (Moronidae) in the Peace River near Fort Ogden, Florida [16]. During investigations into the helminth fauna of fishes from the Rio Lacantún basin in the state of Chiapas (Mexican Pacific), two undescribed species of Aristocleidus were found on the gills of the Mexican mojarra E. mexicanus in January and August 2014. These new species are described in this article.

Materials and methods

Host specimens of E. mexicanus were captured by hook-and-line and throw nets in January and August 2014 in the Rio Lacantún basin in the state of Chiapas, Mexico (16°09′96.6″ N, 90°95′56.9″ W). Live fish were sacrificed bloodlessly by puncturing the brain region (a needle is introduced dorsally via the eye socket and moved about to destroy the spinal cord) [13]. The gills of each fish were removed and placed in finger bowls containing 4–5% formalin solution to fix any of the ectoparasites that might be present. Subsequently, parasites were isolated and stained with Gomori’s trichrome and mounted in Canada balsam. In addition, some specimens were mounted with a mixture of acid-lactic (AL) and glycerin-ammonium picrate [12] to obtain measurements and line drawings of haptoral structures and the copulatory complex. All other measurements were obtained from unflattened specimens stained with Gomori’s trichrome. Drawings were made with the aid of a drawing tube using a Leica microscope DM50 with Nomarski interference contrast. Measurements, all in micrometers, represent straight-line distances between extreme points and are expressed as the mean followed by the range and number (n) of structures measured in parentheses; body length includes that of the haptor; measurements of the copulatory complex, anchor/base are represented in Figures 2 and 3 as the perpendicular distance between parallel lines. Direction of the coil of the copulatory organ, i.e., clockwise, was determined using the procedure suggested by Kritsky et al. [7]. Haptoral terminology for species of Aristocleidus is that provided by Kritsky & Mendoza-Franco [8]. Type specimens are deposited in the National Helminthological Collection of Mexico (CNHE), Institute of Biology, National Autonomous University of Mexico, Mexico.

thumbnail Figures 1–8.

Aristocleidus mexicanus n. sp. from the gills of Eugerres mexicanus. 1: whole-mount (composite, ventral view); 2: ventral anchor (Sh, shaft; Au, angular union; Po, point); 3: copulatory complex (dorsal view); 4: dorsal anchor; 5: Ventral bar; 6: dorsal bar; 7: vagina; 8: hook. Figures are drawn to the following scales: 100 μm (Fig. 1), 25 μm (Figs. 2–7), and 10 μm (Fig. 8).

Results

Aristocleidus mexicanus n. sp.

urn:lsid:zoobank.org:act:8CE4BC57-1863-4101-9A8D-409B5A1476D3

Type-host: Eugerres mexicanus (Steindachner, 1863) (Perciformes, Gerreidae).

Site of infection: Gill lamellae.

Type locality and collection date: Rio Lacantún basin (16°09′96.6″ N, 90°95′56.9″ W), August 2014.

Specimens deposited: holotype, 12 paratypes and 6 vouchers in CNHE (9872, 9873, and 9874, respectively).

Etymology: named after its host.

Description (Figs. 1–8)

Diagnosis (based on 13 specimens collected in August and on 6 collected in January [brackets]) includes the following: Body 515 (425–630; n = 10) long; greatest width 118 (85–150; n = 10) usually near gonads. Cephalic lobes well developed; each head organ comprising groupings of terminations of cephalic-gland ducts. Pharynx 35 (25–45; n = 10) wide, subspherical. Testis 30–40 (n = 2) long, 18 (17–20; n = 3) wide, pyriform; seminal vesicle comparatively large, fusiform, lying in the midline of body; prostatic reservoir pyriform. Copulatory complex 39 (27–50; n = 12) [47 (43–51; n = 5)] long. Male copulatory organ (MCO) comprising proximal funnel-shaped base with proximal thickened edge, coiled tube of less than one ring; J-shaped accessory piece, terminally ornate. Prostatic glands conspicuous surrounding dorsal region of prostatic reservoir. Germarium 54 (35–75; n = 6) long, 19 (15–25; n = 5) wide; vaginal vestibule thick walled, internal, communicating with vaginal pore by short duct; vaginal tube moderately long, delicate, extending to ovate seminal receptacle; vitellarium dense, vitelline ducts not observed. Haptor 102 (90–120; n = 9) wide. Ventral anchor 48 (46–50; n = 22) [50 (43–57; n = 8)] long, with variably bent roots, slightly angular union of elongate arcing shaft and straight point (see Au, Sh and Po in Fig. 2); base 15 (13–18; n = 17) [18 (16–20; n = 8)]. Dorsal anchor 48 (43–51; n = 15) [51 (48–57; n = 11)] long, with elongate superficial root, short to non-existent deep root, slightly arced shaft, elongate recurved point. Ventral bar 26 (23–30; n = 12) [33 (31–35; n = 3)] long, bilaterally flattened with well-differentiated anteromedial process which is basally covered by a vellum-like fine tissue, a concavity divided into two lateral rounded expansions distally. Dorsal bar 45 (42–47; n = 13) [57 (50–67; n = 3)] long, with slightly expanded ends, indistinct saucer-shaped flange closely appressed to bar proper. Hook 12 (12–13; n = 14) [12 (11–13; n = 14)] long; filamentous hooklet (FH) loop about 70% shank length.

thumbnail Figures 9–14.

Haptoral and copulatory complex sclerites of Aristocleidus lacantuni n. sp. from the gills of Eugerres mexicanus. 9: dorsal anchor; 10: ventral anchor; 11: ventral bar; 12: dorsal bar; 13: hook; 14: Copulatory complex. Figures are drawn to the following scales: 20 μm (Figs. 9–12 and 14) and 5 μm (Fig. 13).

Differential diagnosis

Placement of this new species in Aristocleidus is based on agreement with the amended generic diagnosis provided by Kritsky and Mendoza-Franco [8], i.e., species with gonads overlapping, ventral anchors with deeply incised base forming deep and superficial roots, a coiled tube of the MCO (non-articulated with the accessory piece) in a clockwise orientation, and haptoral hooks with upright acute thumb, slender shank comprising one subunit and FH loop. A. mexicanus n. sp. most resembles A. hastatus and Aristocleidus sp. from Gerres cinereus from Chautengo Lagoon from Guerrero State (Mexican Pacific) in having ventral bar with conspicuous anteromedial process and by the general morphology of the vaginal tube. A. mexicanus n. sp. differs from these two latter species and A. lamothei mainly in the length (i.e., 46–50 µm vs. 38–43, 34–37, and 26–33, respectively) and shape (i.e., slightly angular union of elongate arcing shaft and point [see Au, Sh and Po, respectively, in Fig. 2] vs. point and shaft united at a conspicuous angular bend in A. hastatus and Aristocleidus sp. and evenly curved shaft and point in A. lamothei) of their ventral anchors and by having a coiled tube of the MCO with less than one ring (a coiled tube of about 1½ in Aristocleidus sp.), a vaginal tube moderately long (short vaginal tube in A. lamothei and looping in Aristocleidus sp.), and an ornate distal end of the accessory piece (distally flattened and trifid accessory piece in A. hastatus and A. lamothei, respectively) [8, 11].

Aristocleidus lacantuni n. sp.

urn:lsid:zoobank.org:act:6A4D7AD9-B9D8-48E7-85FF-37A182476C2D

Type-host: Eugerres mexicanus (Steindachner, 1863) (Perciformes, Gerridae).

Site of infection: Gill lamellae.

Type locality and collection date: Rio Lacantún basin (16°09′96.6″ N, 90°95′56.9″ W), August 2014.

Specimens deposited: holotype, three paratypes in CNHE (9875 and 9876, respectively).

Etymology: named after the location (i.e., Rio Lacantún) from which this species was found.

Description (Figs. 9–14)

Diagnosis (based on four specimens) includes the following: Body 302–342 long; greatest width 90–102 usually near body midlength. Cephalic lobes well developed; each head organ comprising groupings of terminations of cephalic-gland ducts. Pharynx 27 wide, subspherical to elongate ovate. Testis ovate; seminal vesicle comparatively large, fusiform; prostatic reservoir pyriform. Copulatory complex 27 (23–30; n = 4) long. MCO comprising proximal funnel-shaped base, coiled tube loose, comprising about 0.5 poorly defined ring, appearing U-shaped; poorly defined Z-shaped accessory piece. Germarium 44–48 long, 16 wide; vaginal tube short, opening on left side of the body, poorly sclerotized (not depicted); vitellarium dense, vitelline ducts not observed. Haptor 55–58 wide. Ventral anchor 26 (25–28; n = 7) long, with straight shaft and elongate arcing point, base with fused roots, ventrally bent; base 10 (9–11; n = 7). Dorsal anchor 36 (35–38; n = 7) long, with elongate superficial root with a small distal knob-like extension, short to non-existent deep root, slightly arced shaft, elongate recurved point. Ventral bar 26 (24–28; n = 3) long, with conspicuous anteromedial process with terminal horn-like ornamentation; dorsal bar 25 (22–29; n = 3) long, straight, rod-shaped. Hook 11 (10–13; n = 10) long; FH loop about 60% shank length.

Differential diagnosis

The morphology of the haptoral and copulatory sclerites of this species clearly allows its formal generic assignment within Aristocleidus. A. lacantuni n. sp. resembles A. hastatus and A. lamothei in the length of the copulatory complex, i.e., 23–30 vs. 27–36 and 22–26, respectively. It differs from these latter species as well as A. mexicanus n. sp. and Aristocleidus sp. in having shorter anteromedial process of the ventral bar (comparatively larger in A. hastatus, A. mexicanus n. sp., and Aristocleidus sp. and indistinct in A. lamothei) and a ventral anchor with straight shaft and elongate arcing point (point and shaft united at a conspicuous angular bend in A. hastatus and Aristocleidus sp., evenly curved shaft and point in A. lamothei, and elongate arcing shaft and straight point [slightly angular union] in A. mexicanus n. sp.) [8, 11].

Discussion

The diagnostic characters used previously to differentiate species of Aristocleidus involved the morphology of the haptoral armament (i.e., shape of the connection between shaft and point of anchors) and copulatory complex (i.e., shape of the distal end of the accessory) [8, 11]. This study showed that these characters are reliable for separation of A. mexicanus n. sp. and A. lacantuni n. sp. The occurrence of species of Aristocleidus on primarily marine fish (i.e., species of Diapterus) has generated the hypothesis that these parasite species originated in the marine environment [8]. For example, A. hastatus and A. lamothei have been reported from Eugerres plumieri, Diapterus auratus, and Diapterus rhombeus from rivers (i.e., Rio Maquinas in Veracruz State) and/or estuarine systems (i.e., Ria Celestún in Yucatán State) draining to the Gulf of Mexico. Similarly, on the Pacific coast of Mexico and Panama, these monogeneans as well as Aristocleidus sp. have been reported from Diapterus peruvianus and Gerres cinereus from the Chautengo and Tres Palos Lagoons in Guerrero State and Eugerres brasilianus from Gatun Lake in Panama [8, 11].

However, this study demonstrates that A. mexicanus n. sp. and A. lacantuni n. sp. in Eugerres mexicanus are clearly secondary invaders of freshwater. E. mexicanus inhabit freshwater habitats along the rivers Grijalva-Usumacinta and Coatzacoalcos basins in southeastern Mexico (Chiapas, Tabasco, and Veracruz) and northern Guatemala [14, 15], with a noteworthy distribution in highlands with elevations of 100–300 m [4] (i.e., Río Lacantún basin) and the northern part of Guatemala (upper Usumacinta). Thus, a marine ancestor of these monogeneans along with their hosts could have colonized this freshwater environment from which they speciated through adaptive processes (evolutionary radiation of fish in this region indicates old ichthyofauna dated from the late Cretaceous [60 Mya]) [1, 10]. To date, A. mexicanus n. sp. and A. lacantuni n. sp. appear to be limited or dominant under freshwater conditions, while their euryhaline or marine congeneric species are absent or uncommon. In fact, there are other examples of tropical marine species of monogeneans that have secondarily invaded freshwater, i.e., species of Euryhaliotrema Kritsky & Boeger, 2002 (Dactylogyridae) and Diplectanum Diesing, 1858 (Diplectanidae) from South American freshwater croakers, Plagioscion spp. (Sciaenidae) [6, 9]. Examination of other freshwater gerreids in the Rio Lacantún basin (i.e., Eugerres castroaguirrei González-Acosta & Rodiles-Hernández 2013) would help to clarify the rule of the freshwater vs. saltwater on the presence or absence of species of Aristocleidus. For example, salinity has been reported to be a determining factor for the occurrence of species of Rhabdosynochus (Diplectanidae) on snooks, Centropomus spp. (Centropomidae) in Florida [5].

Knowledge about the phylogenetic affinities between gerreids and the moronid type host (i.e., M. saxatilis) of the first described species of Aristocleidus (i.e., A. hastatus) is unknown. Chen et al. [2] provided a molecular phylogenetic hypothesis using four genera (D. auratus plus E. plumieri and Eucinostomus gula [Quoy & Gaimard] plus G. cinereus) of the Gerreidae including other percomorph fishes and stated that this latter host family is monophyletic. In that hypothesis, gerreids are placed at an intermediate position in the percomorph tree between early branching lineages such as scombrids (i.e., Scomberomorus commerson [Lacépède]), serranids (i.e., Holanthias chrysostictus [Günther]), and a terminal clade containing tetraodontiforms (i.e., Takifugu rubripes [Temminck & Schlegel]), Lutjanids (i.e., Lutjanus analis [Cuvier]), and other percoid relatives such as north American moronids, i.e., Dicentrarchus labrax (Linnaeus). These gerreids within the phylogenetic hypothesis of Chen et al. [2] suggest that this gerreid group is comparatively old and predates the origins of the Moronidae. If this were true, then, the occurrence of A. hastatus on M. saxatilis apparently took place comparatively recently and probably corresponds to the concomitant colonization of an anadromous common ancestor to this host family that gave rise to the north American estuarine and freshwater species [17]. It is clear that further surveys of species of Aristocleidus infesting gerreids (and probably moronids) from the western Atlantic and the eastern Pacific will be necessary to understand the diversification of Aristocleidus spp. in the tropical areas.

Acknowledgments

This study was supported by the project “Conservación, manejo y restauración de los ecosistemas acuáticos del Río Lacantún”, promoted and coordinated by the Centro Interdisciplinario de Biodiversidad y Ambiente (CeIBA), A.C. with financing from Natura y Ecosistemas Mexicanos A.C.

References

  1. Briggs JC. 1994. The genesis of Central America: biological versus geophysics. Global Ecology Biogeography, 4, 169–172. [CrossRef] [Google Scholar]
  2. Chen WJ, Ruiz-Carus R, Ortí G. 2007. Relationships among four genera of mojarras (Teleostei: Perciformes: Gerridae) from the western Atlantic and their tentative placement among percomorph fishes. Journal of Fish Biology, 70, 202–218. [CrossRef] [Google Scholar]
  3. De La Cruz-Agüero J, García-Rodríguez FJ, De la Cruz-Agüero G, Díaz-Murillo BP. 2014. Identification of gerreid species (Actinopterygii: Perciformes: Gerreidae) from the Pacific coast of Mexico based on sagittal otolith morphology analysis. Acta Ichthyologica et Piscatoria, 42, 297–306. [CrossRef] [Google Scholar]
  4. González-Acosta AF, Rodiles-Hernández R. 2013. New species of Eugerres from the Usumacinta Province, Mexico and Guatemala with a redescription of E. mexicanus (Steindachner, 1863) (Teleostei: Gerreidae). Neotropical Ichthyology, 11, 307–318. [CrossRef] [Google Scholar]
  5. Kritsky DC, Bakenhaster MD, Fajer-Avila EJ, Bullard SA. 2010. Rhabdosynochus spp. (Monogenoidea: Diplectanidae) infecting the gill lamellae of snooks, Centropomus spp. (Perciformes: Centropomidae), in Florida, and redescription of the type species, R. rhabdosynochus. Journal of Parasitology, 96, 879–886. [CrossRef] [Google Scholar]
  6. Kritsky DC, Boeger WA. 2002. Neotropical Monogenoidea. 41: New and previously described species of Dactylogyridae (Platyhelminthes) from the gills of marine and freshwater perciform fishes (Teleostei) with proposal of a new genus and hypothesis on phylogeny. Zoosystema, 24, 7–40. [Google Scholar]
  7. Kritsky DC, Boeger WA, Thatcher VE. 1985. Neotropical Monogenea. 7. Parasites of the pirarucu Arapaima gigas (Cuvier), with descriptions of two new species and redescription of Dawestrema cycloancistrium Price and Nowlin, 1967 (Dactylogyridae: Ancyrocephalinae). Proceedings of the Biological Society of Washington, 98, 321–331. [Google Scholar]
  8. Kritsky DC, Mendoza-Franco EF. 2008. Revision of Aristocleidus Mueller, 1936 (Monogenoidea: Dactylogyridae), rediscovery of Aristocleidus hastatus Mueller, 1936, and description of Aristocleidus lamothei sp. n. from the Peruvian Mojarra, Diapterus peruvianus (Teleostei: Gerreidae), in Mexico. Revista Mexicana de Biodiversidad, 79 75–82. [Google Scholar]
  9. Kritsky DC, Thatcher VE. 1984. Neotropical Monogenea. 6. Five new species of Diplectanum (Diplectanidae) from freshwater teleosts, Plagioscion spp. (Sciaenidae), in Brazil. Proceedings of the Helminthological Society of Washington, 97, 432–441. [Google Scholar]
  10. Lundberg JG, Sullivan PG, Rodiles-Hernandez R, Hendrickson DA. 2007. Discovery of African roots for Mesoamerican Chiapas catfish, Lacantunia enigmatica, requires an ancient intercontinental passage. Proceedings of the Academy of Natural Sciences of Philadelphia, 156, 39–53. [CrossRef] [Google Scholar]
  11. Mendoza Franco EF, Violante-González J, Roche DG. 2009. Interoceanic occurrence of species of Aristocleidus Mueller, 1936 (Monogenoidea: Dactylogyridae) parasitizing the gills of gerreid fishes in the Neotropics. Parasitology Research, 105, 703–708. [CrossRef] [PubMed] [Google Scholar]
  12. Mendoza-Franco EF, Reyes-Lizama C, González-Solís D. 2009. Haliotrematoides spp. (Monogenoidea, Dactylogyridae) infecting the gills of grunts (Perciformes, Haemulidae) from the southern coast of Quintana-Roo, Mexico. Journal of Parasitology, 95, 1360–1363. [CrossRef] [Google Scholar]
  13. Midtlyng PJ, Bleie H, Helgason S, Jansson E, Larsen JL, Olesen NJ, Olsen AB, Vennerstrøm P. 2000. Nordic manual for the surveillance and diagnosis of infectious diseases in farmed salmonids. Nordic Council of Ministers: Copenhagen, Denmark. [Google Scholar]
  14. Miller RR, Smith ML. 1986. Origin and geography of fishes of the Central Mexico, in The Zoogeography of North American Freshwater Fishes. Hocutt CH, Wiley EO, Editors. John Wiley & Sons: New York. p. 487–517. [Google Scholar]
  15. Miller RR, Minckley WL, Norris SM. 2006. Freshwater fishes of México. The University of Chicago Press: Chicago, 490 p. [copyright date 2005; published in 2006]. [Google Scholar]
  16. Mueller JF. 1936. New gyrodactyloid trematodes from North American fishes. Transactions of the American Microscopical Society, 55, 457–464. [CrossRef] [Google Scholar]
  17. Williams EP, Peer AC, Miller TJ, Secor DH, Place AR. 2012. A phylogeny of the temperate seabasses (Moronidae) characterized by a translocation of the mt-nd6 gene. Journal of Fish Biology, 80, 110–130. [CrossRef] [PubMed] [Google Scholar]

Cite this article as: Mendoza-Franco EF, Osorio MT & Caspeta-Mandujano JM: Two new species of Aristocleidus (Monogenea) from the gills of the Mexican mojarra Eugerres mexicanus (Perciformes, Gerreidae) from southwestern Mexico. Parasite, 2015, 22, 33.

All Figures

thumbnail Figures 1–8.

Aristocleidus mexicanus n. sp. from the gills of Eugerres mexicanus. 1: whole-mount (composite, ventral view); 2: ventral anchor (Sh, shaft; Au, angular union; Po, point); 3: copulatory complex (dorsal view); 4: dorsal anchor; 5: Ventral bar; 6: dorsal bar; 7: vagina; 8: hook. Figures are drawn to the following scales: 100 μm (Fig. 1), 25 μm (Figs. 2–7), and 10 μm (Fig. 8).
In the text
thumbnail Figures 9–14.

Haptoral and copulatory complex sclerites of Aristocleidus lacantuni n. sp. from the gills of Eugerres mexicanus. 9: dorsal anchor; 10: ventral anchor; 11: ventral bar; 12: dorsal bar; 13: hook; 14: Copulatory complex. Figures are drawn to the following scales: 20 μm (Figs. 9–12 and 14) and 5 μm (Fig. 13).

In the text

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.