Heterobothrium lamothei n. sp. (Monogenea: Diclidophoridae) from the gills of Sphoeroides testudineus (Pisces: Tetraodontidae) from the coast of Yucatán, Mexico

 

Heterobothrium lamothei n. sp. (Monogenea: Diclidophoridae) de las branquias de Sphoeroides testudineus (Pisces: Tetraodontidae) de la costa de Yucatán, México

 

Víctor M. Vidal–Martínez^1* and Edgar F. Mendoza–Franco²

 

¹Laboratorio de Parasitología, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV–IPN) Unidad Mérida, Carretera antigua a Progreso Km. 6, 97310 Mérida, Yucatán, México.

²Smithsonian Tropical Research Institute (STRI), Naos Island Laboratories, Apartado 0843–03092 Balboa, Ancon, Panamá, Republic of Panama.

 

*Correspondent:
vvidal@mda.cinvestav.mx

 

Recibido: 14 septiembre 2007
Aceptado: 27 marzo 2008

 

Abstract

The presence of a member of the genus Heterobothrium is described for the first time from the coast of Yucatán Peninsula, southeastern Mexico. Heterobothrium lamothei n. sp. is recorded parasitizing the gills of the tetraodontid fish Sphoeroides testudineus (Linnaeus, 1758) from 4 coastal lagoons in Yucatán: Celestún (20° 52' N, 90° 24' W), Chelem (21°15'N89°45'W), Dzilam (21°35'N 88°35'W) and Río Lagartos (21°22'N 87°30'W). The new species differs from the other species described in the genus, by a combination of characters including a copulatory organ armed with 12–15 genital hooks, the distal pair of clamps smaller in comparison with the 3 other pairs and by having 15–26 testes. The infection parameters were for Celestun, 47 % of prevalence, number of fish examined (n) = 47, mean abundance of 1.76 ± 9.62; Chelem, 20 % (n = 30), 0.53 ± 8.48; Dzilam, 2 % (n = 60), 0.02 ± 0.00; Río Lagartos, 25 % (n = 59), 0.34 ± 1.58. Heterobothrium lamothei n. sp. may be considered as potentially dangerous species for the aquaculture of S. testudineus due to its direct life cycle hat high fish densities would increase the transmission of this monogenean.

Key words: Monogenea, Heterobothrium, Sphoeroides, Yucatán Peninsula, Gulf of Mexico.

 

Resumen

Se registra por primera vez la presencia de un miembro del género Heterobothrium en la costa de la península de Yucatán, México: Heterobothrium lamothei n. sp., parásito de las branquias del pez tetraodóntido Sphoeroides testudineus (Linnaeus, 1758) en 4 lagunas costeras de Yucatán: Celestún (20° 52' N, 90° 24' O), Chelem (21°15'N89°45'O), Dzilam (21°35'N 88°35'O) y Río Lagartos (21°22'N 87°30'O). La especie nueva difiere de otras del género por un conjunto de características que incluyen un órgano copulador con 12 a 15 ganchos genitales, un par distal de pinzas más pequeño que los 3 pares superiores y un número reducido de testículos (15–26). Los parámetros de infección para las 4 localidades fueron: Celestún: 47 % de prevalencia, 47 peces examinados (n = 47), abundancia media de 1.76 ± 9.62; Chelem: 20 % (n = 30), 0.53 ± 8.48; Dzilam: 2 % (n = 60), 0.02 ± 0.00 y Río Lagartos, 25 % (n = 59), 0.34 ± 1.58. Heterobothrium lamothei se considera potencialmente peligrosa para el cultivo de S. testudineus debido a su ciclo de vida directo y a que las altas densidades de peces en acuacultura propician la transmisión de monogéneos entre hospederos.

Palabras clave: Monogenea, Heterobothrium, Sphoeroides, península de Yucatán, golfo de México.

 

Introduction

Heterobothrium Cerfontaine, 1895 includes 11 species of monogeneans infecting the gills of puffer fishes of the family Tetraodontidae (Williams, 1986; Ogawa, 1991). Some of the species in Heterobothrium, such as Heterobothrium okamotoi Ogawa, 1991, are considered a serious problem for the aquaculture of puffer fish, such as Takifugu rubripes Temminck and Schlegel, 1850 in Japan, and extensive research has been undertaken on its biology (Ogawa et al., 2005a, b; Nakane et al., 2005; Kimura et al., 2006). Only 1 species of Heterobothrium has been reported from the Pacific coast in Mesoamerica: Heterobothrium ecuadori (Meserve, 1938) Sproston, 1946 from the bullseye puffer Sphoeroides annulatus (Jenyns, 1842) from Sinaloa and Salina Cruz, Oaxaca in Mexico (Fajer–Ávila et al., 2004; Lamothe–Argumedo, 1967) and Panama (Caballero et al., 1953), and from an unidentified species of Sphoeroides Lacepède, 1798 from Costa Rica (Caballero and Brenes–Madrigal, 1957). In the Gulf of Mexico, there is only a record of H. ecuadori from the checkered puffer Sphoeroides testudineus (Linnaeus, 1758) in an unpublished MSc. Thesis in Coral Glabes, Florida (Boucher, 1974).

During studies on the helminth fauna of S. testudineus along the coast of Yucatán as part of the POETCY program (Program of Ecological Ordination of the Coastal Territory of Yucatán), a new species of Heterobothrium was found infecting the gills of this host. In this paper, the new species is described and data on its infection parameters on the puffer fish and its geographical distribution in coastal lagoons of Yucatán are provided.

 

Material and methods

Puffers were caught using hook and line and throw nets in 4 coastal lagoons of Yucatán State, Mexico. A total of 196 specimens of S. testudineus were sampled in May 2005. Captured fish were transported to the laboratory of Parasitology at Cinvestav–Mérida, kept alive in aquaria, and in all cases were examined within 8 hours. The gills of each host were removed and examined under dissection microscope and the monogeneans obtained were fixed in 4% formalin, labeled and stored in vials for later evaluation. In some cases, entire fish were fixed in 4% formalin for confirmation of its taxonomic identity. Unstained, flattened specimens mounted in Gray and Wess medium or in glycerin ammonium picrate mixture (GAP) were used only to recognize the morphology of sclerotized structures. After evaluation, specimens fixed with GAP were remounted in Canada balsam (Ergens, 1969). All other measurements were obtained from unflattened specimens stained in acid carmine and mounted in Canada balsam (for details on this technique see Vidal–Martínez et al., 2001). Drawings were made with the aid of a drawing tube using an Olympus microscope with Nomarski interference contrast. Average measurements (all in µm) and standard deviation are followed by ranges and the number of specimens or structures measured (n) in parentheses. Prevalence and mean abundance concepts were applied following Bush et al. (1997). Type and voucher specimens were deposited in the National Helminthological Collection of Mexico (CNHE), Institute of Biology, National Autonomous University of Mexico, Mexico, the United State National Parasite Collection, Beltsville, Maryland (USNPC), the Helminthological Collection of the Laboratory of Parasitology, at Centre for Research and Advanced Studies, National Polytechnic Institute, Mérida, Yucatán, Mexico (CHCM) and the Helminthological Collection of the Institute of Parasitology, Academy of Sciences of the Czech Republic, Ceské Budêjovice, Czech Republic (IPCAS).

 

Description

Heterobothrium lamothei n. sp. (Figs. 1–5)

Measurements based on 13 specimens: Body proper elongate, robust, tapering anteriorly. Total length (including haptor) 2433 ± 381 (1880–3030; n = 13). Maximum width at ovarian level, 503 ± 138 (270–780; n = 13). Haptor 601 ± 103 (450–800; n = 9) long, 560 ± 107 (400–800; n = 12) width. Isthmus absent. Paired buccal organs, 90 ± 8 (80–110; n = 12) in diameter. Pharynx diameter 95 ± 15 (72–120; n = 13). Oesophagus with diverticula; bifurcation of intestine at level of gonopore. Caeca with lateral and median diverticula extending to anterior margin of the haptor. Median branches joined. Caeca confluent at anterior margin of the haptor. Haptor rectangular shaped with 4 short non pedunculated clamps arranged symmetrically about midline. Diameters of clamps: anteriormost (first pair, 180° inverted), 188 ± 43 (125–280; n = 19); second pair largest, 187 ± 33 (130–290); third pair, 180 ± 23 (132–230); fourth pair smallest, 164 ± 22 (117–210). Embryonal marginal hooks absent. Clamp comprising 6 sclerites, 5 in posterior fold and 1 in anterior fold as described by Bychowsky et al. (1976) and Williams (1986). Gonopore midventral. Copulatory organ consisting of muscular subspherical cup armed with 12 to 15 genital hooks arranged in a circle, 80 ± 9 (60–95; n = 13) in diameter. Ejaculatory bulb 36 ± 9 (24–50; n = 8) long by 57 ± 16 (38–84; n = 8) width. Testes numerous, irregularly shaped, between caeca, extending from the postovarian region to the anterior margin of opistohaptor. The mean number of testis per individual was 20 ± 4 (15–26). Ovary elongate, inverted U–shaped 328 ± 97 (201–460; n = 5) long by 189 ± 57 (116–296; n = 7) width, situated at the end of first third of body length. Oviduct running left with genito–intestinal canal entering from right intestinal limb, posteriorly connecting with a vitelline duct and followed by ootype. Uterus large. Large vitelline reservoir lying right to the ovary. Vitelline follicles densely scattered from level of gonopore to the anterior margin of the haptor, coextensive with caecal branches; few follicles extending medially in ovarian region. Eggs not observed. Seminal receptacle and vagina absent.

Taxonomic summary

Type–host: checkered puffer fish Sphoeroides testudineus (Linnaeus, 1798) (Tetraodontidae).

Site of infection: gills.

Type–locality, date, prevalence (%) (n = number of fish examined) and mean abundance ± standard deviation: Celestún, Yucatán, Mexico (20° 52' N, 90° 24' W) May, 2005, 47 % (n = 47), 1.76 ± 9.62 worms per infected fish.

Other localities: Chelem, Yucatán (21°15'N89°45'W), May 2005, 20 % (n = 30), 0.53 ± 8.48 worms per infected fish; Dzilam (21°35'N 88°35'W), May 2005, 2 % (n = 60), 0.02 ± 0.00; Río Lagartos (21°22'N 87°30'W), May 2005, 25 % (n = 59), 0.34 ± 1.58.

Type–specimens: holotype (CNHE 5922) and 1 paratype (CNHE 5923); 2 paratypes (USNPC 100508); 2 paratypes (CHCM 505), and 3 paratypes (IPCAS: M–462).

Etymology: this species is dedicated to Dr. Rafael Lamothe Argumedo in recognition to his outstanding contribution to the Mexican helminthology.

Remarks

Heterobothrium lamothei n. sp. most resembles H. ecuadori in general appearance, however it differs from this latter species by having a smaller copulatory organ (80–95 vs. 114–116 in H. ecuadori) armed with 12–15 genital hooks arranged in a circle instead of 14–16 in H. ecuadori. Furthermore, H. lamothei n. sp. has a rectangular haptor with the distal pairs of clamps smaller in diameter than the 3 previous ones, while H. ecuadori has all clamps similar in size (see Table 1 in Williams, 1986). Heterobothrium lamothei n. sp. also differs from this latter species in the number of testes (15–26 vs. 27–40 in H. ecuadori) (see Table 1 in Williams, 1986). It is noteworthy that the number of testes in H. lamothei n. sp. is relatively similar to that observed in Heterobothrium yamagutii Ogawa, 1991 with 25–30 testes. However, this latter species has a copulatory organ armed with 10 hooks, its 4 pairs of clamps are very similar in size and it is substantially longer in size (7400–14400) than H. lamothei n. sp. (1880–3030).

 

Discussion

Heterobothrium lamothei n. sp. is added to the 11 species currently recognized in Heterobothrium: H. torquigeneri Williams, 1986, H. elongatum Williams, 1986, H. tetrodonis (Goto, 1894) Cerfontaine 1895, H. tonkinensis Yamaguti, 1958, H. praeorchis Bychowsky, Mamaev and Nagibina, 1976, H. ecuadori Meserve, 1938, H. fluviatilis Euzet and Birgi, 1975, H. okamotoi Ogawa, 1991, H. yamagutii Ogawa, 1991, H. shanagawai Ogawa, 1991 and H. bychowskyi Ogawa, 1991. Most of these species have been described from Australian (Williams, 1986) and Japanese (Ogawa, 1991) marine waters. The only species described from America is H. ecuadori. This species was originally described as H. ecuadori by Meserve (1938) from Galapagos. Later, Sproston (1946) erected the new genus Tagia and considered H. ecuadori as a member of Tagia. Tagia ecuadori was described from the gills of Sphoeroides sp. in Mata de Limón, Puntarenas, Costa Rica (see Caballero and Brenes–Madrigal, 1957; Lamothe–Argumedo, 1967). However, as Williams (1986) noted, Euzet and Birgi (1975) revised the genus and considered that species to be a synonym of Heterobothrium Cerfontaine1895 and Gempylitrema Yamaguti, 1968. Thus, by the principle of priority of the ICZN (International Code of Zoological Nomenclature (http://www.iczn.org/iczn/index.jsp), the valid name of the genus is the oldest one, in this case Heterobothrium. There are several records of H. ecuadori in America, from Cheilichthys annulatus Müller, 1841 from Tagus Cove, Albermale, Galapagos Islands and San Francisco (Meserve, 1938). All other geographical records for this monogenean species are those from Sphoeroides annulatus from waters of the Pacific Ocean in the Canal zone, Panama (Caballero et al., 1953), Salina Cruz, Oaxaca (Lamothe–Argumedo, 1967) and Sinaloa in Mexico (Fajer–Ávila et al. 2004). In the Atlantic coast, there is only 1 record for H. ecuadori parasitizing the gills of S. testudineus in Biscayne Bay, Florida in an unpublished MSc. thesis (Boucher, 1974). Boucher (1974) did not provide a formal description of his specimens but, the metric data of the total length (mean = 2200, range 1300–2850, n = 13 specimens) and width (620, 350–850) provided by Boucher are similar to those of H. lamothei n. sp. Due to the geographical closeness between Florida and the Peninsula of Yucatán and the fact that the monogenean was parasitizing the same host species (S. testudineus), it is possible that the material of Boucher belongs to H. lamothei n. sp. If this is true, H. ecuadori is restricted to the Pacific Ocean and H. lamothei n. sp. to the Atlantic coast, and specifically to the Gulf of Mexico at this point.

The prevalence and mean abundance of H. lamothei n. sp. were low for all 4 coastal lagoons that were sampled. The sample size for each of the coastal lagoons was large enough to have a reliable estimation of these infection parameters. However, in the eventual case of aquaculture of this host species, it is predicted that the first helminth species to present numerical increase and a sanitary risk will be H. lamothei n. sp. The basis for this, is that transmission would be enhanced due to the direct life cycle of this monogenean and the increased density of host populations typical of aquaculture. Other authors have stressed this potential danger for the aquaculture of the bullseye pufferfish S. annulatus in the Mexican Pacific coast (Sinaloa) (Fajer–Ávila et al., 2004). This has been found to be a problem for Japanese aquaculture of the puffer fish Takifugu spp., where H. okamotoi is a serious sanitary problem. As a consequence, extensive research has been undertaken on its biology to control the infection (see Ogawa et al., 2005a, b; Nakane et al., 2005; Kimura et al., 2006). Thus, further studies on the biology and therapeutic treatment of H. lamothei n. sp. on its hosts are strongly recommended.

 

Acknowledgements

The authors are indebted to Clara Vivas Rodríguez, Trinidad Sosa Medina, Abril González Rodríguez, Reyna Rodríguez Olayo, Gregory Arjona Torres, Marcela del Río, Francisco Rodríguez, Javier Ramírez, Victor Ceja Moreno, and Mirella Hernández de Santillana from Cinvestav Parasitology, Geochemistry, Toxicology, and Primary Productivity and Necton laboratories for their field and laboratory assistance. This research was financially supported by PEMEX Exploración y Producción through contracts 418815846 (Xcambo II) and 422276804 (Agua de lastre). The financial support for the POETCY program (Plan de Ordenamiento Territorial Costero de Yucatán) to V.V–M., was provided by SEMARNAT, Secretaría de Ecología del Gobierno del Estado de Yucatán, SEDESOL and Sistema Arrecifal Mesoamericano.

 

Literature cited

Boucher, G. C. 1974. Parasites of the checkered puffer, Sphoeroides testudineus, in Biscayne Bay, Florida, with an analysis of host–parasite relationships. M.S. Thesis. The University of Miami, Coral Gables, Florida. 69 p.        [ Links ]

Bush, A. O., K. D. Lafferty, J. M. Lotz and A. W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575–583.        [ Links ]

Bychowsky, B. E., L. Mamaev–Yu and L. F. Nagibina. 1976. Revision of the genus Heterobothrium Cerfontaine, 1895 (Diclidophoridae). Trudy–Biologo–Pochvennogo–Instituta–Issledovaniya–monogenticheskikh–sosal'shchikov,–Novaya–Seriya 34:29–40.        [ Links ]

Caballero, C. E., M. Bravo–Hollis and R. G. Grocott. 1953. Helmintos de la República de Panamá. VII. Descripción de algunos tremátodos de peces marinos. Anales del Instituto de Biología, Universidad Nacional Autónoma de México, Serie Zoología 24:98–136.        [ Links ]

Caballero, C. E. and R. Brenes–Madrigal. 1957. Helmintos de la República de Costa Rica. VI. Algunos tremátodos de peces, reptiles y mamíferos. Anales del Instituto de Biología, Universidad Nacional Autónoma de México, Serie Zoología 28:217–240.        [ Links ]

Ergens, R. 1969. The suitability of ammonium picrate–glycerin in preparing slides of lower Monogenoidea. Folia Parasitologica 16:320.        [ Links ]

Euzet, L. and E. Birgi. 1975. Heterobothrium fluviatilis n. sp. (Monogenea, Diclidophoridae), gill parasite of Tetraodon fahaka Bennett 1834 (Teleostei) in Chad. Bulletin de la Societe Zoologique de France 100:411–420.        [ Links ]

Fajer–Ávila, E. J., A. Roque, G. Aguilar and N. Duncan. 2004. Patterns of occurrence of the platyhelminth parasites of the wild bullseye puffer (Sphoeroides annulatus) of Sinaloa, Mexico. Journal of Parasitology 90:415–418.        [ Links ]

Kimura, T., M. Sameshima, Y. Nomura, J. Morita, H. Mizoguchi and M. Ishihara 2006. Efficacy of Orally Administered Febantel against Monogenean Heterobothrium okamotoi infection of Cultured Tiger Puffer Takifugu rubripes. Fish Pathology 41:147–151.        [ Links ]

Lamothe–Argumedo, R. 1967. Monogeneos de peces. V. Redescripción de Tagia ecuadori (Meserve, 1938) Sproston, 1946. Anales del Instituto de Biología, Universidad Nacional Autónoma de México, Serie Zoología 38:35–46.        [ Links ]

Meserve, F. G. C. 1938. Some monogenetic trematodes from Galapagos Islands and the neighbouring Pacific. Allan Hancock Pacific Expedition 2:31–89.        [ Links ]

Nakane, M., K. Ogawa, T. Fujita, M. Sameshima and H. Wakabayashi. 2005. Acquired protection of tiger puffer Takifugu rubripes against infection with Heterobothrium okamotoi (Monogenea: Diclidophoridae). Fish Pathology 40:95–101.        [ Links ]

Ogawa, K. 1991. Redescription of Heterobothrium tetrodonis (Goto, 1894) (Monogenea: Diclidophoridae) and other related new species from puffers of the genus Takifugu (Teleostei: Tetraodontidae). Japanese Journal of Parasitology 40:388–396.        [ Links ]

Ogawa, K., N. Yamabata and T. Yoshinaga 2005a. Egg–laying of the monogenean Heterobothrium okamotoi on experimentally infected tiger puffer Takifugu rubripes. Fish Pathology 40:111–118.        [ Links ]

Ogawa, K., M. Yasusaki and T. Yoshinaga 2005b. Experiments of the blood feeding of Heterobothrium okamotoi (Monogenea: Diclidophoridae). Fish Pathology 40:169–174.        [ Links ]

Vidal–Martínez, V. M., M. L. Aguirre–Macedo, T. Scholz, D. González–Solís and E. F. Mendoza–Franco. 2001. Atlas of the helminth parasites of cichlid fish of Mexico. Academia, Prague. 185 p.        [ Links ]

Williams, A. 1986. Taxonomy of two new species of Heterobothrium (Monogenea: Diclidophoridae) from Torquigener pleurogramma (Pisces: Tetraodontidae) from western Australia. Australian Journal of Zoology 34:707–715.        [ Links ]