versión impresa ISSN 1870-3453
Rev. Mex. Biodiv. v.78 n.2 México dic. 2007
Didymozoid Monilicaecum type trematodes in chaetognaths from the Mexican Caribbean Sea
Tremátodos didimozoides tipo Monilicaecum en quetognatos del mar caribe mexicano
María del Carmen Gómez del PradoRosas1, José N. ÁlvarezCadena2, Lourdes SeguraPuertas2 and Rafael LamotheArgumedo3*
1 Universidad Autónoma de Baja California Sur, Departamento de Biología Marina, Apartado postal 19B, 23080, La Paz, Baja California Sur, México.
2 Instituto de Ciencias del Mar y Limnología, Unidad Académica Puerto Morelos, Universidad Nacional Autónoma de México, Apartado postal 1152, 77501, Cancún, Quintana Roo, México.
3 Instituto de Biología, Universidad Nacional Autónoma de México, Apartado postal 70153, 04510, México.
Recibido: 14 marzo 2006
Aceptado: 01 febrero 2007
Analyses of 22,508 holoplanktonic chaetognaths collected at 21 stations were made from four oceanographic campaigns along the coasts of Quintana Roo, Mexico, in 1991 (Caribe I = February; Caribe II = March; Caribe III = May; Caribe IV= August). Unencysted larval didymozoid parasites were identified as belonging to the Monilicaecum type because of the arrangement of the chambers of the heavily twisted intestinal caeca, which occupy nearly the entire body. These larvae were found in the coelom of seven individuals of the chaetognath Flaccisagitta enflata (prevalence = 0.03, mean intensity = 1) and in two of Serratosagitta serratodentata (prevalence = 0.009, mean intensity = 1). The Mexican Caribbean Sea is reported as a new locality for this type of helminth larvae.
Key words: Didymozoidae, Monilicaecum, chaetognaths, Mexican Caribbean Sea.
Se analizan 22,508 quetognatos holoplánticos capturados en 21 estaciones a lo largo de las costas del estado de Quintana Roo, México durante 1991 (Caribe I= febrero; Caribe II= marzo; Caribe III mayo; Caribe IV= agosto). Las formas no enquistadas de los parásitos didimozoides fueron identificadas como tipo Monilicaecum debido al arreglo de las cámaras de los ciegos intestinales fuertemente sinuosas que ocupan casi la totalidad de la cavidad corporal. Las larvas tipo Monilicaecum fueron encontradas en el celoma de siete quetognatos de la especie Flaccisagitta enflata (prevalencia= 0.03; intensidad promedio de parasitismo = 1) y en dos ejemplares de Serratosagitta serratodentata (prevalencia = 0.009, intensidad promedio = 1). El mar caribe mexicano es registrado como una nueva localidad para esta larva de helminto.
Palabras clave: Didymozoide, Monilicaecum, quetognatos, mar caribe mexicano.
Didymozoid trematode larvae have been frequently reported from the coelomic cavity of planktonic chaetognaths (Nagasawa, 1991, Øresland and Bray, 2005), from the digestive tract of cephalopod paralarvae (Vidal and Haimovici, 1999), as endoparasites (Tolonen and Karlsbakk, 2003) or externally on the dorsal musculature of fish larvae (Karlsbakk, 2001), or even in the digestive tract of snakes (Fischthal and Kuntz, 1965). Although two didymozoid larval types are presently recognized, Torticaecum and Monilicaecum, the second is more frequently found in tropical, subtropical and temperate waters (Nagasawa, 1991).
Adult didymozoids have been recorded in the tissues of pelagic bony fishes (Yamaguti, 1970, 1971), particularly in the subfamily Thunninae (Scombridae) (Cribb et al., 2000). Nagasawa and Marumo (1981) suggested that the fl atfish Cleisthenes pinetorum Jordan et Starks, 1904 is one of the definitive hosts for this kind of helminth. In Todos Los Santos Bay, Ensenada, México, Caballero y Caballero and CaballeroRodríguez (1971) described Unitubulotestis maris as a new adult species of didymozoid from the scombrid fish Sarda lineolata (Girard, 1858). In the present study didymozoid trematode metacercariae were found in the coelom of the chaetognaths Flaccisagitta enflata Grassi 1881 and Serratosagitta serratodentata (Krohn,1853) and are reported for the first time for the Mexican Caribbean Sea.
Studies on chaetognath species assemblages were carried out along the Caribbean Sea, in the vicinity of the coasts of Mexico, during February, March, May and August 1991, using a conic net 0.5m mouth diameter, with 330µ mesh (see Gasca et al., 1996 for study area and methods). A total of 22,508 chaetognaths were identified to species, and those containing parasites were sorted out and further analyzed. Hosts and parasites were stained together with acetic carmine, cleared with methyl salicylate and mounted in permanent slides in Canada balsam. Minimum and maximum size measurements of parasites (in mm, mean and SD in parenthesis) were made with a scaled eye piece, and prevalence and mean infection intensity follows Bush et al. (1997). Parasites are deposited at the Colección Parasitológica del Museo de Historia Natural de la Universidad Autónoma de Baja California Sur (CPMHNUABCS), catalog numbers 233 to 240.
Flaccisagitta enflata and Serratosagitta serratodentata are chaetognaths with a wide distribution in all seas of the world (Alvariño, 1965). Both species are common and frequently collected in the Puerto Morelos coral reef lagoon (RamírezÁvila and ÁlvarezCadena, 1999), and both have been reported previously as host for other didymozoid metacercariae (Torticaecum type) (Gómez del PradoRosas et al., 1999a) or other trematodes (Gómez del PradoRosas et al., 1999b; 2002, 2005).
Nine Monilicaecum type larvae were found in 22,508 chaetognaths, seven in the coelom of Flaccisagitta enflata (Caribe I, II and IV) and two in Serratosagitta serratodentata (Caribe IV). Prevalence was low (0.03 for the first chaetognath species and 0.009 for the second). Mean intensity in both cases was 1 (Table 1).
The Monilicaecum type metacercariae recorded here present the following features and measurements: Body cylindrical, 0.117 to 0.242 (0.167; SD = 0.040) long and 0.04to 0.075 (0.056; SD= 0.010) wide. Hindbody wider than forebody. Tegument smooth. Oral sucker slightly elongated, relatively large and muscular, 0.014 to 0.035 (0.019; SD=0.007) long and 0.010 to 0.021 (0.015; SD= 0.004) wide. Acetabulum preequatorial, 0.018 to 0.035 (0.026; SD=0.010) in length, and 0.017 to 0.034 (0.026; SD=0.005) wide. Sucker ratio 1:1.3 in average. Pharynx inconspicuous, observed only in four specimens, 0.006 to 0.009 (0.008; SD= 0.004) long and 0.005 to 0.011 (0.008; SD= 0.004) wide. Esophagus not observed, due to contraction of parasites. Stomach dorsal to acetabulum. Parenchymal tissue finely granulated, observed along the entire body. Caeca heavily twisted and occupying nearly all body. Nine intestinal chambers observed running from postacetabular region to posterior end of body. Caeca wider posteriorly ending blindly and independently. One specimen with two small genital primordia posterior to ventral sucker. Excretory vesicle globular, short, ending in a conspicuous excreting pore near posterior end of body (Fig. 1).
The metacercariae from this study were identified as belonging to the Monilicaecum type because of the presence of a stomach and the arrangement of the chambers of the intestinal caeca, in contrast with the absence of the stomach and the tubular caeca of the Torticaecum type (Yamaguti, 1970, 1971). The larvae analyzed in this study are similar to those described by Shimazu (1978) in the form and position of the stomach. However, his larvae were different in the number of chambers (48) instead of 9 from the larvae of this study. Our larvae are different from those moniliform reported by Nikolaeva (1965) larvae I, as in her specimens the acetabulum is smaller than the oral sucker, presented a preacetabular glandular region and also showed a tubular narrow caeca anterior to the formation of the caecal chambers. Our larvae are different from Nikolaeva's Monilicaecum ventricosum Yamaguti, 1942 for lacking glands external to the stomach. Didymozooids reported by Fischthal and Kuntz (1964) are also different from parasites of this work for lacking stomach (immature didymozoid A and Torticaecum nipponicum) and some of them also lack acetabulum (immature didymozoid B).
The parasites reported by Fischthal and Thomas (1968) and Køie and Lester (1985) differ from our material in presenting a compact glandular mass surrounding the stomach and the ceca (didymozoids D, E), or a considerable larger glandular part in the walls of each ceca (didymozoids F, G); also, the acetabulum is smaller than the oral sucker (didymozoids Nikolaeva's larvae I, D, F.). Didymozoids reported by Koie and Lester (1985) also differ from our material by having numerous gland cells at the posterior half of forebody and anterior third of hindbody (sp. 1, 3, 4), by the presence of a cecal bifurcation at anteriormost acetabular level (sp. 1), by an anterior tubular part of each cecum (sp. 1, 3, 7), by having long tubular ducts connecting the anteriormost cecal chambers (sp.4), by the presence of eyespots (sp.7), and by having cecum of different length (sp. 8). Differences with the didymozoid larvae reported by Karlsbakk (2001) are: glandular regions on the forebody, an anterior non granular zone and a posterior glandular area between the ganglion and the hindbody, stomach absent, presence of non granular cells in the parenchyma of the hindbody, and the larger size of the parasites (23.5 to 41.8 mm). However, his metacercariae have a small pharynx, a similar number of chambers as ours and the caeca are also moniliform.
For classification of didymozoid larvae, Nikolaeva (1965) considered features as body size, body lengthwidth ratio, the distance between suckers, and the identity of parasitized hosts. However, Fischthal and Kuntz (1964) and Yamaguti (1970) considered those criteria to be doubtful due to the extreme variability associated with age. Kurochkin and Nikolaeva established differences among didymozoid larvae based on the presenceabsence of acetabulum, pharynx, stomach, gland cells and the relative position of the cecal bifurcation and acetabulum. Later, Køie and Lester (1985) reported that the stomach always disappears with age, and observed that the younger developmental stages show the presence of a pharynx and an acetabulum. These structures are therefore, of no taxonomic value. They concluded that it is impossible to assign larval didymozoids to genera or higher taxonomic levels, suggesting that the larval didymozoids should not be given Latin names to avoid a double taxonomic system, one for the larvae and one for the adults, a position that we share in this study.
The prevalence and infection intensity of Monilicaecum type larvae is low in planktonic animals as it has been reported for chaetognaths by Shimazu (1978), for copepods by Madhavi (1968) and in reef fish larvae by Cribb et al. (2000).
The didymozoid life cycle is complex, and it is accepted that three or four hosts can be required to complete it (Hochberg, 1990). Madhavi (1968) believes that crustaceans are possibly the second intermediate host for hemiuriforms (Hemiuridae and Didymozoidae), because she recorded Monilicaecum type larvae in the body cavity of Paracalanus aculeatus Giesbrecht in Waltair, Bengala Bay. Cable and Nahhas (1962) suggested that the cirripedian genus Lepas acts as a second intermediate host as they found Monilicaecum type larvae in these crustaceans and later found both, the crustaceans and helminths, in the stomach of the dolphin fish Coryphaena hippurus Linnaeus.
Madhavi (1968) suggested that fish larvae are paratenic hosts, obtaining the infection when consuming parasitized copepods. Cribb et al. (2000) mentioned that although coral reef fishes, as Lethrinidae and Serranidae, with carnivorous feeding habits, can be the third intermediate host, pelagic fishes like tuna (Scombridae), particularly the subfamily Thunninae (tropical Pacific) are the top and final hosts for adults. Lester (1980) found didymozoid larvae in the intestinal wall of several forager species such as Engraulis australis Steindachner, 1879, Pranesus ogilbyi Whitley, 1930, Sillago analis Whitley, 1943, S. maculata Quoy et Gaimard, 1824, Pelates quadrilineatus Cuvier et Valenciennes, 1829, Rhinogobius leftwitchi Ogilby, 1910; Favonigobius exquisitus Whitley, 1930 and Pseudogobius sp., suggesting that these species may be paratenic hosts, and that infection of the final host would be accomplished when larger pelagic fishes feed on them.
In other words the metacercariae do not show any preference for paratenic hosts and can be found in cartilaginous fishes as Rhinobatidae or several orders of bony fishes such as Clupeiforms (Clupeidae, Engraulidae), Atheriniforms (Atherinidae), Beloniforms (Exocoetidae) Scorpaeniforms (Scorpaenidae ) Perciforms (Serranidae, Pomadasydae,Carangidae, Sciaenidae, Labridae, Sparidae, Gerreidae, Gobiidae, Scombridae, Mullidae), Pleuronectiforms (Cynoglossidae, Bothidae) or Tetraodontiforms (Tetraodontidae,) among others.
Nagasawa and Marumo (1981) reported that fl atfishes can be final hosts for Monilicaecum as is Cleisthenes pinetorum. On the other hand, Cribb et al. (2000) suggested that chaetognaths are paratenic hosts for Monilicaecum, and Shimazu (1978) believes that chaetognaths, due to its importance in the food web, can be also a link for the third intermediate host or for the final host, i.e. pelagic bony fishes (Yamaguti, 1971). Considering the findings of Madhavi (1968), the infection route for chaetognaths with Monilicaecum type larvae is possibly with parasitized microcrustaceans such as copepods. In Puerto Morelos reef lagoon, México, trematode larvae have been observed going through the chaetognath skin (unpublished data). Another possibility is that chaetognaths could be infected in the same way as are squids i.e. chaetognaths ingesting the cercariae directly from the water column (Hochberg, 1990).
For the Mexican Caribbean Sea, there is only one previous report for dydimozoids, identified as Torticaecum type (Gómez del PradoRosas et al., 1999a), thus, this is the first report for Monilicaecum larvae in this area. In both cases the life cycle of these parasites are far from being completely known.
We thank Eduardo Suárez Morales and Rebeca Gasca from El Colegio de la Frontera SurUnidad Chetumal, for supplying the biological material. Alma Rosa Almaral helped with the edition of the figure and search of literature.
Alvariño, A. 1965. Chaetognaths. Oceanography and Marine Biology Annual Review 3:115195. [ Links ]
Bush, L. G., W. Esch, J.C. Holmes, A.M. Kuris, and G.A. Schad. 1997. The use of ecological terms in parasitology. Journal of Parasitology 68:131133. [ Links ]
Caballero y Caballero, E. and G. CaballeroRodríguez. 1971. Presencia de una nueva especie de tremátoda de la familia Didymozoidae que parasita a peces marinos de Ensenada, Baja California, México. Anales del Instituto de Biología, Universidad Nacional Autónoma de México. 42. Serie Ciencias del Mar y Limnología 1:5764. [ Links ]
Cable, R. M. and F.M. Nahhas. 1962. Lepas sp., second intermediate host of a didymozoid trematode. Journal of Parasitology 48:34. [ Links ]
Cribb, T. H., S. Pichelin, V. Dufour, R. A. Bray, C. Chauvet, E. Faliex, R. Galzin, C. M. Lo, A. LoYat, S. Morand, M. C. Rigby and P. Sasal. 2000. Parasites of recruiting coral reef larvae in New Caledonia. International Journal of Parasitology 30:14451451. [ Links ]
Fischthal, J.H. and R. E. Kuntz. 1964. Digenetic trematodes of fishes from Palawan Island, Phillipines. IV. Some immature Didymozoidae, a bucephalid; a new hemiuroid genus and subfamily. Journal of Parasitology 50:253260. [ Links ]
Fischthal, J.H.and R. E. Kuntz. 1965. Digenetic trematodes of amphibians and reptiles from North Borneo (Malaysia). Proceedings of the Helminthological Society of Washington 32:125136. [ Links ]
Fischthal, J.H. and J.D. Thomas. 1968. Digenetic trematodes of marine fishes from Ghana: families Acanthocolpidae, Bucephalidae, Didymozoidae. Proceedings of the Helminthological Society of Washington 35:237247. [ Links ]
Gasca, R., J. N. ÁlvarezCadena, and E. SuárezMorales. 1996. Chaetognath assemblages in the Mexican Caribbean sea (1991). Caribbean Marine Studies 5:110. [ Links ]
Gómez del PradoRosas, M. C., J. N. ÁlvarezCadena, L. SeguraPuertas, and R. LamotheArgumedo. 1999a. First record of Torticaecum sp. (Trematoda: Didymozidae) in the chaetognath Serratosagitta serratodentata (Krohn, 1853) from Caribbean waters. Journal of Plankton Research 21:10051008. [ Links ]
Gómez del PradoRosas, M. C. 1999b. New records, hosts, and SEM observations of Cercaria owreae (Hutton,1954) from the Mexican Caribbean Sea. Journal of the Helminthological Society of Washington 66:194197. [ Links ]
Gómez del PradoRosas, M. C. 2002. An accacoelidmetacercaria parasitizing Flaccisagitta enflata (Grassi,1881) from the Mexican Caribbean Sea. ComparativeParasitology 69:108111. [ Links ]
Gómez del PradoRosas, M. C.. 2005. Hemiurid metacercariae (Trematoda) in Chaetognaths from the Mexican Caribbean Sea. Comparative Parasitology 72:230233 [ Links ]
Hochberg, F. G. 1990. Diseases of Mollusca: Cephalopoda. Diseases caused by protistans and metazoans. In Diseases of Marine Animals. O. Kinne (ed.). Biologische Anstalt Helgoland, Hamburg, Germany. p. 115125. [ Links ]
Karlsbakk, E. 2001. Didymozoid larvae (Trematoda) in the body musculature of cultured Atlantic herring larvae (Clupea harengus). Acta Parasitologica 46:164170. [ Links ]
Køie, M. and R. J. G. Lester. 1985. Larval didymozoids (trematoda) in fishes from Moreton Bay, Australia. Proceedings of the Helminthological Society of Washington 52:196203. [ Links ]
Lester, J.G. 1980. Hostparasite relation in some didymozoid trematodes. Journal of Parasitology 66:527531. [ Links ]
Madhavi, R. 1968. A didymozoid metacercaria from the copepod Paracalanus aculeatus Giesbrecht, from Bay of Bengal. Journal of Parasitology 54:629. [ Links ]
Nagasawa, S. 1991. Parasitism and diseases in Chaetognaths. In The Biology of Chaetognaths, Q. Bone, H. Kapp and A. C. PierrotBults (eds.). Oxford Science Publications, Oxford. p. 7685. [ Links ]
Nagasawa, S. and R. Marumo. 1981. Chaetognaths as food of demersal fishes in the East China Sea. Bulletin Seikai Regional Fishery Research Laboratory 56:113. [ Links ]
Nikolaeva, V. M. 1965. On the developmental cycle of trematodes belonging to the family Didimozoidae (Monticelli, 1888) Poche, 1907. Zoologicheskii. Zhurnal 44:13171327. (Russian text). [ Links ]
Øresland, V. and R.A. Bray. 2005. Parasites and headless chaetognaths in the Indian Ocean. Marine Biology 147:725734. [ Links ]
RamírezÁvila, Y. and J. N. ÁlvarezCadena. 1999. Chaetognath species composition from a coral reef lagoon in the Mexican Caribbean Sea. Revista de Biología Tropical Suplemento 1:157163. [ Links ]
Shimazu, T. 1978. Some helminth parasites of the Chaetognatha from Suruga Bay, Central Japan. Bulletin of the National Science Museum Serie A (Zoology) 4:105116. [ Links ]
Tolonen, A. and E. Karlsbakk. 2003. Parasites of herring (Clupea harengus L.) larvae from a local Norwegian fjord stock. Sarsia 88:154157. [ Links ]
Vidal, E. A. G. and M. Haimovici. 1999. Digestive tract parasites in Rhynchoteuthion squid paralarvae, particularly in Illex argentinus (Cephalopoda: Ommastrephidae). Fishery Bulletin 97:402405. [ Links ]
Yamaguti, S. 1970. Digenetic trematode of hawaiian fishes. Keigaku Publishing Co.Tokyo. 436p. [ Links ]
Yamaguti, S. 1971. Synopsis of digenetic trematodes of vertebrates. Vol. I. Keigaku Publishing Co. Tokyo. 1074 pp. [ Links ]