Cestodes of the Family Dilepididae (Cestoda: Cyclophyllidea) from fish-Eating Birds in Mexico: a Survey of Species
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Systematic Parasitology 52: 171–182, 2002. 171 © 2002 Kluwer Academic Publishers. Printed in the Netherlands. Cestodes of the family Dilepididae (Cestoda: Cyclophyllidea) from fish-eating birds in Mexico: a survey of species Tomaš´ Scholz1,2, Roman Kuchta3 & Guillermo Salgado-Maldonado4 1Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovsk´a 31, 370 05 Cesk´ˇ eBudˇejovice, Czech Republic (Address for correspondence) 2Laboratory of Parasitology, Centre for Investigation and Advanced Studies of the National Polytechnic Institute (CINVESTAV-IPN) M´erida Unit, A.P. 73 “Cordemex”, C.P. 97310 M´erida, Yucat´an, Mexico 3Faculty of Biological Sciences, University of South Bohemia, Branišovsk´a 31, 370 05 Cesk´ˇ eBudˇejovice, Czech Republic 4Institute of Biology, National Autonomous University of Mexico (UNAM), A.P. 53-173, C.P. 04510 M´exico, D.F., Mexico Accepted for publication 6th November, 2001 Abstract A survey of adults of dilepidid tapeworms (Cyclophyllidea) from piscivorous birds from Mexico is presented on the basis of the taxonomic evaluation of freshly collected and voucher specimens. The following species are reported (first records from Mexico marked with an asterisk): Cyclustera capito (Rudolphi, 1819); ∗C. ibisae (Schmidt & Bush, 1972); ∗Dendrouterina ardeae Rausch, 1955; ∗D. herodiae Fuhrmann, 1912; ∗D. papillifera (Fuhrmann, 1908); Glossocercus auritus (Rudolphi, 1819); ∗Neogryporhynchus cheilancristrotus (Wedl, 1855); Paradilepis caballeroi Rysavy & Macko, 1973; Paradilepis sp.; Parvitaenia cochlearii Coil, 1955; and Valipora mutabilis Linton, 1927. Dendrouteria herodiae is reported from America for the first time. New definitive hosts are Phalacrocorax olivaceus for C. capito, N. cheilancristrotus and P. caballeroi; Casmerodius albus and Egretta thula for G. auritus;andE. thula for D. herodiae. Data on the morphology of the rostellar hooks of all species, their hosts and distribution in Mexico are provided. Introduction from the boat-billed heron Cochlearius cochlearius (L.) from both Oaxaca and Chiapas. More recently, Tapeworms of the family Dilepididae Railliet & Lamothe-Argumedo et al. (1997) listed four species Henry, 1909 (Eucestoda: Cyclophyllidea) are frequent of dilepidids found in Mexico; namely, Dendrouterina and widely distributed parasites of birds, with many botauri Rausch, 1948 from Egretta thula (Molina), species parasitising fish-eating birds, such herons, Dilepis hilli Polk, 1941 from Bubulcus ibis (L.), and spoonbills and cormorants (Bona, 1994). The taxon- Ophiovalipora minuta (Coil, 1950) and O. nyctico- omy of the group has been treated in detail by Bona racis (Olsen, 1936) from Nycticorax nycticorax (L.). (1975, 1994), but the information on the occurrence of However, no data on the morphology of these species dilepidid cestodes, their species composition and dis- have been provided. tribution in Latin America is rather limited (see Bona, Scholz & Salgado-Maldonado (2001) have re- 1975, 1983a,b). cently found metacestodes of as many as 13 species This is also valid for Mexico, from where only of dilepidid tapeworms in fishes from Mexico, which three records of adult dilepidids have been pub- indicates that cestodes of this family may be relatively lished. Coil (1955a) reported adults of Cyclustera frequent parasites. During studies on the helminth capito (Rudolphi, 1819) from the roseate spoonbill parasites of piscivorous birds from central and south- Platalea ajaja L. from Oaxaca, and the same au- eastern Mexico, several species of dilepidid cestodes thor (Coil 1955b) described Parvitaenia cochlearii 172 were found, with most tapeworms being reported as the National Helminthological Collection of Mexico adults from Mexico for the first time. (CNHE); US National Parasite Collection (USNPC), During the evaluation of this material, all vouch- Beltsville, Maryland, USA; Institute of Parasitology, ers of dilepidids found in Mexico and deposited in Academy of Sciences of the Czech Republic, Ceskéˇ the National Helminthological Collection of Mexico Budejoviceˇ (IPCAS); and The Natural History Mu- (CNHE), Instituto de Biología, Universidad Nacional seum, London, UK (BMNH). The classification pro- Autónoma de México, Mexico City, were also ex- posed by Bona (1975, 1994) is followed in this paper amined and numerous misidentifications were found. and the nomenclature of bird species follows that of Therefore, all available material of dilepidid tape- del Hoyo et al. (1992). Species being reported from worms parasitising fish-eating birds in Mexico has Mexico for the first time are marked with an asterisk. been revised and a survey of species is presented, together with the information on the spectrum of their definitive hosts, geographical distribution and Survey of species life-cycles. Cyclustera capito (Rudolphi, 1819) Fuhrmann, 1901 (Figure 1A) Materials and methods Host and locality: Phalacrocorax olivaceus (Hum- The specimens studied were found in fish-eating birds boldt) – State of Yucatán: Chelém lagoon at Chuburná from several localities in central and southeastern (January, 1994). Mexico (see ‘Survey of species’). Freshly collected Site: Intestine. specimens were fixed with 4% formaldehyde solu- Specimens deposited: IPCAS C-278. tion, either under pressure or with hot (almost boiling) Comments: The specimens found were in bad condi- fixative. Scoleces of some specimens were squashed tion, which made it impossible to obtain detailed data to place the rostellar hooks into one layer and then on their strobilar morphology. However, the shape and fixed with glycerine-ammonium picrate, using the size of the hooks (Table 1; compare Figure 1A with methodology outlined by Ergens (1969). The follow- plate 67, figure Aa in Bona, 1975) and the internal ing voucher specimens from the National Helmintho- morphology, such as the regularly alternating genital logical Collection of Mexico have been examined: pores, the distribution (surrounding the seminal recep- Dendrouterina botauri Rausch, 1948 (CNHE Collec- tacle) and number (about 50) of testes, the dilation of tion No. 1314); Dilepis hilli Polk, 1941 (CNHE 393); the vagina in premature proglottids, the shape of thick- Ophiovalipora minuta Coil, 1950 (CNHE 392); and O. walled cirrus-sac, and the presence of cyclusteroid nycticoracis (Olsen, 1937) (CNHE 1315). The types rostellar apparatus with a very large pouch, are iden- (holotype and paratypes) of Glossocercus caribaensis tical to those typical of Cyclustera capito (see Bona, (Rysavy & Macko, 1973) from the helminthologi- 1975, 1994). cal collection of the Parasitological Institute, Slovak This species was redescribed by Coil (1955a) and Academy of Sciences, Košice (PISAS 9673a,b,c,e), Bona (1975). The former author found adults of 9 type-specimens (8 specimens labelled as ‘syntypes’ C. capito in the roseate spoonbill Platalea ajaja from and one as ‘paratype’) of Paradilepis brevis Burt, Tututepec, Oaxaca, Mexico, and reported the hooks 1940 and vouchers of Paradilepis scolecina (Rudol- being 213–250 (distal) and 147–169 (proximal) in phi, 1819) from The Natural History Museum, Lon- length. The tapeworms from Yucatán have distal hooks don, UK (BMNH 1983.7.19.13-17 and 1946.5.6.41- of a similar size (length 218–234; Table 1) to those 55, respectively), and vouchers of P. scolecina from redescribed by Coil (1955a), but the proximal hooks the helminthological collection of the Institute of Para- are longer (173–186). Bona (1975) found the hooks sitology, Academy of Sciences of the Czech Republic, to be 218–227 (distal) and 169–178 (proximal) long, Ceskéˇ Budejoviceˇ (IPCAS C-168) were also studied. whilst Rysavy & Macko (1973) recorded them as 224– As most species were redescribed by Bona (1975), 233 and 167–180 long; both of these correspond more morphological descriptions of the Mexican material closely to the present material. are largely limited to data on the rostellar hooks. Mea- Adults of C. capito have been found in P. ajaja and surements in descriptions are in micrometres (µm) un- Eudocimus albus (L.) from South America and North less otherwise stated. The specimens are deposited in America, including Mexico and Cuba (Coil, 1955a; 173 Figure 1. Rostellar hooks of adults of dilepidid cestodes from Mexico (distal hooks on the left). A. Cyclustera capito (Rudolphi, 1819); B. C. ibisae (Schmidt & Bush, 1972); C. Dendrouterina ardeae (Rausch, 1955) (two distal hooks on the left); D. Dendrouterina herodiae Fuhrmann, 1912 (CNHE 1314); E. Dendrouterina papillifera (Fuhrmann, 1908) (CNHE 393); F. Glossocercus auritus (Rudolphi, 1819); G. Neogryporhynchus cheilancristrotus (Wedl, 1855); H. Paradilepis caballeroi Rysavy & Macko, 1973; I. Paradilepis sp. (proximal hook in the middle); J, K. Valipora mutabilis Linton, 1927 (J, CNHE 392; K, CNHE 1315). 174 Table 1. Measurements of rostellar hooks of species of the Dilepididae from fish-eating birds in Mexico (range with mean ± standard deviation). Cyclustera capito Cyclustera ibisae Dendrouterina Dendrouterina Dendrouterina (n=17) (n=15) ardeae herodiae papillifera (n=4) (n=6) (n =2) Distal hooks 218–234 227–243 45–48 38–40 41–42 228 ± 4.7 233 ± 5.5 47 39 Blade 128–134 160–176 19–21.5 15–21.5 21–22 131 ± 2.8 168 ± 6.4 20 17 Handle 122–141 77–96 34–37 21.5–28 24–25 128 ± 5.1 88 ± 6.3 35 26 Ratio 0.9–1.1 1.7–2.2 0.5–0.6 0.5–1.0 0.9 Proximal hooks 173–186 179–198 44–45 25–30 26–27 179 ± 4.3 190 ± 6.4 44 27 Blade 83–106 128–141 18–21.5 9–11 12 95 ± 5.9 135 ± 5.2 19.5 10 Handle 99–112 70–86 32–33 15–18 17 105 ± 3.9 80 ± 4.6 32 16.5 Ratio 0.8–1.0