J. Parasitol., 90(3), 2004, pp. 598–603 q American Society of Parasitologists 2004
TWO NEW SPECIES OF FALCAUSTRA AND COMMENTS ON HELMINTHS OF NOROPS TROPIDOLEPIS (SAURIA: POLYCHROTIDAE) FROM COSTA RICA Charles R. Bursey, Stephen R. Goldberg*, and Christine L. Miller† Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146. e-mail:
[email protected] ABSTRACT:
Falcaustra costaricae n. sp. from the intestines of the lizard Norops tropidolepis and F. heosemydis n. sp. from the large intestine of the turtle Heosemys depressa are described and illustrated. Falcaustra costaricae represents the 10th Neotropical species assigned to this genus and is distinguished from other Neotropical species by the distribution pattern of caudal papillae (10 preanal, 0 adanal, 12 postanal, and 1 median), length and width of spicules (510–561 mm long, 18–24 mm wide), and absence of pseudosucker. Falcaustra heosemydis represents the 29th Oriental species and is distinguished from other Oriental species by the distribution pattern of caudal papillae (10 preanal, 0 adanal, 12 postanal, and 1 median), length of spicules (790–890 mm), and absence of pseudosucker. Norops tropidolepis was found to harbor 3 species of Nematoda, F. costaricae, Rhabdias anolis, and acuariid larvae, and 2 species of Acanthocephala (centrorhynchid cystacanths and oligacanthorhynchid cystacanths).
Species of Falcaustra Lane, 1915 occur in the digestive tracts of fish, amphibians, and reptiles. Of the 80 nominal species listed by Bursey et al. (2000) and Bursey and Kinsella (2003), 9 occur in the Neotropical zoogeographical realm and 28 occur in the Oriental zoogeographical realm. This article describes the 10th and 29th species of Falcaustra from the Neotropical realm and Oriental realm, respectively.
species of Acanthocephala (centrorhynchid cystacanths and oligacanthorhynchid cystacanths). Prevalence, mean intensity, and site of infection for these helminth species are given in Table I. Selected helminths were deposited in the United States National Parasite Collection (USNPC), Beltsville, Maryland (Table I). Heosemys depressa was found to harbor an undescribed species of Falcaustra. Description of the 2 new species follows.
MATERIALS AND METHODS
DESCRIPTION
Two collections of helminths were sent to the senior author for identification. The first collection was from the examination of 13 Norops tropidolepis (7 females and 6 males, mean snout–vent length 5 44 6 3 mm, range 5 39–48 mm; collected in September 1963, Heredia Province, Costa Rica) from the herpetology collection of the Natural History Museum of Los Angeles County, Los Angeles, California (LACM 148917, 148918, 148924, 148926–148928, 148938, 148946, 148948– 148952). These lizards had been fixed in 10% formalin and preserved in 70% ethanol. The body cavity was opened by a longitudinal incision from throat to vent, and the digestive tract was excised by cutting across the esophagus and rectum. The esophagus, stomach, and small and large intestines were opened longitudinally under 70% alcohol and examined with a dissecting microscope. The liver, lungs, urinary bladder, and body cavity were also searched. Helminths were placed in vials of 70% ethanol for storage and transport. The second collection was from 2 Heosemys depressa (Anderson, 1875) from Burma (locality unknown) obtained in October 2001 by the Miami MetroZoo, Miami, Florida, from a wildlife importer. One turtle died in August 2002, and on necropsy, mature nematodes were found in the colon. The second turtle died in December 2002, and again mature individuals of the same species of nematode were found in the colon on necropsy. The nematodes were fixed in hot 70% ethanol and then placed in vials of 70% ethanol for storage and transport. Helminths from N. tropidolepis were examined using the standard glycerol method (Gray, 1954) and identified from these mounts; nematodes from H. depressa were dehydrated in graded ethanol and cleared in cedarwood oil for examination with a light microscope. Drawings were made with the aid of a microprojector. Unless otherwise stated, measurements are in micrometer and presented as range, with mean 6 1 SD in parentheses. Lizard taxonomy follows that of Savage (2002); turtle taxonomy follows that of Ernst and Barbour (1989).
Falcaustra costaricae n. sp. (Figs. 1–11)
RESULTS Norops tropidolepis was found to harbor 3 species of Nematoda, Rhabdias anolis Bursey, Goldberg and Telford, 2003, acuariid larvae, an undescribed species of Falcaustra, and 2 Received 8 August 2003; revised 5 December 2003; accepted 5 December 2003. * Department of Biology, Whittier College, Whittier, California 90608. † Miami MetroZoo, 12400 SW 152 Street, Miami, Florida 33177. 598
General: Family Kathlaniidae Lane, 1914. Nematodes with cylindrical body tapering posteriorly, truncate anteriorly. Cuticle with transverse striations of approximately 2 width. Mouth opening triangular, surrounded by 3 large lips, each with 2 forked papillae. Amphids on ventrolateral lips. Additional cephalic papillae absent. Esophagus with subspherical isthmus and spherical bulb. Excretory pore anterior to isthmus. Tail conical in both sexes. Male (on the basis of holotype and 9 paratypes): Length, 5.7–7.9 mm (6.71 6 0.75 mm); width 180–280 (220 6 30) at level of esophageointestinal junction. Pharynx 70–90 (80 6 8) long; corpus 765–944 (833 6 58) long; isthmus 85–110 (99 6 8) long, 49–67 (58 6 6) wide; bulb 122–153 (137 6 10) long, 116–153 (129 6 14) wide. Nerve ring 255–306 (281 6 15), excretory pore 740–918 (838 6 65) from anterior end, respectively. Tail 230–332 (265 6 30) long, curved ventrally. Spicules 510–561 (541 6 20) long, similar, well sclerotized, hollow, narrow alae reaching almost to bluntly pointed tips. Gubernaculum 104–116 (110 6 5) long, 18–24 (21 6 3) wide, distal end pointed, proximal end slightly expanded. Pseudosucker absent. Single median papilla immediately anterior to anus. Eleven pairs of caudal papillae, 5 pairs preanal, 6 pairs postanal, of which 3 ventral, 2 lateral, and 1 ventrolateral in position. Phasmids situated laterally on tail equidistant between anterior and median postanal lateral papillae. Single group of approximately 35 preanal diagonally directed caudal muscles. Female (on the basis of allotype and 9 paratypes): Length 6.9–9.7 mm (8.1 6 0.9 mm); width at level of esophageointestinal junction 179–357 (252 6 52). Pharynx 79–98 (86 6 6) long; corpus 842–1,071 (956 6 67) long; isthmus 98–122 (106 6 7) long, 64–76 (70 6 4) wide; bulb 134–171 (155 6 12) long, 123–164 (142 6 14) wide. Nerve ring 281–319 (302 6 13), excretory pore 816–1,020 (911 6 75) from anterior end,
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TABLE I. Site of infection, number of helminths, prevalence, mean intensity, range of infection, and USNPC accession numbers for 5 helminth species in Norops tropidolepis from Costa Rica.
Helminth species
Site of infection
Number
Prevalence (%)
Mean intensity 6 SD
Range
USNPC voucher no.
92 (12/13) 15 (2/13) 15 (2/13)
15.8 6 15.2 5.5 6 6.4 2.5 6 0.7
2–60 1–10 2–3
93524 93525 93526
8 (1/13) 31 (4/13)
2 2.0 6 2.0
— 1–5
93527 93528
Nematoda Falcaustra costaricae Rhabdias anolis Acuariidea (larvae)
Intestines Lungs Body cavity
190 11 5
Acanthocephala Centrorhynchidae (cystacanth) Oligacanthorhynchidae (cystacanth)
Body cavity Body cavity
2 8
respectively. Tail 510–765 (668 6 80) long. Vulva transverse slit, 1.9–3.1 mm (2.4 6 0.38 mm) from posterior end; vagina directed anteriodorsally, giving rise to 2 divergent uteri. Eggs oval 40–49 3 31–37 (46 6 3 3 34 6 2), thick shelled; in early stages of cleavage at deposition (5 eggs each from 6 specimens). Taxonomic summary Type host: Norops tropidolepis (Boulenger, 1885), swift anole. Symbiotype, Natural History Museum of Los Angeles County, LACM 148952; collection date 10 September 1963. Type locality: Costa Rica, Heredia Province, Uvita (108059N, 848239W, 1,595-m elevation). Site of infection: Small and large intestines. Type specimens: Holotype male, USNPC, Beltsville, Maryland, USNPC 93521; allotype female, USNPC 93522; paratypes, 9 females, 9 males, USNPC 93523; voucher specimens, USNPC 93524. Etymology: The new species is named in reference to the country of origin.
Falcaustra heosemydis n. sp. (Figs. 12–22) General: Stout nematodes, body cylindrical, tapering posteriorly, truncate anteriorly. Cuticle with fine transverse striations of approximately 2 widths. Mouth opening triangular, surrounded by 3 large lips, each with 2 forked papillae. One amphid on each ventrolateral lip. Additional cephalic papillae absent. Esophagus with spherical isthmus and posterior spherical bulb. Pigmented arcade cells in region of nerve ring. Tail conical in both sexes. Male: (holotype, 7 paratypes): Length 13.2–14.7 mm (14.1 6 0.5 mm); width 460–690 (530 6 70) at level of esophageointestinal junction. Vestibule length 20–35 (30 6 7), pharynx length 80–130 (100 6 10), corpus length 1,530–1,840 (1,680 6 120), isthmus length 140–170 (150 6 10), isthmus width 140–170 (160 6 10), bulb length 260–310 (260 6 20), bulb width 280–330 (310 6 20). Nerve ring 430–510 (460 6 30), excretory pore 1,230–1,530 (1,370 6 90) from anterior end, respectively. Tail length 540–610 (560 6 30), curved ventrally, with conical termination. Approximately 30 oblique caudal muscle bands. Single median papilla immediately anterior to anus. Eleven pairs of sessile caudal papillae, 5 pairs preanal, 6 pairs postanal, of which 2 are lateral and 4 ventral. Phasmid
openings laterally situated on tail dorsal to second pair of postanal ventral papillae. Spicules similar 790–890 (850 6 40) in length, 60–70 (65 6 5) in width, slightly curved, sclerotized, alae reaching almost to pointed tips. Gubernaculum 180–220 (200 6 20), sclerotized, elongated, proximal half with triangular alae, distal end bluntly pointed. Preanal pseudosucker absent. Female: (allotype and 6 paratypes): Length 10.0–14.7 mm (12.7 6 1.3 mm); width 700–900 (810 6 60) at level of esophageointestinal junction. Vestibule length 30–40 (34 6 2), pharynx length 90–120 (100 6 10), corpus length 1,530–1,840 (1,700 6 100), isthmus length 130–150 (140 6 10), isthmus width 150–190 (170 6 10), bulb length 260–360 (290 6 40), bulb width 280–360 (320 6 30). Nerve ring 430–490 (470 6 20), excretory pore 1,330–1,430 (1,420 6 100) from anterior end. Tail length 830–1,020 (920 6 60). Vulva, transverse slit, salient, 3.7–4.5 mm (3.9 6 0.2 mm) from posterior end; vagina directed anteriorly, giving rise to 2 opposing uteri. Egg oval, length 80–104 (95 6 8), width 55–73 (62 6 6), thick shelled, unembryonated (5 eggs each from 4 specimens). Taxonomic summary Type host: Heosemys depressa (Anderson, 1875), Arakan forest turtle. Type locality: Burma (locality unknown). Site of infection: Large intestine. Type specimens: Holotype, male, USNPC, Beltsville, Maryland, USNPC 93670; Allotype, female, USNPC 93671. Paratypes, 6 females, 7 males, USNPC 93672. Etymology: The species is named for its host genus. Remarks Chabaud (1978) defined the Kathlaniidae by the presence of an esophageal isthmus expanded into a bulb and ventral musculature of the male tail in bundles directed toward a more or less formed preanal sucker. Lane (1915) described the posterior portion of the esophagus to be hourglass shaped; Chitwood and Chitwood (1974) used the term ‘‘subspheroid’’ to describe the shape of the isthmus. Chabaud (1978) defined the Kathlaniinae by the presence of a valved, muscular esophageal bulb and assigned 8 genera to the subfamily, i.e., Amblyonema Linstow, 1898; Chabaudinema Dı´az-Ungrı´a, 1968; Cissophyllus Railliet and Henry, 1922; Falcaustra, Kathlania Lane, 1914; Megalobatrachonema Yamaguti, 1941; Tonaudia Travassos, 1918; and Spectatus Travassos, 1923. Of these, only the Falcaustra pos-
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FIGURES 1–11. Falcaustra costaricae n. sp. 1. Female, anterior end, lateral view. 2. Female, en face view. 3. Female, anterior end, dorsal view. 4. Egg. 5. Female, vulvar region, lateral view. 6. Gubernaculum, dorsal view. 7. Gubernaculum, lateral view. 8. Male, posterior end, ventral view. 9. Female, posterior end, lateral view. 10. Spicules and gubernaculum. 11. Male, posterior end, lateral view.
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FIGURES 12–22. Falcaustra heosemydis n. sp. 12. Female, anterior end, lateral view. 13. Female, en face view. 14. Female, anterior end, dorsal view. 15. Egg. 16. Female, vular region, lateral view. 17. Male, posterior end, lateral view. 18. Gubernaculum, lateral view. 19. Gubernaculum, dorsal view. 20. Female, posterior end, lateral view. 21. Spicules and gubernaculum. 22. Male, posterior end, ventral view.
sess 3 or 6 well-developed lips. All 4 characters, i.e., subspherical isthmus, valved esophageal bulb, 3 well-developed lips, and ventral musculature of the male tail directed ventrally, are evident in F. costaricae n. sp. (Figs. 1, 3, 8) and F. heosemydis n. sp. (Figs. 12, 15, 17). Lane (1915) in his redescription of
Oxysoma falcatum Linstow, 1906 (the type species for Falcaustra) noted the absence of a preanal sucker. Thirty-five of the 80 species assigned to Falcaustra lack a preanal sucker (see Bursey et al., 2000; Bursey and Kinsella, 2003). Chabaud’s (1978) key should be amended to read ‘‘esophageal bulb mus-
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cular, with valves; preanal ventral sucker absent or present, sometimes multiple.’’ Species of Falcaustra are distinguished on the basis of characters of the male, i.e., number and arrangement of caudal papillae, length of spicules, and presence or absence of preanal pseudosuckers (see table I of Bursey et al., 2000; table I of Bursey and Kinsella, 2003). In addition to F. costaricae n. sp. and F. heosemydis n. sp., species lacking a pseudosucker include F. affinis (Leidy, 1856); F. belemensis Baker and Bain, 1981; F. bengalensis Mana and Mahapatra, 1989; F. caballeroi Chabaud and Golvan, 1957; F. chauhani (Soota, 1975); F. falcata (Linstow, 1906); F. fernandoi (Sathananthan, 1972); F. fordoniae (Jones, 1978); F. golvani Chabaud and Brygoo, 1957; F. greineri Bursey and Kinsella, 2003; F. guatamalana (Caballero, 1953); F. hinkeli Jackson, 2000; F. khadrai (Karve, 1941); F. kutcheri Bursey, Platt, and Rainwater, 2000; F. leptocephala Baylis and Daubney, 1922; F. longispicula Walton, 1927; F. nilgiriensis (Soota and Chaturvedi, 1971); F. pectinospiculata (Koo, 1939); F. piscicola (Linstow, 1907); F. plethodontis Baker, Goater and Esch, 1987; F. pretiosa (Ingles, 1935); F. procera (Canavan, 1929); F. puylaerti Jackson, 2000; F. ranae (Walton, 1941); F. rankini (Walton, 1941); F. pillaii (Sathananthan, 1972); F. stewarti Baylis and Daubney, 1922; F. testudinis Baylis and Daubney, 1922; F. therezieni Petter, 1979; F. tikasinghi (Schoenecker, Schmidt, and Everard, 1977); F. tricirratus (Linstow, 1901); F. trilokiae (Signh, 1958); F. verbekei Campana-Rouget, 1961; F. washingtonensis Bursey and Aker, 2001; and F. wuyiensis (Wang, 1981). Of these, only F. hinkeli, F. longispicula, F. pretiosa, F. puylaerti, F. tikasinghi, F. testudinis, F. tricirratus, F. washingtonensis, F. costaricae n. sp., and F. heosemydis n. sp. have 6 pairs of postanal papillae. These species are separated first on the basis of spicule length, i.e., F. longispicula has spicules greater than 1 mm in length; F. pretiosa, F. testudinis, F. tricirratus, and F. heosemydis n. sp. have spicules less than 1 mm but greater than 700 mm in length; F. hinkeli, F. tikasinghi, F. washingtonensis, and F. costaricae n. sp. have spicule lengths between 700 and 300 mm; and F. puylaerti has spicules less than 300 mm (see Bursey et al., 2000; Bursey and Kinsella, 2003). Further separation is by caudal papillae pattern. Falcaustra pretiosa has 6 pairs of preanal papillae, F. heosemydis n. sp. has 5 pairs of preanal papillae, F. testudinis has 3 pairs of preanal papillae, and F. tricirratus has no preanal papillae. Falcaustra washingtonensis has 1 pair of adanal papillae, and F. hinkeli, F. tikasinghi, and F. costaricae n. sp. lack adanal papillae (see Bursey et al., 2000). Final separation of the remaining 3 species is by gubernaculum length and shape. The gubernaculum of F. hinkeli is Y-shaped and 44–65 mm in length (Jackson, 2000), that of F. tikasinghi is triangular and 310–340 mm in length (Schoenecker et al., 1977), and in F. costaricae, claviform and 104–116 mm in length. The 2 new species should be added to table I of Bursey et al. (2000): F. costaricae, lizard type host, spicule length 0.51– 0.56, papillae pattern 10–0–12 1 1, pseudosucker absent; F. heosemydis, turtle type host, spicule length 0.79–0.89, papillae pattern 10–0–12 1 1, pseudosucker absent. DISCUSSION To our knowledge, there is no previous report on helminths from N. tropidolepis or H. depressa. With the exception of F.
costaricae, none of the helminths found was unique to N. tropidolepis. Rhabdias anolis was originally described from Anolis frenatus from Panama (Bursey et al., 2003). Norops tropidolepis represents a new host record, and Costa Rica is a new locality record for R. anolis. It should be noted that Rhabdias of an undetermined species has been reported from the Caribbean lizards A. cristatellus, A. evermanni, A. gundlachi, A. lineatopus, and A. wattsi (Torres Ortiz, 1980; Bundy et al., 1987; Dobson et al., 1992). Reptiles presumably acquire infections of Rhabdias orally (Anderson, 2000). Species of the Acuariidea are mainly parasites of the upper alimentary tract of birds although several species are found in mammals; an arthropod intermediate host is required (Anderson, 2000). Likewise, species of Acanthocephala require an arthropod intermediate host (Schmidt, 1985). The fact that the acuariid larvae and cystacanths occurred in cysts is an indication that N. tropidolepis is an inappropriate definitive host. However, Roca (1993) suggested that prevalence of encysted helminths in a lizard population indicates their degree of importance as prey and that in these cases, the lizards are paratenic hosts. ACKNOWLEDGMENTS Peggy Firth prepared Figs. 1–22. We thank J. M. Kinsella for reviewing early versions of the manuscript.
LITERATURE CITED ANDERSON, R. C. 2000. Nematode parasites of vertebrates: Their development and transmission, 2nd ed. CABI Publishing, Wallingford, U.K., 650 p. BUNDY, D. A. P., P. VOGEL, AND E. A. HARRIS. 1987. Helminth parasites of Jamaican anoles (Reptilia: Iguanidae): A comparison of the helminth fauna of 6 Anolis species. Journal of Helminthology 61: 77– 83. BURSEY, C. R., S. R. GOLDBERG, AND S. R. TELFORD JR. 2003. Rhabdias anolis n. sp. (Nematoda: Rhabdiasidae) from the lizard, Anolis frenatus (Sauria: Polychrotidae), from Panama. Journal of Parsitology 89: 113–117. ———, AND J. M. KINSELLA. 2003. Falcaustra greineri n. sp. (Nematoda: Kathlaniidae) from Orlitia borneensis (Testudines: Emydidae). Journal of Parasitology 89: 961–964. ———, S. G. PLATT, AND T. R. RAINWATER. 2000. Falcaustra kutcheri n. sp. (Nematoda: Kathlaniidae) from Geoemyda yuwonoi (Testudines: Emydidae) from Sulawesi, Indonesia. Journal of Parasitology 86: 344–349. CHABAUD, A. G. 1978. No. 6. Keys to genera of the superfamilies Cosmocercoidea, Seuratoidea, Heterakoidea and Subuluroidea. In CIH keys to the nematode parasites of vertebrates, R. C. Anderson, A. G. Ghabaud, and S. Willmott (eds.). Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, U.K., 71 p. CHITWOOD, B. G., AND M. B. CHITWOOD. 1974. Introduction to nematology. University Park Press, Baltimore, Maryland, 334 p. DOBSON, A. P., S. V. PACALA, J. D. ROUGHGARDEN, E. R. CARPER, AND E. H. HARRIS. 1992. The parasites of Anolis lizards in the northern Lesser Antilles. I. Patterns of distribution and abundance. Oecologia 91: 110–117. ERNST, C. H., AND R. W. BARBOUR. 1989. Turtles of the world. Smithsonian Institution Press, Washington, D.C., 313 p. GRAY, P. 1954. The microtomist’s formulary and guide. The Blakiston Company, Inc., New York, 794 p. JACKSON, J. A. 2000. Two new Falcaustra Lane, 1915 species (Nematoda: Kathlaniidae) from African pipids (Anura). Journal of Natural History 34: 663–677. LANE, C. 1915. Falcaustra falcata an investigation of Oxysoma falcatum von Linstow, 1906. Indian Journal of Medical Research 3: 109–115. ROCA, V. 1993. Methods and aims in parasitology of Mediterranean reptiles, mainly lizards. In Lacertids of the Mediterranean region a
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(eds.). Cambridge University Press, Cambridge, U.K., p. 273– 306. SCHOENECKER, S. A., G. D. SCHMIDT, AND C. O. R. EVERARD. 1977. Spironoura tikasinghi sp. n. (Nematoda: Kathlaniidae) from a turtle in Trinidad, W. I. Journal of Parasitology 63: 341–343. TORRES ORTIZ, R. A. 1980. Otro hospedador final para Rhabdias sp. (Nematoda) e implicaciones evolutivas de las especies del hospedador. Caribbean Journal of Science 16: 109–114.
