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Flukes of the Microscaphidiidae Looss, 1900 (Trematoda: Digenea) from the Green Sea , Chelonia mydas L. (Reptilia: Chelonia) in the with Description of Three New

Salcedo L. Eduardo1·, DVM, MS, PhD and Jose L. Diaz2, DVM

'Department of Veterinary Paraclinical Sciences, College of VeterinaryMedicine, University of the Philippines Los Banos, Laguna 4031, Philippines: and 'Protected Areas and Wildlife Bureau, Department of Environment and Natural Resources, Quezon City, Philippines

ABSTRACT

A total of 15 green sea , Chelonia mydas L. were examined at various times for parasites from the coastal areas of Bohol and Zamboanga, Philippines. Among others, trematodes belonging to the family Microscaphidiidae Looss, 1900 were recovered following the concentration sedimentation decantation technique. Specimens were stained in borax carmine, cleared in oil of cloves and mounted in balsam for microscopic examination. Twelve species including 3 new species of trematodes representing 6 genera of the family Microscaphidiidae Looss, 1900 were identified. These are: Microscaphidium reticulare (van Beneden, 1854) Looss, 190L Microscaphidium aberans Looss, 1902,

Microscaphidium warui Blair, 1986; Deuterobaris proteus (Brandes, 1891) Looss, 1900; Angiodictyum parallelum(Looss, 1901) Looss, 1902; Angiodictyum glossoides Blair, 1986; Angiodictyum longumBlair, 1986: Angiodictyum undulatumn. sp.; Angiodictyum dejesusi n. sp.; Polyangium manueli n. sp.; Octagium sagitta (Looss, 1899) Looss, 1902 and Polygorgyra choladus Blair, 1986. Angiodictyum undulatum, A. dejesusi and Polyangium manueli were described and illustrated as new species. A. undulatum differs from all species of the by its lateral margin thrown into folds giving an undulating appearance of the , vitellaria present only in the median area and their absence in lateral fields. A. dejesusi is differentiated from the closely related species," A. Jongum by its vitellaria extending anteriorly to level of anterior testis and not beyond it, the pharyngeal-position of the genital pore and the relatively short esophagus. P manueli differs from P linguatulum, the only valid species of the genus, by its ovoid shape, the limited extent of vitellaria which is behind the testes and the more anterior location of the genital pore just behind the pharynx. This is the first report of these trematodes in the Philippines constituting a new locality record for these species. Keys to separate the genera of the family Microscaphidiidae and species of the genera Microscaphidium and Angiodictyum occurring in marine turtles in the Philippines are provided.

Keywords: Angiodictyum dejesusi, Angiodictyum undulatum, Chelonia mydas, Microscaphidiidae, Philippines, Polyangium manueli

------Philipp. J. Vet.Med., 45: 75·85, 2008

INTRODUCTION are: Polystomoides cyclemydis, a monogenetic trematodes from dentata (serrated The chelonian (turtle) fa una of the freshwater turtle) in Palawan (Fischthal & Philippines consist of 8 species, 3 freshwater Kuntz, 1964) and Spironoura duyagi, a and 5 marine (Alcala, 1986; Wildlife from Cuora amboinensis (Malayan Conservation Society of the Philippines, 1997). fresh water turtle) and Cyclemys dentata in As far as the authors are aware, only two Novaliches, Luzon and Palawan (Tubangui & parasites have been reported so far from only Villaamil, 1933; Schmidt & Kuntz, 1972). As two turtles species in the Philippines. These far as can be ascertained no report on the *FOR CORRESPONDENCE parasites of the other species of turtles 76 SL EDUARDO AND JL DIAZ

including the sea or marine turtles. The true Physiological salt solution was added and sea turtles, Chelonia mydas (green ) shaken to relax any worm present. This was and Eretmochelys imbricata (hawksbill sea then processed following the concentration turtle) had a wide distribution locally but sedimentation decantation technique, worldwide these are listed by the International repeatedly done until the supernatant fluid is Union for Conservation of Nature (IUCN) as clear. The resulting sediment was stored in 10% globally endangered (Wildlife Conservation formalin solution and brought to the laboratory Society of the: Philippines, 1997; DENR-UNEP, for further examination. The preserved 1997). Although many species of parasites sediment was examined for parasite in the particularly trematodes from marine turtles in laboratory using a Zeiss Stemi DV4 other parts of the world have been recorded stereomicroscope. Parasites were collected and (Gupta, 196L Rodriguez, 196L Chat­ post-fixed in formalin-alcohol-acetic acid topadhyaya, 1972; Groschaft et al, 1977; Blair, solution (FAA) for at least 48 hours and stored 1983, 1986, 1987; Dyer et al., 1991), none have in 80% ethyl alcohol until further study. been reported from these hosts in the Specimens were then stained in aceta alum Philippines. We have had opportunities to carmine overnight, destained in 1% examine at various times marine turtles for hydrochloric acid solution until the desired color parasites from the coastal areas of Bohol and (pale pink) is reached, neutralized in 1% Zamboanga, Philippines. This paper dealing solution of sodium hydroxide to stop further with the species of the family Microscaphidiidae destaining. Specimens were then gradually from the has been written to dehydrated in increasing grades of ethyl record some of our findings contributing to our alcohol, cleared in oil of cloves and mounted knowledge of biodiversity in the whole in Canada balsam. In addition, country. Such information on the health aspects representative specimens of thick and muscular is also vital in conservation programs when were stained and cleared as above but these are raised initially in captivity. were hand sectioned in the sagittal, cross and Furthermore, chelonians (turtles) belong to an longitudinal planes following the procedure of ancient group dating back 200 million years to Eduardo (1982) for amphistomes. These were the Jurassic era. Consequently, their parasites then arranged accordingly in the proper are of great importance from an evolutionary sequence on a glass slide and mounted in perspective due to their presumed ancient Canada balsam. This technique has enabled the origin (Jakes et al.,2001). The other trematode observation of the internal organs of thick families including those recovered from the specimens which otherwise are not readily seen (Eretmochelys imbricata) in whole mounts. will form the subject of a separate paper. Measurements were made with the aid of a calibrated eyepiece micrometer. Photo· MATERIALS AND METHODS micrographs were taken using an Olympus BX51 research microscope with digital camera A total of 15 green sea turtles (Chelonia attachment. Drawings were made with the aid mydas L.) were examined at various times for of an Olympus drawing apparatus attached to parasites, twelve from and an Olympus CX31 research microscope. three from Jagna, Bohol. In almost all cases, Additional microscaphidiid materials only the digestive tract was made available for deposited at the Swedish Museum of Natural examination. The digestive tract was tied by History were examined for comparative segment with a thread to separate one section purposes by the senior author during his visit from the other, and to avoid free flowof contents there as follows: Microscaphidium reticulare from one segment to another. The mucosa of (NHR Nos. 1908, 1914, 2649, 2650); M. each digestive section was scraped with a fine adherens (NHR Nos. 1889, 1905, 2648, 2649); knife to dislodge any attached parasite and the Angiodictyum parallelum (NHR Nos. 1890, contents placed in a wide-mouth bottle. 1895, 1908); A. longum (NHR Nos. 867, 2934, FLUKES IN GREEN SEA TURTLES 77

2961); Polyangium linguatulum (NHR Nos. recently have been sufficiently described by 850, 891, 1893, 1932, 2651). Many of these Blair (1986, 1987), these are no longer described specimens were reexamined and identified by here but photographs of them are provided Blair (1986). based on the Philippine materials. The three Taxonomic allocation of the trematodes at new species however are described and the family and generic levels follows that of illustrated by photographs and drawings below, Jones et al. (2005). and other taxonomic data are also provided. Voucher and type (holotype and paratype) specimens were deposited in the Parasite Description of new species: Collection of the College of Veterinary Medicine, UPLB under the accession number indicated Angiodictywn undulatum n. sp. for each species. (Figs. 8, 13, 14)

RESULTS (Based on one whole and several fragmented specimens, the latter however were not included Twelve species representing six genera of in the measurements) the family Microscaphidiidae were identified Body is elongate, measures 5.820 mm long in the present collections. Of these, nine are and 2.250 mm wide, linguiform with sides known species but are reported for the firsttime almost parallel, rounded on both ends. Marginal in the Philippines constituting new locality bodies are absent. Lateral margins are thrown record for these species, while three are species into folds giving a characteristic undulating new to science. The known species are listed in appearance of the worm. Edges of folds are the table showing their organ location, marked by fine muscle fibers. accession number of voucher specimens and Pharynx is barrel·shaped, measures 0.265 their local distribution. Since the known species by 0.275 mm, anterior rim surrounded by small

Table. New record of species of the family Microscaphidiidae from green sea turtle, Chelonia mydas L. in the Philippines. Species (Figure) Organ location Locality Voucher S ecimens Microscaphidium reticulare (van Pseuclocecum and Jagna, Bohol: Barrio No. 84-13, Beneden, 1854) Looss, 1901 large intestine Sinunuc, Zamboanga City slides 1 to 8 (Fig. 1) Microscaphidium aberans Looss, Stomach and small Rio Hondo, Zamboanga No. 84-14, 1902 intestine City slides 1 to 3 (Fig. 2) Microscaphidium waruiBlair, 1986 Pseudocecum and Jagna, Bohol: Barrio No. 84-15, (Fig. 3) large intestine Sinunuc & Rio Hondo slides 1 to 17 Zamboanga City Deuterobaris proteus (Brandes, Stomach and small Rio Hondo, Zamboanga No. 84-12, 1891) 1900 Looss, intestine City slides 1 & 2 (Fig. 4) Angiodictyum parallelum (Looss, Stomach and small Barrio Sinunuc, No. 84-18. 1901) 1902 Looss, intestine Zamboanga City slides 1 & 2 (Fig. 5) 1986 Angiodictyum glossoides Blair, Large intestine Jagna, Bohol: Barrio No. 84-20, 6) (Fig. Sinunuc. Zamboanga City slide 1 to 4 Angiodictyum longum Blair, 1986 Large intestine Jagna, Bohol: Barrio No. 84-16, 7) (Fig. Sinunuc & Rio Hondo, slides 1 to 14 Zamboanga City Octagium sagitta (Looss, 1899) Stomach, small and J agna, Bohol: Barrio No. 84-17, 1902 Looss, large intestines Sinunuc & Rio Hondo, slides 1 to 10 (Fig. 11) Zamboanga City Polygorgyra choladus Blair, 1986 Large intestine Barrio Sinunuc & Rio No. 84-18, 12) (Fig. Hondo, Zamboanga City slides 1 to 3 78 SL EDUARDO AND JL DIAZ

E E E E E E It) � It) .,.. N .,..

E E � .,..

Figs. 1-6. Microscaphidiid species, whole worms, ventral view. 1. Microscaphidium reticulare; 2. Microscaphidium aberans; 3. Microscaphidium warui; 4. Deuterobaris proteus; 5. Angiodictyum parallelum; 6. Angiodictyum glossoides (aceto-alum ·carmine stain). FLUKES IN GREEN SEA TURTLES 79

7

10 12

2.5mm

Figs. 7-12. Microscaphidiid species, whole worms, ventral view. 7. Angiodictyum longum; 8. Angiodictyum undulatum n. sp.; 9. Angiodictyum dejesusin. sp.; 10. Polyangium manuelin. sp.; 11. Octagium sagitta; 12. Polygorgyra choladus(aceto·alum·carmine stain). 80 SL EDUARDO AND JL DIAZ

Figs. 13-15. New microscaphidiid species. 13. Angiodictyum undulatum n. sp. (holotype), whole worm ventral view; 14. Pharynx of A. undulatum showing scallop-like papillae on anterior margin and the small intramural sacs; 15. Angiodictyum dejesusi n. sp., (holotype) whole worm, ventral view. scallop-like papillae. Esophagus measures body; anterior testis measures 0.812 by 1. 501 mm long, about one third as long as the 0.387mm; posterior testis measures 0.750 by body length, bifurcates about 0.847 mm from 0.250 mm. Genital pore is located ventral and anterior end, flanked in its entire length by at level of esophageal bifurcation. presumed glandular cells, posterior end slightly Ovary lies immediately behind posterior thickened to form a very weak bulb; Ceca have testis, transversely oval and measures 0.310 undulating edges, are parallel in their course by 0.160 mm. Uterus is intercecal, loops extend in the lateral fields terminating blindly near near posterior end of body passing between posterior extremity. testes to end anteriorly in the genital pore. Testes are tandem in position, intercecal, Vitellaria consist entirely of a median group of transversely elongate in posterior half of the follicles extending from a level beyond anterior FLUKES IN GREEN SEA TURTLES 81 testis to near posterior end, occupying nearly to eight diverticula; bladder is small, sac-like. the posterior half of the body, lateral groups of Typehost: Chelonia mydas L. follicles are lacking. Mehlis' gland lies close to Organ location: Stomach and small ovary and measures 0.300 by 0.150 mm. intestine. measures 75-87.5 by 45-52.5J.L. Excretory Type locality: Barrio Sinunuc, Zamboanga bladder is small, excretory pore located City, Mindanao Island, Philippines. subventral. Type specimens: Holotype (No. 84-22a) and Type host: Chelonia mydas L. paratype (No. 84-22b) Organ location: Small intestine Etymology: Species name after the late Dr. Type locality: Rio Hondo, Zamboanga City, Zacarias de Jesus, Parasitologist, Mindanao Island, Philippines. Emeritus Professor and former Type specimens: Holotype (No. 84-21). Chairman of the then Department Etymology: Species name refers to the of Veterinary Parasitology & undulating appearance of the lateral Protozoology, U.P. College of Veterinary margins of the worm. Medicine and who has contributed to our knowledge of parasites of domesticated Angiodictyum dejesusi n. sp. animals in the Philippines. (Figs. 9, 15) (Based on three whole and a number of Polyangium manueli n. sp. fragmentedspecimens, the latter however were (Figs. 10, 16, 17) not included in the measurements) (Based on five whole specimens) Body is elongate, measures 5.950-6.520 mm Body is ovoid, wider posteriorly than long, 2.200-3.010 mm wide; its greatest width anteriorly, measures 2.421-4.432 mm long, is attained at level of posterior testis. Marginal 1.832-1.986 mm wide, greatest width is bodies are present but irregularly distributed, attained at level of posterior testis. Marginal mostly in anterior half of the body. bodies are absent. Preoral space measures 0. 158-0.193 mm. Pharynx is round, measures 0.200--0.300 by Pharynx is barrel-shaped, measures 0.400- 0.075-0.285 mm. Esophagus measures 0.787- 0.450 by 0.320--0.450 mm. Esophagus measures 0.859 mm long, bifurcates about 0.857-0.893 1.320-1.625 mm long, bifurcates about 2.010-- mm fromanterior end. Ceca are inflated, almost 2.134 mm from anterior end. Ceca are inflated; parallel in their course terminating blindly lie in lateral fieldsterminating blindly close to close to posterior end of the body. posterior extremity. Testes are spherical, oval in the dorso­ Testes lie tandem in middle third of body, ventral direction, lie tandem and intercecal in transversely oval, irregular in outline or posterior half of the body; anterior testis slightly lobed, intercecaL anterior testis measures 0.400-0.462 by 0.462-0.702 mm; measures 0. 750-0.783 by 0. 850-0.937 mm; posterior testis 0.400--0.487 by 0.537-0725 mm. posterior testis 0.537-0.687 by 0.012-0.937 Genital pore lies ventral and immediately mm. Genital pore is located ventral at level of posterior to pharynx. posterior border of pharynx. Ovary is spherical, lies submedian behind Ovary appears round to spherical, lies posterior testis, measures 0.200-0.265 by median to submedian behind posterior testis, 0.165-0.220 mm. Vitellaria consist of compact measures 0.260-0.325 by 0. 015-0.375 mm. follicles, lateral groups extend from level of Vitellaria consist of large follicles, in lateral and posterior border of posterior testis to near medial groups; lateral group extend from level posterior extremity, median group occupies of anterior testes to posterior end of body and space between ovary and posterior end. Eggs are confluentmedially in their posterior limits; measure 90-95 by 53-55 J.l. median group occupies the area posterior to Excretory in rosette form consisting of six ovary. Eggs measure 57.5-62.5 by 37.5-40 il· to ten diverticula;bladder is small and sac like. Excretory in rosette form consisting of six Typehost: Chelonia mydas L. 82 SL EDUARDO AND JL DIAZ

O.Bmm

Figs.16--17. Polyangium manuelin. sp. 16. Whole worm, ventral view (holotype); 17. whole worm, sagittal view (paratype).

Organ location: Pseudocecum and large 1900, Deuterobaris Looss, 1900, Angiodictyum intestine. Looss, 1902, Polyangium Looss, 1902, Octagium Type locality: Rio Hondo, Zamboanga City, Looss, 1902 and Polygorgyra Blair 1986 are Mindanao Island, Philippines. Other represented in the present materials and are locality: Jagna, Bohol. recorded for the first time in the Philippines. Typespecimens: Holotype (No. 84·23a) and The following known species identified in the paratypes (No. 84-23b & c). present work have been recorded in the Etymology: Species name after Dr. Mauro countries as indicated: Microscaphidium F. Manuel, Parasitologist, former Dean reticulare in , Cuba, , Ghana, of the College of Veterinary Medicine, , , and the North Sea (Blair, UPLB and whose works have 1986), M. aberans in Australia, Egypt and advanced our knowledge of Philippine Ghana (Blair, 1986), M warui in Australia. avian coccidia and haematozoa. Panama and Taiwan, (Blair, 1986), Deuterobaris proteus in Egypt, , USA DISCUSSION and (Looss, 1901, Nigrelli, 1941; Dyer et al., 1991), Angiodictyum parallelum in The family Microscaphidiidae Looss, 1900 Egypt, Florida, USA and Puerto Rico (Looss, presently consists of 19 genera (Blair, 2005). 1901; Nigrelli, 1941; Blair, 1986; Dyer et al., Six of these namely, Microscaphidium Looss, 1991), A. glossoides in Panama (Blair, 1986); FLUKES IN GREEN SEA TURTLES 83

A. longum in Australia, Malaysia and (1986). P. manueli differs from P.linguatulum (Blair, 1986); Octagium sagitta in Australia, by its ovoid shape, the limited extent of Egypt, , Singapore, Puerto Rico and vitellaria whose anterior limit is behind the Taiwan (Blair, 1987; Dyer et al., 1991); posterior testis and the genital pore just behind Polygorgyra choladus in Australia and India the pharynx. P. linguatulum is tongue·shaped; (Bair, 1986). The Philippine materials of the its vitellaria extend anteriorly far beyond the above species all conform to the description of level of the anterior testis and its genital pore Looss (1901) and Blair (1986, 1987) and are at a level much posterior to the pharynx. reported for the first time in the country To separate the genera of the family constituting a new locality record for these Microscaphidiidae and the species of the genera species. Microscaphidium and Angiodictyum occurring Angiodictyum undulatum n. sp. is in marine turtles in the Philippines, keys to characterized among others by its lateral these taxa are given below. margins thrown into folds giving an undulating appearance of the worm. This feature is not Key to the genera of the family exhibited by any known member of the genus Microscaphidiidae occurring in marine turtles or any memher of the other genera of the family in the Philippines Microscaphidiidae. Because of this, it cannot be readily assigned to any of the genera of the la. Ventral surface bears longitudinal

family. It is possible that this species belongs rows of papillae...... Deut erobaris to a new genus but until additional materials lb. Ventral surface does not are examined, it is for the mean time placed bear papillae...... 2 under the genus Angiodictyum because it exhibits most features of the genus as defined 2a. Pharyngeal sacs extramural...... 3 by Blair (2005) than any other genera of the 2b. Pharyngeal sacs family. This species differs further from all entirely intramural...... 4 species of the genus Angiodictyum in the vitellaria which is limited to the median area, 3a. Anterior part of esophagus with the lack of lateral groups of follicles and the spines in its lumen; pharynx presence of scallop·like papillae on the anterior elongate with posterior sacs margin of the pharynx. nearly as long as A. dejesusi n. sp. is assigned to the genus pharynx...... Microscaphidium Angiodictyum because its features conform to 3b. Anterior part of esophagus the diagnosis of the genus as provided by Blair without spines in its lumen; (2005). Of the valid species of the genus A. pharynx barrel·shaped with dejesusi stands closest to A. longum but differs posterior sacs less than half from it in the much shorter esophagus, the the length of pharynx...... Polygorgyra position of the genital pore which is at level of the posterior border of the pharynx and the 4a. Vitellaria extensively confluent vitellaria which does not extend beyond the in their posterior limits, anterior testis. In A. longum, the esophagus is marginal bodies proportionately greater than any of the other absent ...... Polyangium species, its vitellaria extending well beyond the 4b. Vitellaria not confluent or anterior testis and genital pore which is just confluentnear ceca, posterior to the pharynx. marginal bodies present P. manueli n. sp. belongs to the genus or absent...... Angiodictyum Polyangium because its features agree well with the diagnosis of the genus as defined by Key to the species of Microscaphidium occurring in marine turtles in the Philippines Blair (2005). Polyangium linguatulum is the only valid species of the genus according to Blair (modified from Blair, 1987) 84 SL EDUARDOAND JL DIAZ

la. Spinous region of esophagus Fernando P. Micosa for his help in arranging half as long as pharyngeal photographs into composite plates. This work

sacs ...... 2 was supported in part in its final stages lb. Spinous region of esophagus through a research fellowship grant to the as long as pharyngeal sacs senior author by the National Academy of

or almost so...... M reticulare Science and Technology, Philippines.

2a. Marginal bodies 1-3 REFERENCES

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