The Sulawesi Black Racer, Coluber (Ptyas) Dipsas, and a Remarkable Ectoparasitic Aggregation!

The Sulawesi Black Racer, Coluber (Ptyas) dipsas, and a Remarkable Ectoparasitic Aggregation!

JAMES D. LAZELL,2 JAMES E. KEIRANS,3 AND G. ALLAN SAMUELSON 4

ABSTRACT: Twelve specimens of the Sulawesi black racer, Coluber (Ptyas) dipsas, have been reported in the literature; none of these is from American collections. Morphology and relationships of the snake, based on a fresh specimen, are discussed. Thirteen ticks of two species, Amblyomma cordiferum and A. helvolum (Ixodidae), and the beetle Aplosonyx nigripennis (Chrysome lidae) were recovered from an old wound site on a 1465-mm female Coluber dipsas from Minahasa, Sulawesi Utara, Indonesia. Both tick species are new island and new host records. There have been no specific plant hosts reported to date for this beetle, of a phytophagous family.

ONEOF US (JDL) led an expedition to Sulawesi, mucosus usually placed with it in the spurious Halmahera, and the Far Moluccas, Indonesia, genus Ptyas, apparently on purely geographi in 1986. A number of remarkable discoveries cal grounds. The insular range of C. dipsas were made, including a specimen ofan appar and its close relationship to C. constrictor ently rare snake, a black racer. A tradition of argue for its status as a relict, not a recently ectoparasite collection resulted in a far more derived autochthon, on Sulawesi. unusual discovery in this case. A cluster of ticks on the snake contained in their midst a Taxonomy beetle, firmly attached and apparently feeding in an ectoparasitic manner. All of the organ The species was originally described as isms found seem to require some comment Herpetodryas dipsas by Schlegel (1843). The and attention: snake, ticks, and beetle. description consists ofa single paragraph. No type specimen was designated, and Schlegel did not state how many specimens he saw. He THE SULAWESI BLACK RACER, gave scale counts for only one individual. Coluber dipsas He mentioned no locality except "Celebes." Nevertheless, the color pattern and scale Coluber dipsas is a rare snake in museum counts leave no room for doubt as to the collections and very scantily reported in the species he had before him. literature. It bears a striking and detailed Schlegel (1843) separated Herpetodryas resemblance to the widespread, abundant from Coluber (in which he put constrictor) on North American Coluber constrictor, proba grounds of more elongate, slender habitus in bly its closest living relative. It bears far the former and the fact that most Herpeto less resemblance to the widespread continen dryas were green (H. dipsas being an obvious tal Asian snakes Coluber korros and C. exception by his own description: "shining bluish-black"). The generic name Herpeto

1 Manuscript accepted 12 January 1991. dryas is not in use today. 2 The Conservation Agency, 6 Swinburn e Street, Boulenger (1893) recognized the relation Jamestown, Rhode Island 02835. ship ofdipsas and constrictor and placed both 3 Institute of Arthropodology and Parasitology, in his genus Zamenis. Boulenger (1894) noted Landrum Box 8056, Georgia South ern University, Statesboro, Georgia 30460. that Coluber closely " parallels Zamenis;" the 4Department of Entomology, Bishop Museum, P.O. only difference being in dentition. This claim , Box 19000-A, Honolulu, Hawaii 96817. which haunts us today, is that Zamenis has 355 356 PACIFIC SCIENCE, Volume 45, October 1991 enlarged teeth on the posterior maxillary mostly on the Minahasa Peninsula (north while Coluber has teeth ofnearly equal size all eastern Sulawesi), but as close to the center along the maxilla. In fact, most individuals of of the island as Kantewu and Lemo in the most of the relevant species of Coluber sensu Kulawi region at the peninsula's base (Bosch lato have the largest teeth on the rear of 1985). the maxilla . This is usually true in Coluber constrictor, type species ofthe genus. There is Characteristics great individual variation in tooth size. Barbour (1912) was the first to refer to Basic morphometries from MCZ 171461 , our species as Ptyas, but this designation was with variation taken from specimens exam not accepted by Rooij (1917), who retained ined at The Natural History Museum, Lon Zamenis and virtually rewrote Boulenger's don (BMNH) and gleaned from the literature (in (1897) description. Barbour (1912 : 193) listed parentheses) follow: dorsals at midbody, 13 C. dipsas from Halmahera in the Moluccas. (13); ventrals, 194 (187-198); subcaudals, 134 He did so only in a table , however , and there (132-139, discounting those with truncated was no mention of the species anywhere in tails); snout-vent length, 980 mm (other his text. The high probability that Barbour adults, 1297-1355 mm); tail length, 485 mm never examined a specimen is indicated by the (no other adults seen have complete tails). fact that ours is the first ever accessioned at Boulenger (1897) claimed a 2-m male with the Museum of Comparative Zoology (MCZ 550-mm tail, and Rooij (1917) gave appar 171461). Barbour always referred to Coluber ently the same specimen as 1450 mm with a constrictor as such. 550-mm tail. This specimen seems to be BMNH Haas (1950) followed Barbour in placing C. 1946.1.7.87 (formerly BMNH 64.4.7.10), a male dipsas in Ptyas without comment. Bosch from Manado that now measures 1355 mm (1985) followed suit, giving the now long snout-vent and has a truncated 505-mm tail. defunct tooth character as definitive of the In MCZ 171461the tail is 33% of total length genus Ptyas and also listing Halmahera as a (1465 mm). In two juveniles, BMNH 96.12.9.52 locality. and 53, the tails are 31% and 32% of total length, respectively. Roux (1904) reported a Distribution specimen with a tail 30% of total length . Available color descriptions are so brief as The Halmahera record apparently comes to be misleading. MCZ 171461 was basically from Roux (1904), who simply stated that tricolor in life: satin black dorsally, olive the species was previously known only from gray-brown along the anterior sides, and ivo North Celebes but is now known from Hal ry-white or cream on the anterior venter. The mahera too. He gave locality data only for olive gray-brown includes the lips, lateral Celebes (Sulawesi) and cited no Halmahera edges of the ventrals, and first three dorsal specimen. The record should be discounted. rows anteriorly. At ventral 20 black breaks Before the collection of MCZ 171461, a through the gray-brown as a subrectangular minimum of 12 known specimens had been bar to the ventrals. Thereafter posteriorly reported in the literature. Schlegel (1843) there are nine more black bars breaking the certainly had one. Boulenger (1893) examined lateral gray-brown; the series terminates at another. Boulenger (1897) examined four ventrals 48-50. Then gray-brown appears more. Roux (1904) seems to have had at as four irregular blotches on the sides in a least one. Rooij (1917) examined specimens ground of marbled black and cream-white to from two localities, Manado and Rurukan, ventral 90. The chin, throat, and anterior but these are the same as seen by Boulenger. venter are cream to ventral 54. Here black Bosch (1985) saw five individuals. spotting, giving way to marbling, in turn Localities range from Manado at essential giving way to cream spots in a black ground, ly sea level (Boulenger 1893) to Rurukan extends to ventral 100. The posterior venter is at ca. 1100 m (3600 ft: Boulenger 1897), satin black . See Figure I. Ectoparasites of Coluber (P .) dipsas-LAzELL, K ElRANS, AND S AMUELSON 357

FI G UR ~ 1. C~luber dipsas, MCZ 171461, from Minah asa, Sulawesi: top, lateral view of head ; bottom , dorsal view of head. Th is specimen was ~o st to two species of Amblyomma ticks and the beetle Aplosonyx nigripennis. Specimen in the Museum of Compar ati ve Zo olog y, Harvard Un iversity.

The other adults seen are basically similar. These stop at ventral 60. There are irregular In BMNH 1980.926, a male from Torro, gray-brown spots ventrolaterally as far back Kulawi, central Sulawesi, there are 16 exten as ventral 80. In BMNH 1946.1.7.87 seven black sions of dorsal black (some just as scale spots are present in the ventrolateral gray edging) into the ventrolateral gray-brown. brown to ventral 34. Then these connect 358 PACIFIC SCIENCE, Volume 45, October 1991 dorsally to make bars, as previously described, organ is not bilobate and probably tapers to ventral 82. There are then irregular gray distally when everted . It is most like that of brown and cream spots and marblings to Coluber diadema (Schatti 1986, fig. 6), but the ventral 96. In this specimen there is a cream flounces are on the sulcate surface in C. white middorsal stripe, breaking into spots, to diadema and on the absculate surface in C. the level of ventral 50. Posteriorly this snake dipsas. is satin black . Examination of hemipenes of Coluber Color of juveniles closely resembles that korros and C. mucosus (at MCZ by JDL) seen in Coluber constrictor. BMNH 19.12.9.52, revealed conditions intermediate between from Tomohon, Minahasa, is gray-brown these simple organs and the strongly bilo with bold , anterior, saddlelike blotches. There bate hemipenes of Coluber constrictor, C. are 24 blotches on the anterior 60% of the flagellum, and other American members ofthe body. Thereafter the markings become irregu genus . Schatti (1987) referred to Coluber as lar transverse mottlings that fade to uniform "polyphyletic" but provided no evidence. It is gray-brown on the posterior body and tail. merely diverse in hemipenial structure. In The most anterior six saddlelike blotches are deed, had Schatti included the species placed connected by narrow dorsolateral bars and in Ptyas , both the morphological and geo are biconcave middorsally. This individual's graphic gaps in his concept ofthe genus would total length is 537 mm. have been filled. Variation in the direction of the adult BMNH 1946.1.7.87 with the remnant middorsal light Ecology stripe is seen in juvenile BMNH 96.12.9.53 from Rurukan. On the anterior 39% of the body There is nothing in the published literature the blotches are amalgamated dorsolaterally on ecology. MCZ 171461 was found still by a continuous dark stripe, two to three twitching on the tarmacadam road 2 km south scales wide, and broken middorsally to form ofWakan Kampong, Minahasa, at ca. 500 m, a light nape stripe . The ventral extensions of in clove and coffee plantations with natural dark pigment into the ventrolateral gray vegetation clumps dominated by tree ferns. brown (i.e., the ends of the remnant blotches) The snake was run over at midday, so the are subtended after a two-scale gap by irregu species is apparently diurnal. There was noth lar blackish areas, largely as scale edging. ing in the stomach or intestine to indicate diet . The midbody pattern is of irregular dark All ticks and the beetle Aplosonyx nigri reticulation merging into uniform gray on pennis were clustered on an old, healing the posterior body and tail. Total length is wound area extending from ventral 182 to 456mm. ventral 187. The wound was largely on the The hemipenes of some Coluber have been left side, extending from the ventrals across described by Schatti (1986, 1987). He did not 10 dorsal scale rows. The skin burst beside consider any members of nominal genus this old wound site when the snake was Ptyas. The left retracted hemipenis of BMNH mortally wounded before collection, but the 1946.1.7.87 had been dissected before exami ectoparasites were not at the fresh wound. nation by JDL. Its interpretation was facil The evidence is that dense congregations of itated by Dr. Garth Underwood, present Amblyomma may be facultative exploiters of at BMNH with JDL on 15 June 1988. The wound sites on Coluber dipsas. hemipenis extends to subcaudal 14. The base is bare. Six large flounces extend from the THE TICKS (ACARI: IXODIDAE) levels of subcaudals 3 to 6. Spines extend to the level of subcaudal 12; the largest are as Two species ofthe genus Amblyomma were long as one subcaudal width . Small flounces, found, one female A. cordiferum Neumann forming a reticulate pattern not very different (1899) and 12 male A. helvolum Koch from calyces, cover the tip. The sulcus is (1844); all specimens were closely congregated simple and scarcely discernible distally . The around the old wound site described above. Ectoparasites of Coluber (P.) dipsas-LAz ELL, K EIRANS, AND SAM UELSON 359

Amb/yomma cordiferum. This species was parthenogenetic species (Hoogstraal 1978). described by Neumann (1899) from an Its lifecyclehas been studied, and the duration engorged female found in the Zoological from adult to adult ranged from 168 to 209 Museum, Hamburg, that was obtained from days. All adults reared from the eggs of a an unspecified host collected on Banda Island, female were also females. These females fed Moluccas . Amb/yomma cordiferum was also and deposited fertile eggs, indicating that reported on a python on Krakatau Island , reproduction was by parthenogenesis (Ho and Indonesia (Krijgsman and Ponto 1931). These Ismail 1984). However, we have two males python ticks may well have been sent to (RML 81381) taken on vegetation, Lake Lindu Professor Nuttall at Cambridge University, area, 945 m, Sulawesi, that probably represent Nuttall Collection (N) 3616, and were sub the undescribed male of A. cordiferum. sequently cited by Keirans (1985). Amb/y Amb/yomma he/vo/um. This species described omma cordiferum has also been reported from by Koch (1844) is almost exclusively a reptile Thailand on Ophiophagus hannah (Anastos tick; most collections are from snakes or 1950), from Malaysia on Python reticu/atus varanid lizards. This small Aponomma-like and Rattus tiomanicus ja/orensis (Audy et al. tick is found from the Nicobar Islands of 1960), and from a snake on Upolu Island , India eastward through Thailand, Malaysia, Western Samoa (Buxton and Hopkins 1927). This last collection was donated to Nuttall (N Singapore, Vietnam , the Philippines, and In donesia. The records of A. he/vo/um from 3568) and redetermined by Keirans (1985). Australia (Robinson 1926, Anastos 1950, The specimen ofA . cordiferum in this study is the first published record for Sulawesi and Kohl s 1950, Hoogstraal et al. 1968) are in correct (Roberts 1970). a new host record for Co/uber dipsas. How ever, the U.S. National Museum of Natural The male specimens of A. he/vo/um collect ed in this study are the only records of the History (USNM) has the following unpublished species from Co/uber dipsas and the first from records for this tick in Sulawesi: from pig, Sus the island of Sulawesi. Nothing is known of scrofa (3 collections); vegetation (1); domestic the biology or life cycle of this tick. buffalo, Bos buba/us (I); and one record ofthe tick crawling on a human. Five of the collec tions were in the Lake Lindu area and one from Soroako (Rocky Mountain Laboratory THE BEETLE (COLEOPTERA: CHRYSOMELIDAE) [RML] 81380- 81385). The USNM also has 51 unpublished records Ap/osonyx nigripennis. The occurrence of of A . cordiferum (RML 103168-103218) from this species on an old healing wound of the the Malaysian states of Jahore, Kedah, black racer, Co/uber dipsas, in company with Malacca, Pehang, Pedis, and Selangore, on ticks and apparently feeding there is most the following reptiles: Cuora amboinensis, unusual. Nothing is known of the beetle's life Python reticu/atus, Naja naja, Ophiophagus cycle, though it belongs to a phytophagous hannah, Boiga dendrophila, Geoche/one emys, family. The beetle's attraction to the old and Varanus sa/vator. Mammal records in wound site may have been a response to odor. clude Sus scrofa jubatus, Felis tigris, Manis Plant compounds, insect pheremones, and javanica, Arctogalidia trivirgata sumatrana, various other compounds can be powerful Herpestes brachyurus, and Rattus tiomanicus attractants for certain insects. ja/orensis. Jacoby (1884) described Ap/osonyx ni In addition, there are 20 unpublished gripennis from specimens collected in the records of A. cordiferum in the USNM from " Sanghir Islands" and " North Celebes." collections made on Taiwan, all from snakes This species is distinctive among congeners of the genera Bungarus, E/aphe, Naja, and in usually having its elytra entirely black. Co/uber (as Ptyas). Jacoby (1894) reported further specimens Very little is known about the biology from Sulawesi and discussed color variations of this tick, but it has been considered a in the species. Weise (1913) and Laboissiere 360 PACIFIC SCIENCE, Volume 45, October 1991

(1932, 1940) reported further on its distri bution. This species is catalogued in Weise (1924) and Wilcox (1971). This species is reported from Belitung Island, Borneo, Sulawesi, and Sangihe (Sanghir) Islands. Most records come from the Minahasa Peninsula ofnorthern Sulawesi . None of the references cited for this beetle included information on plant hosts. Aplosonyx occurs throughout the Oriental Region. Species are known from India, Nepal, Sikkim, southern China, countries through out Southeast Asia, plus insular Malaysia, Indonesia, and the Philippines. Some 39 species are listed in the latest catalog (Wilcox 1971); of these, 20 are reported through insular Malaysia and Indonesia. Neither Maulik (1936) nor Gressitt and Kimoto (1963) cited plant host records in their respective treatments ofAplosonyx from India or China. In fact, little is reported on the life FIGURE 2. The chrysomelid beetle Aplosonyx nigripen histories of most tropical chrysomelids. In nis, collected clustered with ticks on the Sulawesi black general, these beetles are plant feeders in the racer, Coluber dipsas. Specimen in the Bishop Museum, larval and adult stages. Larvae are often Honolulu. found in the soil, where they feed on roots. Also , larvae may bore into roots, stems, leaves, or fruit, and some are surface feeders LITERATURE CITED . on stems and leaves. Adults may occur in large numbers on or near the host plants; this would ANASTOS, G. 1950. The scutate ticks, or explain why sometimes long series of certain Ixodidae, ofIndonesia. Entomol. Am., n.s. species are found in museum collections. 30: 1-44. However, our specimen from Coluber dipsas, AUDY, J. R. , M. NADCHATRAM, and B. L. LIM. a female, is the first accessioned in the Bishop 1960. Malaysian parasites XLIX. Host Museum, Honolulu, Hawaii. It is shown in distribution of Malayan ticks (Ixodoidea). Figure 2. Stud. Inst. Med. Res. Malaya (29): 225 246. BARBOUR, T. 1912. A contribution to the zoogeography of the East Indian Islands. ACKNOWLEDGMENTS Mem. Mus. CompoZoo!' 154(1): 1-203. BOSCH, H. A. J. 1985. Snakes of Sulawesi: The expedition that resulted in collection of Checklist, key and additional biogeograph the specimens reported was sponsored by The ical remarks. Zoo!' Verh . Leiden 217: I-50. Conservation Agency. It was part of an on BOULENGER, G. A. 1893. Catalogue of the going exchange program with Universitas snakes in the British Museum (Natural Sam Ratulangi, Manado, Sulawesi Utara. History). Vo!. I. British Museum (Natural Logistics were arranged by and with Bernard History), London. xiii + 448 pp . Page, Dr. Arini Wawaroentoe, and Dr. - - -. 1894. Catalogue of the snakes in the Dantje Sembe!. The photographs of C. dipsas British Museum (Natural History). Vo!. 2. were prepared by Gregory Mayer. Dr. Garth British Museum (Natural History), Lon Underwood provided critically valuable don. xi + 304 pp. advice . - - - . 1897. A catalogue of the reptiles and Ectoparasites of Coluber (P.) dipsas-LAzELL, KEIRANS, AND SAMUELSON 361

batrachians of the Celebes, with special scientifiques du voyage aux Indes Orien reference to the collections made by Drs. P. tales Neerlandaises. Mem. Mus. R. Hist. and F. Sarasin, 1893-1896. Proc. Zool. Nat. Belg., hors ser. 4(4): 145-184, pI. 1-2. Soc. London 13: 193-237. ---. 1940. Observations sur les Galeru BUXTON, P. A., and G . H. E. HOPKINS. 1927. cinae des collections du Musee Royal Researches in Polynesia and Melanesia. d'Histoire Naturelle de Belgique et descrip London School of Hygiene and Tropical tions d'especes nouvelle. Bull. Mus. R. Hist. Medicine, London. 260 pp. Nat. Belg. 16(3): 1-31. GRESSITT, J. L., and S. KIMOTO. 1963. MAULIK, S. 1936. Fauna India, Coleoptera, Chrysomelidae (Coleoptera) of China and Chrysomelidae (Galerucinae). Taylor and Korea, Part 2. Pac. Insects Monogr. 1B: Francis, London. 648 pp . 301-1026. NEUMANN, L. G. 1899. Revision de la famille HAAS, C. P. E. de . 1950. Checklist of the des ixodides. Mem. Soc. Zoo\. Fr. 12: 107 snakes of the Indo-Australia archipelago 249. (Reptilia, Ophidia). Treubia 20 : 511-625. ROBERTS, F. H. S. 1970. Australian ticks. Ho, T. M., and S. ISMAIL. 1984. Life cycle of Commonwealth Scientific and Industrial the tick Amblyomma cordiferum Neumann Research Organization, Australia, Mel under laboratory conditions. Malay. Nat. bourne. 267 pp. J.38:73-77. ROBINSON, L. E. 1926. Ticks. A monograph HOOGSTRAAL, H . 1978. Biology ofticks. Pages of the Ixodoidea. Part IV. The genus 3-14 in J. K. H . Wilde, ed. Tick-borne Amblyomma. Cambridge University Press, diseases and their vectors. Proc. Int. Conf. Cambridge. 302 pp. on Tick-borne Diseases and Their Vectors ROOIJ, N . de. 1917. The reptiles of the Indo (Edinburgh, September, October 1976). Australian archipelago, II. Ophidia. E. J. Edinburgh University Press. Brill, Leiden. xiv + 334 pp. HOOGSTRAAL, H., F. J. SANTANA, and P. F . D. Roux, J, 1904. Reptilien und Amphibian aus VAN PEENEN. 1968. Ticks (Ixodoidea) of Celebes. Verh. Naturforsch. Ges. Basel Mt. Sontra, Danang, Republic ofVietnam. 15(3): 425-433. Ann. Entomo\. Soc. Am. 61 : 722- 729. SCHATTI, B. 1986. Morphological evidence for JACOBY, M. 1884. A new species of the phy a partition of the genus Coluber (Reptilia: tophagous genus Haplosonyx. Notes Leyden Serpentes). Pages 235-236 in Z. Rocek, ed. Mus. 6:71. Studies in herpetology. Charles University, --- . 1894. Descriptions of new genera Prague. and species of phytophagous Coleoptera ---. 1987. The phylogenetic significance obtained by W. Doherty in the Malayan of morphological characters in the Hol Archipelago. Novitates Zoo\. 1(2): 267 arctic racers ofthe genus Coluber Linnaeus, 330. 1758 (Reptilia, Serpentes). Amphilia KEIRANS, J. E. 1985. George Henry Falkiner Reptilia 8 :401 -418. Nuttall and Nuttall tick catalogue. U.S. SCHLEGEL, H. 1843. Essay on the physiogno Dep. Agric. Misc. Publ. 1438. vii + 1785 my of serpents. T . S. Traill translation. pp . MacLachlan, Stewart, and Co., Edinburgh. KOCH, C. L. 1844. Systematiche Uebersicht vii + 254 pp. uber die Ordnung der Zecken. Arch. Natur WEISE, J. 1913. Uber Chrysomeliden und gesch. 10(1): 217-239. Coccinelliden der Philippinen: II. Teil KOHLS, G . M. 1950. Ticks (Ixodoidea) of the (Coleoptera). Philipp. J. Sci. 8(3D): 215 Philippines. Natl. Inst. Health Bull. 192. 242. 28 pp. --- . 1924. Chrysomelidae: 13. Galeru KRIJGSMAN, B. J., and S. A. S. PONTO. 1931. cinae. Coleopt. Cat. 25(78): 1-225. Die Verbreitung er Zecken in Neiderlanisch WILCOX, J . A. 1971. Chrysomelidae: Galeru Ostindien. Z. Parasitenkd. 4: 140-146. cinae, Oidini. Coleopt. Cat. Supp\. 25(78, LABOISSIERE, V. 1932. Galerucinae. Resultats fasc. I): 1-220.