THE RAFFLES BULLETIN OF ZOOLOGY 2013 THE RAFFLES BULLETIN OF ZOOLOGY 2013 Supplement No. 29: 155–159 http://zoobank.org/urn:lsid:zoobank.org:pub:7EDF5454-3970-4CF1-AED6-CFC9A4A77052 Date of Publication: 30 Nov.2013 © National University of Singapore ECOLOGICAL STUDY OF THE MALAYSIAN WATER SHREW CHIMARROGALE HANTU (HARRISON, 1958) WITH REMARKS ON “ECOLOGICAL LABELLING” BY PARASITE PATTERNS Lim Boo Liat No 12, Jln Koop Cuepacs 3E, Taman Cuepacs, 43200 Cheras, Selangor Darul Ehsan, Malaysia Email: [email protected] Daicus M. Belabut Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia Email: [email protected] Rosli Hashim Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia Email: [email protected] ABSTRACT. — Since 1957, 14 specimens of the Malaysian water shrew Chimarrogale hantu (nine males and fi ve females) have been obtained from various forest reserves in the western, eastern, central and northern parts of Peninsular Malaysia. Their habitats ranged from lowland and hill forest to montane forest. Though widely distributed, the species is nowhere common. Identifi able stomach contents included a partly decomposed larval caecilian, scales and shells probably representing aquatic crustaceans and molluscs, and abundant insect fragments. Endoparasites identifi ed from the gut included trematodes and cestodes, nematodes and acanthocephalans, while ectoparasites comprised terrestrial ticks and trombiculid mites. The fi nding of two gravid female shrews, and a captive animal that survived for three weeks in captivity, are signifi cant records. KEY WORDS. — Malaysian water shrew, Chimarrogale hantu, habits, diet, distribution, body measurements, parasites INTRODUCTION 1957. More biological information on this little known animal has thus become available and is presented here. The Malaysian water shrew Chimarrogale hantu of the family Soricidae is nearly as large as the house shrew Suncus murinus. Its identity is obvious from its apparent lack of an MATERIAL AND METHODS external ear and the presence of distinctive fringes of stiff hairs on the sides of its partially webbed feet, both adaptations Cage traps, hand nets and pitfall traps were deployed to a life in water. The Malaysian water shrew was first along forest streams in the various forest reserves, during described from Peninsular Malaysia as Chimarrogale hantu extensive mammal surveys throughout Peninsular Malaysia by Harrison (1958). Specimens have since been recorded that were intended to investigate the mammalian fauna and under a variety of names by different scientists. It was treated associated ecto- and endoparasites. Fourteen water shrews as a subspecies of C. platycephala by Medway (1969), as were obtained. Two each were caught by cage traps and a subspecies of C. himalayica by Medway (1978), and as a pitfalls, and 10 were hand-netted. Only two specimens were synonym of C. phaeura by Corbet & Hill (1992). Current brought in apparently healthy; the rest came in dead or died taxonomic treatment recognises C. hantu as a valid species overnight. The two live animals were caught in cage traps endemic to Peninsular Malaysia (Wilson & Reeder, 2005; at Ulu Langat Forest Reserve, Selangor in Aug.1957 and Francis, 2008). Feb.1962. The former specimen (female) died a day after capture, and the latter (male) survived for three weeks in In addition to the fi ve specimens reported by Medway (1969, captivity. 1978), 14 additional specimens have been collected since 155 Lim et al.: Malaysian water shrew The male was kept in a fi sh aquarium measuring 15 × 29 × Reserve in Selangor, foraging in forest streams. On each 29 cm. The fl oor of the aquarium was layered with sand and occasion the shrew was seen wandering about at the edge medium and small pebbles. A long zinc water tray 15 × 10 of the stream. They were highly sensitive and upon sensing ×10 cm was placed at the glass front from end to end. Sand any slight disturbance by intruders (rats or small carnivores, and pebbles covered the inner height of the tray to facilitate snakes, etc.) nearby, submerged into deeper water and swam the animal climbing for water in the tray. The bottom of the away rapidly. According to the Orang Asli, water shrews were tray was spread with small river pebbles. Various sized stones also sighted well away from water courses, and occasionally collected from an old forest stream were used to structure a were caught in traps on land. We were shown a few nesting nest with a small opening for the animal to rest. Dry leaves sites of the animal, all of which were among rocks and and small twigs were spread on the sandy and gravel fl oor. boulders above the banks of streams. The entrance to the The whole structure of the glass enclosure was intended to nest was very small with the animal having to squeeze its simulate a natural water stream environment for the animal. body into the nest. Body measurements, head and body (HB), tail (T) and Distribution. — During 53 years (1957–2009) only 14 hindfoot (HF) in mm were taken using a ruler. Weight in specimens (9 males, 5 females) were obtained. These came grams was taken using a portable balance TANITA 1476 from eight forest localities in fi ve states (Table 1, Fig. 2). of 0–100 grams scale. The external body surfaces were All except two were caught in hill forest between 600 and examined for ectoparasites following standard procedures. 800 m elevation. The exception was one from mountain Ticks were preserved in 70% alcohol for visual examination forest at 1500 m and one from lowland forest below 200 m. of external characters to determine genus and species under a stereoscope. Chiggers were also preserved in 70% Stomach contents. — Out of seven stomachs examined, alcohol, and cleared in lactophenol solutions, after which three (collected in Nov.1969, Apr.1997, and Oct.1998) had each was mounted in Canada balsam on a glass slide, dried food remains, including both invertebrate and vertebrate taxa and identifi ed through a high-powered research microscope. (Table 2). These were remnant pieces of shells and scales. Though it was not possible to identify the species from For endoparasites, the viscera were removed and examined which these particles were derived, based on the semi-aquatic immediately. Trematodes were preserved in 70% alcohol, habits of the water shrew, the shell particles were probably cestodes and acanthocephalans in 5% formalin. Trematodes, those of aquatic and terrestrial molluscs and possibly of cestodes and acanthocephalans were stained with borax crabs. Some of the scales were oblong in shape, indicating carmine or alum carmine, cleared in creosote, and mounted that they derived from freshwater prawns. Decomposed in Canada balsam. Nematodes were cleared in lactophenol earthworms were found in two of the three water shrews and studied as temporary mounts. examined. Identifi cation of millipedes and centipedes was based on decomposed remnants of the chaetae and claws of these animals. A part of the tibia with three-segmented tarsus RESULTS of a mole cricket was also found in one of the water shrews. Capture. — Nine specimens were captured in forest reserves In the vertebrate group of animals found in the stomach in Selangor, two in Pahang and one each in Perak, Kedah contents were scales of fi sh. Digits of frogs were also found. and Kelantan during the period from 1957 to 2009 (Table An interesting fi nding was a decomposed part of a larval 1, Fig. 1). Trapping was carried out at irregular times, thus caecilian. the collection was opportunistic in nature. Among the three trapping methods used, cage traps were the least effi cient. Reproduction. — Two of the fi ve females (May 1967 and Hand nets, though productive, stressed the animals resulting Nov.1969) were found with early pregnancies. The May1967 in death overnight after being transferred into cages. Pitfall specimen had two and the Nov.1969 had three embryonic traps were most effi cient, yielding two individuals in this stems. study during one trapping period. Description. — The body was covered with velvety water- proof fur. Upper parts were uniform dark grey to black, with silvery guard hairs that were most conspicuous over the hind-quarters. The tail was uniformly greyish brown to dark brown. Underparts were dark brown. Feet were brown and toes partially webbed. Younger animals were uniformly lighter in colour than fully grown adults. All had characteristic fringes of stiff hairs edging the sides of the feet and all lacked an external ear (Fig. 1). The body measurements (14 specimens) of both age-classes are shown in Table 1. Habits in natural environment. — Animals were observed on four occasions at Ulu Gombak and Ulu Langat Forest Fig. 1. Malaysian water shrew, Chimarrogale hantu. 156 THE RAFFLES BULLETIN OF ZOOLOGY 2013 Captive diet. — Based on identifi ed stomach contents, the or or or or or or surviving male water shrew (Nov.1969) was offered several g). *Skull was extracted. Locality Ulu Langat Forest Reserve (<1000 m a.s.l.), Hulu Langat, Selangor Ulu Langat Forest Reserve (<1000 m a.s.l.), Hulu Langat, Selangor Ulu Gombak Forest Reserve (<1000 m a.s.l.), Ulu Gombak, Selang Ulu Gombak Forest Reserve (<1000 m a.s.l.), Ulu Gombak, Selang Ulu Gombak Forest Reserve (<1000 m a.s.l.), Ulu Gombak, Selang Ulu Gombak Forest Reserve (<1000 m a.s.l.), Ulu Gombak, Selang Kepong Forest Reserve (< 1000 m a.s.l.), Kepong, Selangor Cameron Highlands (1676 m a.s.l), Pahang Janda Baik Forest Reserve (<1000 m a.s.l.), Pahang Sungai Singor, Temenggor Forest Reserve (<1000 m a.s.l.), Perak National Park, (<1000 m a.s.l.), Kelantan Ulu Muda Forest Reserve, Baling, Kedah Ulu Gombak Forest Reserve (<1000 m a.s.l.), Ulu Gombak, Selang Ulu Gombak Forest Reserve (<1000 m a.s.l.), Ulu Gombak, Selang ifsoaCwDeotwototlPhhoatrnnvfcufeaaoaatuee adcteemhrtttspm rsiahhe rcnaw ialitm sssnrsaeidis vift s iva,ng gsisoeioe o onttlehte gl mue enllrfei tobr .es,nrs ehaa bseo beO .taadlcte wetct le snmr—thi denwhrenitae tii eitv hrma cynsotpact vcehao k.vts rpFa aalaertteioi eyOi oanirclcorf ntkvt rm o nkcgsiuhmnigf evmu,lceeeoae ro i ieodntiatmaq .osorasnh avn dninud,fol—itaten i d noias:fnttcarnitw t iot mh ogf tsiostpgih wtchIeneauc b reaat eo et skac ritcelhb1 t fto n wtkrwr hnheo o2emoc aotlte enu mhai oalhbonn etssotsteckeseneme ehtga,v ht , rssr rrnhr aoierc ogvte eamaeenn.eosnrcreiwn nw dsa gsnSficoedddacti b s ia un trd senen a sfdgiarbdnebn.tdrag eblaehs boarcasl ,dsy oeoa irmolbsntaloq iaautiuus uds ynaf snuct,gcd,t ,it ngu aei ktehtsawhttmd srrenrhnlathyear i r ntht,eainan edr in eeoi onitele tg cwnidhlsophsb scgs hv etdnieta mashsir l i ec tenaecgoiarteeaaiaoro pdotcmecrnvln fdlnp rl ,edodtlasudn e smere.uhrtwenw adeaci isOrbleoanrirntteaeik nnrheeincotruttwli.tgdhodeeeesssft. ( positive for both ecto- and endoparasitic infections. Five ht g species of ectoparasites and six of endoparasites were ei oot, Wt = W T/HB (%) 86.2 97.5 79 96.9 88.9 86.1 86.6 101.9 77 77.9 83.5 84.4 87.6 89.5 87.3 77.1–101.9 raeoennfc ddtoro evtpwmearroaeat dsooi.dt feeT scsh hwaein geedrgce ect aroes pss tap(olredaacersivsiet asea lson tfdwr nooeemnrmeeb aiottchofur dlaeeined, taswmcpaoeitn cestisphe)eos,c coiaeenfps dh tea iactlhcakhnes f d (Table 3). n F = Hi 36.0 ail, H Wt 36 29.4 34 29.4 33.6 35.2 34.8 28.8 31.8 33.7 32.5 35.2 26.4 23.8 31.8 28.8– T = T ody, 2.2 B 2 ad & HF 22.2 21.9 22 21.2 22.1 21.4 22 20.4 22 21.9 22.2 21.8 23 23 21.9 20.4– e H = er shrew. HB T 97.3 87.8 90.2 90.3 102.3 95.8 98.5 86.8 91.6 94.3 98.4 94.8 85 85 95.7 86.8–102.3 at w n a 2 of Malaysi HB 112.8 90.2 114.2 93.1 115.3 111.3 113.8 85.1 117.5 121.2 117.8 112.3 97 95 106.9 85.1–121. m) m ( s nt ureme Sex F M M M F M F M M M F F M* M eas n ge m a n y Me Ra d Table 1. Bo Date Jan.1955 Aug.1957 Dec.1958 Feb.1962 Jul.1963 Jul.1966 May.1967 Sep.1968 Nov.1969 Mar.1995 Apr.1997 Oct.1998 Feb.2009 Feb.2009 Fhaign.t 2u.. Distribution map of the Malaysian water shrew Chimarrogale 157 Lim et al.: Malaysian water shrew Table 2. Analysis of contents of three stomachs of the Malaysian water shrew. Animal material recovered Date of specimen collected State of stomach contents Invertebrates Vertebrates Nov.1969 50% full earthworms, millipedes, shells, scales-? prawn fi sh scales Apr.1997 25% full tibia of mole cricket, shells, centipedes digits of frogs Oct.1998 75% full shells, earthworm, mole cricket caecilian Table 3. Parasites of the Malaysian water shrew. Date of specimen Eectoparasites Endoparasites Site of Infection** collected Ticks Chiggers Nematode Trematode Cestode Jul.1966 B, Si 1 Dm 3A 2 Hd May 1967 B, Si 5 Wa 4 Dic 6 Hd Mar.1995 B 3 Dm Apr.1997 B, Si 2 Ix 4 L(L)d 5 Ch 2 Lec Oct.1998 B 1 Amb ** B = Body; Si = small intestine; M = lip muscle Ticks: Dm = Dermacentor sp.; Ix = Ixodes granulates; Amb = Amblyomma sp. Chiggers: Wa = Walchella oudemasi; L(L)d = Leptotrombidium (L.) deliense Nematode: A = Acanthocephala = Moniliformis moniliformis; Ch = Capilaria hepatica Trematode: Dic = Dicrocaelid sp.; Lec = Lecithodendid sp. Cestode: Hd = Hymenolepis diminata DISCUSSION Medway (1969) reported that food items consist of freshwater crabs and a variety of other aquatic animals. Our results The low number of the Malaysian water shrews captured showed a considerably broader range, including fi sh and at the eight locations and also during previous studies frogs, and an array of invertebrates. An interesting fi nding in (Medway, 1969, 1978) could have involved three factors: our study was part of a larval caecilian. The larval caecilian (a) unusual sensitivity to disturbance or trap-shyness, (b) normally dwells embedded in sandy ground at the edge of inappropriate types of traps deployed, (c) low trapping effort. a river or stream. Thus, the presence of the larval caecilian Belief that the bite of this animal is poisonous may have and also the earthworms in the stomach suggests that the made the trappers reluctant to search for it. It may also have water shrew has a rooting habit similar to that of the moonrat accounted for 90% of the catches brought in having been (Lim, 1967). The analysis of stomach contents revealed that, dead specimens. Pitfall traps have been found most effi cient like the moonrat, the water shrew is a generalist feeder. in capturing frogs and reptiles, and are most effective for small insectivores such as ground shrews Crocidura spp. Life-styles in nature are refl ected in parasite loads. Audy and Suncus estrucus (Muhomad et al., 2007). Our pitfall (1948, 1958) established that ectoparasites, particularly traps were the least harmful to water shrews. Even so, only chiggers, serve as ecological labels related to the pattern of one specimen lived for any time; it was found dead in the habitat use and behaviour of the hosts. Among endoparasites, corner of the cage after 21 days in captivity. Post mortem helminths such as Melastrongylus malayensis occurring in did not show abnormality in any organs, but there was a certain rodents have been found to serve as a good indicator weight loss from 35.2 g on arrival to 24.8 g at the time of of the food habits of these hosts (Lim & Ramachandran, its death. The cause could possibly have been inappropriate 1979). In water shrews, the dicrocaeliid and leeithodrendriid food types or stress in captivity. trematodes and Heanthocephala found are similarly likely to correlate with the host’s food preferences as their intermediate The water shrew, though mainly aquatic, is also partially hosts are insects and snails that, in turn, are infected when terrestrial in habit. When on the forest fl oor, like the moonrat they feed on defi nitive host faeces. This further indicates Echinosorex gymnurus, another semi-aquatic insectivore that the water shrew eats insects and molluscs in nature as (Lim, 1967), it is always close to a water environment. well as under laboratory conditions. Medway (1983) reported that water shrews “are occasionally caught in fi sh traps set at the edge of large pools or in Ectoparasitic ticks and trombiculid mites, particularly bends in the river in relatively still water one or two feet the latter group, are distributed throughout a wide range deep, fl owing over a gravelly bottom in the upper Sungai of habitats, from lalang (Imperata) grassland, scrub Nenggiri, Kelantan”. and secondary forest to primary forest at all elevations, although some of them are more habitat-specifi c than others (Nadchatram, 1970). With the exception of the scrub typhus 158 THE RAFFLES BULLETIN OF ZOOLOGY 2013 vector, Leptotrombidium (L.) deliense, found in forest LITERATURE CITED fringe, scrub and secondary forest habitats, the ectoparasites recovered from water shrews occur in general forest type Audy, J. R., 1948. Natural history and scrub typhus. Malayan habitats—further evidence of their terrestrial habits. Nature Journal, 3: 114–129. Audy, J. R., 1958. The role of mite vectors in the natural history All the six species of endoparasites are also common of scrub typhus. Proceedings of 10th International Congress of intestinal parasites of murids and insectivores (Suncus Entomology, 3: 639–649. murinus, Crocidura malayana), the intermediate hosts of Audy, J. R., 1963. The zoogeography of the genus Leptotrombidium, all these endoparasites are insects (Leong et al., 1979; Lim trombuculid mite vectors of scrub typus. Proceedings of 9th et al., 1983). Pacifi c Science Congress, Bangkok, 9: 16–18. Corbet, G. B. & J. E. Hill, 1992. The Mammals of the Indomalayan The ectoparasites, i.e., the ticks and chiggers with the Region: A Systematic Review. Natural History Museum exception of the cattle tick Boophilus sp. which is host Publications. London and Oxford University Press, Oxford. specifi c, are free-living organism opportunistically clinging 488 pp. onto any vertebrate hosts that crosses its path. Of the three DWNP, 2010. Red List of Mammals for Peninsular Malaysia, species of ticks and two of chiggers identifi ed from the 2010. Department of Wildlife and National Parks, Peninsular water shrews, the ixoidid tick, Ixodes granulatus and the Malaysia. 150 pp. trombiculid mite, Leptotrombidium (L.) deliense are of Francis, C. M., 2008. A Field Guide to the Mammals of Southeast medical importance. Langat virus has been isolated only from Asia. New Holland Publishers, London. 392 pp. Ixodes granulatus from the Ulu Langat Forest Reserve, Hulu Langat District, Malaya (Smith, 1956) and Leptotrombidium Harrison, J. L., 1958. Chimarrogale hantu, a new water shrew from (L.) deliense is a vector of scrub typhus (Audy, 1963). the Malay Peninsula, with a note on the genera Chimarrogale and Crossogale (Insectivora, Soricidae). Annals and Magazine of Natural History, Series 13, 1: 282–290. It is obvious from the results that the Malaysian water shrew attracts a fairly wide variety of ecto-and endoparasites despite Leong, T. S., B. L. Lim, L. F. Yap & M. Krishnansamy, 1979. the small number of specimens examined. Their agility in Parasite fauna of the house rat, Rattus rattus diardii in Kuala quest of food in various different niches of the forest could Lumpur and nearby villages. Southeast Asian Journal of Tropical Medicine and Public Health, 10: 112–126. be an important factor in exposure to infection by a diversity of parasites. This could be through direct or indirect contact Lim, B. L., 1967. Notes on the food habits of Ptilocerus lowii and through consuming reservoir host species that harbour Gray (Pentail tree-shrew) and Echinosorex gymnurus (Raffl es) parasites. (Moonrat) in Malaya with remarks on “ecological labeling” by parasite patterns. Journal of Zoology, London, 152: 375–379. Medway (1983) reported specimens of water shrews from Lim, B. L. & C. P. Ramachandran, 1979. Ecology studies on Selangor, Pahang and Kelantan at all altitudes up to 5300 Angiostrongylus malaysiensis (Nematode, Metastrongylidae) in ft (1615 m). Our study increased the known localities and Malaysia. In: Cross, J. H. (ed.), Studies on Angiostrongyliasis the total geographical and ecological range. Based on our in Eastern Asia and Australia. Special Publication of the U.S. present results, the water shrew is found in localities studied Naval Medical Research Unit No. 2, Taipei, Taiwan. Pp. 25–56. in western, central, eastern and northern parts of Peninsular Lim, B. L., I. N. Ladera & A. Munif, 1983. Parasite fauna of the Malaysia. Failure to obtain the species in the southern part of commensal rats and shrews in Jakarta city, West Java, Indonesia. the country could have been due to less fi eld activities being Hemera Zoa, 71: 213–220. carried out there. Although the species is widely distributed, Medway, Lord, 1969. The Wild Mammals of Malaya. Oxford fi eld activities in each of the locations investigated confi rm University Press, Kuala Lumpur. 127 pp. that its population density is genuinely low. With the river Medway, Lord, 1978. The Wild Mammals of Malaya and Singapore. systems, the primary habitat of this species, being degraded Oxford University Press, Kuala Lumpur. 130 pp. and polluted through deforestation, it is anticipated that the Medway, Lord, 1983. The Wild Mammals of Malaya (Peninsular natural population through time would further decline. The Malaysia) and Singapore. 2nd Edition. Oxford University Press, species is protected, Appendix II and listed in the Threat Kuala Lumpur. 131 pp. status for Mammals in Peninsular Malaysia as VuB2ab Muhomad, N. Z., J. Senawi & B. L. Lim, 2007. A note on the (11.111) (DWNP, 2010). arboreal monkey-footed rat in a pit-fall trap. Journal of Wildlife and Parks, 24: 63–65. ACKNOWLEDGEMENTS Nadchatram, M., 1970. Correlation of habitat, environment and colour of chiggers, and their potential in the epidemiology of scrub typhus in Malaya. (Protosigmata: Trombiculidae) Journal This paper is a contribution to Supplement No. 29 of the of Medical Entomology, 7: 131–144. Raffl es Bulletin of Zoology, marking the eightieth birthday of the Earl of Cranbrook (V). The authors are grateful to Smith, C. E. G., 1956. A virus resembling Russian spring-summer Fred Dunn and the late M. Natchatram at the Institute of encephalitis virus from ixodid tick in Malaya. Nature, 178: Medical Research for the confi rmation and identifi cation of 581–582. the endo- and ectoparasites. Without the assistance of the Wilson, D. E. & D. M. Reeder (eds.), 2005. Mammal Species of Orang Asli trappers in the various states, who collected these the World: A Taxonomic and Geographic Reference. 3rd Edition. animals, and without their expert knowledge of the forest and Johns Hopkins University Press. 2000 pp. its mammal fauna, this paper would not have been possible. 159