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Rediscovery of Malaysia’s marine tardigrades after over half a century: a new species (Batillipes malaysianus sp. nov.) and a new record of B. rotundiculus

Published online by Cambridge University Press:  18 June 2025

Cheng-Ann Chen*
Affiliation:
Borneo Marine Research Institute, Universiti Malaysia Sabah, Kota Kinabalu, Sabah, Malaysia
Wei-Ling Ng
Affiliation:
Borneo Marine Research Institute, Universiti Malaysia Sabah, Kota Kinabalu, Sabah, Malaysia
Sing-Tung Teng
Affiliation:
Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, Kota Samarahan, Sarawak, Malaysia
Tadashi Kajita
Affiliation:
Iriomote Station, Tropical Biosphere Research Center, University of the Ryukyus, Taketomi-cho, Yaeyama-gun, Japan
*
Corresponding author: Cheng-Ann Chen; Email: chengann@ums.edu.my

Abstract

This study marks the first update on Malaysia’s marine tardigrades after more than 50 years, presenting both the discovery of a new species, Batillipes malaysianus sp. nov., and a new record, Batillipes rotundiculus. The specimens were collected from the intertidal zone at Pantai Pancur Hitam, Labuan, Malaysia, during two separate sampling efforts. Despite extensive sampling, the density of marine tardigrades in the area was found to be exceptionally low, with only a single specimen of B. malaysianus sp. nov. and a limited number of other Batillipes individuals collected. The new species, B. malaysianus sp. nov., is distinguished by unique morphological features, including setae scattered across the ventral cuticle – a trait not observed in any other species of the genus – and constricted primary clavae, a characteristic absent in other species of the B1 toe arrangement group. Additionally, B. rotundiculus represents the first confirmed record of this species in Malaysia, expanding its known distribution. This study also updates the global species count of Batillipes to 42, incorporating recent taxonomic changes and this new addition. An updated dichotomous key for the genus is provided, incorporating all species described to date. These findings underscore the importance of exploring understudied marine habitats and highlight the potential for discovering more tardigrade species in Malaysia.

Type
Research Article
Copyright
© The Author(s), 2025. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom.

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References

Arakawa, K, Yoshida, Y and Tomita, M (2016) Genome sequencing of a single tardigrade Hypsibius dujardini individual. Scientific Data 3(1), . https://doi.org/10.1038/sdata.2016.63CrossRefGoogle ScholarPubMed
Bartels, PJ, Fontoura, P, Nelson, DR, Orozco-Cubero, S, Mioduchowska, M, Gawlak, M, Kaczmarek, Ł and Cortés, J (2021) A trans-isthmus survey of marine tardigrades from Costa Rica (Central America) with descriptions of seven new species. Marine Biology Research 17(2), 120166. https://doi.org/10.1080/17451000.2021.1901936CrossRefGoogle Scholar
Boaden, PJS (1963) The interstitial fauna of some North Wales beaches. Journal of the Marine Biological Association of the United Kingdom 43(1), 7996.10.1017/S0025315400005270CrossRefGoogle Scholar
Boaden, PJS (1966) Interstitial fauna from Northern Ireland. Veröffentlichungen Des Instituts Für Meeresforschung in Bremerhaven 2, 125130.Google Scholar
Chang, CY and Rho, HS (1997a) Two new marine tardigrades of genus Batillipes (Heterotardigrada: Batillipedidae) from Korea. The Korean Journal of Systematic Zoology 13(2), 93102.Google Scholar
Chang, CY and Rho, HS (1997b) Two new marine tardigrades from Palawan Island, the Philippines. Korean Journal of Biological Science 1, 419423.Google Scholar
D’Addabbo, MG, Sandulli, R and Grimaldi, SDZ (2005) A new Batillipedidae (Tardigrada, Heterotardigrada) from the Orosei Gulf, Sardinia, Tyrrhenian Sea. Zoologischer Anzeiger 243, 219225.10.1016/j.jcz.2004.07.004CrossRefGoogle Scholar
D’Addabbo Gallo, M, Grimaldi De Zio, S and Morone De Lucia, MR (1999) Diversity and dynamics of an interstitial Tardigrada population in the Meloria Shoals, Ligurian Sea, with a redescription of Batillipes similis (Heterotardigrada, Batillipedidae). Italian Journal of Zoology 66, 5161.10.1080/11250009909356237CrossRefGoogle Scholar
D’Addabbo Gallo, M, Morone De Lucia, MR and Grimaldi De Zio, S (1987). Heterotardigrada of the Amendolara Shoal, High Ionian Sea. In Bertolani, R (ed.), Biology of Tardigrades, 103110. Proceedings of the 4th International Symposium on the Tardigrada, Modena, September 3–5 , 1985. Collana U.Z.I. Selected Symposia and Monographs I.Google Scholar
De Zio, S (1962) Descrizione di Batillipes annulatus n. sp. e note su B. pennaki Marcus nuovo rinvenimento nel Mediterraneo (Heterotardigrada). Annuario dell’Istituto E Museo Di Zoologia Della Università Di Napoli 14, 17.Google Scholar
De Zio, S and Grimaldi, P (1964) Ricerche sulla distribuzione ed ecologia di Batillipes pennaki Marcus in una spiaggia pugliese (Heterotardigrada). Cahiers Biologie Marine 5, 271285.Google Scholar
D’Hondt, J-L (1970) Gastrotriches, Kinorhynques, Rotiferes, Tardigrades. Inventaire de la Faune Marine de Roscoff. France: Station Biologique Roscoff.Google Scholar
Fenchel, T (1969) The ecology of marine microbenthos IV. Structure and function of the benthic ecosystem, its chemical and physical factors, and the macrofauna communities with special reference to the ciliated protozoa. Ophelia 6, 1182.10.1080/00785326.1969.10409647CrossRefGoogle Scholar
Fenchel, T, Jansson, BO and Thun, WV (1967) Vertical and horizontal distribution of the metazoan microfauna and of some physical factors in a sandy beach in the northern part of the Oresund. Ophelia 4, 227243.10.1080/00785326.1967.10409622CrossRefGoogle Scholar
Fize, A (1957) Description d’une espèce nouvelle de Tardigrade Batillipes carnonensis n. sp. Bulletin de la Société Zoologique de France 82, 430433.Google Scholar
Fize, A (1963) Contribution à l’étude de la microfaune des sables littoraux du Golfe d’Aigues-Mortes. Vie Et Milieu 14, 669774.Google Scholar
Fleeger, JW (1978) Free-living invertebrates. Phylum Tardigrada. In Zingmark, RG (ed.), An Annotated Checklist of the Biota of the Coastal Zone of South Carolina. Columbia: University of South Carolina Press, .Google Scholar
Gaugler, MS and Nelson, DR (1997) Marine interstitial tardigrades of Dauphin Island, Alabama [USA]. Association of Southern Biologists Bulletin 44, .Google Scholar
Gaugler, MS and Romano, FA (1995) A preliminary survey of marine sand tardigrades of Dauphin Island, Alabama. Journal of the Alabama Academy of Science 66, .Google Scholar
Grimaldi De Zio, S and D’Addabbo, GM (1975b). Reproductive cycle of Batillipes pennaki Marcus (Heterotardigrada) and observations on the morphology of the female genital apparatus. In VII European Marine Biology Symposium, Sorrento (Naples), 1973, 39, Pubblicazioni Stazione Zoologica di Napoli (212225).Google Scholar
Grimaldi De Zio, S and D’Addabbo Gallo, M (1975a) Sviluppo postembrionale e mute in Batillipes pennaki Marcus (Heterotardigrada). Rivista Di Biologia 68, 246263.Google Scholar
Grimaldi De Zio, S, D’Addabbo Gallo, M and Morone De Lucia, M (1983) Marine tardigrades of the ‘Secca dell’Armellina’ (Ionian Sea), and redescription of Raiarctus colurus Renaud-Mornant 1988 (Heterotardigrada). Oebalia 9, 3342.Google Scholar
Grimaldi De Zio, S, D’Addabbo Gallo, M, Morone De Lucia, MR and Grimaldi, P (1980) Ulteriori dati sui Tardigradi del mesopsammon di alcune spiagge pugliesi. Thalassia Salentina 10, 4565.Google Scholar
Grimaldi De Zio, S, D’Addabbo Gallo, M, Morone De Lucia, MR, Sandulli, R, D’Addabbo, R, Faienza, MG and Pietanza, R (1999) First data on subtidal Meiofauna of Tremiti Islands. Biologia Marina Mediterranea 6, 380382.Google Scholar
Grimaldi De Zio, S, Morone De Lucia, MR, D’Addabbo Gallo, M and Grimaldi, P (1979) Osservazioni su alcuni tardigradi di una spiaggia pugliese e descrizione di Batillipes adriaticus sp. nov. (Heterotardigrada). Thalassia Salentina 9, 3950.Google Scholar
Guerin, M (1960) Observations écologiques sur Convoluta roscoffensis Graff. Cahiers de Biologie Marine 1, 205220.Google Scholar
Guidetti, R and Bertolani, R (2005) Tardigrade taxonomy: An updated check list of the taxa and a list of characters for their identification. Zootaxa 845(1). https://doi.org/10.11646/zootaxa.845.1.1CrossRefGoogle Scholar
Guidetti, R, McInnes, SJ, and Kristensen, RM (2024). Accessed at https://www.marinespecies.org/tardigrada.Google Scholar
Halberg, KA, Persson, D, Møbjerg, N, Wanninger, A and Kristensen, RM (2009) Myoanatomy of the marine tardigrade Halobiotus crispae (Eutardigrada: Hypsibiidae). Journal of Morphology 270(8), 9961013. https://doi.org/10.1002/jmor.10734CrossRefGoogle ScholarPubMed
Hay, WP (1917) A new species of bear-animalcule from the coast of North Carolina. Proceedings of the United States National Museum 53(2203), 251254.10.5479/si.00963801.53-2203.251CrossRefGoogle Scholar
Hummon, WD (1994) Trans-and cis-Atlantic distributions of three marine heterotardigrades. Transactions of the American Microscopical Society 113(3), 333342.10.2307/3226627CrossRefGoogle Scholar
Jägersten, G (1952) Studies on the morphology, larval development, and biology of Protodrilus. Zoologiska Bidrag Från Uppsala 29, 425512.Google Scholar
Jørgensen, A, Boesgaard, TM, Møbjerg, N and Kristensen, RM (2014) The tardigrade fauna of Australian marine caves: With descriptions of nine new species of Arthrotardigrada. Zootaxa 3802(4), 401443.10.11646/zootaxa.3802.4.1CrossRefGoogle Scholar
Kaczmarek, Ł, Bartels, PJ, Roszkowska, M and Nelson, DR (2015) The zoogeography of marine Tardigrada. Zootaxa 4037(1), 1189. https://doi.org/10.11646/zootaxa.4037.1.1CrossRefGoogle ScholarPubMed
Kayastha, P, Stec, D, Sługocki, Ł, Gawlak, M, Mioduchowska, M and Kaczmarek, Ł (2023) Integrative taxonomy reveals new, widely distributed tardigrade species of the genus Paramacrobiotus (Eutardigrada: Macrobiotidae). Scientific Reports 13(1), . https://doi.org/10.1038/s41598-023-28714-wCrossRefGoogle ScholarPubMed
King, CE (1962) The occurrence of Batillipes mirus Richters (Tardigrada) in the Gulf of Mexico. Bulletin of Marine Science of the Gulf and Caribbean 12, 201203.Google Scholar
Kristensen, RM (1978) Notes on marine Heterotardigrada. 1. Description of two new Batillipes species, using the electron microscope. Zoologischer Anzeiger 200, 117.Google Scholar
Kristensen, RM and Mackness, BS (2000) First record of the marine tardigrade genus Batillipes (Arthrotardigrada: Batillipedidae) from South Australia with a description of a new species. Records of the South Australian Museum 33(2), 7387.Google Scholar
McGinty, M (1969) Batillipes gilmartini, a new marine tardigrade from a California beach. Pacific Science 23, 394396.Google Scholar
McGinty, MM and Higgins, RP (1968) Ontogenetic variation of taxonomic characters of two marine tardigrades with the description of Batillipes bullacaudatus n. sp. Transactions of the American Microscopical Society 87(2), 252262.10.2307/3224449CrossRefGoogle Scholar
Mcintyre, AD and Eleftheriou, A (1968) The bottom fauna of a flatfish nursery ground. Journal of Marine Biological Association of United Kingdom 48, 113142.10.1017/S0025315400032471CrossRefGoogle Scholar
McIntyre, AD and Murison, DJ (1973) The meiofauna of a flatfish nursery ground. Journal of the Marine Biological Association of the United Kingdom 53, 93118.10.1017/S0025315400056666CrossRefGoogle Scholar
McKirdy, DJ (1975) Batillipes (Heterotardigrada): Comparison of six species from Florida (USA) and a discussion of taxonomic characters within the genus. Memorie Dell’Istituto Italiano Di Idrobiologia 32, 177223.Google Scholar
Menechella, AG, Bulnes, VN and Cazzaniga, NJ (2015) A new Batillipedidae (Tardigrada, Arthrotardigrada) from Argentina. Zootaxa 4032(3), 339344.10.11646/zootaxa.4032.3.11CrossRefGoogle ScholarPubMed
Menechella, AG, Bulnes, VN and Cazzaniga, NJ (2017) Two new species of Batillipes (Tardigrada, Arthrotardigrada, Batillipedidae) from the Argentinean Atlantic coast, and a key to all known species. Marine Biodiversity 48(1), 239247. https://doi.org/10.1007/s12526-017-0640-4CrossRefGoogle Scholar
Møbjerg, N, Halberg, KA, Jørgensen, A, Persson, D, Bjørn, M, Ramløv, H and Kristensen, RM (2011) Survival in extreme environments – On the current knowledge of adaptations in tardigrades. Acta Physiologica 202(3), 409420. https://doi.org/10.1111/j.1748-1716.2011.02252.xCrossRefGoogle ScholarPubMed
Møbjerg, N, Jørgensen, A, Eibye-Jacobsen, J, Agerlin Halberg, K, Persson, D and Møbjerg Kristensen, R (2007) New records on cyclomorphosis in the marine eutardigrade Halobiotus crispae (Eutardigrada: Hypsibiidae). Journal of Limnology 66(1s), . https://doi.org/10.4081/jlimnol.2007.s1.132CrossRefGoogle Scholar
Ng, W-L, Chen, C-A, Mustafa, S, Soo, C-L, Liao, Y-C and Shih, T-W (2022) Free-living marine nematodes community structure in the conservation area (Chaojing Park) and its adjacent area of Keelung, Taiwan. PLoS ONE 17(5), . https://doi.org/10.1371/journal.pone.0268691CrossRefGoogle Scholar
Papi, F (1952) Su alcuni Tardigradi raccolti nell’Italia centrale. Atti Della Società Toscana Di Scienze Naturali 59(1), 116118.Google Scholar
Petelina, OY and Tchesunov, AV (1983) A new representative of the fauna of the White Sea Hypsibius apelloefi (Tardigrada). Zoologischeskii Zhurnal 62, .Google Scholar
Pollock, LW (1970a) Batillipes dicrocercus n. sp., Stygarctus granulatus n. sp. and other Tardigrada from Woods Hole. Transactions of the American Microscopical Society 89(1), 3852 (Massachusetts, U.S.A). https://doi.org/10.2307/3224613CrossRefGoogle Scholar
Pollock, LW (1970b) Marine interstitial Heterotardigrada from the Georgia coast, U.S.A. Transactions of the American Microscopical Society 89, 380400.Google Scholar
Pollock, LW (1971) On some British marine Tardigrada, including two new species of Batillipes. Journal of Marine Biological Association of the United Kingdom 51, 93103.10.1017/S0025315400006482CrossRefGoogle Scholar
Pollock, LW (1989) Marine interstitial Tardigrada from the Pacific Coast of North America. Transactions of the American Microscopical Society 108, 161176.Google Scholar
Rahm, G (1937) Eine neue Tardigraden-Ordnung aus den heißen Quellen von Unzen, Insel Kyushu, Japan. Zoologischer Anzeiger 120, 6571.Google Scholar
Ramazzotti, J and Maucci, W (1989) II Phylum Tardigrada. Memorie Dell’Istituto Italiano Di Idrobiologia Dott. Macro de Marchi 41, 11012.Google Scholar
Renaud-Debyser, J (1956) Répartition de deux tardigrades Batillipes mirus Richters et Stygarctus bradycephalus Schulz dans unsegment de plage du Bassin d’Arcachon. Comptes Rendus de l’Académie Des Sciences (Paris) 243(1), 13651379.Google Scholar
Renaud-Debyser, J (1959) Sur quelques tardigrades du bassin d’Arcachon. Vie Et Milieu 10, 135146.Google Scholar
Renaud-Debyser, J and Salvat, B (1963) Eléments de prospérité des biotopes des sédiments meubles intertidaux et écologie de leurs populations en microfaune et macrofaune. Vie Et Milieu 14, 463550.Google Scholar
Rho, HS, Min, BH and Chang, CY (1999) Taxonomic study of marine tardigrades from Korea I. Genus Batillipes (Heterotardigrada: Batillipedidae). The Korean Journal of Systematic 15(1), 107118.Google Scholar
Riggin, GT (1959). The Tardigrada of Southwest Virginia: With the addition of a description of a new species from Florida [Doctoral dissertation]. Virginia Polytechnic Institute.Google Scholar
Riggin, GT (1962) Tardigrada of Southwest Virginia: With the addition of a new marine tardigrade species from Florida. Virginia Agricultural Experiment Station Technical Bulletin 152, 1145.Google Scholar
Rossi, GC and Claps, MC (1983) Batillipes mirus Richters, 1909 (Tardigrada), nuevo registro para la Argentina. Physis, Sección B 41(100), 105107.Google Scholar
Rubal, M, Veiga, P, Fontoura, P and Sousa-Pinto, I (2016). A new Batillipes (Tardigrada, Heterotardigrada, Batillipedidae) from North Portugal (Atlantic Ocean). Marine Biodiversity. https://doi.org/10.1007/s12526-016-0526-xCrossRefGoogle Scholar
Rudescu, L (1964) Tardigrada. Fauna Republicii Populare Romîne, Arthropoda 4, 1400. Fasc. 7.Google Scholar
Santos, E, da Rocha, CMC, Gomes, E, Jr and Fontoura, P (2017) Three new Batillipes species (Arthrotardigrada: Batillipedidae) from the Brazilian coast. Zootaxa 4243(3), 483502.10.11646/zootaxa.4243.3.4CrossRefGoogle ScholarPubMed
Santos, E, Gomes, E, Jr., da Rocha, CMC, Bartels, PJ and Fontoura, P (2018a) A closer look at Batillipes dicrocercus and new records of Batillipes potiguarensis (Tardigrada: Arthrotardigrada) from the Brazilian coast with comments on intra- and interspecific variability. Iheringia. Série Zoologia 108, .10.1590/1678-4766e2018041CrossRefGoogle Scholar
Santos, E, Rubal, M, Veiga, P, Da Rocha, CMC and Fontoura, P (2018b) Batillipes (Tardigrada, Arthrotardigrada) from the Portuguese coast with the description of two new species and a new dichotomous key for all species. European Journal of Taxonomy 425, 132. https://doi.org/10.5852/ejt.2018.425Google Scholar
Schulz, E (1955) Studien an marinen Tardigraden. Kieler Meeresforschungen 11(1), 7379.Google Scholar
Seinhorst, JW (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica 4, 6769.10.1163/187529259X00381CrossRefGoogle Scholar
Stec, D, Dudziak, M and Michalczyk, Ł (2020) Integrative descriptions of two new Macrobiotidae species (Tardigrada: Eutardigrada: Macrobiotoidea) from French Guiana and Malaysian Borneo. Zoological Studies 59, . https://doi.org/10.6620/ZS.2020.59-23Google ScholarPubMed
Tchesunov, AV and Mokievsky, VO (1995) A new marine tardigrade, Batillipes crassipes sp. nov., from the Japan Sea (Tardigrada Arthrotardigrada, Batillipedidae). Cah Biol Mar 36, 153157.Google Scholar
Valkanov, A (1950) Echiniscoides sigismundi (M. Schultze) from the Black Sea. Trudy Morskogo Biologicheskogo Instituta 15(1), 181186.Google Scholar
Valkanov, A (1954) Czernomorskyte Tardigradi. Die Tardigraden des Schwarzen Meeres. Sofiicki Universitet 48(1), 5961.Google Scholar
Veiga, P (2002) Galiza: Universidade De Santiago De Compostela La Meiofauna Intermareal De Sustratos Blandos De La Ría De O Barqueiro (Galiza).Google Scholar
Vishnudattan, NK, Rubal, M and Nandan, SB (2024) A new marine tardigrade species (Heterotardigrada: Batillipedidae) from the southeast coast of India. Zootaxa 5446(4), 488498. https://doi.org/10.11646/zootaxa.5446.4.2CrossRefGoogle ScholarPubMed
Zieritz, A, Lee, PS, Eng, WWH, Lim, SY, Sing, KW, Chan, WN, Loo, JS, Mahadzir, FN, Ng, TH, Yeo, DCJ, Gan, LX, Gan, JY, Gibbins, C, Zoqratt, MZHM and Wilson, J (2022) DNA metabarcoding unravels unknown diversity and distribution patterns of tropical freshwater invertebrates. Freshwater Biology 67(8), 14111427. https://doi.org/10.1111/fwb.13926CrossRefGoogle Scholar