Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-25T06:14:25.226Z Has data issue: false hasContentIssue false

Distribution of the newly invasive New Guinea flatworm Platydemus manokwari (Platyhelminthes: Geoplanidae) in Thailand and its potential role as a paratenic host carrying Angiostrongylus malaysiensis larvae

Published online by Cambridge University Press:  20 September 2018

K. Chaisiri*
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchavithi Rd, Ratchathewi, Bangkok, 10400Thailand
S. Dusitsittipon
Affiliation:
Department of Parasitology and Entomology, Faculty of Public Health, Mahidol University, Bangkok, 10400, Thailand
N. Panitvong
Affiliation:
Siamensis Biodiversity Conservation Group, 408/144 Phaholyothin Place Building, 34th floor, Phaholyothin Rd., Phayathai, Bangkok, 10400, Thailand
T. Ketboonlue
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchavithi Rd, Ratchathewi, Bangkok, 10400Thailand
S. Nuamtanong
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchavithi Rd, Ratchathewi, Bangkok, 10400Thailand
U. Thaenkham
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchavithi Rd, Ratchathewi, Bangkok, 10400Thailand
S. Morand
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchavithi Rd, Ratchathewi, Bangkok, 10400Thailand CIRAD ASTRE, Faculty of Veterinary Technology, Kasetsart University, 10900 Bangkok, Thailand Intitut des Sciences de l'Evolution, CNRS, IRD, University of Montpellier, Montpellier 34290, France
P. Dekumyoy
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, 420/6 Ratchavithi Rd, Ratchathewi, Bangkok, 10400Thailand
*
Author for correspondence: K. Chaisiri, Fax: +66 (0)2643-5600 E-mail: kittipong.cha@mahidol.ac.th

Abstract

Invasive species constitute one of the most serious threats to biodiversity and ecosystems, and they potentially cause economic problems and impact human health. The globally invasive New Guinea flatworm, Platydemus manokwari (Platyhelminthes: Geoplanidae), has been identified as a threat to terrestrial biodiversity, particularly soil-dwelling native species (e.g. molluscs, annelids and other land planarians), and is listed among 100 of the world's worst invasive alien species. We report here, for the first time, P. manokwari occurrences in many locations throughout Thailand, using voluntary digital public participation from the social network portals associated with the Thailand Biodiversity Conservation Group and collections of living flatworm specimens. Mitochondrial cytochrome c oxidase subunit I (COI) sequences confirmed that all collected flatworms were P. manokwari and placed them in the “world haplotype” clade alongside other previously reported specimens from France, Florida (USA), Puerto Rico, Singapore, French Polynesia, New Caledonia, and the Solomon Islands. In addition, infective stage larvae (L3) of the nematode Angiostrongylus malaysiensis were found in the flatworm specimens, with a 12.4% infection rate (15/121 specimens examined). Platydemus manokwari occurrence in Thailand and its capacity to carry L3 of Angiostrongylus should be of concern to biodiversity conservation and human health practitioners, because this invasive flatworm species may be involved in the life cycle of angiostrongylid worms in Thailand.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alicata, JE and Jindrak, K (1970) Angiostrongylosis in the Pacific and Southeast Asia. American lecture series: Monograph in American lectures in tropical medicine. University of Michigan, USA, 105 p.Google Scholar
Alto, W (2001) Human infections with Angiostrongylus cantonensis. Pacific Health Dialog 8, 176182.Google Scholar
Arts, K, van der Wal, R and Adams, WM (2015) Digital technology and the conservation of nature. Ambio 44, 661673.Google Scholar
Asato, R et al. (2004) Changing epidemiology of Angiostrongyliasis cantonensis in Okinawa Prefecture, Japan. Japanese Journal of Infectious Diseases 57, 184186.Google Scholar
Ash, LR (1976) Observations on the role of mollusks and planarians in the transmission of Angiostrongylus cantonensis infection to man in New Caledonia. Revista de Biología Tropical 24, 163174.Google Scholar
Beck, KG et al. (2008) Invasive species defined in a policy context: recommendations from the Federal Invasive Species Advisory Committee. Invasive Plant Science and Management 1, 414421.Google Scholar
Bivand, R and Lewin-Koh, N (2017) maptools: Tools for Reading and Handling Spatial Objects. R package version 0.9-2. Available at https://CRAN.R-project.org/package=maptools. (accessed 26 February 2018).Google Scholar
Blackburn, TM and Duncan, RP (2001) Determinants of establishment success in introduced birds. Nature 414, 195197.Google Scholar
Carney, WP and Stafford, EE (1979) Angiostrongyliasis in Indonesia – a review. In Cross, JH (ed.), Studies on Angiostrongyliasis in Eastern Asia and Australia. NAMRU-2 Special Publication No. 44. Taipei, Taiwan, pp. 1425.Google Scholar
Cheng, TC and Alicata, JE (1964) Possible role of water in the transmission of Angiostrongylus cantonensis (Nematoda: Metastrongylidae). Journal of Parasitology 50, 3940.Google Scholar
Conrad, C and Hilchey, K (2011) A review of citizen science and community-based environmental monitoring: issues and opportunities. Environmental Monitoring and Assessment 176, 273291.Google Scholar
Convention on Biological Diversity (2018) What are invasive alien species? Available at https://www.cbd.int/invasive/WhatareIAS.shtml (accessed 4 August, 2018).Google Scholar
Cowie, RH (2013) Pathways for transmission of angiostrongyliasis and the risk of disease associated with them. Hawaii Journal of Medicine & Public Health 72, 7074.Google Scholar
Cross, JH (1979) Experimental studies of Angiostrongylus species and strains in monkeys and laboratory animals. In Cross, JH (ed.), Studies on Angiostrongyliasis in Eastern Asia and Australia. NAMRU-2 Special Publication No. 44. US Naval Medical Research Unit, Taipei, Taiwan, pp, 118137.Google Scholar
Dickinson, J, Zuckerberg, B and Bonter, D (2010) Citizen science as an ecological research tool: challenges and benefits. Annual Review of Ecology, Evolution, and Systematics 41, 149172.Google Scholar
Dunn, AM et al. (2012) Indirect effects of parasites in invasions. Functional Ecology 26, 12621274.Google Scholar
Dusitsittipon, S et al. (2017) Cryptic lineage diversity in the zoonotic pathogen Angiostrongylus cantonensis. Molecular Phylogenetics and Evolution 107, 404414.Google Scholar
Eamsobhana, P (2013) Angiostrongyliasis in Thailand: epidemiology and laboratory investigations. Hawaii Journal of Medicine & Public Health 72, 2832.Google Scholar
Eamsobhana, P et al. (2018) Cytochrome c oxidase subunit I haplotype reveals high genetic diversity of Angiostrongylus malaysiensis (Nematoda: Angiostrongylidae). Journal of Helminthology 92, 254259.Google Scholar
Folmer, O et al. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google Scholar
Freestone, AL, Ruiz, GM and Torchin, ME (2013) Stronger biotic resistance in tropics relative to temperate zone: effects of predation on marine invasion dynamics. Ecology 94, 13701377.Google Scholar
Fridley, JD and Sax, DF (2014) The imbalance of nature: revisiting a Darwinian framework for invasion biology. Global Ecology and Biogeography 23, 11571166.Google Scholar
Gibbons, LM and Krishnasamy, M (1986) Malayometastrongylus diardinematus n. g., n. sp. (Metastrongyloidea: Angiostrongylidae) from Rattus rattus diardii in Malaysia and a redescription of Thaistrongylus harinasutai Ohbayashi, Kamiya & Bhaibulaya. Systematic Parasitology 8, 107115.Google Scholar
Graeff-Teixeira, C, Aramburu da Silva, AC and Yoshimura, K (2009) Update on eosinophilic meningoencephalitis and its clinical relevance. Clinical Microbiology Reviews 22, 322348.Google Scholar
Hall, T (2011) BioEdit: An important software for molecular biology. GERF Bulletin of Biosciences 2, 6061.Google Scholar
Heyneman, D and Lim, BL (1967) Angiostrongylus cantonensis: Proof of direct transmission with its epidemiological implications. Science 158, 10571058.Google Scholar
Justine, JL et al. (2014) The invasive New Guinea flatworm Platydemus manokwari in France, the first record for Europe: time for action is now. PeerJ 2, e297.Google Scholar
Justine, JL et al. (2015) The invasive land planarian Platydemus manokwari (Platyhelminthes, Geoplanidae): records from six new localities, including the first in the USA. PeerJ 3, e1037.Google Scholar
Kaneda, M, Kitagawa, K and Ichinohe, F (1990) Laboratory rearing method and biology of Platydemus manokwari De Beauchamp (Tricladida: Terriocola: Rhyncodermidae). Applied Entomology and Zoology 25, 524528.Google Scholar
Keane, RM and Crawley, MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution 17, 164170.Google Scholar
Kelly, DW et al. (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90, 20472056.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.Google Scholar
Larkin, MA et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 29472948.Google Scholar
Lim, BL and Ramachandran, CP (1979) Ecological studies on Angiostrongylus malaysiensis (Nematoda: Metastrongylidae) in Malaysia. In Cross, JH (ed.) Studies on Angiostrongyliasis in Eastern Asia and Australia. NAMRU-2 Special Publication No. 44. Taipei, Taiwan, pp. 2648.Google Scholar
Littlewood, DTJ, Rohde, K and Clough, KA (1997) Parasite speciation within or between host species?—Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27, 12891297.Google Scholar
Lowe, S et al. (2000) 100 of the World's Worst Invasive Alien Species Database. The Invasive Species Specialist Group (ISSG), IUCN, Auckland, New Zealand.Google Scholar
Lowry, E et al. (2013) Biological invasions: a field synopsis, systematic review, and database of the literature. Ecology and Evolution 3, 182196.Google Scholar
Marbuah, G, Gren, I and McKie, B (2014) Economics of harmful invasive species: a review. Diversity 6, 500523.Google Scholar
Melbourne, BA et al. (2007) Invasion in a heterogeneous world: resistance, coexistence or hostile takeover? Ecology Letters 10, 7794.Google Scholar
Montero-Pau, J, Gómez, A and Muñoz, J (2008) Application of an inexpensive and high-throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnology and Oceanography Methods 6, 218222.Google Scholar
Morand, S (2015) Infections and diseases in wildlife by non-native organisms. In Vila, M, Hulme, P and Ruiz, G (eds), Impact of Biological Invasions on Ecosystem Services. Cham, Switzerland: Springer International Publishing, pp. 177190.Google Scholar
Ohbayashi, M, Kamiya, M and Bhaibulaya, M (1979) Studies on the parasite fauna of Thailand I. Two new metastrongylid nematodes, Angiostrongylus siamensis sp. n. and Thaistrongylus harinasutai gen. et sp. n. (Metastrongyloidea; Angiostrongylidae) from wild rats. Japanese Journal of Veterinary Research 27, 510.Google Scholar
Ohbayashi, T et al. (2007) Rapid decline of endemic snails in the Ogasawara Islands, Western Pacific Ocean. Applied Entomology and Zoology 42, 479485.Google Scholar
Panitvong, N (2017) Report of New Guinea Flatworm Occurrence in Thailand. Thailand Biodiversity Conservation Group. Available at http://siamensis.org/article/41220 (accessed 7 February 2018).Google Scholar
Pipitgool, V et al. (1997) Angiostrongylus infections in rats and snails in northeast Thailand. Southeast Asian Journal of Tropical Medicine & Public Health 28, 190193.Google Scholar
Prociv, P, Spratt, DM and Carlisle, MS (2000) Neuro-angiostrongyliasis: unresolved issues. International Journal for Parasitology 30, 12951303.Google Scholar
Qvarnstrom, Y, Bishop, HS and da Silva, AJ (2013) Detection of rat lungworm in intermediate, definitive, and paratenic hosts obtained from environmental sources. Hawaii Journal of Medicine and Public Health 72, 6369.Google Scholar
R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/ (accessed 2 December 2017).Google Scholar
Reaser, JK et al. (2007) Ecological and socioeconomic impacts of invasive alien species in island ecosystems. Environmental Conservation 34, 98111.Google Scholar
Rodpai, R et al. (2016) Angiostrongylus cantonensis and A. malaysiensis broadly overlap in Thailand, Lao PDR, Cambodia and Myanmar: a molecular survey of larvae in land snails. PLoS ONE 11, e0161128.Google Scholar
Rozsa, L, Reiczigel, J and Majoros, G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228232.Google Scholar
Strauss, A, White, A and Boots, M (2012) Invading with biological weapons: the importance of disease-mediated invasions. Functional Ecology 26, 12491261.Google Scholar
Sugiura, S (2009) Seasonal fluctuation of invasive flatworm predation pressure on land snails: implications for the range expansion and impacts of invasive species. Biological Conservation 142, 30133019.Google Scholar
Sugiura, S, Okochi, I and Tamada, H (2006) High predation pressure by an introduced flatworm on land snails on the oceanic Ogasawara Islands. Biotropica 38, 700703.Google Scholar
Sugiura, S and Yamaura, Y (2009) Potential impacts of the invasive flatworm Platydemus manokwari on arboreal snails. Biological Invasions 11, 737742.Google Scholar
Tesana, S et al. (2009) Prevalence and intensity of infection with third stage larvae of Angiostrongylus cantonensis in mollusks from Northeast Thailand. American Journal of Tropical Medicine & Hygiene 80, 983987.Google Scholar
Veciana, M et al. (2014) New data on Malayometastrongylus diardinematus (Gibbons and Krishnasamy, 1986) (Metastrongyloidea: Angiostrongylidae) a lungworm occurring in Rattus tanezumi (Temminck, 1844) from South-East Asia. Helminthologia 51, 331336.Google Scholar
Vitta, A et al. (2011) Survey of Angiostrongylus cantonensis in rats and giant African land snails in Phitsanulok province, Thailand. Asian Pacific Journal of Tropical Medicine 4, 597599.Google Scholar
Vitta, A et al. (2016) Phylogeny of Angiostrongylus cantonensis in Thailand based on cytochrome c oxidase subunit I gene sequence. Southeast Asian Journal of Tropical Medicine & Public Health 47, 377386.Google Scholar
Wang, QP et al. (2008) Human angiostrongyliasis. The Lancet Infectious Diseases 8, 621630.Google Scholar
Zenni, RD and Nuñez, MA (2013) The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122, 801815.Google Scholar
Supplementary material: File

Chaisiri et al. supplementary material

Chaisiri et al. supplementary material 1

Download Chaisiri et al. supplementary material(File)
File 4.1 MB