Abstract
The island of Penang lying off the northwestern coast of Peninsular Malaysia, is one of the historical places for ichthyological exploration in Southeast Asia and the type locality of three freshwater species and one euryhaline species. Freshwater ecosystems on the island are currently threatened by multiple causes. To facilitate further environmental-oriented monitoring actions, we reexamined the fish diversity by surveying several freshwater localities across the island. All collected specimens were vouchered, morphologically identified and then genetically characterized using the “Barcode” fragment of the cytochrome oxidase I gene. We collected a total of 52 fish species, including 37 (21 native + 16 introduced) strictly-adapted freshwater species. Five native and 10 introduced species represent new records for the island. Genetic analyses revealed low cryptic diversity within morphologically identified species. Combining our results with those of previous surveys, a total of 63 fish species are now known from Penang freshwaters, however, five native species were not collected in the last 60 years and their conservation status is certainly at risk on the island. Overall, the presence of many introduced species along with the general degradation of freshwater habitats of Penang Island threaten its native fish diversity.
Similar content being viewed by others
Data availability
Data are publicly available in the Barcode of Life Datasystem (BOLD) (https://boldsystems.org/) under the project “Inventorying the biodiversity of inland waters of the Penang Hill (Project code: BIOPH)”. Representative sequences were deposited in GenBank (Accession Numbers MW590986-MW591187).
Code availability
Not applicable.
References
Abdul Kadir SR, Abdul Rasid MHF, Kwong KO, Wong LL, Arai T (2017) Occurrence and the ecological implication of a tropical anguillid eel Anguilla marmorata from peninsular Malaysia. ZooKeys 695:103–110. https://doi.org/10.3897/zookeys.695.13298
Abell R, Thieme ML, Revenga C, Bryer M, Kottelat M, Bogutskaya N, Coad B, Mandrak N, Balderas SC, Bussing W, Stiassny MLJ, Skelton P, Allen GR, Unmack P, Naseka A, Ng R, Sindorf N, Robertson J, Armijo E, Higgins JV, Heibel TJ, Wikramanayake E, Olson D, López HL, Reis RE, Lundberg JG, Sabaj Pérez MH, Petry P (2008) Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience 58(5):403–414
Ahmad Sobri NZ, Lavoué S, Aziz F, Mohd Nor SA, Mohammed Akib NA, Khaironizam MZ (2021) To lump, to split or to maintain? Molecular taxonomy of the spotted barb Barbodes binotatus (Cyprinidae) and closely related species in Peninsular Malaysia. J Fish Biol 99(2):656–668. https://doi.org/10.1111/jfb.14754
Alfred ER (1961) The Cantor collection of Malayan fresh-water fishes. Raffles Bull Zool 26:183–186
Alfred ER (1963) Notes on a collection of freshwater fishes from Penang. Bul Nat Sing Mus 32:143–153
Amir Shah RMS (1993) A preliminary study of freshwater fishes of Penang Island. BSc Thesis. Universiti Sains Malaysia, Penang
Amirrudin A, Lim KP (2006) Inland fishes recorded from the Langkawi Island, Peninsular Malaysia. Malay Nat J 59(1):103–120
Amirrudin A, Yusuf Y, Nor SAM, Ali A (2004) The fish fauna of Pantai Acheh Forest Reserve in Penang, Malaysia: species composition, local distribution and inter-site relationship. J Biosains 15(1):49–61
Animal Welfare Board (2020) Malaysian Code of Practice for the Care and Use of Animals for Scientific Purposes (MY CODE), 2nd edn. Department of Veterinary Services Malaysia, Putrajaya, Malaysia. http://www.dvs.gov.my/dvs/resources/user_1/2020/Kebajikan%20Haiwan/GP01.pdf)
Azmir IA, Samat A (2010) Diversity and distribution of stream fishes of Pulau Langkawi, Malaysia. Sains Malays 39(6):869–875
Canonico GC, Arthington A, McCrary JK, Thieme ML (2005) The effects of introduced tilapias on native biodiversity. Aquat Conserv 15(5):463–483. https://doi.org/10.1002/aqc.699
Cantor T (1849) Catalogue of the Malayan fishes. J Asiat Soc Bengal 18(2):1–12
Carstens BC, Pelletier TA, Reid NM, Satler JD (2013) How to fail at species delimitation. Mol Ecol 22:4369–4383
Chee SY, Othman AG, Sim YK, Adam ANM, Firth LB (2017) Land reclamation and artificial islands: walking the tightrope between development and conservation. Glob Ecol Conserv 12:80–95. https://doi.org/10.1016/j.gecco.2017.08.005
Cucherousset J, Olden JD (2011) Ecological impacts of non-native freshwater fishes. Fisheries 36(5):215–230. https://doi.org/10.1080/03632415.2011.574578
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. https://doi.org/10.1186/1471-2148-7-214
Dudgeon D (2003) The contribution of scientific information to the conservation and management of freshwater biodiversity in tropical Asia. In: Martens K (ed) Aquatic biodiversity. Developments in hydrobiology. Springer, Dordrecht, pp 295–314
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:e113. https://doi.org/10.1186/1471-2105-5-113
Fricke R, Eschmeyer WN, Van der Laan R (2021) Eschmeyer’s Catalog of Fishes: Genera, Species, References. California Academy of Sciences, San Francisco, California. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Accessed 23 Jan 2021
Gozlan RE, Britton RE, Cowx I, Copp GH (2010) Current knowledge on non-native freshwater fish introductions. J Fish Biol 76(4):751–786. https://doi.org/10.1111/j.1095-8649.2010.02566.x
Günther A (1861) Catalogue of the fishes in the British Museum. Catalogue of the acanthopterygian fishes in the collection of the British Museum. Gobiidae, Discoboli, Pediculati, Blenniidae, Labyrinthici, Mugilidae, Notacanthi. London 3:i-xxv + 1–586 + i-x
Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19(9):470–474. https://doi.org/10.1016/j.tree.2004.07.005
Herre AWCT (1940) New species of fishes from the Malay Peninsula and Borneo. Raffles Bull Zool 16:5–26
Lee P, Sulaiman Z (2015) Genetic identification and structure of Clarias batrachus (Linnaeus, 1758) from Southeast Asia using a mitochondrial DNA marker. Zootaxa 3962(1):182–190. https://doi.org/10.11646/zootaxa.3962.1.11
Lim H, Zainal Abidin M, Pulungan CP, de Bruyn M, Nor SAM (2016) DNA Barcoding reveals high cryptic diversity of the freshwater halfbeak genus Hemirhamphodon from Sundaland. PLoS ONE 11(9):e0163596. https://doi.org/10.1371/journal.pone.0163596
Ng HH, Kottelat M (2008) The identity of Clarias batrachus (Linnaeus, 1758), with the designation of a neotype (Teleostei: Clariidae). Zool J Linn Soc 153(4):725–732. https://doi.org/10.1111/j.1096-3642.2008.00391.x
Norén M, Kullander S, Rahman M, Mollah A (2017) First records of Croaking Gourami, Trichopsis vittata (Cuvier, 1831) (Teleostei: Osphronemidae), from Myanmar and Bangladesh. Check List 13(4):81–85. https://doi.org/10.15560/13.4.81
Nurul Farhana S, Muchlisin ZA, Duong TY, Tanyaros S, Page LM, Zhao Y, Adamson EAS, Khaironizam MZ, de Bruyn M, Nor SAM (2018) Exploring hidden diversity in Southeast Asia’s Dermogenys spp. (Beloniformes: Zenarchopteridae) through DNA barcoding. Sci Rep 8:e10787. https://doi.org/10.1038/s41598-018-29049-7
Nurul-Ruhayu M-R, An YJ, Khairun Y (2015) Detection of river pollution using water quality index: a case study of tropical rivers in Penang Island. Malaysia Open Access Libr J 2:e1209. https://doi.org/10.4236/oalib.1101209
Olson DM, Dinerstein E (2002) The Global 200: Priority ecoregions for global conservation. Ann Mo Bot Gard 89(2):199–224
Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7:16. https://doi.org/10.1186/1742-9994-7-16
Panijpan B, Laosinchai P, Senapin S, Kowasupat C, Ruenwongsa P, Kühne J, Phiwsaiya K (2015) Mitochondrial COI and nuclear RAG1 DNA sequences and analyses of specimens of the three morphologically established species in the genus Trichopsis (Perciformes: Osphronemidae) reveal new/cryptic species. Meta Gene 4:17–28. https://doi.org/10.1016/j.mgene.2015.02.003
Peh KS (2010) Invasive species in Southeast Asia: the knowledge so far. Biodivers Conserv 19:1083–1099. https://doi.org/10.1007/s10531-009-9755-7
Pons J, Barraclough TG, Gomezzurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609. https://doi.org/10.1080/10635150600852011
Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol 21(8):1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
Radinger J, Britton JR, Carlson SM, Magurran AE, Alcaraz-Hernández JD, Almodóvar A, Benejam L, Fernández-Delgado C, Nicola GG, Oliva-Paterna FJ, Torralva M, García-Berthou E (2019) Effective monitoring of freshwater fish. Fish Fish 20(4):729–747. https://doi.org/10.1111/faf.12373
Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer (Version 1.6) [Software]. http://beast.bio.ed.ac.uk/Tracer
Ratnasingham S, Hebert PDN (2013) A DNA-based registry for all animal species: the Barcode Index Number (BIN) System. PLoS ONE 8(7):e66213. https://doi.org/10.1371/journal.pone.0066213
Robinson AK (2017) The growth of Singapore and Hong Kong in the face of climate change and environmental degradation, International Immersion Program Papers 64. University of Chicago Law School, Chicago
Rüber L, Tan HH, Britz R (2020) Snakehead (Teleostei: Channidae) diversity and the Eastern Himalaya biodiversity hotspot. J Zool Syst Evol Res 58(1):356–386. https://doi.org/10.1111/jzs.12324
Saba AO, Ismail A, Zulkifli SZ, Halim MRA, Wahid NAA, Amal MNA (2020a) Species composition and invasion risks of alien ornamental freshwater fishes from pet stores in Klang Valley, Malaysia. Sci Rep 10:17205. https://doi.org/10.1038/s41598-020-74168-9
Saba AO, Ismail A, Zulkifli SZ, Shohaimi S, Jamil NR, Nawi NM, Ghani IFA, Halim MRA, Amal MNA (2020b) Checklists, production trends, and potential ecological and socioeconomic impacts of non-native freshwater fishes in Malaysia: a review. Aqua Invasions 15(4):646–670. https://doi.org/10.3391/ai.2020.15.4.07
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor, New York
Seebens H, Blackburn TM, Dyer EE, Genovesi P, Hulme PE, Jeschke JM, Pagad S, Pyšek P, Winter M, Arianoutsou M, Bacher S, Blasius B, Brundu G, Capinha C, Celesti-Grapow L, Dawson W, Dullinger S, Fuentes N, Jäger H, Kartesz J, Kenis M, Kreft H, Kühn I, Lenzner B, Liebhold A, Mosena A, Moser D, Nishino M, Pearman D, Pergl J, Rabitsch W, Rojas-Sandoval J, Roques A, Rorke S, Rossinelli S, Roy HE, Scalera R, Schindler S, Štajerová K, Tokarska-Guzik B, Van Kleunen M, Walker K, Weigelt P, Yamanaka T, Essl F (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8:e14435. https://doi.org/10.1038/ncomms14435
Seebens H, Bacher S, Blackburn TM, Capinha C, Dawson W, Dullinger S, Genovesi P, Hulme PE, van Kleunen M, Kühn I, Jeschke JM, Lenzner B, Liebhold AM, Pattison Z, Pergl J, Pyšek P, Winter M, Essl F (2020) Projecting the continental accumulation of alien species through to 2050. Glob Chang Biol 27(5):970–982. https://doi.org/10.1111/gcb.15333
Sholihah A, Delrieu-Trottin E, Condamine FL, Wowor D, Rüber L, Pouyaud L, Agnèse J-F, Hubert N (2021) Impact of pleistocene eustatic fluctuations on evolutionary dynamics in Southeast Asian biodiversity hotspots. Syst Biol 70(5):940–960. https://doi.org/10.1093/sysbio/syab006
Sholihah A, Delrieu-Trottin E, Sukmono T, Dahruddin H, Risdawati R, Elvyra R, Wibowo A, Kustiati K, Busson F, Sauri S, Nurhaman U, Dounias E, Zein MSA, Fitriana Y, Utama IV, Muchlisin ZA, Agnèse JF, Hanner R, Wowor D, Steinke D, Keith P, Rüber L, Hubert N (2020) Disentangling the taxonomy of the subfamily Rasborinae (Cypriniformes, Danionidae) in Sundaland using DNA barcodes. Sci Rep 10(1):2818. https://doi.org/10.1038/s41598-020-59544-9
Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337. https://doi.org/10.1007/s13127-011-0056-0
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stecher G, Tamura K, Kumar S (2020) Molecular Evolutionary Genetics Analysis (MEGA) for macOS. Mol Biol Evol 37(4):1237–1239. https://doi.org/10.1093/molbev/msz312
Strayer DL, Dudgeon D (2010) Freshwater biodiversity conservation: recent progress and future challenges. J N Am Benthol Soc 29(1):344–358. https://doi.org/10.1899/08-171.1
Supiwong W, Pinthong K, Seetapan K, Saenjundaeng P, Bertollo LAC, de Oliveira EA, Yano CF, Liehr T, Phimphan S, Tanomtong A, Cioffi MB (2019) Karyotype diversity and evolutionary trends in the Asian swamp eel Monopterus albus (Synbranchiformes, Synbranchidae): a case of chromosomal speciation? BMC Evol Biol 19(1):e73. https://doi.org/10.1186/s12862-019-1393-4
Tan HH, Tan SH (1996) Redescription of the Malayan fighting fish Betta pugnax (Teleostei: Belontiidae), and description of Betta pulchra, new species from Peninsular Malaysia. Raffles Bull Zool 44(2):419–434
Tan HH, Low BW, Yeo DCJ, Lim KKP (2015) An update to the Inland Fishes of Pulau Tioman, Malaysia. Raffles Bull Zool 63:555–563
Tan HH, Lim KKP, Ng PYC (2018) Recent records of the pink mud-eel in Singapore. Singap Biodivers Rec 2018:4–6
Tew YL, Tan ML, Samat N, Yang X (2019) Urban Expansion Analysis using Landsat Images in Penang, Malaysia. Sains Malays 48(11):2307–2315. https://doi.org/10.17576/jsm-2019-4811-02
UNESCO, UN-Water (2020) United Nations World Water Development Report 2020: Water and Climate Change, Paris
Vörösmarty C, McIntyre P, Gessner M, Dudgeon D, Prusevich A, Green P, Glidden S, Bunn SE, Sullivan CA, Reidy Liermann C, Davies PM (2010) Global threats to human water security and river biodiversity. Nature 467:555–561. https://doi.org/10.1038/nature09440
Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B 360(1462):1847–1857. https://doi.org/10.1098/rstb.2005.1716
Weigand H, Beermann AJ, Čiampor F, Costa FO, Csabai Z, Duarte S, Geiger MF, Grabowski M, Rimet F, Rulik B, Strand M, Szucsich N, Weigand AM, Willassen E, Wyler SA, Bouchez A, Borja A, Čiamporová-Zaťovičová Z, Ferreira S, Dijkstra BK-D, Eisendle U, Freyhof J, Gadawski P, Graf W, Haegerbaeumer A, van der Hoorn BB, Japoshvili B, Keresztes L, Keskin E, Leese F, Macher JN, Mamos T, Paz G, Pešić V, Pfannkuchen DM, Pfannkuchen MA, Price BW, Rinkevich B, Teixeira MAL, Várbíró G, Ekrem T (2019) DNA barcode reference libraries for the monitoring of aquatic biota in Europe: gap-analysis and recommendations for future work. Sci Total Environ 678:499–524. https://doi.org/10.1016/j.scitotenv.2019.04.247
Wong WY, Chow LH, Wu TH, Ma KY, Tsang LM, Chu KH (2019) Conservation of freshwater wildlife in Hong Kong: a genetic perspective. Aquat Conserv 29(12):2204–2218. https://doi.org/10.1002/aqc.3211
Young HS, McCauley DJ, Galetti M, Dirzo R (2016) Patterns, causes, and consequences of Anthropocene defaunation. Annu Rev Ecol Evol Syst 47(1):333–358. https://doi.org/10.1146/annurev-ecolsys-112414-054142
Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29(22):2869–2876. https://doi.org/10.1093/bioinformatics/btt499
Acknowledgements
We would like to acknowledge Lim Teow Yeong for his assistance in collecting the samples. Fieldwork was conducted under permissions issued by the Forestry Department Peninsular Malaysia (Penang State Forestry Department) [Reference no: JPNPP/100-1/7/1 Jld. 2(6)]. Our thanks also go to Penang Hill Corporation and the Habitat Penang Hill for logistics support.
Funding
This work was funded by Universiti Malaysia Terengganu and Ministry of Water, Land and Natural Resources of Malaysia (UMT/IMB/2019/53308—An inventory of aquatic macrofauna and fishes in the proposed Penang Hill UNESCO Biosphere Reserve).
Author information
Authors and Affiliations
Contributions
Conceptualization: JAFJ, SL, AA, AT, CLL, SAMN; Sampling: JAFJ, SL, NFMAHA, SZBG; Laboratory analyses: JAFJ, NFMAHA, SZBG; Data management and analyses; JAFJ, SL, NFMAHA, SZBG; Draft preparation: JAFJ, SL, SAMN; Review and editing: JAFJ, SL, NFMAHA, SZBG, AA, AT, CLL, SAMN; Funding acquisition: SAMN. All authors approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
This manuscript is the authors’ own original research and has not been submitted or published elsewhere simultaneously.
Consent to participate and publish
There was a full consent of all authors to participate; all authors accepted the revised draft and gave consent to the corresponding author to submit it for publishing.
Additional information
Communicated by Mike Kevin Joy.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jamaluddin, J.A.F., Lavoué, S., Alshari, N.F.M.A.H. et al. Reassessing fish diversity of Penang Island’s freshwaters (northwest Peninsular Malaysia) through a molecular approach raises questions on its conservation status. Biodivers Conserv 31, 1551–1576 (2022). https://doi.org/10.1007/s10531-022-02409-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-022-02409-6