Marine Biodiversity

, Volume 48, Issue 1, pp 117–126 | Cite as

An approach based on nematode descriptors for the classification of ecological quality (EcoQ) of the Malaysian coasts

  • Cheng-Ann Chen
  • Chen-Lin Soo
  • Maria Balsamo
  • Federica Semprucci
Meio Extreme

Abstract

Free-living marine nematodes were employed in ecological studies and were proven to be suitable bioindicators of pollution-induced effects on the benthic domain. This study represents the first attempt to use nematode descriptors in order to assign ecological quality (EcoQ) status to areas along the Sarawak coasts, thus integrating the methods actually applied by the Department of Environment (DOE). Three nematode parameters, i.e. colonizer–persister percentage, maturity index (MI), and Shannon diversity index (Hˈ), were used, as they are recognized as the best descriptors of EcoQ status in coastal habitats. The thresholds applied to the nematode parameters for the Sarawak study sites showed predominantly moderate and bad EcoQ status, with the exception of the Similajau site, which being close to a national park was found to have good EcoQ. The sites with the worst EcoQ were characterized by low salinity values, suggesting riverine inflows as a primary source of pollution, likely from the discharge of untreated wastes. This was confirmed by both the Hˈ and MI indices, which showed a close positive relation with salinity. Results obtained for the Niah site may suggest that “traces” of pollution were left in the nematode assemblages that could not be detected from other parameters of the water column. This investigation shows that analysis of nematode descriptors could be effectively applied to ecological assessment criteria within environmental policies of rapid growth countries such as Malaysia. Furthermore, it certainly suggests the need for management and conservation actions in the Sarawak coasts aimed at more sustainable use of the marine resources to prevent the loss of biodiversity.

Keywords

Zoobenthos Meiofauna Ecological quality assessment Anthropogenic impact Malaysia 

Notes

Acknowledgements

We would like to thank Professor Dr. Shabdin Mohd Long for his guidance. In addition, we would like to thank Universiti Malaysia Sabah for financial support through research grants (SLB0123-STWN-2016 and GKP0015-STWN-2016). The authors would also like to thank Universiti Malaysia Sarawak for providing the facilities and for administrative and logistic support during fieldwork. Finally, we would like to thank all the reviewers and the editor for their critical and constructive comments, which helped to improve the manuscript.

References

  1. Adão H, Alves AS, Patrício J, Neto JM, Costa MJ, Marques JC (2009) Spatial distribution of subtidal nematode communities along the salinity gradient in southern European estuaries. Acta Oecol 35:287–300CrossRefGoogle Scholar
  2. Amneera WA, Najib NW, Yusof SR, Ragunathan S (2013) Water quality index of Perlis River, Malaysia. Int J Civil Environ Eng 13:55–59Google Scholar
  3. Appeltans W, Ahyong ST, Anderson G et al (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202CrossRefPubMedGoogle Scholar
  4. Armenteros M, Ruiz-Abierno A, Fernández-Garce R, Pérez-García JA, Díaz-Asencio L, Vincx M, Decraemer W (2009) Biodiversity patterns of free-living marine nematodes in a tropical bay: Cienfuegos, Caribbean Sea. Estuar Coast Shelf Sci 85:179–189CrossRefGoogle Scholar
  5. Bale AJ, Kenny AJ (2005) Sediment analysis and seabed characterization. In: Eleftheriou A, Mclntyre A (eds) Methods for the study of marine benthos, 3rd edn. Blackwell Science Ltd, Oxford, pp 43–81CrossRefGoogle Scholar
  6. Balsamo M, Albertelli G, Ceccherelli VU et al (2010) Meiofauna of the Adriatic Sea: current state of knowledge and future perspectives. Chem Ecol 26(1):45–63CrossRefGoogle Scholar
  7. Balsamo M, Semprucci F, Frontalini F, Coccioni R (2012) Meiofauna as a tool for marine ecosystem biomonitoring. In: Cruzado A (ed) Marine ecosystems. InTech Publisher, pp 77–104Google Scholar
  8. Boi P, Amalfitano S, Manti A, Semprucci F, Sisti D, Rocchi MB, Balsamo M, Papa S (2015) Strategies for water quality assessment: multiparametric analysis of the bacterial community in river waters. River Res Appl.  https://doi.org/10.1002/rra.2872
  9. Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19CrossRefPubMedGoogle Scholar
  10. Bongers T, Alkemade R, Yeates GW (1991) Interpretation of disturbance-induced maturity decrease in marine nematode assemblages by means of the maturity index. Mar Ecol Prog Ser 76:135–142CrossRefGoogle Scholar
  11. Borja A, Franco J, Pérez V (2000) A marine biotic index to establish the ecology quality of soft-bottom benthos within European estuarine coastal environments. Mar Pollut Bull 40:1100–1114CrossRefGoogle Scholar
  12. Borja A, Mader J, Muxika I, Germán Rodríguez J, Bald J (2008) Using M-AMBI in assessing benthic quality within the water framework directive: some remarks and recommendations. Mar Pollut Bull 56:1377–1379CrossRefPubMedGoogle Scholar
  13. Borja A, Prins TC, Simboura N, Andersen JH, Berg T, Marques JC et al (2014) Tales from a thousand and one ways to integrate marine ecosystem components when assessing the environmental status. Front Mar Sci 1:72Google Scholar
  14. Buchnan JB (1984) Sediment analysis. In: Holme NA, Mclntyre AD (eds) Methods for the study of marine benthos. Blackwell Science Ltd, Oxford, pp 41–65Google Scholar
  15. Casazza G, Silvestri C, Spada E (2002) The use of bio-indicators for quality assessments of the marine environment: example from the Mediterranean Sea. J Coast Conserv 8:147–156CrossRefGoogle Scholar
  16. Chen CA, Mohd Long S, Mohd Rosli N (2012) Spatial distribution of tropical estuarine nematode communities in Sarawak, Malaysia (Borneo). Raffles Bull Zool 60:173–181Google Scholar
  17. Coccioni R, Frontalini F, Marsili A, Mana D (2009) Benthic foraminifera and trace element distribution: a case-study from the heavily polluted lagoon of Venice (Italy). Mar Pollut Bull 56:257–267CrossRefGoogle Scholar
  18. Danovaro R, Gambi C, Dell’Anno A, Corinaldesi C, Fraschetti S, Vanreusel A, Vincx M, Gooday AJ (2008) Exponential decline of deep-sea ecosystem functioning linked to benthic biodiversity loss. Curr Biol 18:1–8CrossRefPubMedGoogle Scholar
  19. Danovaro R, Gambi C, Manini E, Fabiano M (2000) Meiofauna response to a dynamic river plume front. Mar Biol 137:359–370CrossRefGoogle Scholar
  20. Danovaro R, Gambi C, Mirto S, Sandulli R, Ceccherelli VU (2004) Meiofauna. Biol Mar Mediterr 11:55–97Google Scholar
  21. Doney SC (2010) The growing human footprint on coastal and open-ocean biogeochemistry. Science 328:1512–1516CrossRefPubMedGoogle Scholar
  22. Franco MA, Steyaert M, Cabral HN, Tenreiro R, Chambel L, Vincx M, Costa MJ, Vanaverbeke J (2008) Impact of discards of beam trawl fishing on the nematode community from the Tagus estuary (Portugal). Mar Pollut Bull 56:1728–1736CrossRefPubMedGoogle Scholar
  23. Frontalini F, Semprucci F, Coccioni R, Balsamo M, Bittoni P, Covazzi-Harriague A (2011) On the quantitative distribution and community structure of the meio and macrofaunal communities in the coastal area of the central Adriatic Sea (Italy). Environ Monit Assess 180:325–344CrossRefPubMedGoogle Scholar
  24. Goodsell PJ, Underwood AJ, Chapman MG (2009) Evidence necessary for taxa to be reliable indicators of environmental conditions or impacts. Mar Pollut Bull 58:323–331CrossRefPubMedGoogle Scholar
  25. Guilini K, Bezerra TN, Eisendle-Flöckner U et al (2016) NeMys: world database of free-living marine nematodes. http://nemys.ugent.be. Accessed 13 October 2016
  26. Hamli H, Idris MH, Abu Hena MK, Wong SK (2012) Taxonomic study of edible bivalve from selected division of Sarawak, Malaysia. Int J Zool Res 8:52–58CrossRefGoogle Scholar
  27. Hill H, Yean TS, Zin RHM (2012) Malaysia's development challenges: graduating from the middle. Routledge, LondonGoogle Scholar
  28. Ho C, Quan CB (2012) Runoff quality and pollution loading from a residential catchment in Miri, Sarawak. Int J Environ Chem Ecol Geol Geophys Eng 6:732–735Google Scholar
  29. Huang YF, Ang SY, Lee KM, Lee TS (2015) Quality of water resources in Malaysia. In: Lee TS (Ed) Research and practices in water quality. InTech Publisher 3:63–94Google Scholar
  30. Jouili S, Essid N, Semprucci F, Boufahja F, Nasri A, Beyrem H (2017) Environmental quality assessment of El Bibane lagoon (Tunisia) using taxonomical and functional diversity of meiofauna and nematodes. J Mar Biol Assoc UK.  https://doi.org/10.1017/S0025315416000990
  31. Losi V, Montefalcone M, Mariapaola Moreno M, Giovannetti E, Gaozza L, Grondona M, Albertelli G (2012) Nematodes as indicators of environmental quality in seagrass (Posidonia Oceanica) meadows of the NW Mediterranean Sea. Adv Oceanogr Limnol 3:69–91CrossRefGoogle Scholar
  32. Madaki YS, Seng L (2013) Pollution control: how feasible is zero discharge concepts in Malaysia palm oil Mills. Am J Eng Res 02:239–252Google Scholar
  33. Myers N (1990) The biodiversity challenge: expanded hot-spots analysis. Environmentalist 10:243–256CrossRefPubMedGoogle Scholar
  34. Moens T, Somerfield P (2007) Marine vs terrestrial nematodes as bioindicators: different approaches to very similar questions? 1st International Symposium on Nematodes as Environmental Bioindicators. Heriot Watt University, Edinburgh, UK, 11–13 June 2007Google Scholar
  35. Moens T, Braeckman U, Derycke S et al (2013) Ecology of free-living marine nematodes. In: Schmidt-Rhaesa A (ed) Handbook of zoology: Gastrotricha, Cycloneuralia and Gnathifera, vol. 2: Nematoda. De Gruyter, Berlin, pp 109–152Google Scholar
  36. Moreno M, Semprucci F, Vezzulli L, Balsamo M, Fabiano M, Albertelli G (2011) The use of nematodes in assessing ecological quality status in the Mediterranean coastal ecosystems. Ecol Indic 11:328–336CrossRefGoogle Scholar
  37. Nagarajan R, Jonathan MP, Roy PD, Muthusankar G, Lakshumanan C (2015) Decadal evolution of a spit in the Baram river mouth in eastern Malaysia. Cont Shelf Res 105:18–25CrossRefGoogle Scholar
  38. Ndaro SGM, Ólafsson E (1999) Soft-bottom fauna with emphasis on nematode assemblage structure in a tropical intertidal lagoon in Zanzibar, eastern Africa: I. Spatial variability. Hydrobiologia 405:133–148CrossRefGoogle Scholar
  39. Nyanti L, Ling TY, Jongkar G (2012) Fish and crustacean communities and fish length-weight relationship of Lutong River, Miri, Sarawak, Malaysia. World J Fish Mar Sci 4:102–110Google Scholar
  40. Piamthipmanus M (1999) Temporal changes in the abundance of macrobenthos in the South China Sea, Area II: Sarawak, Brunei and Sabah. Proceedings of the second Technical Seminar on Marine Fishery Resources survey in the South China Sea, 323–337Google Scholar
  41. Platt HM, Warwick RM (1983) Free-living marine nematodes, part I. British Enoplids. Cambridge University Press, CambridgeGoogle Scholar
  42. Platt HM, Warwick RM (1988) Free-living marine nematodes, part II. British Chromadorids. Cambridge University Press, CambridgeGoogle Scholar
  43. Primack RB, Hall P (1992) Biodiversity and forest change in Malaysian Borneo. Bioscience 42:829–837CrossRefGoogle Scholar
  44. Sale PF, Agardy T, Ainsworth CH et al (2014) Transforming management of tropical coastal seas to cope with challenges of the 21st century. Mar Pollut Bull 85:8–23CrossRefPubMedGoogle Scholar
  45. Sandulli R, Semprucci F, Balsamo M (2014) Taxonomic and functional biodiversity variations of meiobenthic and nematode assemblages across an extreme environment: a study case in a blue hole cave. Ital J Zool 81:508–516CrossRefGoogle Scholar
  46. Santos J, Gomes R, Vasconcellos R, Silva D, Araújo F (2014) Effects of morphodynamics and across-shore physical gradients on benthic macroinfauna on two sandy beaches in south-eastern Brazil. J Mar Biol Assoc UK 94(4):671–680.  https://doi.org/10.1017/S0025315414000010 CrossRefGoogle Scholar
  47. Saw LG (2010) Vegetation of peninsular Malaysia. In: Kiew R, Chung RCK, Saw LG, Soepadmo E, Boyce PC (Eds) Flora of peninsular Malaysia. Series II: seed plants, Vol. 1, edition: Malayan Forest Records No. 49, Publisher: Forest Research Institute Malaysia, pp 21–300Google Scholar
  48. Semprucci F, Balsamo M (2014) Free-living marine nematodes as bioindicators: past, present and future perspectives. Trends Environ Sci 6(1):17–36Google Scholar
  49. Semprucci F, Balsamo M, Sandulli R (2016) Assessment of the ecological quality (EcoQ) of the Venice lagoon using the structure and biodiversity of the meiofaunal assemblages. Ecol Indic 67C:451–457.  https://doi.org/10.1016/j.ecolind.2016.03.014 CrossRefGoogle Scholar
  50. Semprucci F, Boi P, Manti A, Covazzi Harriague A, Rocchi M, Colantoni P, Papa S, Balsamo M (2010) Benthic communities along a littoral of the central Adriatic Sea (Italy). Helgol Mar Res 64:101–115CrossRefGoogle Scholar
  51. Semprucci F, Balsamo M, Frontalini F (2014a) The nematode assemblage of a coastal lagoon (Lake Varano, southern Italy): ecology and biodiversity patterns. Sci Mar 78:579–588CrossRefGoogle Scholar
  52. Semprucci F, Colantoni P, Sbrocca C, Baldelli G, Balsamo M (2014b) Spatial patterns of distribution of meiofaunal and nematode assemblages in the Huvadhoo lagoon (Maldives, Indian Ocean). J Mar Biol Assoc UK 94:1377–1385CrossRefGoogle Scholar
  53. Semprucci F, Losi V, Moreno M (2015a) A review of Italian research on free-living marine nematodes and the future perspectives in their use as ecological indicators (EcoInd). Mediterr Mar Sci 16:352–365CrossRefGoogle Scholar
  54. Semprucci F, Sbrocca C, Rocchi M, Balsamo M (2015b) Temporal changes of the meiofaunal assemblage as a tool for the assessment of the ecological quality status. J Mar Biol Assoc UK 95:247–254CrossRefGoogle Scholar
  55. Sia SG, Abdullah WH (2012) Enrichment of arsenic, lead, and antimony in Balingian coal from Sarawak, Malaysia: modes of occurrence, origin, and partitioning behaviour during coal combustion. Int J Coal Geol 101:1–15CrossRefGoogle Scholar
  56. Shannon CE, Wiener W (1949) The mathematical theory of communication. University of Illinois, UrbanaGoogle Scholar
  57. Shuttleworth C (1981) Malaysia green and timeless world. Heinemann Asia Pub, Kuala LumpurGoogle Scholar
  58. Soetaert K, Vincx M, Wittoeck J, Tulkens M (1995) Meiobenthic distribution and nematode community structure in five European estuaries. Hydrobiologia 311:185–206CrossRefGoogle Scholar
  59. Somerfield PJ, Clarke KR (1995) Taxonomic levels, in marine community studies, revisited. Mar Ecol Prog Ser 127:113–119CrossRefGoogle Scholar
  60. Somerfield PJ, Warwick RM, Moens T (2005) Meiofauna techniques. In: Eleftheriou A, McIntyre A (eds) Methods for the study of marine benthos, 3rd edn. Blackwell Science Ltd, Oxford, pp 269–272Google Scholar
  61. Soo CL, Chen CA, Mohd Long S (2017) Assessment of near-bottom water quality of southwestern coast of Sarawak, Borneo, Malaysia: a multivariate statistical approach. J Chem 2017:1–12CrossRefGoogle Scholar
  62. Soto LA, Salcedo DL, Arvizu K, Botello AV (2017) Interannual patterns of the large free-living nematode assemblages in the Mexican exclusive economic zone, NW gulf of Mexico after the deepwater horizon oil spill. Ecol Indic 79:371–381CrossRefGoogle Scholar
  63. Steyaert M, Deprez T, Raes M et al (2005) Electronic key to the free-living marine nematodes. http://nemys.ugent.be. Accessed 13 October 2016
  64. Simboura N, Zenetos A (2002) Benthic indicators to use in ecological quality classification of Mediterranean soft bottom marine ecosystems, including a new biotic index. Mediterr Mar Sci 3:77–111CrossRefGoogle Scholar
  65. Tita G, Desrosiers G, Vincx M (2000) New type of hand-held corer for meiofaunal sampling and vertical profile investigation: a comparative study. J Mar Biol Assoc UK 80:171–172CrossRefGoogle Scholar
  66. Van Hoey G, Borja A, Birchenough S, Buhl-Mortensen L, Degraer S, Fleischer D, Kerckhof F, Magni P, Muxika I, Reiss H, Schröder A, Zettler ML 2010. The use of benthic indicators in Europe: from the water framework directive to the marine strategy framework directive. Mar Pollut Bull 60: 2187–2196Google Scholar
  67. Van Steenis CGGJ (1979) Plant-geography of east Malesia. Bot J Linn Soc 79:97–178CrossRefGoogle Scholar
  68. Ürkmez D, Sezgin M, Bat L (2014) Use of nematode maturity index for the determination of ecological quality status: a case study from the Black Sea. J Black Sea/Mediterr Environ 20:96–107Google Scholar
  69. Vanaverbeke J, Merckx B, Degraer S, Vincx M (2011) Sediment-related distribution patterns of nematodes and macrofauna: two sides of the benthic coin? Mar Environ Res 71:31–40CrossRefPubMedGoogle Scholar
  70. Warwick RM, Platt HM, Somerfield PJ (1998). Free-living nematodes (Part III) Monhysterids. In: Barnes RSK, Crothers JH (eds) Synopsis of British fauna, No. 53. Shewsbury, Field Studies Council, 296 ppGoogle Scholar
  71. Whitmore TC (1984) Tropical rain forests of the far east. Second Edition. ELBS/Oxford University Press, OxfordGoogle Scholar
  72. Zeppilli D, Sarrazin J, Leduc D et al (2015) Is the meiofauna a good indicator for climate change and anthropogenic impacts? Mar Biodivers 45:505–535.  https://doi.org/10.1007/s12526-015-0359-z CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Borneo Marine Research InstituteUniversiti Malaysia Sabah, Jalan UMSKota KinabaluMalaysia
  2. 2.Faculty of Resource Science and TechnologyUniversiti Malaysia SarawakKota SamarahanMalaysia
  3. 3.Department of Biomolecular Sciences (DISB)University of UrbinoUrbinoItaly

Personalised recommendations