Marine Biology

, 163:15 | Cite as

Food availability in an anthropogenically impacted habitat determines tolerance to hypoxia in the Asian green mussel Perna viridis

  • Mareike HuhnEmail author
  • Neviaty P. Zamani
  • Karen von Juterzenka
  • Mark Lenz
Original paper


The Asian green mussel Perna viridis is tolerant to environmental stress, but its robustness varies between populations from habitats that differ in quality. So far, it is unclear whether local adaptations through stress-induced selection or phenotypic plasticity are responsible for these inter-population differences. We tested for the relevance of both mechanisms by comparing survival under hypoxia in mussels that were transplanted from an anthropogenically impacted (Jakarta Bay, Indonesia) to a natural habitat (Lada Bay, Indonesia) and vice versa. Mussels were retrieved 8 weeks after transplantation and exposed to hypoxia in the laboratory. Additional hypoxia tests were conducted with juvenile mussels collected directly from both sites. To elucidate possible relationships between habitat quality and mussel tolerance, we monitored concentrations of inorganic nutrients, temperature, dissolved oxygen, salinity, phytoplankton density and the mussels’ body condition index (BCI) for 20 months before, during and after the experiments. Survival under hypoxia depended mainly on the quality of the habitat where the mussels lived before the hypoxia tests and only to a small degree on their site of origin. Furthermore, stress tolerance was only higher in Jakarta than in Lada Bay mussels when the BCIs were substantially higher, which in turn correlated with the phytoplankton densities. We explain why phenotypic plasticity and high BCIs are more likely the causes of population-specific differences in hypoxia tolerance in P. viridis than stress-induced selection for robust genotypes. This is relevant to understanding the role of P. viridis as mariculture organism in eutrophic ecosystems and invasive species in the (sub)tropical world.


Phytoplankton Dinoflagellate Phenotypic Plasticity Phytoplankton Abundance Paralytic Shellfish Poisoning 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Indra Jaya and Azbas Taurusman for providing research facilities at the Marine Habitat Laboratory and the Integrated Laboratory at the faculty of Fisheries and Marine Science, Bogor Agricultural University (FPIK-IPB) and the German Academic Exchange Service (DAAD) for funding this project with a PhD scholarship. We very much acknowledge the help by the mussel farmers from Muara Kamal and Lada Bay.

Compliance with ethical standards

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.


  1. Altieri AH (2006) Inducible variation in hypoxia tolerance across the intertidal–subtidal distribution of the blue mussel Mytilus edulis. Mar Ecol Prog Ser 325:295–300CrossRefGoogle Scholar
  2. Andayani W, Sumartono A (2012) Saxitoxin in green mussels (Perna viridis, Mytiliae), blood cockle (Anadara granosa) and feathers cockle (Anadara antiquata, Arcidae) using high pressure liquid. J Coast Dev 15(3):252–259Google Scholar
  3. Anestis A, Lazou A, Pörtner HO, Michaelidis B (2007) Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. Am J Physiol Regul Integr Comp Physiol 293(2):R911–R921CrossRefGoogle Scholar
  4. APHA (American Public Health Association) (2012) Standard methods for the examination of water and wastewater, 22nd edn. American Public Health Association, American Water Works Association, and Water Environment Federation, Washington, DCGoogle Scholar
  5. Arifin Z (2006) Pollution prevention and reduction strategies and implementation in the Jakarta Bay. Research Centre for Oceanography—LIPI Report, Jakarta, Indonesia, 21 ppGoogle Scholar
  6. Cheung SG (1991) Energetics of transplanted populations of the green-lipped mussel Perna viridis (Linnaeus) (Bivalvia: Mytilidae) in Hong Kong. I: growth, condition and reproduction. Asian Mar Biol 8:117–131Google Scholar
  7. Cheung S (1993) Population dynamics and energy budgets of green-lipped mussel Perna viridis (Linnaeus) in a polluted harbour. J Exp Mar Biol Ecol 168(1):1–24CrossRefGoogle Scholar
  8. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11(12):1304–1315CrossRefGoogle Scholar
  9. Dam HG (2013) Evolutionary adaptation of marine zooplankton to global change. Annu Rev Mar Sci 5:349–370CrossRefGoogle Scholar
  10. Damar A (2003) Effects of enrichment on nutrient dynamics, phytoplankton dynamics and productivity in Indonesian tropical waters: a comparison between Jakarta Bay, Lampung Bay and Semangka Bay. PhD Thesis. Christian-Albrecht-University Kiel, GermanyGoogle Scholar
  11. Decker MB, Reitburg DL, Marcus N (2003) Geographical differences in behavioral responses to hypoxia: Local adaptation to an anthropogenic stressor? Ecol Soc Am 13(4):1104–1109Google Scholar
  12. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321(5891):926–929CrossRefGoogle Scholar
  13. Dsikowitzky L, Heruwati E, Ariyani F, Irianto HE, Schwarzbauer J (2014) Exceptionally high concentrations of the insect repellent N,N-diethyl-m-toluamide (DEET) in surface waters from Jakarta, Indonesia. Environ Chem Lett. doi: 10.1007/s10311-014-0462-6 Google Scholar
  14. Duarte C, Navarro JM, Acuña K et al (2014) Combined effects of temperature and ocean acidification on the juvenile individuals of the mussel Mytilus chilensis. J Sea Res 85:308–314CrossRefGoogle Scholar
  15. Fang JKH, Wu RSS, Chan KY, Yip CKM, Shin PKS (2008) Influences of ammonia–nitrogen and dissolved oxygen on lysosomal integrity in green-lipped mussel Perna viridis: laboratory evaluation and field validation in Victoria Harbour, Hong Kong. Mar Pollut Bull 56(12):2052–2058CrossRefGoogle Scholar
  16. Galimany E, Ramón M, Ibarrola I (2011) Feeding behavior of the mussel Mytilus galloprovincialis (L.) in a Mediterranean estuary: a field study. Aquaculture 314(1–4):236–243CrossRefGoogle Scholar
  17. Hawkins AJS, Smith RFM, Tan SH, Yasin ZB (1998) Suspension-feeding behaviour in tropical bivalve molluscs: Perna viridis, Crassostrea belcheri, Crassostrea iradelei, Saccostrea cucculata and Pinctada margarifera. Mar Ecol Prog Ser 166:173–185CrossRefGoogle Scholar
  18. Hoffmann AA, Hercus MJ (2000) Environmental stress as an evolutionary force. Bioscience 50(3):217–226CrossRefGoogle Scholar
  19. Holmes MJ, Teo SLM, Lee FC, Khoo HW (1999) Persistent low concentrations of diarrhetic shellfish toxins in green mussels Perna viridis from the Johor Strait, Singapore: first record of diarrhetic shellfish toxins from South-East Asia. Mar Ecol Prog Ser 181:257–268CrossRefGoogle Scholar
  20. Jalius (2008) Bioakumulasi logam berat dan pengaruhnya terhadap gametogenesis kerang hiju Perna viridis: Studi kasus di teluk Jakarta, Teluk Banten dan Teluk Lada. PhD Thesis. Bogor Agricultural University, IndonesiaGoogle Scholar
  21. Jalius SDD, Sumantadinata K, Riani E, Ernawati Y (2008) Akumulasi Logam Berat dan Pengaruhnya Terhadap Spermatogenesis Kerang Hijau (Perna viridis). J Ilmu-Ilmu Perair Perikan Indones 15(1):77–83Google Scholar
  22. Jenkins BRJ (1979) Mussel cultivation in the Marlborough sounds (New Zealand). NZ Fishing Industry Board, Wellington, 75 ppGoogle Scholar
  23. Jury M, Golingi T, Foster T (2011) Rapid environmental assessment for coastal development in Jakarta Bay. Report, DHI Water & Environment, Singapore, 53 ppGoogle Scholar
  24. Krishnakumar PK, Asokan PK, Pillai VK (1990) Physiological and cellular responses to copper and mercury in the green mussel Perna viridis (Linnaeus). Aquat Toxicol 18(5):163–173CrossRefGoogle Scholar
  25. Leung PT, Ip JC, Mak SS et al (2014) De novo transcriptome analysis of Perna viridis highlights tissue-specific patterns for environmental studies. BMC Genom 15(1):1–14CrossRefGoogle Scholar
  26. Li SC, Wang WX, Hsieh DPH (2002) Effects of toxic dinoflagellate Alexandrium tamarense on the energy budgets and growth of two marine bivalves. Mar Environ Res 53(2):145–160CrossRefGoogle Scholar
  27. Lockwood BL, Sanders JG, Somero GN (2010) Transcriptomic responses to heat stress in invasive and native blue mussels (genus Mytilus): molecular correlates of invasive success. J Exper Biol 213(Pt 20):3548–3558CrossRefGoogle Scholar
  28. Lucas A, Beninger PG (1985) The use of physiological condition indices in marine bivalve aquaculture. Aquaculture 44:187–200CrossRefGoogle Scholar
  29. Melzner F, Stange P, Trübenbach K et al (2011) Food supply and seawater pCO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS ONE 6(9):e24223CrossRefGoogle Scholar
  30. Mills M (2011) Introducing survival and event history analysis. SAGE Publications Ltd, London, p 279. ISBN 9781848601024Google Scholar
  31. Monari M, Foschi J, Rosmini R, Marin MG, Serrazanetti GP (2011) Heat shock protein 70 response to physical and chemical stress in Chamelea gallina. J Exp Mar Biol Ecol 397(2):71–78CrossRefGoogle Scholar
  32. Nicholson S (1999) Cytological and physiological biomarker responses from green mussels, Perna viridis (L.) transplanted to contaminated sites in Hong Kong coastal waters. Mar Pollut Bull 39(1–12):261–268CrossRefGoogle Scholar
  33. Nicholson S (2003) Cardiac and branchial physiology associated with copper accumulation and detoxication in the mytilid mussel Perna viridis (L.). J Exp Mar Biol Ecol 295(2):157–171CrossRefGoogle Scholar
  34. Ong CC, Yusoff K, Yap CK, Tan SG (2009) Genetic characterization of Perna viridis L. in peninsular Malaysia using microsatellite markers. J Genet 88(2):153–163CrossRefGoogle Scholar
  35. Parsons PA (1994) Habitats, stress, and evolutionary rates. J Evol Biol 7:387–397CrossRefGoogle Scholar
  36. Piacentini L, Fanti L, Specchia V, Bozzetti MP, Berloco M, Palumbo G, Pimpinelli S (2014) Transposons, environmental changes, and heritable induced phenotypic variability. Chromosoma 123(4):345–354CrossRefGoogle Scholar
  37. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  38. Radiarta IN, Albasri H, Sudradjat A (2011) Geographic information system-based modeling and analysis for site selection of green mussel, Perna viridis, mariculture in Lada Bay, Pandeglang, Banten province. Indones Aquac J 6(1):83–90Google Scholar
  39. Rinawati KT, Koike H et al (2012) Distribution, source identification, and historical trends of organic micropollutants in coastal sediment in Jakarta Bay, Indonesia. J Hazard Mater 217–218:208–216CrossRefGoogle Scholar
  40. Siregar V, Koropitan AF (2013) Primary productivity of Jakarta Bay in a changing environment: anthropogenic and climate change impacts. Biotropia 20(2):89–103Google Scholar
  41. Sudharyanto A, Muchtar M, Razak H, Tanabe DS (2005) Kontaminasi organoklorin persisten dalam kerang hijau. Oseanol Limnol Indones 37:1–14Google Scholar
  42. Takarina ND, Adiwibowo A (2011) Impact of heavy metals contamination on the biodiversity of marine benthic organisms in Jakarta Bay. J Coast Dev 14(2):2009–2012Google Scholar
  43. Therneau T (2013) A package for survival analysis in S. R package version 2.37-4.
  44. Thoha H, Adnan Q, Sidabutar T (2007) Note on the occurrence of phytoplankton and its relation with mass mortality in the Jakarta Bay, May and November 2004. Makara, Sains 11(2):63–67Google Scholar
  45. Tomas CR (1997) Identifying marine phytoplankton. Academic Press, San DiegoGoogle Scholar
  46. Vakily JM (1992) Determination and comparison of bivalve growth, with emphasis on Thailand and other tropical areas. ICLARM Technical reports 36, 125 ppGoogle Scholar
  47. Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. PNAS 105(40):15452–15457CrossRefGoogle Scholar
  48. Walsh B, Blows MW (2009) Abundant genetic variation + strong selection = multivariate genetic constraints: a geometric view of adaptation. Annu Rev Ecol Evol Syst 40(1):41–59CrossRefGoogle Scholar
  49. Wang Y, Hu M, Wong WH, Shin PKS, Cheung SG (2011) The combined effects of oxygen availability and salinity on physiological responses and scope for growth in the green-lipped mussel Perna viridis. Mar Pollut Bull 63(5–12):255–261CrossRefGoogle Scholar
  50. Wendling C, Huhn M, Ayu N, Bachtiar R, von Juterzenka K, Lenz M (2013) Habitat degradation correlates with tolerance to climate-change related stressors in the green mussel Perna viridis from West Java, Indonesia. Mar Pollut Bull 71:222–229CrossRefGoogle Scholar
  51. Williams T (2000) Metals and trace organic compounds in sediments and waters of Jakarta Bay and the Pulau Seribu complex, Indonesia. Mar Pollut Bull 40(3):277–285CrossRefGoogle Scholar
  52. Woo S, Denis V, Won H, Shin K, Lee G, Lee TK, Yum S (2013) Expressions of oxidative stress-related genes and antioxidant enzyme activities in Mytilus galloprovincialis (Bivalvia, Mollusca) exposed to hypoxia. Zool Stud 52(1):15CrossRefGoogle Scholar
  53. Wouthuyzen S, Tan CK, Tong JI, Hoang P, Ransi V, Tarigan S, Sediadi A (2008) Monitoring of Algal Blooms and Massive Fish Kill in the Jakarta Bay, Indonesia using satellite imageries. Proceedings of the first PI joint Symposium of ALOS data node for ALOS Science Program in Kyoto, Japan, 19–23 Nov 2007Google Scholar
  54. Yamaji CS (1979) Illustration of the Marine Plankton of Japan. Hoikiska, JapanGoogle Scholar
  55. Yap CK, Tan SG, Ismail A, Omar H (2002) Genetic variation of the green-lipped mussel Perna viridis (L.) (Mytilidae: Mytiloida: Mytilicae) from the West Coast of Peninsular Malaysia. Zool Stud 41(4):376–387Google Scholar
  56. Yaqin K (2010) Potential use of cholinesterase activity from tropical green mussel, Perna viridis as a biomarker in effect-based marine monitoring in Indonesia. Coast Mar Sci 34(1):156–164Google Scholar
  57. Zhang G, Fang X, Guo X et al (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490(7418):49–54CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Marine Science and Technology, Faculty of Fisheries and Marine SciencesBogor Agricultural UniversityBogorIndonesia
  2. 2.GEOMAR Helmholtz Centre for Ocean Research KielKielGermany
  3. 3.Institute for Ecosystem ResearchKiel UniversityKielGermany

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