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Microbial Ecology

, Volume 76, Issue 1, pp 92–101 | Cite as

Influence of Macrofaunal Burrows on Extracellular Enzyme Activity and Microbial Abundance in Subtropical Mangrove Sediment

  • Ling Luo
  • Ji-Dong Gu
Soil Microbiology

Abstract

Bioturbation and bioirrigation induced by burrowing macrofauna are recognized as important processes in aquatic sediment since macrofaunal activities lead to the alteration of sediment characteristics. However, there is a lack of information on how macrofauna influence microbial abundance and extracellular enzyme activity in mangrove sediment. In this study, the environmental parameters, extracellular enzyme activities, and microbial abundance were determined and their relationships were explored. Sediment samples were taken from the surface (S) and lower layer (L) without burrow, as well as crab burrow wall (W) and bottom of crab burrow (B) located at the Mai Po Nature Reserve, Hong Kong. The results showed that the burrowing crabs could enhance the activities of oxidase and hydrolases. The highest activities of phenol oxidase and acid phosphatase were generally observed in B sediment, while the highest activity of N-acetyl-glucosaminidase was found in W sediment. The enzymatic stoichiometry indicated that the crab-affected sediment had similar microbial nitrogen (N) and phosphorous (P) availability relative to carbon (C), lower than S but higher than L sediment. Furthermore, it was found that the highest abundance of both bacteria and fungi was shown in S sediment, and B sediment presented the lowest abundance. Moreover, the concentrations of phosphorus and soluble phenolics in crab-affected sediment were almost higher than the non-affected sediment. The alterations of phenolics, C/P and N/P ratios as well as undetermined environmental factors by the activities of crabs might be the main reasons for the changes of enzyme activity and microbial abundance. Finally, due to the important role of phenol oxidase and hydrolases in sediment organic matter (SOM) decomposition, it is necessary to take macrofaunal activities into consideration when estimating the C budget in mangrove ecosystem in the future.

Keywords

Extracellular enzyme activity Microbial abundance Crab burrow Mangrove sediment 

Notes

Acknowledgments

This research project was supported by a Ph.D. studentship from Graduate School, The University of Hong Kong (LL) and financial support of Environmental Toxicology Education and Research Fund of this laboratory.

Supplementary material

248_2016_844_MOESM1_ESM.docx (96 kb)
ESM 1 (DOCX 95 kb)

References

  1. 1.
    Kristensen E, Kostka J (2005) Macrofaunal burrows and irrigation in marine sediment: microbiological and biogeochemical interactions. Interactions between macro-and microorganisms in marine sediment:125–157Google Scholar
  2. 2.
    Stief P (2007) Enhanced exoenzyme activities in sediment in the presence of deposit-feeding Chironomus riparius larvae. Freshw Biol 52(9):1807–1819CrossRefGoogle Scholar
  3. 3.
    Pischedda L, Militon C, Gilbert F, Cuny P (2011) Characterization of specificity of bacterial community structure within the burrow environment of the marine polychaete Hediste (Nereis) diversicolor. Res Microbiol 162(10):1033–1042CrossRefPubMedGoogle Scholar
  4. 4.
    Laverock B, Smith CJ, Tait K, Osborn AM, Widdicombe S, Gilbert JA (2010) Bioturbating shrimp alter the structure and diversity of bacterial communities in coastal marine sediment. ISME J 4(12):1531–1544CrossRefPubMedGoogle Scholar
  5. 5.
    Gutiérrez JL, Jones CG, Groffman PM, Findlay SE, Iribarne OO, Ribeiro PD, Bruschetti CM (2006) The contribution of crab burrow excavation to carbon availability in surficial salt-marsh sediment. Ecosystems 9(4):647–658CrossRefGoogle Scholar
  6. 6.
    Kristensen E (2008) Mangrove crabs as ecosystem engineers; with emphasis on sediment processes. J Sea Res 59(1):30–43CrossRefGoogle Scholar
  7. 7.
    Chapuis-Lardy L, Le Bayon R-C, Brossard M, López-Hernández D, Blanchart E (2011) Role of soil macrofauna in phosphorus cycling. In: Phosphorus in action. Springer, pp 199–213Google Scholar
  8. 8.
    Wieltschnig C, Fischer UR, Velimirov B, Kirschner AK (2008) Effects of deposit-feeding macrofauna on benthic bacteria, viruses, and protozoa in a silty freshwater sediment. Microb Ecol 56(1):1–12CrossRefPubMedGoogle Scholar
  9. 9.
    Witte U, Wenzhöfer F, Sommer S, Boetius A, Heinz P, Aberle N, Sand M, Cremer A, Abraham W-R, Jørgensen B (2003) In situ experimental evidence of the fate of a phytodetritus pulse at the abyssal sea floor. Nature 424(6950):763–766CrossRefPubMedGoogle Scholar
  10. 10.
    Wang JQ, Zhang XD, Jiang LF, Bertness MD, Fang CM, Chen JK, Hara T, Li B (2010) Bioturbation of burrowing crabs promotes sediment turnover and carbon and nitrogen movements in an estuarine salt marsh. Ecosystems 13(4):586–599CrossRefGoogle Scholar
  11. 11.
    Stief P (2013) Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications. Biogeosciences 10(12):7829–7846CrossRefGoogle Scholar
  12. 12.
    Roskosch A (2011) The influence of macrozoobenthos in lake sediment on hydrodynamic transport processes and biogeochemical impacts. Humboldt-Universität zu Berlin, Mathematisch-Naturwissenschaftliche Fakultät IIGoogle Scholar
  13. 13.
    Heilskov AC, Holmer M (2001) Effects of benthic fauna on organic matter mineralization in fish-farm sediment: importance of size and abundance. ICES J Mar Sci 58(2):427–434CrossRefGoogle Scholar
  14. 14.
    Papageorgiou N, Moreno M, Marin V, Baiardo S, Arvanitidis C, Fabiano M, Eleftheriou A (2007) Interrelationships of bacteria, meiofauna and macrofauna in a Mediterranean sedimentary beach (Maremma Park, NW Italy). Helgol Mar Res 61(1):31–42CrossRefGoogle Scholar
  15. 15.
    Crowther TW, Jones TH, Boddy L, Baldrian P (2011) Invertebrate grazing determines enzyme production by basidiomycete fungi. Soil Biol Biochem 43(10):2060–2068CrossRefGoogle Scholar
  16. 16.
    Sinsabaugh R, Carreiro M, Repert D (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60(1):1–24CrossRefGoogle Scholar
  17. 17.
    Toberman H, Evans CD, Freeman C, Fenner N, White M, Emmett BA, Artz RR (2008) Summer drought effects upon soil and litter extracellular phenol oxidase activity and soluble carbon release in an upland Calluna heathland. Soil Biol Biochem 40(6):1519–1532CrossRefGoogle Scholar
  18. 18.
    Fenner N, Freeman C, Reynolds B (2005) Observations of a seasonally shifting thermal optimum in peatland carbon-cycling processes; implications for the global carbon cycle and soil enzyme methodologies. Soil Biol Biochem 37(10):1814–1821CrossRefGoogle Scholar
  19. 19.
    Freeman C, Ostle N, Kang H (2001) An enzymic‘latch’on a global carbon store. Nature 409(6817):149–149CrossRefPubMedGoogle Scholar
  20. 20.
    Moscatelli M, Lagomarsino A, Garzillo A, Pignataro A, Grego S (2012) β-Glucosidase kinetic parameters as indicators of soil quality under conventional and organic cropping systems applying two analytical approaches. Ecol Indic 13(1):322–327CrossRefGoogle Scholar
  21. 21.
    Moorhead DL, Lashermes G, Sinsabaugh RL (2012) A theoretical model of C- and N-acquiring exoenzyme activities, which balances microbial demands during decomposition. Soil Biol Biochem 53:133–141CrossRefGoogle Scholar
  22. 22.
    Sinsabaugh RL, Shah JJF, Hill BH, Elonen CM (2012) Ecoenzymatic stoichiometry of stream sediment with comparison to terrestrial soils. Biogeochemistry 111(1–3):455–467CrossRefGoogle Scholar
  23. 23.
    Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117(1):101–113CrossRefGoogle Scholar
  24. 24.
    Kristensen E, Bouillon S, Dittmar T, Marchand C (2008) Organic carbon dynamics in mangrove ecosystems: a review. Aquat Bot 89(2):201–219CrossRefGoogle Scholar
  25. 25.
    Qin P, Wong Y, Tam N (2000) Emergy evaluation of Mai Po mangrove marshes. Ecol Eng 16(2):271–280CrossRefGoogle Scholar
  26. 26.
    Luo L, Gu J-D (2015) Seasonal variability of extracellular enzymes involved in carbon mineralization in sediment of a subtropical mangrove wetland. Geomicrobiol J 32(1):68–76CrossRefGoogle Scholar
  27. 27.
    Lee SY (2008) Mangrove macrobenthos: assemblages, services, and linkages. J Sea Res 59(1):16–29CrossRefGoogle Scholar
  28. 28.
    Ashton EC (2002) Mangrove sesarmid crab feeding experiments in Peninsular Malaysia. J Exp Mar Biol Ecol 273(1):97–119CrossRefGoogle Scholar
  29. 29.
    Cao H, Li M, Hong Y, Gu J-D (2011) Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment. Syst Appl Microbiol 34(7):513–523CrossRefPubMedGoogle Scholar
  30. 30.
    Dick RP (2011) Methods of soil enzymology. In: Soil Science Society of America MadisonGoogle Scholar
  31. 31.
    Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4(10):1340–1351CrossRefPubMedGoogle Scholar
  32. 32.
    De Vries FT, Hoffland E, van Eekeren N, Brussaard L, Bloem J (2006) Fungal/bacterial ratios in grasslands with contrasting nitrogen management. Soil Biol Biochem 38(8):2092–2103CrossRefGoogle Scholar
  33. 33.
    Laverock B, Kitidis V, Tait K, Gilbert J, Osborn A, Widdicombe S (2013) Bioturbation determines the response of benthic ammonia-oxidizing microorganisms to ocean acidification. Philos Trans R Soc Lond 368(1627):20120441CrossRefGoogle Scholar
  34. 34.
    Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11(11):1252–1264CrossRefPubMedGoogle Scholar
  35. 35.
    Jégou D, Schrader S, Diestel H, Cluzeau D (2001) Morphological, physical and biochemical characteristics of burrow walls formed by earthworms. Appl Soil Ecol 17(2):165–174CrossRefGoogle Scholar
  36. 36.
    Sardans J, Rivas-Ubach A, Penuelas J (2012) The elemental stoichiometry of aquatic and terrestrial ecosystems and its relationships with organismic lifestyle and ecosystem structure and function: a review and perspectives. Biogeochemistry 111(1–3):1–39CrossRefGoogle Scholar
  37. 37.
    Hill BH, Elonen CM, Jicha TM, Kolka RK, Lehto LL, Sebestyen SD, Seifert-Monson LR (2014) Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry 120(1–3):203–224CrossRefGoogle Scholar
  38. 38.
    Gerbersdorf SU, Jancke T, Westrich B, Paterson DM (2008) Microbial stabilization of riverine sediment by extracellular polymeric substances. Geobiology 6(1):57–69PubMedGoogle Scholar
  39. 39.
    Thongtham N, Kristensen E, Puangprasan S-Y (2008) Leaf removal by sesarmid crabs in Bangrong mangrove forest, Phuket, Thailand; with emphasis on the feeding ecology of Neoepisesarma versicolor. Estuar Coast Shelf Sci 80(4):573–580CrossRefGoogle Scholar
  40. 40.
    Micheli F (1993) Feeding ecology of mangrove crabs in North Eastern Australia: mangrove litter consumption by Sesarma messa and Sesarma smithii. J Exp Mar Biol Ecol 171(2):165–186CrossRefGoogle Scholar
  41. 41.
    Freeman C, Ostle N, Fenner N, Kang H (2004) A regulatory role for phenol oxidase during decomposition in peatlands. Soil Biol Biochem 36(10):1663–1667CrossRefGoogle Scholar
  42. 42.
    Qin S, Hu C, He X, Dong W, Cui J, Wang Y (2010) Soil organic carbon, nutrients and relevant enzyme activities in particle-size fractions under conservational versus traditional agricultural management. Appl Soil Ecol 45(3):152–159CrossRefGoogle Scholar
  43. 43.
    Salazar S, Sánchez L, Alvarez J, Valverde A, Galindo P, Igual J, Peix A, Santa-Regina I (2011) Correlation among soil enzyme activities under different forest system management practices. Ecol Eng 37(8):1123–1131CrossRefGoogle Scholar
  44. 44.
    Šnajdr J, Valášková V, Merhautová V, Herinková J, Cajthaml T, Baldrian P (2008) Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil. Soil Biol Biochem 40(9):2068–2075CrossRefGoogle Scholar
  45. 45.
    Papaspyrou S, Gregersen T, Kristensen E, Christensen B, Cox RP (2006) Microbial reaction rates and bacterial communities in sediment surrounding burrows of two nereidid polychaetes (Nereis diversicolor and N. virens). Mar Biol 148(3):541–550CrossRefGoogle Scholar
  46. 46.
    Reichardt W (1988) Impact of bioturbation by Arenicola marina on microbiological parameters in intertidal sediment. Mar Ecol Prog Ser Oldendorf 44(2):149–158CrossRefGoogle Scholar
  47. 47.
    Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2011) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. In: Soil enzymology. Springer, pp 229–243Google Scholar
  48. 48.
    Böer SI, Hedtkamp SI, Van Beusekom JE, Fuhrman JA, Boetius A, Ramette A (2009) Time-and sediment depth-related variations in bacterial diversity and community structure in subtidal sands. ISME J 3(7):780–791CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.College of Environmental SciencesSichuan Agricultural UniversityChengduPeople’s Republic of China
  2. 2.School of Biological SciencesThe University of Hong KongHong KongPeople’s Republic of China

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