, Volume 172, Issue 1, pp 271–278 | Cite as

Species mixing boosts root yield in mangrove trees

  • Joseph K. Sigi Lang’atEmail author
  • Bernard K. Y. Kirui
  • Martin W. Skov
  • James G. Kairo
  • Maurizio Mencuccini
  • Mark Huxham
Ecosystem ecology - Original research


Enhanced species richness can stimulate the productivity of plant communities; however, its effect on the belowground production of forests has scarcely been tested, despite the role of tree roots in carbon storage and ecosystem processes. Therefore, we tested for the effects of tree species richness on mangrove root biomass: thirty-two 6 m by 6 m plots were planted with zero (control), one, two or three species treatments of six-month-old Avicennia marina (A), Bruguiera gymnorrhiza (B) and Ceriops tagal (C). A monoculture of each species and the four possible combinations of the three species were used, with four replicate plots per treatment. Above- and belowground biomass was measured after three and four years’ growth. In both years, the all-species mix (ABC) had significant overyielding of roots, suggesting complementarity mediated by differences in rhizosphere use amongst species. In year four, there was higher belowground than aboveground biomass in all but one treatment. Belowground biomass was strongly influenced by the presence of the most vigorously growing species, A. marina. These results demonstrate the potential for complementarity between fast- and slow-growing species to enhance belowground growth in mangrove forests, with implications for forest productivity and the potential for belowground carbon sequestration.


Root biomass Overyielding Mangrove forests Species richness Ecosystem function 



The study was supported by the Earthwatch Institute, the Leverhulme and Rufford Trusts, and by a grant from Aviva Ltd to JKSL. Our gratitude goes to Laitani Suleiman and the Earthwatch volunteers who assisted in the fieldwork. Thanks to Beth Middleton and Ken Krauss (both of USGS), and two anonymous reviewers for their comments on this paper.


  1. Aarssen LW (1997) High productivity in grassland ecosystems: affected by species diversity or productive species? Oikos 80:183–184CrossRefGoogle Scholar
  2. Alongi DM (2009) The energetics of mangrove forests. Springer, DordrechtGoogle Scholar
  3. Alongi DM, Sasekumar A, Chong VC, Pfitzner J, Trott LA, Tirendi F, Dixon P, Brunskill GJ (2004) Sediment accumulation and organic material flux in a managed mangrove ecosystem: estimates of land–ocean–atmosphere exchange in peninsular Malaysia. Mar Geol 208:383–402CrossRefGoogle Scholar
  4. Alongi DM, Pfitzner J, Trott LA, Tirendi F, Dixon P, Klumpp DW (2005) Rapid sediment accumulation and microbial mineralization in forests of the mangrove Kandelia candel in the Jiulongjiang Estuary, China. Estuar Coast Shelf Sci 63:605–618CrossRefGoogle Scholar
  5. Bosire JO, Dahdouh-Guebas F, Kairo JG, Koedam N (2003) Colonization of non-planted mangrove species into restored mangrove stands in Gazi Bay, Kenya. Aquat Bot 76:267–279CrossRefGoogle Scholar
  6. Bouillon S, Borges AV, Castaneda-Moya E, Diele K, Dittmar T, Duke NC, Kristensen E, Lee SY, Marchand C, Middelburg JJ, Rivera-Monroy VH, Smith TJ III, Twilley RR (2008) Mangrove production and carbon sinks: a revision of global budget estimates. Glob Biogeochem Cycl 22:1–12CrossRefGoogle Scholar
  7. Brassard BW, Chen HYH, Bergeron Y, Paré D (2011) Differences in fine root productivity between mixed- and single-species stands. Funct Ecol 25:238–346CrossRefGoogle Scholar
  8. Briggs SV (1977) Estimates of biomass in a temperate mangrove community. Austral Ecol 2:369–373CrossRefGoogle Scholar
  9. Cahoon DR, Hensel P, Rybczyk J, McKee KL, Proffitt CE, Perez BC (2003) Mass tree mortality leads to mangrove peat collapse at Bay Islands, Honduras after Hurricane Mitch. J Ecol 91:1093–1105Google Scholar
  10. Cairns MA, Brown S, Helmer EH, Baumgardner GA (1997) Root biomass allocation in the world’s upland forests. Oecologia 111:1–11CrossRefGoogle Scholar
  11. Cardinale BJ, Ives AR, Inchausti P (2004) Effects of species diversity on the primary productivity of ecosystems: extending our spatial and temporal scales of inference. Oikos 104:437–450CrossRefGoogle Scholar
  12. Cavard X, Bergeron Y, Chen HYH, Paré D (2010) Mixed-species effect on tree aboveground carbon pools in the east-central boreal forests. Can J For Res 40:37–47CrossRefGoogle Scholar
  13. Chmura GL, Anisfeld SC, Cahoon DR, Lynch JC (2003) Global carbon sequestration in tidal, saline wetland soils. Glob Biogeochem Cycle 11:1111–1120Google Scholar
  14. Dahdouh-Guebas F, Van Pottelbergh I, Kairo JG, Cannicci S, Koedam N (2004) Human-impacted mangroves in Gazi (Kenya): predicting future vegetation based on retrospective remote sensing, social surveys, and distribution of trees. Mar Ecol Prog Ser 272:77–92CrossRefGoogle Scholar
  15. Dittmar T, Hertkorn N, Kattner G, Lara RJ (2006) Mangroves, a major source of dissolved organic carbon to the oceans. Glob Biogeochem Cycle 20:GB1012. doi: 1010.1029/2005GB002570 CrossRefGoogle Scholar
  16. Donato DC, Kauffman JB, Murdiyarso D, Kurnianto S, Stidham M, Kanninen M (2011) Mangroves among the most carbon-rich forests in the tropics. Nat Geosci 4:293–297CrossRefGoogle Scholar
  17. Erskine PD, Lamb D, Bristow M (2006) Tree species diversity and ecosystem function: can tropical multi-species plantations generate greater productivity? For Ecol Manag 233:205–210CrossRefGoogle Scholar
  18. Ewel KC, Twilley R, Ong JE (1998) Different kinds of mangrove forest provides different goods and services. Glob Ecol Biogeogr Lett 7:83–94CrossRefGoogle Scholar
  19. Fargione J, Tilman D, Dybzinski R, Lambers JHR, Clark C, Harpole WS, Knops JMH, Reich PB, Loreau M (2007) From selection to complementarity: shifts in the causes of biodiversity–productivity relationships in a long-term biodiversity experiment. Proc R Soc B 274:871–876PubMedCrossRefGoogle Scholar
  20. Fox JW (2005) Interpreting the “selection effect” of biodiversity on ecosystem function. Ecol Lett 8:846–856Google Scholar
  21. Fujimoto K, Imaya A, Tabuchi R, Kuramoto S, Utsugi H, Murofushi T (1999) Belowground carbon storage of Micronesian mangrove forests. Ecol Res 14:409–413CrossRefGoogle Scholar
  22. Gilman EL, Ellison J, Duke NC, Field C (2008) Threats to mangroves from climate change and adaptation options: a review. Aquat Bot 89:237–250CrossRefGoogle Scholar
  23. Giri C, Ochieng E, Tieszen LL, Zhu Z, Singh A, Loveland T, Masek J, Duke N (2011) Status and distribution of mangrove forests of the world using Earth Observation Satellite data. Glob Ecol Biogeogr 20:154–159Google Scholar
  24. Gleason SM, Ewel KC (2002) Organic matter dynamics on the forest floor of a Micronesian mangrove forest: an investigation of species composition shifts. Biotropica 34:190–198Google Scholar
  25. Golley F, Odum HT, Wilson RF (1962) The structure and metabolism of a Puerto Rican Red Mangrove forest in May. Ecology 43:9–19CrossRefGoogle Scholar
  26. Hector A, Bazeley-White E, Loreau M, Otway S, Schmid B (2002) Over yielding in grassland communities: testing the sampling effect hypothesis with replicated biodiversity experiments. Ecol Lett 5:502–511CrossRefGoogle Scholar
  27. Hogarth PJ (1999) The biology of mangroves. Oxford University Press, New YorkGoogle Scholar
  28. Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460CrossRefGoogle Scholar
  29. Huxham M, Langat J, Tamooh F, Kennedy H, Mencuccini M, Skov MW, Kairo J (2010) Decomposition of mangrove roots: effects of location, nutrients, species identity and mix in a Kenyan forest. Estuar Coast Shelf Sci 88:135–142CrossRefGoogle Scholar
  30. Jennerjahn TC, Ittekkot V (2002) Relevance of mangroves for the production and deposition of organic matter along tropical continental margins. Naturwissenschaften 89:23–30PubMedCrossRefGoogle Scholar
  31. Jose S, Williams R, Zamora D (2006) Belowground ecological interactions in mixed-species forest plantations. For Ecol Manag 233:231–239CrossRefGoogle Scholar
  32. Kairo JG, Dahdouh-Guebas F, Bosire J, Koedam N (2001) Restoration and management of mangrove systems—a lesson for and from the East African region. S Afr J Bot 67:383–389Google Scholar
  33. Kairo JG, Lang’at JKS, Dahdouh-Guebas F, Bosire JO, Karachi M (2008) Structural development and productivity of replanted mangrove plantations in Kenya. For Ecol Manag 255:2670–2677CrossRefGoogle Scholar
  34. Kirui BYK, Huxham M, Kairo J, Skov M (2008) Influence of species richness and environmental context on early survival of replanted mangroves at Gazi bay, Kenya. Hydrobiologia 603:171–181CrossRefGoogle Scholar
  35. Komiyama A, Ongino K, Aksornkoae S, Sabhasri S (1987) Root biomass of a forest in Southern Thailand. 1. Estimation by trench method and zonal structure of root biomass. J Trop Ecol 3:97–108CrossRefGoogle Scholar
  36. Komiyama A, Havanond S, Srisawatt W, Mochida Y, Fujimoto K, Ohnishi T, Ishihara S, Miyagi T (2000) Top/root biomass ratio of a secondary mangrove (Ceriops tagal (Perr.) C. B. Rob.) forest. For Ecol Manag 139:127–134CrossRefGoogle Scholar
  37. Kumara MP, Jayatissa LP, Krauss KW, Phillips DH, Huxham M (2010) High mangrove density enhances surface accretion, surface elevation change, and tree survival in coastal areas susceptible to sea-level rise. Oecologia 164:545–553PubMedCrossRefGoogle Scholar
  38. Loreau M (1998) Separating sampling and other effects in biodiversity experiments. Oikos 82:600–602CrossRefGoogle Scholar
  39. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76PubMedCrossRefGoogle Scholar
  40. Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808PubMedCrossRefGoogle Scholar
  41. McKee KL, Faulkner PL (2000) Restoration of biogeochemical function in mangrove forests. Restor Ecol 8:247–259CrossRefGoogle Scholar
  42. McKee KL, Cahoon DR, Feller I (2007) Caribbean mangroves adjust to rising sea level through biotic controls on change in soil elevation. Glob Ecol Biogeogr 16:545–556CrossRefGoogle Scholar
  43. McLeod E, Chmura GL, Bouillon S, Salm R, Björk M, Duarte CM, Lovelock CE, Schlesinger WH, Silliman BR (2011) A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front Ecol Environ 9:552–560CrossRefGoogle Scholar
  44. Medina E, Francisco M (1997) Osmolality and d13C of leaf tissues of mangrove species from environments of contrasting rainfall and salinity. Estuar Coast Shelf Sci 45:337–344CrossRefGoogle Scholar
  45. Meinen C, Hertel D, Leuschner C (2009a) Root growth and recovery in temperate broad-leaved forest stands differing in tree species diversity. Ecosystems 12:1103–1116CrossRefGoogle Scholar
  46. Meinen C, Leuschner C, Ryan N, Hertel D (2009b) No evidence of spatial root system segregation and elevated fine root biomass in multi-species temperate broad-leaved forests. Trees Struct Funct 23:941–950CrossRefGoogle Scholar
  47. Middleton BA, McKee KL (2001) Degradation of mangrove tissues and implications for peat formation in Belizean island forests. J Ecol 89:818–828CrossRefGoogle Scholar
  48. Paquette A, Messier C (2011) The effect of biodiversity on tree productivity: from temperate to boreal forests. Glob Ecol Biogeogr 20:170–180CrossRefGoogle Scholar
  49. Pretzsch H, Schütze G (2009) Transgressive over yielding in mixed compared with pure stands of Norway spruce and European beech in Central Europe: evidence on stand level and explanation on individual tree level. Eur J For Res 128:183–204CrossRefGoogle Scholar
  50. Ruiz-Jaen MC, Potvin C (2010) Tree diversity explains variation in ecosystem function in a neotropical forest in Panama. Biotropica 42:638–646CrossRefGoogle Scholar
  51. Saintilan N (1997a) Above- and below-ground biomass of mangroves in a sub-tropical estuary. Mar Freshw Res 48:601–604CrossRefGoogle Scholar
  52. Saintilan N (1997b) Above- and below-ground biomasses of two species of mangrove on the Hawkesbury River estuary, New South Wales. Mar Freshw Res 48:147–152CrossRefGoogle Scholar
  53. Schmid B, Hector A, Saha P, Loreau M (2008) Biodiversity effects and transgressive over yielding. J Plant Ecol 1:95–102CrossRefGoogle Scholar
  54. Spalding M, Kainuma M, Collins L (eds) (2010) World atlas of mangroves. Earthscan, LondonGoogle Scholar
  55. Tack JF, Polk P (1999) The influence of tropical catchments upon coastal zone: modelling the links between groundwater and mangrove losses in Kenya, India and Florida. In: Harper D, Brown T (eds) Sustainable management in tropical catchments. Wiley, London, pp 359–372Google Scholar
  56. Tamooh F, Huxham M, Karachi M, Mencuccini M, Kairo JG, Kirui B (2008) Below-ground root yield and distribution in natural and replanted mangrove forests at Gazi bay, Kenya. For Ecol Manag 256:1290–1297CrossRefGoogle Scholar
  57. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845PubMedCrossRefGoogle Scholar
  58. Tilman D, Knops J, Wedin D, Reich P (2002) Plant diversity and composition: effects on productivity and nutrient dynamics of experimental grasslands. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning, synthesis and perspectives. Oxford University Press, Oxford, pp 21–35Google Scholar
  59. Tomlinson CB (1986) The botany of mangroves. Cambridge University Press, CambridgeGoogle Scholar
  60. Twilley RR, Chen RH, Hargis T (1992) Carbon sinks in mangroves and their implications to carbon budget of tropical coastal ecosystems. Water Air Soil Poll 64:265–288CrossRefGoogle Scholar
  61. Valiela I, Bowen JL, York JK (2001) Mangrove forests: one of the world’s threatened major tropical environments. Bioscience 51:807–815CrossRefGoogle Scholar
  62. Vila M, Vayreda J, Comas L, Ibanez JJ, Mata T, Obón B (2007) Species richness and wood production: a positive association in Mediterranean forests. Ecol Lett 10:241–250PubMedCrossRefGoogle Scholar
  63. Wang XL, Klinka K, Chen HYH, Montigny LD (2002) Root structure of western hemlock and western redcedar in single- and mixed-species stands. Can J For Res 32:997–1004CrossRefGoogle Scholar
  64. Wardle DA (1999) Is “sampling effect” a problem for experiments investigating biodiversity–ecosystem function relationships? Oikos 87:403–407Google Scholar
  65. Yuan ZY, Chen HYH (2010) Fine root biomass, production, turnover rates, and nutrient contents in boreal forest ecosystems in relation to species, climate, fertility, and stand age: literature review and meta-analyses. Crit Rev Plant Sci 29:204–221CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Joseph K. Sigi Lang’at
    • 1
    • 2
    Email author
  • Bernard K. Y. Kirui
    • 1
  • Martin W. Skov
    • 3
  • James G. Kairo
    • 1
  • Maurizio Mencuccini
    • 4
    • 5
  • Mark Huxham
    • 2
  1. 1.Mangrove Reforestation ProgrammeKenya Marine and Fisheries Research InstituteMombasaKenya
  2. 2.School of Life, Sport and Social SciencesEdinburgh Napier UniversityEdinburghUK
  3. 3.School of Ocean SciencesBangor UniversityAngleseyUK
  4. 4.School of GeosciencesUniversity of EdinburghEdinburghUK
  5. 5.ICREACREAFBarcelonaSpain

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