Advertisement

Aboveground carbon stock in a restored neotropical mangrove: influence of management and brachyuran crab assemblage

  • Alexander C. FerreiraEmail author
  • Luis Ernesto Arruda Bezerra
  • Helena Matthews-Cascon
Original Paper

Abstract

Mangrove forests are important sinks of atmospheric carbon, and the internal deposits and fluxes of organic matter can reflect how these ecosystems respond to disturbances and environmental changes. Data on carbon content of mangrove forests vary geographically due to differences in abiotic (climate, geomorphic settings, tides) and biotic (diversity, herbivory, bioturbation) conditions. Mangroves have been degraded worldwide and ecological restoration is an alternative to recover these ecosystems and their functionality. However, although growing and biomass after disturbances have been addressed, studies on the recovery of faunal groups are rare. The brachyuran crab assemblage is strongly integrated to carbon recycling and ecosystem functioning, since propagule consumption and fossorial activity can affect the diversity and biomass of mangroves. We assessed the aboveground biomass and carbon stock of differently managed mangrove areas in northeastern Brazil, after being deforested for shrimp culture and then abandoned, and compared data with other forests worldwide. After a decade, the area restored with Rhizophora mangle showed higher carbon stock than the self-recovered forest and similar amount as an older forest. We discuss the applied rehabilitation measures regarding the effects of management and brachyuran crabs on forest aboveground carbon storage. The effects of herbivory and bioturbation of brachyurans on the low recruitment of Laguncularia racemosa propagules, contributed to higher biomass levels in the restored forest through reinforcing the predominance of R. mangle, which stocks more aboveground carbon with respect to Laguncularia. This suggests that the particularities of target tree species and brachyuran assemblage need to be considered in mangrove restoration, since they are related to function recovering and carbon cycling in the ecosystem.

Keywords

Mangrove restoration Ecosystem functioning Carbon sequestering Biomass stock Brachyuran crabs Ecosystem engineers 

Notes

Acknowledgements

We are grateful to CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior/MEC, Brazil) for providing post-doctoral grant (AC Ferreira). We also thank Carlos E.R.D Alencar for his support with statistical analysis.

Funding

Post-doctoral Grant (AC Ferreira) provided by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior/MEC), Brazil.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11273_2019_9654_MOESM1_ESM.docx (43 kb)
Supplementary material 1 (DOCX 42 kb)

References

  1. Alongi DM (2002) Present state and future of the world’s mangrove forests. Environ Conserv 29:331–349CrossRefGoogle Scholar
  2. Alongi DM (2009) The energetics of mangrove forests. Springer, BerlinGoogle Scholar
  3. Alongi DM (2012) Carbon sequestration in mangrove forests. Carb Manag 3:313–322CrossRefGoogle Scholar
  4. Alongi DM (2014) Carbon cycling and storage in mangrove forests. Annu Rev Mar Sci 6:195–219CrossRefGoogle Scholar
  5. Anderson TW (1958) Introduction to multivariate statistical analysis. Wiley, New YorkGoogle Scholar
  6. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  7. Ashton EC, Hogarth PJ, Macintosh DJ (2003) A comparison of brachyuran crab community structure at four mangrove locations under different management systems along the Melaka Straits-Andaman Sea Coast of Malaysia and Thailand. Estuaries 26:1461–1471CrossRefGoogle Scholar
  8. Barbier EB, Acreman MC, Knowler D (1997) Economic valuation of wetlands: a guide for policy makers and planners. Ramsar Convention Bureau, GlandGoogle Scholar
  9. Bezerra LEA, Dias CB, Santana GX, Matthews-Cascon H (2006) Spatial distribution of fiddler crabs (genus Uca) in a tropical mangrove of northeast Brazil. Sci Mar 70:759–766CrossRefGoogle Scholar
  10. Bhomia RK, Kauffman JB, McFadden TN (2016) Ecosystem carbon stocks of mangrove forests along the Pacific and Caribbean coasts of Honduras. Wetl Ecol Manag 24:187–201CrossRefGoogle Scholar
  11. Bosire JO, Dahdouh-Guebas F, Kairo JG, Cannicci S, Koedam N (2004) Spatial variations in macrobenthic fauna recolonization in a tropical mangrove Bay. Biodivers Conserv 13:1059–1074CrossRefGoogle Scholar
  12. Bosire JO, Kairo JG, Kazungu J, Koedam N, Dahdouh-Guebas F (2005) Predation on propagules regulates regeneration in a high-density reforested mangrove plantation. Mar Ecol Prog Ser 299:149–155CrossRefGoogle Scholar
  13. Branco JO (1993) Aspectos Bioecológicos do caranguejo Ucides cordatus (Linnaeus 1763) (Crustacea, Decapoda) do manguezal do Itacorubi, Santa Catarina, BR. Arq Biol Tecnol 36:133–148Google Scholar
  14. Burggren W, McMahon B (1988) Biology of the land crabs. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  15. Camacho LD, Gevaña DT, Carandang AP, Camacho SC, Combalicer AE, Rebugio LL, Youn Y (2011) Tree biomassand carbon stock of a community-managed mangrove forest in Bohol, Philippines. For Sci Technol 7:161–167Google Scholar
  16. Cannicci S, Burrows B, Fratini S, Smith TJ III, Offenberg J, Dahdouh-Guebas F (2008) Faunal impact on vegetation structure and ecosystem function in mangrove forests: a review. Aquat Bot 89:186–200CrossRefGoogle Scholar
  17. Chapman MG, Tolhurst TJ (2004) The relationship between invertebrate assemblages and bio-dependant properties of sediment in urbanized temperate mangrove forests. J Exp Mar Biol Ecol 304:51–73CrossRefGoogle Scholar
  18. Chen R, Twilley RR (1998) A gap dynamic model of mangrove forest development along gradients of soil salinity and nutrient resources. J Ecol 86:37–51CrossRefGoogle Scholar
  19. Clough BF (1992) Primary productivity and the growth of mangrove forests. In: Robertson AI, Alongi DM (eds) Coastal and estuarine studies: tropical mangrove ecosystems. American Geophysical Society, Washington, DC, pp 225–250CrossRefGoogle Scholar
  20. Clough BF, Tan DT, Buu DC, Phuong DX (1999) Mangrove forest structure and growth. In: Clough BF (ed) Mixed shrimp farming mangrove forestry models in the Mekong Delta, termination report, part B: technical appendices. Australian Centre for International Agricultural Research, Canberra, pp 235–251Google Scholar
  21. Delgado P, Hensel PF, Jiménez JA, Dayd JW (2001) The importance of propagule establishment and physical factors in mangrove distributional patterns in a Costa Rican estuary. Aquat Bot 71:157–178CrossRefGoogle Scholar
  22. DelVecchia AG, Bruno JF, Benninger L, Alperin M, Banerjee O, Morales JD (2014) Organic carbon inventories in natural and restored Ecuadorian mangrove forests. PeerJ 2:e388.  https://doi.org/10.7717/peerj.388 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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
  24. Doornik JA, Hansen H (2008) An omnibus test for univariate and multivariate normality. Oxford B Econ Stat 70:927–939CrossRefGoogle Scholar
  25. Ellison AM (2000) Mangrove restoration: do we know enough? Restor Ecol 8:219–229CrossRefGoogle Scholar
  26. Ellison AM, Farnsworth EJ (1993) Seedling survivorship, growth, and response to disturbance in a Belizean mangal. Am J Bot 80:1137–1145CrossRefGoogle Scholar
  27. Estrada GCD, Soares MLG, Fernandez V, Almeida PMM (2015) The economic evaluation of carbon storage and sequestration as ecosystem services of mangroves: a case study from southeastern Brazil. Int J Biodivers Sci Ecosyst Serv Manag 11:29–35CrossRefGoogle Scholar
  28. Ferreira AC (1998) Composição de Decapoda (Crustacea) dos manguezais do Município de Macau/RN. Dissertation, Universidade Federal do Rio Grande do Norte, BrazilGoogle Scholar
  29. Ferreira AC, Lacerda LD (2016) Degradation and conservation of Brazilian mangroves, status and perspectives. Ocean Coast Manag 125:38–46CrossRefGoogle Scholar
  30. Ferreira AC, Sankarankutty C (2002) Estuarine Carcinofuna (Decapoda) of Rio Grande do Norte, Brazil. Nauplius 2:121–129Google Scholar
  31. Ferreira AC, Pimenta HCD, da Silva LDR, Souza AS (2007) Gestão ambiental de áreas degradadas: um estudo de caso nas nascentes e manguezais do rio Jaguaribe em Natal-RN. In: Trabalhos Técnicos do XXIV Congresso Brasileiro de Engenharia Sanitária e Ambiental. Assoc. Bras. Eng. Sanit. Ambient. (ABES), São Paulo, pp 1–11. http://www.abes-dn.org.br/eventos/abes/24cbes/Posters.pdf
  32. Ferreira AC, Ganade G, Freire FAM, Attayde JL (2013) Propagule predation in a Neotropical mangrove: the role of the Grapsid crab Goniopsis cruentata. Hydrobiologia 707:135–146CrossRefGoogle Scholar
  33. Ferreira AC, Ganade G, Attayde JL (2015) Restoration versus natural regeneration in a neotropical mangrove: effects on plant biomass and crab communities. Ocean Coast Manag 110:38–45CrossRefGoogle Scholar
  34. Field C (ed) (1996) La Restauración de Ecosistemas de Manglar. OIMT/ISME, ManaguaGoogle Scholar
  35. Fonseca SM (2005) O MDL e as florestas de mangue: avaliação preliminar sobre a geração de CERs a partir de atividades de Projeto para recuperação de ecossistemas manguezais. Biom Energy 2:241–250Google Scholar
  36. Fromard F, Puig H, Mougin E, Marty G, Betoulle JL, Cadamuro L (1998) Structure, above-ground biomass and dynamics of mangrove ecosystems: new data from French Guiana. Oecologia 115:39–53CrossRefPubMedGoogle Scholar
  37. Gillis LG, Belshe FE, Ziegler AD, Bouma TJ (2017) Driving forces of organic carbon spatial distribution in the tropical seascape. J Sea Res 120:35–40CrossRefGoogle Scholar
  38. Goes P, Branco JO, Pinheiro MAA, Barbieri E, Costa D, Fernandes LL (2010) Bioecology of the Uçá-crab, Ucides cordatus (Linnaeus, 1763) in Vitória Bay, Espírito Santo State, Brazil. Braz J Ocean 58:153–163CrossRefGoogle Scholar
  39. Gorman D, Turra A (2016) The role of mangrove revegetation as a means of restoring macrofaunal communities along degraded coasts. Sci Total Environ 566–567:223–229CrossRefPubMedGoogle Scholar
  40. Gotelli NJ, Ellison AM (2004) A Primer of Ecological Statistics. Sinauer, SunderlandGoogle Scholar
  41. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica 4:1–9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm. Accessed 21 June 2017
  42. Hong PN (1996) Restauración de ecosistemas de manglar en Vietnam. In: Field C (ed) Restoration of mangrove ecosystems. International Tropical Timber Organization and International Society for Mangrove Ecosystems, Okinawa, pp 81–104Google Scholar
  43. Hummel S, O’Hara KL (2008) Forest management. Encyclopedia of ecology. Elsevier, Amsterdam, pp 1653–1662CrossRefGoogle Scholar
  44. Hutchison J, Manica A, Swetnam R, Balmford A, Spalding M (2014) Predicting global patterns in mangrove forest biomass. Conserv Lett 7:233–240CrossRefGoogle Scholar
  45. Juman RA (2005) Biomass, litterfall and decomposition rates for the fringed Rhizophora mangle forest lining the Bon Accord Lagoon, Tobago. Rev Biol Trop 53:207–217PubMedGoogle Scholar
  46. Kairo JG, Lang’at JKS, Dahdouh-Guebas F, Bosire J, Karachi M (2008) Structural development and productivity of replanted mangrove plantations in Kenya. For Ecol Manag 255:2670–2677CrossRefGoogle Scholar
  47. Kauffman JB, Heider C, Norfolk J, Payton F (2014) Carbon stocks of intact mangroves and carbon emissions arising from their conversion in the Dominican Republic. Ecol Appl 24:518–527CrossRefPubMedGoogle Scholar
  48. Kauffman JB, Trejo HH, Garcia MCJ, Heider C, Contreras WM (2015) Carbon stocks of mangroves and losses arising from their conversion to cattle pastures in the Pantanos de Centla. Mexico. Wetlands Ecol Manage.  https://doi.org/10.1007/s11273-015-9453-z CrossRefGoogle Scholar
  49. Kauffman JB, Bernardino AF, Ferreira TO, Bolton NW, Gomes LEO, Nobrega GN (2018) Shrimp ponds lead to massive loss of soil carbon and greenhouse gas emissions in northeastern Brazilian mangroves. Ecol Evol 00:1–11Google Scholar
  50. Komiyama A, Ong JE, Poungparn S (2008) Allometry, biomass, and productivity of mangrove forests: a review. Aquat Bot 89:128–137CrossRefGoogle Scholar
  51. Koppel J, van der Heide T, Altieri AH, Eriksson BK, Bouma TJ, Olff H, Silliman BR (2015) Long-distance interactions regulate the structure and resilience of coastal ecosystems. Annu Rev Mar Sci 7:139–158.  https://doi.org/10.1146/annurev-marine-010814-015805 CrossRefGoogle Scholar
  52. Krauss KW, McKee KL, Lovelock CE, Cahoon DR, Saintilan N, Reef R, Chen L (2014) How mangrove forests adjust to rising sea level. New Phytol 202:19–34CrossRefPubMedGoogle Scholar
  53. Kristensen E (2008) Mangrove crabs as ecosystem engineers; with emphasis on sediment processes. J Sea Res 59:30–43CrossRefGoogle Scholar
  54. Kristensen E, Alongi DM (2006) Control by fiddler crabs (Uca vocans) and plant roots (Avicennia marina) on carbon, iron, and sulfur biogeochemistry in mangrove sediment. Limnol Oceanogr 51:1557–1571CrossRefGoogle Scholar
  55. Kristensen E, Kostka JE (2005) Macrofaunal burrows and irrigation in marine sediment: microbiological and biogeochemical interactions. In: Kristensen E, Haese RR, Kostka JE (eds) Interactions between macro- and microorganisms in marine sediments. American Geophysical Union, Washington, DC, pp 125–157CrossRefGoogle Scholar
  56. Kristensen E, Bouillon S, Dittmar T, Marchand C (2008) Organic carbon dynamics in mangrove ecosystems: a review. Aquat Bot 89:201–219CrossRefGoogle Scholar
  57. Lacerda LD (ed) (2002) Mangrove ecosystems: function and management. Springer, BerlinGoogle Scholar
  58. Lacerda LD, Marins RV (2002) River damming and changes in mangrove distribution. Glomis/ISME Electr. J. 2:1–4. http//www.glomis.com/ej/pdf/ej03. Accessed 21 June 2017
  59. Lacerda LD, Menezes MOT, Molisani MM (2007) Changes in mangrove extension at the Pacoti River estuary, CE, NE Brazil due to regional environmental changes between 1958 and 2004. Biota Neotr 7:67–72CrossRefGoogle Scholar
  60. Lee SY (1999) Tropical mangrove ecology: physical and biotic factors influencing ecosystem structure and function. Aust J Ecol 24:355–366CrossRefGoogle Scholar
  61. Lewis RR III (2005) Ecological engineering for successful management and restoration of mangrove forests. Ecol Eng 24:403–418CrossRefGoogle Scholar
  62. Lewis RR III (2009) Methods and criteria for successful mangrove forest restoration. In: Perillo GME, Wolanski E, Cahoon DR, Brinson MM (eds) Coastal wetlands: an integrated ecosystem approach, 2nd edn. Elsevier, Amsterdam, pp 787–800Google Scholar
  63. Lewis RR, Brown B (2014) Ecological mangrove rehabilitation-a field manual for practitioners. Version 3. Mangrove Action Project Indonesia, Blue Forests, Canadian International Development Agency, OXFAMGoogle Scholar
  64. Lewis RR, Streever W (2000) Restoration of mangrove habitat. Technical note ERDC TNWRP-VN-RS-32. Ed. US Army Corps of Engineers, Waterways Exp. Station, VicksburgGoogle Scholar
  65. López-Portillo J, Ezcurra E (1989) Response of three mangroves to salinity in two geoforms. Funct Ecol 3:355–361CrossRefGoogle Scholar
  66. Lu W, Yang S, Chen L, Wang W, Du X, Wang C, Ma Y, Lin G, Lin G (2014) Changes in carbon pool and stand structure of a native subtropical mangrove forest after inter-planting with exotic species Sonneratia apetala. PLoS ONE 9:1–8.  https://doi.org/10.1371/journal.pone.0091238 CrossRefGoogle Scholar
  67. Lugo AE (2002) Conserving latin American and Caribbean mangroves: issues and challenges. Mad Bosq 8:5–25CrossRefGoogle Scholar
  68. Macintosh DJ, Ashton EC, Havanon S (2002) Mangrove rehabilitation and intertidal biodiversity: a study in the Ranong mangrove ecosystem, Thailand. Estuar Coast Shelf Sci 55:331–345CrossRefGoogle Scholar
  69. Maia C, Lima MCP, Silva MMT, Paiva RS (2016) Densidade e estrutura populacional do caranguejo-uçá, Ucides cordatus (Linnaeus, 1763) na Reserva Extrativista Marinha de Tracuateua, Pará, Brasil. Biota Amaz 6:86–92CrossRefGoogle Scholar
  70. Manson FJ, Loneragan NR, Skilleter, GA, Phinn SR (2005) An evaluation of the evidence for linkages between mangroves and fisheries: a synthesis of the literature and identification of research directions. In: Gibson RN, Atkinson RJA, Gordon JDM (eds) Oceanography and marine biology: an annual review, pp 485–515Google Scholar
  71. Marengo JA, Alves LM, Alvala RCS, Cunha AP, Brito S, Moraes OLL (2017) Climatic characteristics of the 2010-2016 drought in the semiarid Northeast Brazil region. An Braz Acad Sci.  https://doi.org/10.1590/0001-3765201720170206 CrossRefGoogle Scholar
  72. Matsui N (1998) Estimated stocks of organic carbon in mangrove roots and sediments in Hinchinbrook Channel, Australia. Mangroves Salt Marshes 2:199–204CrossRefGoogle Scholar
  73. Matsui N, Morimune K, Meepol W, Chukwamdee J (2012) Ten year evaluation of carbon stock in mangrove plantation reforested from an abandoned shrimp pond. Forests 3:431–444CrossRefGoogle Scholar
  74. McGuiness KA (1997a) Tests for artifacts in some methods used to study herbivory and predation in mangrove forests. Mar Ecol Prog Ser 153:37–44CrossRefGoogle Scholar
  75. McGuiness KA (1997b) Seed predation in a tropical mangrove forest: a test of the dominance-predation model in northern Australia. J Trop Ecol 13:293–302CrossRefGoogle Scholar
  76. McKee KL (1993) Soil physicochemical patterns and mangrove species distribution—reciprocal effects? J Ecol 81:477–487CrossRefGoogle Scholar
  77. McKee KL (1995a) Mangrove species distribution and propagule predation in Belize: an exception to the dominance-predation hypothesis. Biotropica 27:334–345CrossRefGoogle Scholar
  78. McKee KL (1995b) Interspecific variation in growth, biomass partitioning, and defensive characteristics of neotropical mangrove seedlings: response to light and nutrient availability. Am J Bot 82:299–307CrossRefGoogle Scholar
  79. McLeod E, Salm RV (2006) Managing mangroves for resilience to climate change. World Conservation Union (IUCN), GlandGoogle Scholar
  80. Medeiros TCC, Sampaio EVSB (2008) Allometry of aboveground biomasses in mangrove species in Itamaraca, Pernambuco, Brazil. Wetl Ecol Manag 16:323–330CrossRefGoogle Scholar
  81. Milbrandt EC, Tinsley MN (2006) The role of saltwort (Batis maritima L.) in regeneration of degraded mangrove forests. Hydrobiologia 568:369–377CrossRefGoogle Scholar
  82. Mokhtari M, Ghaffar MA, Usup G, Cob ZC (2016) Effects of fiddler crab burrows on sediment properties in the mangrove mudflats of Sungai Sepang, Malaysia. Biology 5:1–12CrossRefGoogle Scholar
  83. Morrisey DJ, DeWitt TH, Roper DS, Williamson RB (1999) Variation in the depth and morphology of burrows of the mud crab Helice crassa among different types of intertidal sediment in New Zealand. Mar Ecol Prog Ser 182:231–242CrossRefGoogle Scholar
  84. Murdiyarso D, Boone Kauffman J, Warren M, Pramova E, Hergoualc’h (2012) Tropical wetlands for climate change adaptation and mitigation: science and policy imperatives with special reference to Indonesia. Working Paper 91 CIFOR, Bogor, IndonesiaGoogle Scholar
  85. Nam VN, Sasmito SD, Murdiyarso D, Purbopuspito J, MacKenzie RA (2016) Carbon stocks in artificially and naturally regenerated mangrove ecosystems in the Mekong Delta. Wetl Ecol Manag 24:231–244CrossRefGoogle Scholar
  86. Ng PKL, Guinot D, Davie PJF (2008) Systema brachyurorum: part I. An annotated list of extant brachyuran crabs of the world. Raffles Bull Zool 17:1–286Google Scholar
  87. Nordhaus I (2003) Feeding ecology of the semi-terrestrial crab Ucides cordatus cordatus (Decapoda: Brachyura) in a mangrove forest in northern Brazil. Dissertation, University of Bremen, BremenGoogle Scholar
  88. Nordhaus I, Wolff M, Diele K (2006) Litter processing and population food intake of the mangrove crab Ucides cordatus in a high intertidal forest in northern Brazil. Estuar Coast Shelf Sci 67:239–250CrossRefGoogle Scholar
  89. Pereira RT, Teixeira GM, Bertini G, Lima PA, Alencar CERD, Fransozo V (2014) Environmental factors influencing the distribution of three species within the genus Persephona Leach, 1817 (Crustacea, Decapoda, Leucosiidae) in two regions on the northern coast of São Paulo State, Brazil. Latin Am J Aquat Res 42:307–321CrossRefGoogle Scholar
  90. Pickett STA, Cadenasso ML (2005) Vegetation dynamics. In: van der Maarel E (ed) Vegetation ecology. Blackwell Science, Oxford, pp 172–198Google Scholar
  91. Pickett STA, White PS (1985) Natural disturbance and patch dynamics: an introduction. In: Pickett STA, White PS (eds) The ecology of natural disturbance and patch dynamics. Elsevier Academic Press, New York, pp 3–13Google Scholar
  92. Portillo JTM, Londe V, Moreira FWA (2017) Aboveground biomass and carbon stock are related with soil humidity in a mangrove at the Piraquê-Açu River, Southeastern Brazil. J Coast Conserv 21:139–144CrossRefGoogle Scholar
  93. Putz FE, Chan HT (1986) Tree growth, dynamics, and productivity in a mature mangrove forest in Malaysia. For Ecol Manag 17:211–230CrossRefGoogle Scholar
  94. Rabinowitz D (1978) Early growth of mangrove seedlings in Panama and an hypothesis concerning the relationship of dispersal and zonation. J Biogeogr 5:113–133CrossRefGoogle Scholar
  95. Rakocinski CF, Lyczkowski-Shultz J, Richardson SL (1996) Ichthyoplankton assemblage structure in Mississippi sound as revealed by canonical correspondence analysis. Coast Shelf Sci 43:237–257CrossRefGoogle Scholar
  96. Ray R, Ganguly D, Choudhury C, Dey M, Das S, Dutta MK, Mandal SK, Majumdar N, De TK, Mukhopadhyay SK, Jana TK (2011) Carbon sequestration and annual increase of carbon stock in a mangrove forest. Atmos Environ 45:5016–5024CrossRefGoogle Scholar
  97. Rencher AC (2002) Methods of multivariate analysis. Wiley, New York, p 738CrossRefGoogle Scholar
  98. Rivera-Monroy BH, Twilley RR, Medina E, Moser EB, Botero L, Francisco AM, Bullard E (2004) Spatial variability of soil nutrients in disturbed riverine mangrove forests at different stages of regeneration in the San Juan River Estuary, Venezuela. Estuaries 27:44–57CrossRefGoogle Scholar
  99. Robertson AI, Daniel PA (1989) Decomposition and the annual flux of detritus from fallen timber in tropical mangrove forests. Limnol Oceanogr 34:640–646CrossRefGoogle Scholar
  100. Rodrigues DP, Hamacher C, Estrada GCD, Soares MLG (2014) Variability of carbon content in mangrove species: effect of species, compartments and tidal frequency. Aquat Bot 120:346–351CrossRefGoogle Scholar
  101. Ross MS, Ruiz PL, Telesnicki GJ, Meeder JF (2001) Estimating above-ground biomass and production in mangrove communities of Biscayne National Park, Florida (USA). Wetl Ecol Manag 9:27–37CrossRefGoogle Scholar
  102. Rovai AS, Soriano-Sierra EJ, Pagliosa PR, Cintron G, Schaeffer-Novelli Y, Menghini RP, Coelho C Jr, Horta PA, Lewis RR III, Simonai JC, Alves JAA, Boscatto F, Dutra SJ (2012) Secondary succession impairment in restored mangroves. Wetl Ecol Manag 20:447–459CrossRefGoogle Scholar
  103. Salmo SG III, Duke NC (2010) Establishing mollusk colonization and establishing patterns in planted mangrove stands of different ages in Lingayen Gulf, Phillipines. Wetl Ecol Manag 18:745–754CrossRefGoogle Scholar
  104. Schaeffer-Novelli Y, Cintrón G (1986) Guia para estudo de áreas de manguezal; estrutura, função e flora. Caribbean Ecological Research, São PauloGoogle Scholar
  105. SER—Society for Ecological Restoration International Science & Policy Working Group (2004) The SER international primer on ecological restoration. www.ser.org & Tucson: Society for Ecological Restoration International
  106. Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611CrossRefGoogle Scholar
  107. Sherman RE, Fahey TJ, Howarth RW (1998) Soil-plant interactions in a neotropical mangrove forest: iron, phosphorus and sulfur dynamics. Oecologia 115:553–563CrossRefPubMedGoogle Scholar
  108. Sherman RE, Fahey TJ, Battles JJ (2000) Small-scale disturbance and regeneration dynamics in a neotropical mangrove forest. J Ecol 88:165–178CrossRefGoogle Scholar
  109. Shih HT, Ng PKL, Davie PJF, Schubart CD, Türkay M, Naderloo R, Jones D, Liu MY (2016) Systematics of the family Ocypodidae Rafinesque, 1815 (Crustacea: Brachyura), based on phylogenetic relationships, with a reorganization of subfamily rankings and a review of the taxonomic status of Uca Leach, 1814, sensu lato and its subgenera. Raff Bull Zool 64:139–175Google Scholar
  110. Silva CAR, Oliveira SR, Rego RDP, Mozeto AA (2007) Dynamics of phosphorus and nitrogen through litter fall and decomposition in a tropical mangrove forest. Mar Environ Res 64:524–534CrossRefGoogle Scholar
  111. Skov MW, Hartnoll RG (2002) Paradoxical selective feeding on a low-nutrient diet: why do mangrove crabs eat leaves? Oecologia 131:1–7CrossRefPubMedGoogle Scholar
  112. Smith TJ III, Chan HT, McIvor CC, Robblee MB (1989) Comparisons of seed predation in tropical tidal forests from three continents. Ecology 70:146–151CrossRefGoogle Scholar
  113. Smith TJ III, Boto KG, Frusher SD, Giddins RL (1991) Keystone species and mangrove forest dynamics: the influence of burrowing by crabs on soil nutrient status and forest productivity. Estuar Coast Shelf Sci 33:419–432CrossRefGoogle Scholar
  114. Smith NF, Wilcox Ch, Lessmann JM (2009) Fiddler crab burrowing affects growth and production of the white mangrove (Laguncularia racemosa) in a restored Florida coastal marsh. Mar Biol 156:2255–2266CrossRefGoogle Scholar
  115. Soares MLG (1999) Estrutura vegetal e grau de perturbação dos manguezais da Lagoa da Tijuca, Rio de Janeiro, RJ, Brasil. Rev Bras Biol 59:503–515CrossRefGoogle Scholar
  116. Soares MLG, Schaeffer-Novelli Y (2005) Above ground biomass of mangrove species. I. Analysis of models. Estuar Coast Shelf Sci 65:1–18CrossRefGoogle Scholar
  117. Sousa WP, Mitchell BJ (1999) The effect of seed predators on plant distributions: is there a general pattern in mangroves? Oikos 86:55–66CrossRefGoogle Scholar
  118. Terrados J, Thampanya U, Srichai N, Kheowvongsri P, Geertz-Hansen O, Boromthanarath S, Panapitukkul N, Duarte CM (1997) The effect of increased sediment accretion on the survival and growth of Rhizophora apiculata seedlings. Estuar Coast Shelf Sci 45:697–701CrossRefGoogle Scholar
  119. Thampanya U, Vermaat JE, Terrados J (2002) The effect of increasing sediment accretion on the seedlings of three common Thai mangrove species. Aquat Bot 74:315–325CrossRefGoogle Scholar
  120. Thant YM, Kanzaki M, Ohta S, Than MM (2012) Carbon sequestration by mangrove plantations and a natural regeneration stand in the Ayeyarwady Delta, Myanmar. Tropics 21:1–10CrossRefGoogle Scholar
  121. Twilley RR (2008) Mangrove wetlands. In: Encyclopedia of ecology. Elsevier, Amsterdam, pp 2198–2209Google Scholar
  122. Valiela I, Bowen JL, York JK (2001) Mangrove forests: one of the World’s Threatened major tropical environments. Bioscience 51:807–815CrossRefGoogle Scholar
  123. Van Nedervelde F, Cannicci S, Koedam N, Bosire J, Dahdouh-Guebas F (2015) What regulates crab predation on mangrove propagules? Acta Oecol 63:63–70CrossRefGoogle Scholar
  124. Warner GF (1969) The occurrence and distribution of crabs in a Jamaican mangrove swamp. J Anim Ecol 38:379–389CrossRefGoogle Scholar
  125. Warren JH, Underwood AJ (1986) Effect of burrowing crabs on the topography of mangrove swamps in New South Wales. J Exp Mar Biol Ecol 102:223–235CrossRefGoogle Scholar
  126. Zar JH (2010) Biostatistical analysis, 5th edn. Pearson Prentice-Hall, Upper Saddle River, p 944Google Scholar
  127. Zhang D, Stanturf J (2008) Forest plantations. Encyclopedia of ecology. Elsevier, Amsterdam, pp 1673–1680CrossRefGoogle Scholar
  128. Zimmer M (2018) Ecosystem design: when mangrove ecology meets human needs. In: Makowski C, Finkl CW (eds) Threats to mangrove forests: hazards, vulnerability, and management. Springer, Berlin, pp 367–376CrossRefGoogle Scholar
  129. Zuur AF, Leno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14.  https://doi.org/10.1111/j.2041-210X.2009.00001.x CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Alexander C. Ferreira
    • 1
    • 3
    Email author
  • Luis Ernesto Arruda Bezerra
    • 1
  • Helena Matthews-Cascon
    • 2
  1. 1.Instituto de Ciências do Mar (LABOMAR)Universidade Federal do CearáFortalezaBrazil
  2. 2.Laboratório de Invertebrados Marinhos (LIMCE), Departamento de BiologiaUniversidade Federal do CearáFortalezaBrazil
  3. 3.Laboratorio de ZoobentosInstituto de Ciências do Mar (LABOMAR), Universidade Federal do CearáFortalezaBrazil

Personalised recommendations