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Wetland plant species improve performance when inoculated with arbuscular mycorrhizal fungi: a meta-analysis of experimental pot studies

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Abstract

The presence of arbuscular mycorrhizal fungi (AMF) in wetlands is widespread. Wetlands are transition ecosystems between aquatic and terrestrial systems, where shallow water stands or moves over the land surface. The presence of AMF in wetlands suggests that they are ecologically significant; however, their function is not yet clearly understood. With the aim of determining the overall magnitude and direction of AMF effect on wetland plants associated with them in pot assays, we conducted a meta-analysis of data extracted from 48 published studies. The AMF effect on their wetland hosts was estimated through different plant attributes reported in the studies including nutrient acquisition, photosynthetic activity, biomass production, and saline stress reduction. As the common metric, we calculated the standardized unbiased mean difference (Hedges’ d) of wetland plant performance attributes in AMF-inoculated plants versus non-AMF-inoculated plants. Also, we examined a series of moderator variables regarding symbiont identity and experimental procedures that could influence the magnitude and direction of an AMF effect. Response patterns indicate that wetland plants significantly benefit from their association with AMF, even under flooded conditions. The beneficial AMF effect differed in magnitude depending on the plant attribute selected to estimate it in the published studies. The nature of these benefits depends on the identity of the host plant, phosphorus addition, and water availability in the soil where both symbionts develop. Our meta-analysis synthetizes the relationship of AMF with wetland plants in pot assays and suggests that AMF may be of comparable importance to wetland plants as to terrestrial plants.

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References

  • Abbott LK, Gazey C (1994) An ecological view of the formation of VA mycorrhizas. Plant Soil 159:69–78

    Google Scholar 

  • Abdelhalim TS et al (2013) Species composition and diversity of arbuscular mycorrhizal fungi in White Nile state, Central Sudan. Arch Agron Soil Sci. https://doi.org/10.1080/03650340.2013.793453

    Google Scholar 

  • Aggarwal A et al (2012) Arbuscular mycorrhizal symbiosis and alleviation of salinity stress. J Appl Nat Sci 4(1):144–155

    CAS  Google Scholar 

  • Allen MF (1996) The ecology of arbuscular mycorrhizas: a look back into the 20th century and a peek into the 21st. Mycol Res 100(7):769–782

    Google Scholar 

  • An GH, Miyakawa S, Kawahara A, Osaki M, Ezawa T (2008) Community structure of arbuscular mycorrhizal fungi associated with pioneer grass species Miscanthus sinensis in acid sulfate soils: habitat segregation along pH gradients. Soil Sci Plant Nutr 54(4):517–528

    Google Scholar 

  • Anderson RC, Liberta AE, Dickman LA (1984) Interaction of vascular plants and vesicular-arbuscular mycorrhizal fungi across a soil moisture-nutrient gradient. Oecologia 64:111–117

    CAS  PubMed  Google Scholar 

  • Armstrong W, Justin SHFW, Beckett PM, Lythe S (1991) Root adaptation to soil waterlogging. Aquat Bot 39:57–73

    Google Scholar 

  • Asghari H. R. (2004) Effects of arbuscular-mycorrhizal fungal colonization on management of saline lands. PhD Thesis. School of Earth and Environmental Sciences, The University of Adelaide South Australia. 198 pp.

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Google Scholar 

  • Begg CB (1994) Publication bias. In: Cooper H, Hedges LV (eds) The handbook of research synthesis. Russell Sage Foundation, New York, NY, pp 399–409

    Google Scholar 

  • Bohrer KE, Frese CF, Amon JP (2004) Seasonal dynamics of arbuscular mycorrhizal fungi in differing wetland habitats. Mycorrhiza 14:329–337

    PubMed  Google Scholar 

  • Borenstein M et al (2009) Introduction to meta-analysis. John Wiley & Sons Ltd., West Sussex, UK

    Google Scholar 

  • Brown AM, Bledsoe C (1996) Spatial and temporal dynamics of mycorrhizas in Jaumea Carnosa, a tidal saltmarsh halophyte. J Ecol 84(5):703–715

    Google Scholar 

  • Brundrett M (1991) Mycorrhizas in natural ecosystems. In: Begon M, Fitter AH, Macfadyen A (eds.) Advances in ecological research Vol 21, pp 171–313

    Google Scholar 

  • Brune A, Frenzel P, Cypionka H (2000) Life at the oxic-anoxic interface: microbial activities and adaptations. FEMS Microbiol Rev 24:691–710

    CAS  PubMed  Google Scholar 

  • Caravaca F et al (2004) Effect of mycorrhizal inoculation on nutrient acquisition, gas exchange, and nitrate reductase activity of two Mediterranean-autochthonous shrub species under drought stress. J Plant Nutr 27(1):57–74

    CAS  Google Scholar 

  • Carvalho LM, Caçador I, Martins-Loução MA (2001) Temporal and spatial variation of arbuscular mycorrhizas in salt marsh plants of the Tagus estuary (Portugal). Mycorrhiza 11:303–309

    CAS  PubMed  Google Scholar 

  • Carvalho LM et al (2003) Effects of salinity and flooding on the infectivity of salt marsh arbuscular mycorrhizal fungi in Aster tripolium L. Biol Fertil Soils 38:137–143

    Google Scholar 

  • Chandrasekaran M et al (2014) A meta-analysis of arbuscular mycorrhizal effects on plants grown under salt stress. Mycorrhiza 24:611–625

    CAS  PubMed  Google Scholar 

  • Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23(7):867–902

    CAS  Google Scholar 

  • Cornwell WK, Bedford BL, Chapin CT (2001) Occurrence of arbuscular mycorrhizal Fungi in a phosphorus-poor wetland and mycorrhizal response to phosphorus fertilization. Am J Bot 88(10):1824–1829

    CAS  PubMed  Google Scholar 

  • Cowardin LM et al. (1979). Classification of wetlands and deep-water habitats of the United States. USFWS / OBS-79/31

  • Cuenca G (2015) Las micorrizas arbusculares: aspectos teóricos y aplicados. Ediciones IVIC, Instituto Venezolano de Investigaciones Científicas (IVIC)

  • D’Souza J (2016) Arbuscular mycorrhizal diversity from mangroves: a review. In: Pagano MC (ed) Recent advances on mycorrhizal fungi. Springer International Publishing, Switzerland, pp 109–116

    Google Scholar 

  • de Andrade SAL, Domingues AP Jr, Mazzafera P (2015) Photosynthesis is induced in rice plants that associate with arbuscular mycorrhizal fungi and are grown under arsenate and arsenite stress. Chemosphere 134:141–149

    PubMed  Google Scholar 

  • de Battista J (2005) Neotyphodium research and application: current trends in South America. In: Roberts C, West CP, Spiers D (eds) Neotyphodium in cool-season grasses. Blackwell Scientific, Oxford, UK, pp 65–71

  • Dhillion SS (1992) Host-endophyte specificity of vesicular-arbuscular mycorrhizal colonization of Oryza sativa L. at the pre-transplant stage in low or high phosphorus soil. Soil Biol Biochemist 24(5):405–411

    Google Scholar 

  • Driver CH II (1950) A morphological study of the mycorrhizae on certain southern hardwood tree species of the Georgia Pidemont. M.S. thesis. University of Georgia Athens

  • Dunham RM, Ray AM, Inouye RS (2003) Growth, physiology, and chemistry of mycorrhizal and nonmycorrhizal Typha latifolia seedlings. Wetlands 23(4):890–896

    Google Scholar 

  • Evans DE (2003) Aerenchyma formation. New Phytol 161:35–49

    Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104(7):1263–1280

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feller I, Sitnik M (1996) Mangrove ecology: a manual for a field course. In: A field manual focused on the biocomplexity on mangrove ecosystems. Smithsonian Institution, Washington

    Google Scholar 

  • Fraccaro de Marins J, Carrenho R, Thomaz SM (2009) Occurrence and coexistence of arbuscular mycorrhizal fungi and dark septate fungi in aquatic macrophytes in a tropical river–floodplain system. Aquat Bot 91:13–19

    Google Scholar 

  • Gupta N, Bihari KM, Sengupta I (2016) Diversity of arbuscular mycorrhizal fungi in different salinity of mangrove ecosystem of Odisha. India Adv Plants Agric Res 3(1):00085

    Google Scholar 

  • Gurevitch J, Hedges LV (2001) Meta-analysis: combining the results of independent experiments. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 2nd edn. Oxford University Press, New York, NY, pp 378–398

    Google Scholar 

  • Hajiboland R, Dashtebani F, Aliasgharzad N (2015) Physiological responses of halophytic C4 grass Aeluropus littoralis to salinity and arbuscular mycorrhizal fungi colonization. Photosynthetica 53(4):572–584

    CAS  Google Scholar 

  • Hammer EC et al (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21:117–129

    CAS  PubMed  Google Scholar 

  • Harner MJ et al (2011) Arbuscular mycorrhizal fungi on developing islands within a dynamic river floodplain: an investigation across successional gradients and soil depth. Aquat Sci 73:35–42

    CAS  Google Scholar 

  • Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (phylum Glomeromycota). J Exp Bot 60(9):2465–2480. https://doi.org/10.1093/jxb/erp144

    Article  CAS  PubMed  Google Scholar 

  • Hetrick BAD (1991) Mycorrhizas and root architecture. Experientia 47:355–362

    Google Scholar 

  • Hogarth PJ (2010) The biology of mangrove and seagrasses. Oxford University Press, Oxford

    Google Scholar 

  • Horton TR, van der Heijden MGA (2012) The role of symbioses in seedling establishment and survival. In: Leck MA, Parker VT (eds) Seedling ecology and evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Ipsilantis I, Sylvia DM (2007) Interactions of assemblages of mycorrhizal fungi with two Florida wetland plants. Appl Soil Ecol 35:261–271

    Google Scholar 

  • Jackson MB, Armstrong W (1999) Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biol 1:274–287

    CAS  Google Scholar 

  • Janos D (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91

    PubMed  Google Scholar 

  • Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789

    CAS  PubMed  Google Scholar 

  • Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647

    CAS  PubMed  Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585

    Google Scholar 

  • Johnson NC et al (2006) From Lilliput to Brobdingnag: extending models of mycorrhizal function across scales. BioScience 56(11):889–900

    Google Scholar 

  • Johnson NC et al (2015) Mycorrhizal phenotypes and the law of the minimum. New Phytol 205:1473–1484

    CAS  PubMed  Google Scholar 

  • Johnson-Green PC, Kenkel NC, Booth T (1995) The distribution and phenology of arbuscular mycorrhizae along an inland salinity gradient. Can J Bot 73(9):1318–1327

    Google Scholar 

  • Jun DJ, Allen E (1991) Physiological responses of 6 wheatgrass cultivars to mycorrhizae. J Range Manag 44(4):336–341

    Google Scholar 

  • Juniper S, Abbott L (1993) Review vesicular-arbuscular mycorrhizas and soil salinity. Mycorrhiza 4:45–57

    Google Scholar 

  • Juniper S, Abbott L (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16:371–379

    CAS  PubMed  Google Scholar 

  • Karagiannidis N, Nikolaou N, Ipsilantis I, Zioziou E (2007) Effects of different N fertilizers on the activity of Glomus mosseae and on grapevine nutrition and berry composition. Mycorrhiza 18:43–50

    CAS  PubMed  Google Scholar 

  • Kent DM (2001) Applied wetlands science and technology 2nd ed. CRC Press LLC, Boca Raton

    Google Scholar 

  • Khan AH (1988) Mycorrhizal status of some Bangladesh soils and the effect of indigenous VA-mycorrhizal fungi on the growth of rice plants. Bangladesh J Bot 17(1):49–56

    Google Scholar 

  • Khan A (2004) Mycotrophy and its significance in wetland ecology and wetland. In: Wong MH. Wetlands ecosystems in Asia, pp 95–114

    Google Scholar 

  • Kim CK, Weber DJ (1985) Distribution of VA mycorrhiza on halophytes on inland salt playas. Plant Soil 83:207–214

    CAS  Google Scholar 

  • Koide RT (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol 147:233–235

    Google Scholar 

  • Koricheva J, Gurevitch J, Mengerson K (2013) Handbook of meta-analysis in ecology and evolution. Princeton University Press, Princeton

    Google Scholar 

  • Krishna KR (2005) Mycorrhizas: a molecular analysis. Science Publishers, Inc, New York

    Google Scholar 

  • Kumar T, Ghose M (2008) Status of arbuscular mycorrhizal fungi (AMF) in the Sundarbans of India in relation to tidal inundation and chemical properties of soil. Wetl Ecol Manag 16:471–483

    Google Scholar 

  • Lai W et al (2012) Radial oxygen loss, photosynthesis, and nutrient removal of 35 wetland plants. Ecol Eng 39:24–30

    Google Scholar 

  • Lambert DH, Baker HC (1980) Adaptation of vesicular-arbuscular mycorrhizae to edaphic factors. New Phytol 85:513–520

    Google Scholar 

  • Le Tacon F et al (1983) Spore germination and hyphal growth of a vesicular-arbuscular mycorrhizal fungus, Glomus mosseae (Gerdemann and Trappe), under decreased oxygen and increased carbon dioxide concentrations. Can J Microbiol 29:1280–1285

    Google Scholar 

  • Lichvar RW, Melvin NC, Butterwick ML, Kirchner N (2012) National wetland plant list indicator rating definitions. https://www.fws.gov/wetlands/documents/national-wetland-plant-list-indicator-rating-definitions.pdf. Accessed 15 November 2017

  • Lingua G et al (2015) Effect of arbuscular mycorrhizal and bacterial inoculant on nitrate concentration in mesocosms simulating a wastewater treatment system relying on phytodepuration. Environ Sci Pollut Res 22:18616–18625

    CAS  Google Scholar 

  • Liu ZL et al (2013) Differences in the arbuscular mycorrhizal fungi-improved rice resistance to low temperature at two N levels: aspects of N and C metabolism on the plant side. Plant Physiol Biochem 71:87–95

    CAS  PubMed  Google Scholar 

  • Liu Z et al (2014) Different respiration metabolism between mycorrhizal and non-mycorrhizal rice under low-temperature stress: a cry for help from the host. J Agric Sci. https://doi.org/10.1017/S0021859614000434

    Google Scholar 

  • Lugo A, Snedaker S (1974) The ecology of mangroves. Annu Rev Ecol Syst 5:39–64

    Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • Miller S (2000) Arbuscular mycorrhizal colonization of semi-aquatic grasses along a wide hydrologic gradient. New Phytol 145:145–155

    Google Scholar 

  • Miller SP, Sharitz RR (2000) Manipulation of flooding and arbuscular mycorrhiza formation influences growth and nutrition of two semiaquatic grass species. Funct Ecol 14:738–748

    Google Scholar 

  • Moore P (2006) Biomes of the Earth wetlands. Chelsea House, Hong Kong

    Google Scholar 

  • Moreno-Casasola PE, Peresbarbosa R, Travieso-Bello AC (2006) Estrategias para el manejo costero integral: el enfoque municipal. Instituto de Ecología, A.C., CONANP y Gobierno del Estado de Veracruz-Llave, México

  • Mosse B (1981) Vesicular-arbuscular mycorrhiza research for tropical agriculture. Hawaii Institute of Tropical Agriculture and Human Resources, College of Tropical Agriculture and Human Resources, University of Hawaii

  • Muthukumar T, Udaiyan K, Shanmughavel P (2004) Mycorrhiza in sedges—an overview. Mycorrhiza 14:65–77

    CAS  PubMed  Google Scholar 

  • Nielsen KB et al (2004) Colonisation and molecular diversity of arbuscular mycorrhizal fungi in the aquatic plants Littorella uniflora and Lobelia dortmanna in southern Sweden. Mycol Res 108(6):616–625

    CAS  PubMed  Google Scholar 

  • Odum WE, McIvor CC, Smith TJ III (1985) The ecology of the mangroves of south Florida: a community profile. U.S. Fish and WiId1ife Service, Office of Biological Services, Washington, D.C.

    Google Scholar 

  • Öpik M, Moora M, Liira M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790

    Google Scholar 

  • Parida AK, Jha B (2010) Salt tolerance mechanisms in mangroves: a review. Trees 24:199–217

    Google Scholar 

  • Pedersen CT, Sylvia DM (1996) Mycorrhiza: ecological implications of plant interactions. In: Mukerji KG (ed) Concepts in mycorrhizal research. Kluwer Academic Publishers, Dordrecht, pp 195–222

    Google Scholar 

  • Pennings SC, Grant MB, Bertness MD (2005) Plant zonation in low-latitude salt marshes: disentangling the roles of flooding, salinity and competition. J Ecol 93:159–167

    Google Scholar 

  • Porcel R et al (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200

    CAS  Google Scholar 

  • Pringle A, Bever JD (2002) Divergent phenologies may facilitate the coexistence of arbuscular mycorrhizal fungi in a North Carolina grassland. Am J Bot 89:1439–1446

    PubMed  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Core Team, Vienna

  • Radhika KP, Rodrigues BF (2007) Arbuscular mycorrhizae in association with aquatic and marshy plant species in Goa. India Aquatic Botany 86:291–294

    Google Scholar 

  • Ray AM, Inouye RS (2006) Effects of water-level fluctuations on the arbuscular mycorrhizal colonization of Typha latifolia L. Aquat Bot 84:210–216

    Google Scholar 

  • Read D (2002) The ecophysiology of mycorrhizal symbioses with special reference to impacts upon plant fitness. In: Scholes MC, Barker MG (eds) Physiological plant ecology: the 39th symposium of the British ecological society. Blackwell Science, Oxford, pp 133–152

    Google Scholar 

  • Reddell P, Yun Y, Shipton W (1997) Cluster roots and mycorrhizae in Casuarina cunninghamiana: their occurrence and formation in relation to phosphorus supply. Aust J Bot 45(1):41–51

    Google Scholar 

  • Reddy R, DeLaune RD (2008) Biogeochemistry of wetlands: science and applications. Taylor & Francis Group, United States of America

    Google Scholar 

  • Rejmánková E (2005) Nutrient resorption in wetland macrophytes: comparison across several regions of different nutrient status. New Phytol 167:471–482

    PubMed  Google Scholar 

  • Reuss-Schmidt K et al (2015) Effects of sex and mycorrhizal fungi on gas exchange in the dioecious salt marsh grass Distichlis spicata. Int J Plant Sci 176(2):141–149

    Google Scholar 

  • Rossetti M et al (2017) Responses of insect herbivores and herbivory to habitat fragmentation: a hierarchical meta-analysis. Ecol Lett 20:264–272

    PubMed  Google Scholar 

  • Rothstein HR, Sutton AJ, Borenstein M (2005) Publication bias in meta-analysis. John Wiley & Sons, Chichester, UK

    Google Scholar 

  • Rúa MA et al (2016) Home-field advantage? Evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16:122. https://doi.org/10.1186/s12862-016-0698-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarkar A, Asaeda T, Wang Q, Rashid MH (2016) Arbuscular mycorrhizal association for growth and nutrients assimilation of Pharagmites japonica and Polygonum cuspidatum plants growing on river bank soil. Commun Soil Sci Plant Anal 47(1):87–100

    CAS  Google Scholar 

  • Seerangan K, Thangavelu M (2014) Arbuscular mycorrhizal and dark septate endophyte fungal associations in south Indian aquatic and wetland macrophytes. J Bot 2014. https://doi.org/10.1155/2014/173125

    Google Scholar 

  • Shi S et al (2005) Molecular phylogenetic analysis of mangroves: independent evolutionary origins of vivipary and salt secretion. Mol Phylogenet Evol 34:159–166

    CAS  PubMed  Google Scholar 

  • Sinclair G et al (2014) Influence of colonization by arbuscular mycorrhizal fungi on three strawberry cultivars under salty conditions. Agric Food Sci 23:146–158

    Google Scholar 

  • Small E (1972) Photosynthetic rates in relation to nitrogen recycling as an adaptation to nutrient deficiency in peat bog plants. Can J Bot 50:2227–2233

    CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Elsevier Ltd., New York

    Google Scholar 

  • Solaiman MZ, Hirata H (1996) Effectiveness of arbuscular mycorrhizal colonization at nursery-stage on growth and nutrition in wetland rice (Oryza sativa L.) after transplanting under different soil fertility and water regimes. Soil Sci Plant Nutr 42(3):561–571

    Google Scholar 

  • Solaiman ZM et al (2014) Mycorrhizal fungi: use in sustainable agriculture and land restoration. Springer-Verlag, Berlin Heidelberg

    Google Scholar 

  • Soti PG et al (2014) Mycorrhizal symbiosis and Lygodium microphyllum invasion in South Florida—a biogeographic comparison. Symbiosis 62:81–90

    Google Scholar 

  • Spatafora JW et al (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108(5):1028–1046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Šraj-Kržič N et al (2006) Mycorrhizal colonization in plants from intermittent aquatic habitats. Aquat Bot 85:331–336

    Google Scholar 

  • Stenlund DL, Charvat ID (1994) Vesicular arbuscular mycorrhizae in floating wetland mat communities dominated by Typha. Mycorrhiza 4:131–137

    Google Scholar 

  • Stepniewski W, Glinski J (1988) Gas exchange and atmospheric properties of flooded soils. In: Hook D et al (eds) The ecology and management of wetlands. Springer, United States of America, pp 269–278

    Google Scholar 

  • Stevens KJ, Wellner MR, Acevedo MF (2010) Dark septate endophyte and arbuscular mycorrhizal status of vegetation colonizing a bottomland hardwood forest after a 100-year flood. Aquat Bot 92:105–111

    Google Scholar 

  • Stevens KJ, Wall CB, Janssen JA (2011) Effects of arbuscular mycorrhizal fungi on seedling growth and development of two wetland plants, Bidens frondosa L., and Eclipta prostrata (L.) L., grown under three levels of water availability. Mycorrhiza 21:279–288

    PubMed  Google Scholar 

  • Streitwolf-Engel R, Boller R, Wiemken A, Sanders IR (1997) Clonal growth traits of two Prunella species are determined by co-occurring arbuscular mycorrhizal fungi from a calcareous grassland. J Ecol 85(2):181–191

    Google Scholar 

  • Tawaraya K et al (2003) Arbuscular mycorrhizal colonization of tree species grown in peat swamp forests of Central Kalimantan, Indonesia. Forest Ecol Manag 182:381–386

    Google Scholar 

  • Tiner RW (1991) The concept of a hydrophyte for wetland identification. BioScience 41(4):236–247

    Google Scholar 

  • Tomlinson PB (1986) The botany of mangroves. Cambridge University Press, London

    Google Scholar 

  • Torti SD, Coley PD, Janos DP (1997) Vesicular-arbuscular mycorrhizae in two tropical monodominant trees. J Trop Ecol 13:623–629

    Google Scholar 

  • Tsang A, Maun MA (1999) Mycorrhizal fungi increase salt tolerance of Strophostyles helvola in coastal foredunes. Plant Ecol 144:159–166

    Google Scholar 

  • Tuck SL et al (2014) Land-use intensity and the effects of organic farming on biodiversity: a hierarchical meta-analysis. J Appl Ecol 51:746–755

    PubMed  PubMed Central  Google Scholar 

  • Turner SD, Amon JP, Schneble RM, Friese CF (2000) Mycorrhizal fungi associated with plants in ground-water fed wetlands. Wetlands 20(1):200–204

    Google Scholar 

  • Van Breemen N, Buurman P (2003) Soil formation. Kluwer Academic Publishers, United States of America

    Google Scholar 

  • Van der Heijden MGA et al (1998a) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79(6):2082–2091

    Google Scholar 

  • Van der Heijden MGA et al (1998b) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396(5):69–72

    Google Scholar 

  • Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:1–48

    Google Scholar 

  • Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16(5):299–362

    CAS  PubMed  Google Scholar 

  • Wang FY et al (2004) Arbuscular mycorrhizal status of wild plants in saline-alkaline soils of the Yellow River Delta. Mycorrhiza 14:133–137

    PubMed  Google Scholar 

  • Wang Y et al (2010) Arbuscular mycorrhizal fungi in two mangroves in South China. Plant Soil 331:181–191

    CAS  Google Scholar 

  • Wang Y et al (2011) Flooding greatly affects the diversity of arbuscular mycorrhizal fungi communities in the roots of wetland plants. PLoS One 6(9):e24512. https://doi.org/10.1371/journal.pone.0024512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L et al (2015) Response of arbuscular mycorrhizal fungi to hydrologic gradients in the rhizosphere of Phragmites australis (Cav.) Trin ex. Steudel growing in the Sun Island wetland. BioMed Res Int 2005:9. https://doi.org/10.1155/2015/810124

    Article  Google Scholar 

  • Weinbaum BS, Allen MF, Allen EB (1996) Survival of arbuscular mycorrhizal fungi following reciprocal transplanting across the Great Basin, USA. Ecol Appl 6(4):1365–1372

    Google Scholar 

  • Weishampel PA (2005) Distribution and function of arbuscular mycorrhizal fungi in calcareous fen plant communities. PhD dissertation. Cornell University, Ithaca, New York

  • Wolfe BE, Weishampel PA, Klironomos JH (2006) Arbuscular mycorrhizal fungi and water table affect wetland plant community composition. J Ecol 94:905–914

    Google Scholar 

  • Wu J et al (2008) Natural products from true mangrove flora: chemistry and bioactivities. Nat Prod Rep 25:955–981

    CAS  PubMed  Google Scholar 

  • Xie X et al (2014) Effects of arbuscular mycorrhizal inoculation and phosphorus supply on the growth and nutrient uptake of Kandelia obovata (Sheue, Liu &Yong) seedlings in autoclaved soil. Appl Soil Ecol 75:162–171

    Google Scholar 

  • Xu Z et al (2016) Arbuscular mycorrhizal fungi in wetland habitats and their application in constructed wetland: a review. Pedosphere 26(5):592–617

    Google Scholar 

  • Zhang Q et al (2014) Arbuscular mycorrhizal fungal mediation of plant-plant interactions in a marshland plant community. Sci World J. https://doi.org/10.1155/2014/923610

    Google Scholar 

Download references

Funding

To Posgrado en Ciencias Biológicas of the Universidad Nacional Autónoma de México and to Consejo Nacional de Ciencia y Tecnología.

R.A. is a researcher of CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas) supported by grants PIP 2015-0371 and PICT 2016-0764.

To the projects:

Enseñanza de las metodologías para establecer las bases ecológicas de la restauración y conservación de humedales costeros PAPIME-DGAPA (Programa de Apoyo a Proyectos para la Innovación y Mejoramiento de la enseñanza), PE204012.

Diversidad vegetal y fúngica del sistema lagunar de la Carbonera, Reserva Estatal de Ciénagas y Manglares de la costa norte de Yucatán CONABIO (Comisión Nacional para el Conocimiento y uso de la Biodiversidad), JF078.

Bases metodológicas para la restauración ecológica de ecosistemas costeros: de las dunas a los humedales PAPIME-DGAPA (Programa de Apoyo a Proyectos para la Innovación y Mejoramiento de la enseñanza), PE207216.

Consideraciones bio-ecológicas para establecer zonas prioritarias para la conservación de la biodiversidad costera de Yucatán PAPIIT-DGAPA (Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica), IN219515

Diversidad funcional y diversidad taxonómica de la comunidad de peces que habita en el sistema de humedales de la costa norte de Yucatán PAPIIT-DGAPA (Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica), IN220318

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Authors and Affiliations

  1. Universidad Nacional Autónoma de México, Facultad de Ciencias, Av. Universidad 3000, Circuito Exterior S/N Delegación Coyoacán, Ciudad Universitaria, 04510, Mexico City, Mexico

    Thai Khan Ramírez-Viga & Silvia Castillo-Argüero

  2. Instituto Multidisciplinario de Biología Vegetal, Universidad Nacional de Córdoba CONICET, CC 495, 5000, Córdoba, Argentina

    Ramiro Aguilar

  3. Laboratorio Nacional de Análisis y Síntesis Ecológica (LANASE), Universidad Nacional Autónoma de México, 58190, Morelia, Mexico

    Ramiro Aguilar

  4. Universidad Nacional Autónoma de México, Escuela Nacional de Estudios Superiores Mérida, Ave. Colón 503-F, 97000, Mérida, Yucatán, Mexico

    Xavier Chiappa-Carrara

  5. Unidad Multidisciplinaria de Docencia e Investigación Sisal, Facultad de Ciencias, Universidad Nacional Autónoma de México, Puerto de Abrigo s/n, 97356, Sisal, Yucatán, Mexico

    Patricia Guadarrama

  6. Departamento de Ecología Tropical, Universidad Autónoma de Yucatán, Carretera Mérida-Xmatkuil Km 15.5, 97100, Mérida, Yucatán, Mexico

    José Ramos-Zapata

Authors
  1. Thai Khan Ramírez-Viga
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  2. Ramiro Aguilar
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  3. Silvia Castillo-Argüero
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  4. Xavier Chiappa-Carrara
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  5. Patricia Guadarrama
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  6. José Ramos-Zapata
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Corresponding author

Correspondence to Xavier Chiappa-Carrara.

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Ramírez-Viga, T.K., Aguilar, R., Castillo-Argüero, S. et al. Wetland plant species improve performance when inoculated with arbuscular mycorrhizal fungi: a meta-analysis of experimental pot studies. Mycorrhiza 28, 477–493 (2018). https://doi.org/10.1007/s00572-018-0839-7

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  • DOI: https://doi.org/10.1007/s00572-018-0839-7

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