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Arbuscular mycorrhizal fungal communities in tropical rain forest are resilient to slash-and-burn agriculture

Published online by Cambridge University Press:  08 June 2018

David García de León Open the ORCID record for David García de León [Opens in a new window] ,
Lena Neuenkamp ,
Mari Moora ,
Maarja Öpik ,
John Davison ,
Clara Patricia Peña-Venegas ,
Martti Vasar ,
Teele Jairus  and
Martin Zobel
David García de León*
Affiliation:
Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia
Lena Neuenkamp
Affiliation:
Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia
Mari Moora
Affiliation:
Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia
Maarja Öpik
Affiliation:
Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia
John Davison
Affiliation:
Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia
Clara Patricia Peña-Venegas
Affiliation:
Instituto Amazónico de Investigaciones Científicas Sinchi, Calle 20, 5–44, Bogotá, Colombia
Martti Vasar
Affiliation:
Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia
Teele Jairus
Affiliation:
Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia
Martin Zobel
Affiliation:
Institute of Ecology and Earth Sciences, University of Tartu, Lai 40, 51005 Tartu, Estonia
*
*Corresponding author. Email: [email protected]
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Abstract:

Certain forestry and agricultural practices are known to affect arbuscular mycorrhizal (AM) fungal communities, but the effects of deforestation – including slash-and-burn management and other more severe disturbances – in tropical rain forests are poorly understood. We addressed the effects of anthropogenic disturbance on rain-forest AM fungal communities in French Guiana, by comparing mature tropical rain forest, slash-and-burn (5 y old) and clearcut areas (8 y old). A total of 36 soil samples were collected in six plots and sequenced using a high throughput 454-pyrosequencing platform. A total of 32649 sequences from 103 AM fungal virtual taxa (VT) were recorded. Whereas alpha diversity of AM fungi did not decrease due to land-use intensification, with average richness ranging from 17 to 21 taxa per plot, beta diversity (average distance to multivariate centroid) dropped by 28% from 0.46 in rain forest to 0.33 under clearcutting. AM fungal community composition was correlated with land use and soil chemical properties. Clearcut areas were characterized by the more frequent occurrence of specialist AM fungi, compared with mature forest or slash-and-burn areas. Specifically, clearcuts contained the highest proportions of VT that were geographic (21%), habitat (31%), abundance (97%) or host (97%) specialists based on VT metadata contained in the MaarjAM database. This suggests that certain AM fungi with narrow ecological niches have traits that allow them to exploit conditions of severe disturbance. In conclusion, slash-and-burn management appears to allow diverse AM fungal communities to persist, and may favour regeneration of tropical rain forest after abandonment. More severe disturbance in the form of clearcutting resulted in marked changes in AM fungal communities.

Keywords

AM fungal diversityclearcuttingfunctional traitsslash-and-burntropical rain forest
Type
Research Article
Information
Journal of Tropical Ecology , Volume 34 , Issue 3 , May 2018 , pp. 186 - 199
Copyright
Copyright © Cambridge University Press 2018 

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References

LITERATURE CITED

AMELUNG, T. & DIEHL, M. 1992. Deforestation of tropical rainforest – economic causes and impact on development. Kieler Studien 241. Mohr, Tubingen. 157 pp.Google Scholar
ARIAS, R. M., HEREDIA-ABARCA, G., SOSA, V. J. & FUENTES-RAMÍREZ, L. E. 2012. Diversity and abundance of arbuscular mycorrhizal fungi spores under different coffee production systems and in a tropical montane cloud forest patch in Veracruz, Mexico. Agroforestry Systems 85:179–193.Google Scholar
BÉREAU, M. & GARBAYE, J. 1994. First observations on the root morphology and symbioses of 21 major tree species in the primary tropical rain forest of French Guyana. Annals of Forest Science 51:407–416.Google Scholar
BOUFFAUD, M.-L., CREAMER, R. E., STONE, D., PLASSART, P., VAN TUINEN, D., LEMANCEAU, P., WIPF, D. & REDECKER, D. 2016. Indicator species and co-occurrence in communities of arbuscular mycorrhizal fungi at the European scale. Soil Biology and Biochemistry 103:464–470.CrossRefGoogle Scholar
CARRILLO-SAUCEDO, S. M., GAVITO, M. E. & SIDDIQUE, I. 2018. Arbuscular mycorrhizal fungal spore communities of a tropical dry forest ecosystem show resilience to land-use change. Fungal Ecology 32:29–39.Google Scholar
CARUSO, T., HEMPEL, S., POWELL, J. R., BARTO, E. K. & RILLIG, M. C. 2012. Compositional divergence and convergence in arbuscular mycorrhizal fungal communities. Ecology 93:1115–1124.CrossRefGoogle ScholarPubMed
CHAVE, J., RIERA, B. & DUBOIS, M. A. 2001. Estimation of biomass in a neotropical forest of French Guiana: spatial and temporal variability. Journal of Tropical Ecology 17:79–96.Google Scholar
CLAVEL, J., JULLIARD, R. & DEVICTOR, V. 2011. Worldwide decline of specialist species: toward a global functional homogenization? Frontiers in Ecology and the Environment 9:222–228.Google Scholar
CUENCA, G., CACERES, A. & GONZALEZ, M. G. 2008. AM inoculation in tropical agriculture: field results. Pp. 403–417 in Varma, A. (ed.). Mycorrhiza: genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics. Springer-Verlag, Berlin.Google Scholar
DAVISON, J., ÖPIK, M., ZOBEL, M., VASAR, M., METSIS, M. & MOORA, M. 2012. Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS ONE 7:e41938.CrossRefGoogle Scholar
DAVISON, J., MOORA, M., ÖPIK, M., ADHOLEYA, A., AINSAAR, L., BÂ, A., BURLA, S., DIEDHIOU, A. G., HIIESALU, I., JAIRUS, T., JOHNSON, N. C., KANE, A., KOOREM, K., KOCHAR, M., NDIAYE, C., PÄRTEL, M., REIER, Ü., SAKS, Ü., SINGH, R., VASAR, M. & ZOBEL, M. 2015. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973.Google Scholar
DE ROUW, A. 1995. The fallow period as a weed-break in shifting cultivation (tropical wet forests). Agriculture, Ecosystems and Environment 54:31–43.Google Scholar
DUFRÊNE, M. & LEGENDRE, P. 1997. Species assemblages and indicator species: the need for a flexible assymmetrical approach. Ecological Monographs 67:345–366.Google Scholar
FONSECA, M. B., DIAS, T., CAROLINO, M. M., FRANÇA, M. G. C. & CRUZ, C. 2017. Belowground microbes mitigate plant-plant competition. Plant Science 262:175–181.Google Scholar
FUTUYMA, D. & MORENO, G. 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19:207–233.Google Scholar
GAMPER, H. A., YOUNG, J. P. W., JONES, D. L. & HODGE, A. 2008. Real-time PCR and microscopy: are the two methods measuring the same unit of arbuscular mycorrhizal fungal abundance? Fungal Genetics and Biology 45:581–596.Google Scholar
GARCÍA DE LEÓN, D., MOORA, M., ÖPIK, M., JAIRUS, T., NEUENKAMP, L., VASAR, M., BUENO, C. G., GERZ, M., DAVISON, J. & ZOBEL, M. 2016a. Dispersal of arbuscular mycorrhizal fungi and plants during succession. Acta Oecologica 77:128–135.Google Scholar
GARCÍA DE LEÓN, D., MOORA, M., ÖPIK, M., NEUENKAMP, L., GERZ, M., JAIRUS, T., VASAR, M., BUENO, C. G., DAVISON, J. & ZOBEL, M. 2016b. Symbiont dynamics during ecosystem succession: co-occurring plant and arbuscular mycorrhizal fungal communities. FEMS Microbiology Ecology 92: fiw097.Google Scholar
GARCÍA DE LEÓN, D., CANTERO, J. J., MOORA, M., ÖPIK, M., DAVISON, J., VASAR, M., JAIRUS, T. & ZOBEL, M. 2018a. Soybean cultivation supports a diverse arbuscular mycorrhizal fungal community in central Argentina. Applied Soil Ecology 124:289–297.Google Scholar
GARCÍA DE LEÓN, D., DAVISON, J., MOORA, M., ÖPIK, M., FENG, H., HIIESALU, I., JAIRUS, T., KOOREM, K., LIU, Y., PHOSRI, C., SEPP, S. K., VASAR, M. & ZOBEL, M. 2018b. Anthropogenic disturbance equalizes diversity levels in arbuscular mycorrhizal fungal communities. Global Change Biology 24:2649–2659.Google Scholar
GAZOL, A., ZOBEL, M., CANTERO, J. J., DAVISON, J., ESLER, K. J., JAIRUS, T., ÖPIK, M., VASAR, M. & MOORA, M. 2016. Impact of alien pines on local arbuscular mycorrhizal fungal communities – evidence from two continents. FEMS Microbiology Ecology 92: fiw073.CrossRefGoogle ScholarPubMed
GOTTSHALL, C. B., COOPER, M. & EMERY, S. M. 2017. Activity, diversity and function of arbuscular mycorrhizae vary with changes in agricultural management intensity. Agriculture, Ecosystems & Environment 241:142–149.Google Scholar
HELGASON, T., MERRYWEATHER, J. W., YOUNG, J. P. W. & FITTER, A. 2007. Specificity and resilience in the arbuscular mycorrhizal fungi of a natural woodland community. Journal of Ecology 95: 623–630.Google Scholar
JANOS, D. P. 1980. Vesicular-arbuscular mycorrhizae affect lowland tropical rain forest plant growth. Ecology 61:151–162.Google Scholar
JANOS, D. P. & CAIN, C. L. 1998. Mycorrhiza in review. Mycorrhiza 7:331–333.Google Scholar
JUNQUEIRA, A. B., STOMPH, T. J., CLEMENT, C. R. & STRUIK, P. C. 2016. Variation in soil fertility influences cycle dynamics and crop diversity in shifting cultivation systems. Agriculture, Ecosystems and Environment 215:122–132.CrossRefGoogle Scholar
KALINHOFF, C., CÁCERES, A. & LUGO, L. 2009. Changes in root biomass and arbuscular mycorrhizae in shifting crops of the Venezuelan Amazon. Interciencia 34:571–576.Google Scholar
KIVLIN, S. N. & HAWKES, C. V. 2011. Differentiating between effects of invasion and diversity: impacts of aboveground plant communities on belowground fungal communities. New Phytologist 189:526–535.Google Scholar
KLIRONOMOS, J., ZOBEL, M., TIBBETT, M., STOCK, W. D., RILLIG, M. C., PARRENT, J. L., MOORA, M., KOCH, A. M., FACELLI, J. M., FACELLI, E., DICKIE, I. A. & BEVER, J. D. 2011. Forces that structure plant communities: quantifying the importance of the mycorrhizal symbiosis. New Phytologist 189:366–370.Google Scholar
KRASHEVSKA, V., KLARNER, B., WIDYASTUTI, R., MARAUN, M. & SCHEU, S. 2015. Impact of tropical lowland rainforest conversion into rubber and oil palm plantations on soil microbial communities. Biology and Fertility of Soils 51:697–705.Google Scholar
LEE, J., LEE, S. & YOUNG, J. P. 2008. Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiology Ecology 65:339–349.Google Scholar
MARTÍNEZ-GARCÍA, L. B., RICHARDSON, S. J., TYLIANAKIS, J. M., PELTZER, D. A. & DICKIE, I. A. 2015. Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development. New Phytologist 205:1565–1576.Google Scholar
MOORA, M. & ZOBEL, M. 2010. Arbuscular mycorrhizae and plant-plant interactions: impact of invisible world on visible patterns. Pp. 79–98 in Pugnaire, F. I. (ed.). Positive interactions and plant community dynamics. CRC Press, Boca Raton. 178 pp.Google Scholar
MOORA, M., BERGER, S., DAVISON, J., ÖPIK, M., BOMMARCO, R., BRUELHEIDE, H., KÜHN, I., KUNIN, W. E., METSIS, M., RORTAIS, A., VANATOA, A., VANATOA, E., STOUT, J. C., TRUUSA, M., WESTPHAL, C., ZOBEL, M. & WALTHER, G.-R. 2011. Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. Journal of Biogeography 38:1305–1317.Google Scholar
MOORA, M., DAVISON, J., OPIK, M., METSIS, M., SAKS, U., JAIRUS, T., VASAR, M. & ZOBEL, M. 2014. Anthropogenic land use shapes the composition and phylogenetic structure of soil arbuscular mycorrhizal fungal communities. FEMS Microbiology Ecology 90:609–621.Google Scholar
MUMMEY, D. L., CLARKE, J. T., COLE, C. A., O'CONNOR, B. G., GANNON, J. E. & RAMSEY, P. W. 2010. Spatial analysis reveals differences in soil microbial community interactions between adjacent coniferous forest and clearcut ecosystems. Soil Biology and Biochemistry 42:1138–1147.CrossRefGoogle Scholar
NEUENKAMP, L., MOORA, M., ÖPIK, M., DAVISON, J., GERZ, M., MÄNNISTÖ, M., JAIRUS, T., VASAR, M. & ZOBEL, M. 2018. The role of plant mycorrhizal type and status in modulating the relationship between plant and arbuscular mycorrhizal fungal communities. New Phytologist in press. doi: 10.1111/nph.14995.Google Scholar
NIELSEN, K. B., KJØLLER, R., BRUUN, H. H., SCHNOOR, T. K. & ROSENDAHL, S. 2016. Colonization of new land by arbuscular mycorrhizal fungi. Fungal Ecology 20:22–29.Google Scholar
OEHL, F., LACZKO, E., BOGENRIEDER, A., STAHR, K., BÖSCH, R., VAN DER HEIJDEN, M. & SIEVERDING, E. 2010. Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biology and Biochemistry 42:724–738.Google Scholar
OHSOWSKI, B. M., ZAITSOFF, P. D., ÖPIK, M. & HART, M. M. 2014. Where the wild things are: looking for uncultured Glomeromycota. New Phytologist 204:171–179.Google Scholar
ÖPIK, M., VANATOA, A., VANATOA, E., MOORA, M., DAVISON, J., KALWIJ, J. M., REIER, Ü. & ZOBEL, M. 2010. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist 188:223–241.Google Scholar
ÖPIK, M., ZOBEL, M., CANTERO, J., DAVISON, J., FACELLI, J., HIIESALU, I., JAIRUS, T., KALWIJ, J., KOOREM, K., LEAL, M., LIIRA, J., METSIS, M., NESHATAEVA, V., PAAL, J., PHOSRI, C., PÕLME, S., REIER, Ü., SAKS, Ü., SCHIMANN, H., THIÉRY, O., VASAR, M. & MOORA, M. 2013. Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430.Google Scholar
PÄRTEL, M., ÖPIK, M., MOORA, M., TEDERSOO, L., SZAVA‐KOVATS, R., ROSENDAHL, S., RILLIG, M. C., LEKBERG, Y., KREFT, H., HELGASON, T., ERIKSSON, O., DAVISON, J., BELLO, F., CARUSO, T. & ZOBEL, M. 2017a. Historical biome distribution and recent human disturbance shape the diversity of arbuscular mycorrhizal fungi. New Phytologist 216:227–238.Google Scholar
PÄRTEL, M., ZOBEL, M., ÖPIK, M. & TEDERSOO, L. 2017b. Global patterns in local and dark diversity, species pool size and community completeness in ectomycorrhizal fungi. Pp. 395–406 in Tedersoo, L. (ed.). Biogeography of mycorrhizal symbiosis. Springer, Cham.Google Scholar
PEÑA-VENEGAS, C. P., VERSCHOOR, G., STOMPH, T. J. & STRUIK, P. C. 2017. Challenging current knowledge on Amazonian dark earths: indigenous manioc cultivation on different soils of the Colombian Amazon. Culture, Agriculture, Food and Environment 39:127–137.Google Scholar
RILLIG, M. C. 2004. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters 7:740–754.Google Scholar
RILLIG, M. C., WRIGHT, S. F. & EVINER, V. T. 2002. The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species. Plant and Soil 238:325–333.Google Scholar
SAKS, Ü., DAVISON, J., ÖPIK, M., VASAR, M., MOORA, M. & ZOBEL, M. 2014. Root-colonizing and soil-borne communities of arbuscular mycorrhizal fungi in a temperate forest understorey. Botany 92:277–285.CrossRefGoogle Scholar
SEPP, S.-K., JAIRUS, T., VASAR, M., ZOBEL, M. & ÖPIK, M. 2018. Effects of land use on arbuscular mycorrhizal fungal communities in Estonia. Mycorrhiza 28:259–268.Google Scholar
SHARMAH, D. & JHA, D. K. 2014. Diversity of arbuscular mycorrhizal fungi in undisturbed forest, slash-and-burn field, and monoculture forest of indo-burma megadiverse region. Brazilian Journal of Botany 37:339–351.Google Scholar
SIEVERDING, E. 1991. Vesicular-arbuscular mycorrhiza management in tropical agrosystems. Eschborn, Bremen. 371 pp.Google Scholar
SIMON, L., LALONDE, M. & BRUNS, T. D. 1992. Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Applied and Environmental Microbiology 58:291–295.Google Scholar
SMITH, S. E. & READ, D. J. 2008. Mycorrhizal symbiosis. Academic Press, Amsterdam. 787 pp.Google Scholar
STANDISH, R., CRAMER, M. & YATES, C. 2009. A revised state-and-transition model for the restoration of woodlands in Western Australia. Pp. 169–187 in New models for ecosystem dynamics and restoration. Island Press, Washington. 366 pp.Google Scholar
STÜRMER, S. L. & SIQUEIRA, J. O. 2011. Species richness and spore abundance of arbuscular mycorrhizal fungi across distinct land uses in western Brazilian Amazon. Mycorrhiza 21:255–267.Google Scholar
TURRINI, A., AVIO, L., BEDINI, S. & GIOVANNETTI, M. 2007. In situ collection of endangered arbuscular mychorrhizal fungi in a Mediterranean UNESCO Biosphere Reserve. Biodiversity and Conservation 17:643–657.CrossRefGoogle Scholar
UIBOPUU, A., MOORA, M., ÖPIK, M. & ZOBEL, M. 2012. Temperate forest understorey species performance is altered by local arbuscular mycorrhizal fungal communities from stands of different successional stages. Plant and Soil 356:331–339.Google Scholar
VÁLYI, K., RILLIG, M. C. & HEMPEL, S. 2015. Land-use intensity and host plant identity interactively shape communities of arbuscular mycorrhizal fungi in roots of grassland plants. New Phytologist 205:1577–1586.Google Scholar
VAN DER HEYDE, M., OHSOWSKI, B., ABBOTT, L. K. & HART, M. 2017. Arbuscular mycorrhizal fungus responses to disturbance are context-dependent. Mycorrhiza 27:431–440.Google Scholar
VAN DER MAAREL, E. & FRANKLIN, J. 2005. Vegetation ecology. Wiley-Blackwell, Oxford. 572 pp.Google Scholar
VERBRUGGEN, E., VAN DER HEIJDEN, M. G., WEEDON, J. T., KOWALCHUK, G. A. & ROLING, W. F. 2012. Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Molecular Ecology 21:2341–2353.Google Scholar
WALLACE, R. B. & PAINTER, R. L. E. 2002. Phenological patterns in a southern Amazonian tropical forest: implications for sustainable management. Forest Ecology and Management 160: 19–33.Google Scholar
WARREN-THOMAS, E., DOLMAN, P. M. & EDWARDS, D. P. 2015. Increasing demand for natural rubber necessitates a robust sustainability initiative to mitigate impacts on tropical biodiversity. Conservation Letters 8:230–241.Google Scholar
ZHAI, D.-L., CANNON, C. H., SLIK, J. W. F., ZHANG, C.-P. & DAI, Z.-C. 2012. Rubber and pulp plantations represent a double threat to Hainan's natural tropical forests. Journal of Environmental Management 96:64–73.Google Scholar