Functional traits and symbiotic associations of geoxyles and trees explain the dominance of detarioid legumes in miombo ecosystems.

Fabaceae Detarioideae Rhizobia ectomycorrhiza geoxyles geoxylic grasslands trait-based plant strategies trees

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
04 2021
Historique:
received: 30 07 2020
accepted: 18 12 2020
pubmed: 8 1 2021
medline: 15 5 2021
entrez: 7 1 2021
Statut: ppublish

Résumé

The miombo region in Africa is covered by a mosaic of woodlands and geoxylic grasslands and is subject to disturbances such as fires, frost and drought, and low nutrient availability. The dominance of Fabaceae Detarioideae species in miombo ecosystems is remarkable but little understood. We therefore compared plant functional traits (PFTs) of common woody species of the Angolan plateau, grouped by life form (trees, geoxyles), lineage (Fabaceae: Detarioideae, non-Detarioideae) and symbiont association (ectomycorrhiza, rhizobia). PFTs reflect group-specific adaptations to prevalent environmental conditions. To analyse the impact of environmental drivers, we selected PFTs reflecting ecophysiological aspects of leaf morphology, nutrient content and water transport. Traits were measured following standardized protocols. We found differences in key PFTs between trees and geoxyles reflecting both life form-specific adaptations to environmental conditions and lineage-specific strategies to cope with environmental stresses. We interpret higher leaf thickness and higher wood density of geoxyles as responses to harsher open environments. Fabaceae in general and ectomycorrhizal species showed better nutrient status. Symbiotic associations of detarioid legumes with ectomycorrhiza show specific advantages for phosphorous uptake as compared to Rhizobia-associated Fabaceae and to non-Fabaceae and thus may be crucial for the stunning dominance of Detarioideae in miombo landscapes.

Identifiants

pubmed: 33411968
doi: 10.1111/nph.17168
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

510-520

Informations de copyright

© 2021 The Authors. New Phytologist © 2020 New Phytologist Foundation.

Références

Aerts R, Chapin FS. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecology Research 30: 1-67.
Barbosa LAG. 1970. Carta Fitogeográfica de Angola. Luanda, Angola: Instituto de Investigação Científica de Angola.
Barotto AJ, Monteoliva S, Gyenge J, Martinez-Meier A, Fernandez ME. 2018. Functional relationships between wood structure and vulnerability to xylem cavitation in races of Eucalyptus globulus differing in wood density. Tree Physiology 38: 243-251.
Blonder B, Violle C, Bentley LP, Enquist BJ. 2011. Venation networks and the origin of the leaf economics spectrum. Ecology Letters 2: 91-100.
Borchert R. 1994. Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 75: 1437-1449.
Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C. 2015. How tree roots respond to drought. Frontiers in Plant Science 6: 547.
Campbell B. 1996. The miombo in transition: woodlands and welfare in Africa. Bogor, Indonesia: Center for International Forestry Research.
Chidumayo E. 1994. Phenology and nutrition of miombo woodland trees in Zambia. Trees 2: 67-72.
Chidumayo E. 1995. Handbook of miombo ecology and management. Stockholm, Sweden: Stockholm Environment Institute.
Colgan MS, Martin RE, Baldeck CA, Asner GP. 2015. Tree foliar chemistry in an African savanna and its relation to life history strategies and environmental filters. PLoS ONE 10: e0124078.
Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA et al. 2003. A handbook of protocols for standardised and easy measurements of plant functional traits worldwide. Australian Journal of Botany 51: 335-380.
Corrales A, Henkel TW, Smith ME. 2018. Ectomycorrhizal associations in the tropics - biogeography, diversity patterns and ecosystem roles. New Phytologist 220: 1076-1091.
Dakora FD, Phillips DA. 2002. Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil 245: 35-47.
Díaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili A, Montserrat-Martí G, Grime JP, Zarrinkamar F, Asri Y et al. 2004. The PFT that drive ecosystems: evidence from three continents. Journal of Vegetation Science 15: 295-304.
de la Estrella M, Forest F, Wieringa JJ, Fougere-Danezan M, Bruneau A. 2017. Insights on the evolutionary origin of Detarioideae, a clade of ecologically dominant tropical African trees. New Phytologist 214: 1722-1735.
Finckh M, Revermann R, Aidar MPM. 2016. Climate refugees going underground - a response to Maurin et al. (2014). New Phytologist 209: 904-909.
Frost P. 1996. The ecology of miombo woodlands. In: Campbell B, ed. The Miombo in transition: woodlands and welfare in Africa. Bogor, Indonesia: Centre for International Forestry Research, 11-57.
Garnier E, Navas ML. 2012. A trait-based approach to comparative functional plant ecology: concepts, methods and applications for agroecology. A review. Agronomy for Sustainable Development 32: 365-399.
Garnier E, Shipley B, Roumet C, Laurent G. 2001. A standardized protocol for the determination of specific leaf area and leaf dry matter content. Functional Ecology 15: 688-695.
Gomes AL, Revermann R, Gonçalves FMP, Lages F, Aidar MPM, Finckh M, Jüergens N. 2019. Tree or not a tree: differences in plant functional traits among suffrutex and closely related tree species. South African Journal of Botany 127: 176-184.
Gonçalves FMP, Revermann R, Gomes AL, Aidar MPM, Finckh M, Juergens N. 2017. Tree species diversity and composition of miombo woodlands in south-central Angola: a chronosequence of forest recovery after shifting cultivation. International Journal of Forestry Research 2017: 1-13.
Grime JP, Thompson K, Hunt R, Hodgson JG, Cornelissen JHC, Rorison IH, Hendry GAF, Ashenden TW, Askew AP, Band SR et al. 1997. Integrated screening validates primary axes of specialisation in plants. Oikos 79: 259-281.
Gröngröft A, Luther-Mosebach J, Landschreiber L, Eschenbach A. 2013. Cusseque soils. Biodiversity & Ecology 5: 51-54.
Güsewell S. 2005. Nutrient resorption of wetland graminoids is related to the type of nutrient limitation. Functional Ecology 19: 344-354.
Güsewell S, Koerselman W. 2002. Variation in nitrogen and phosphorus concentrations of wetland plants. Perspectives in Plant Ecology, Evolution and Systematics 5: 37-61.
Hall JS, Harris DJ, Saltonstall K, Medjibe VP, Ashton MS, Turner BL. 2019. Resource acquisition strategies facilitate Gilbertiodendron dewevrei monodominance in African lowland forests. Journal of Ecology 108: 433-448.
Hedin LO. 2004. Global organization of terrestrial plant-nutrient interactions. Procedings of the National Academy of Sciences, USA 101: 10849-10850.
Hermans C, Hammond JP, White PJ, Verbruggen N. 2006. How do plants respond to nutrient shortage by biomass allocation?. Trends in Plant Science 11: 610-617.
Hoffmann WA, Franco AC, Moreira MZ, Haridasan M. 2005. Specific leaf area explains differences in leaf traits between congeneric savanna and forest trees. Functional Ecology 19: 932-940.
Högberg P. 1982. Mycorrhizal associations in some woodland and forest trees and shrubs in Tanzania. New Phytologist 92: 407-415.
Högberg P, Nylund JE. 1981. Ectomycorrhizae in coastal miombo woodland of Tanzania. Plant and Soil 63: 283-289.
Högberg P, Piearce GD. 1986. Mycorrhizas in Zambian trees in relation to host taxonomy, vegetation type and successional pattern. Journal of Ecology 74: 775-785.
Houlton BZ, Wang YP, Vitousek PM, Field CB. 2008. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454: 327-330.
Hugouvieux V, Murata Y, Young JJ, Kwak JM, Mackesy DZ, Schroeder JI. 2002. Localization, ion channel regulation, and genetic interactions during abscisic acid signalling of the nuclear mRNA cap-binding protein, ABH1 130. Plant Physiology 130: 1276-1287.
Husson F, Le S, Pages J. 2010. Exploratory multivariate analysis by example using R. Boca Raton, FL, USA: Chapman & Hall/CRC Press.
Jew EKK, Dougill AJ, Sallu SM, O'Connell J, Benton TG. 2016. Miombo woodland under threat: consequences for tree diversity and carbon storage. Forest Ecology and Management 361: 144-153.
Josse J, Husson F. 2016. missMDA: a package for handling missing values in multivariate data analysis. Journal of Statistical Software 70: 1-31.
Kalaba FK, Quinn CH, Dougill AJ. 2012. Carbon storage, biodiversity and species diversity composition of Miombo woodlands in recovery trajectory after charcoal production in slash and burn agriculture in Zambia’s Copperbelt. Sustainable Research Institute, Paper no. 40; Centre for Climate Change Economics and Policy, Working Paper no. 119. Leeds, UK: University of Leeds.
Kassambara A, Mundt F. 2017. Package ‘factoextra’. Extract and visualize the results of multivariate data analyses, R package v.1.0.5. [WWW document] URL https://CRAN.R-project.org/package=factoextra. [accessed 23 November 2020].
Kattge J, Díaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, Garnier E, Westoby M, Reich PB, Wright IJ et al. 2011. TRY - a global database of plant traits. Global Change Biology 17: 2905-2935.
King DA, Davies SJ, Tan S, Noor NSM. 2006. The role of wood density and stem support costs in the growth and mortality of tropical trees. Journal of Ecology 94: 670-680.
Lewis GP, Schrire B, Mackinder B, Lock M. 2016. Legumes of the World. Kew, UK: Royal Botanic Gardens.
Loehle C. 1988. Tree life history strategies: the role of defenses. Canadian Journal of Forestry Research 18: 209-222.
LPWG. 2017. A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: The Legume Phylogeny Working Group (LPWG). Taxon 66: 44-77.
Malloch DW, Pirozynski KA, Raven PH. 1980. Ecological and evolutionary significance of mycorrhizal symbioses in vascular plants (a review). Proceedings of the National Academy of Sciences, USA 77: 2113-2118.
McGroddy ME, Daufresne T, Hedin LO. 2004. Scaling of C/N/P stoichiometry in forests worldwide: implications for terrestrial Redfield-like ratios. Ecology 85: 2390-2401.
McKey D. 1994. Legumes and nitrogen: the evolutionary ecology of a nitrogen-demanding lifestyle. In: Sprent JI, McKey D, eds. Advances in legume systematics 5: the nitrogen factor. Kew, UK: Royal Botanic Gardens, 211-228.
Meerts P. 2017. Geoxylic suffrutex of African savannas: short but remarkably similar to trees. Journal of Tropical Ecology 33: 295-298.
Midgley JJ, Lawes M, Chamaillé-Jammes S. 2010. Savanna woody plant dynamics: the role of fire and herbivory, separately and synergistically. Australian Journal of Botany 58: 1-11.
Miller C. 2000. Understanding the carbon-nitrogen ratio. A Voice for Eco-Agriculture 30: 20-21.
Minden V, Kleyer M. 2014. Internal and external regulation of plant organ stoichiometry. Plant Biology 16: 897-907.
Muller J. 2014. Dumas or Kjeldahl for reference analysis? Comparison and considerations for nitrogen/protein analysis of food and feed. Fossanalytics Denmark 1: 1-5.
Olson DM, Dinerstein E. 2002. The global 200: priority ecoregions for global conservation. Annals of the Missouri Botanical Garden 89: 199-224.
Osazuwa-Peters O, Zanne AE. 2011. Wood density protocol. [WWW document] URL http://prometheuswiki.publish.csiro.au/tiki-dex.php?page=Wood+density+protocol [accessed 5 March 2014].
Pausas JG, Lamont BB, Paula S, Appezzato-da-Glória B, Fidelis A. 2018. Unearthing belowground bud banks in fire-prone ecosystems. New Phytologist 217: 1435-1448.
Pérez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MSS, Cornwell WKK, Craine JMM, Gurvich DEE et al. 2013. New Handbook for standardized measurement of plant functional traits worldwide. Australian Journal of Botany 61: 167-234.
Poorter L, Bongers F. 2006. Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87: 1733-1743.
Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB. 2003. The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences 164: S143-S164.
Revermann R, Finckh M. 2013. Cusseque - microclimate. In: Oldeland J, Erb C, Finckh M, Jürgens N, eds. Environmental assessments in the okavango region. Biodiversity & Ecology 5: 47-50.
Revermann R, Gomes AL, Gonçalves FM, Wallenfang J, Hoche T, Jürgens N, Finckh M. 2016. Vegetation database of the Okavango Basin. Phytocoenologia 46: 103-104.
Revermann R, Gonçalves FM, Gomes AL, Finckh M. 2017. Woody species of the miombo woodlands and geoxylic grasslands of the Cusseque area, south-central Angola. Check List 13: 2030.
Revermann R, Oldenland J, Gonçalves FMP, Luther-Mosebach J, Gomes AL, Jürgens N, Finckh M. 2018. Dry tropical forests and woodlands of the Cubango basin in southern Africa- First classification and assessment of their woody species diversity. Phytocoenologia 48: 23-50.
Rodriguez-Zaccaro FD, Groover A. 2019. Wood and water: how trees modify wood development to cope with drought. Plants People Planet 1: 346-355.
Ryan CM, Williams M. 2011. How does fire intensity and frequency affect miombo woodland tree populations and biomass? Ecological Applications 21: 48-60.
Sanfilippo M. 2014. Trinta árvores e arbustos do miombo angolano. Guia de campo para idenificação. Firenzi, Italy: Cooperazione per lo Sviluppo dei Paesi Emergenti (COSPE).
Schneibel A, Stellmes M, Frantz D, Finckh M, Revermann R. 2013. Cusseque-earth observation. Biodiversity and Ecology 5: 55-57.
Schneibel A, Stellmes M, Röder A, Frantz D, Kowalski B, Haß E, Hill J. 2017. Assessment of spatio-temporal changes of smallholder cultivation patterns in the Angolan Miombo belt using segmentation of Landsat time series. Remote Sensing of Environment 195: 118-129.
Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA. 1965. Sap pressure in vascular plants. Science 148: 339-346.
Seyed LYS, Motafakkerazad R, Hossain MM, Rahman IMM. 2012. Water stress in plants : causes, effects and responses. In: Rahman IMM, ed. Water stress. London, UK: INTECH, 1-14. [WWW document] URL: https://www.intechopen.com/books/water-stress/water-stress-in-plants-causes-effects-and-responses [accessed 30 December 2016].
Shirima DD, Munishi PKT, Lewis SL, Burgess ND, Marshall AR, Balmford A, Swetnam RD, Zahabu EM. 2011. Carbon storage, structure and composition of miombo woodlands in Tanzania’s Eastern Arc Mountains. African Journal of Ecology 49: 332-342.
Singh S, Verma A. 2020. Plant functional traits in tropical dry forests. A review. In: Bhadouria R, Tripathi S, Srivastava P, Singh P, eds. Handbook of research on the conservation and restoration of tropical dry forests, IGI global publisher of timely knowledge. Hershey, PA, USA: IGI Global, 66-88.
Smart SM, Glanville HC, Blanes MC, Mercado LM, Emmett B, Jones D, Cosby B Jr, Marrs R, Butler A, Marshall M et al. 2017. Leaf dry matter content is better at predicting above-ground net primary production than specific leaf area. Functional Ecology 31: 1336-1344.
Stellmes M, Frantz D, Finckh M, Revermann R. 2013a. Okavango basin - earth observation. In: Oldeland J, Erb C, Finckh M, Jürgens N, eds. Environmental assessments in the Okavango region. Biodiversity & Ecology 5: 23-27.
Stellmes M, Frantz D, Finckh M, Revermann R, Röder A, Hill J. 2013b. Fire frequency, fire seasonality and fire intensity within the Okavango region derived from MODIS fire products. Biodiversity & Ecology 5: 351-362.
Syampungani S, Chirwa PW, Akinnifesi FK, Sileshi G, Ajayi OC. 2009. The miombo woodlands at the cross roads: potential threats, sustainable livelihoods, policy gaps and challenges. Natural Resources Forum 33: 150-159.
Tedersoo L, Bahram M, Zobel M. 2020. How mycorrhizal associations drive plant population and community biology. Science 367: eaba1223.
Tiessen H. 2008. Phosphorus in the global environment. In: White PJ, Hammond JP, eds. The ecophysiology of plant-phosphorus interactions, Berlin, Germany: Springer: 1-8.
Timberlake J, Chidumayo E. 2011. Miombo ecoregion, vision report. In: Occasional publications in biodiversity. Bulawayo, Zimbabwe: Biodiversity Foundation for Africa.
Tůma J, Skalický M, Tůmová L, Bláhová P, Rosůlková M. 2004. Potassium, magnesium and calcium content in individual parts of Phaseolus vulgaris L. plant as related to potassium and magnesium nutrition. Plant Soil and Environment 50: 18-26.
Tuohy JM, Prior JAB, Stewart GR. 1991. Photosynthesis in relation to leaf nitrogen and phosphorus content in Zimbabwean trees. Oecologia 88: 378-382.
Vendramini F, Díaz S, Gurvich DE, Wilson PJ, Thompson K, Hodgson JG. 2002. Leaf traits as indicators of resource-use strategy in floras with succulent species. New Phytologist 154: 147-157.
Vinya R, Malhi Y, Brown N, Fisher JB. 2012. Functional coordination between branch hydraulic properties and leaf functional traits in miombo woodlands: implications for water stress management and species habitat preference. Acta Physiologiae Plantarum 34: 1701-1710.
Violle C, Navas M, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E. 2007. Let the concept of trait be functional! Oikos 116: 882-892.
Volaire F. 2018. A unified framework of plant adaptive strategies to drought: crossing scales and disciplines. Global Change Biology. 24: 2929-2938.
Waite M, Sack L. 2010. How does moss photosynthesis relate to leaf and canopy structure? Trait relationships for 10 Hawaiian species of contrasting light habitats. New Phytologist 185: 156-172.
Weber T. 2013. Cusseque climate. Biodiversity & Ecology 5: 45-46.
White F. 1976. The underground forests of Africa: a preliminary review. Gardens Bulletin Singapore 29: 57-71.
White PJ, Hammond JP. 2008. The ecophysiology of plant-phosphorus interactions. Berlin, Germany: Springer.
Williams M, Ryan CM, Rees RM, Sambane E, Femando J, Grace J. 2008. Carbon sequestration and biodiversity of re-growing miombo woodlands in Mozambique. Forest Ecology and Management 254: 145-155.
Wilson PJ, Thompson K, Hodgson JG. 1999. Specific leaf area and dry leaf matter content as alternative predictors of plant strategies. New Phytologist 143: 155-162.
Zigelski P, Gomes A, Finckh M. 2019. Suffrutex dominated ecosystems in Angola. In: Huntley BJ, Russo V, Lages F, Ferrand N, eds. Biodiversity of Angola. Science and conservation: a modern synthesis. Berlin, Germany: Springer, 109-121.

Auteurs

Amândio L Gomes (AL)

Faculty of Sciences, Agostinho Neto University, Av. 4 de Fevereiro 71, Luanda, CP 815, Angola.
Biodiversity, Evolution and Ecology of Plants, Institute of Plant Science and Microbiology, University of Hamburg, Ohnhorststr. 18, Hamburg, 22609, Germany.

Rasmus Revermann (R)

Biodiversity, Evolution and Ecology of Plants, Institute of Plant Science and Microbiology, University of Hamburg, Ohnhorststr. 18, Hamburg, 22609, Germany.
Faculty of Natural Resources and Spatial Sciences, Namibia University of Science and Technology, Windhoek, 10005, Namibia.

Paulina Meller (P)

Biodiversity, Evolution and Ecology of Plants, Institute of Plant Science and Microbiology, University of Hamburg, Ohnhorststr. 18, Hamburg, 22609, Germany.

Francisco M P Gonçalves (FMP)

Biodiversity, Evolution and Ecology of Plants, Institute of Plant Science and Microbiology, University of Hamburg, Ohnhorststr. 18, Hamburg, 22609, Germany.
Department of Natural Sciences, Herbarium of Lubango, ISCED Huíla, Sarmento Rodrigues str., Lubango, CP 230, Angola.

Marcos P M Aidar (MPM)

Plant Physiology and Biochemistry, Institute of Botany, São Paulo, CP 3005, CEP 01061-970, Brazil.

Fernanda Lages (F)

Department of Natural Sciences, Herbarium of Lubango, ISCED Huíla, Sarmento Rodrigues str., Lubango, CP 230, Angola.

Manfred Finckh (M)

Biodiversity, Evolution and Ecology of Plants, Institute of Plant Science and Microbiology, University of Hamburg, Ohnhorststr. 18, Hamburg, 22609, Germany.

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