Asteropeia Mcphersonii, a Potential Mycorrhizal Facilitator for Ecological Restoration in Madagascar Wet Tropical Rainforests
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Forest Ecology and Management 358 (2015) 202–211 Contents lists available at ScienceDirect Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco Asteropeia mcphersonii, a potential mycorrhizal facilitator for ecological restoration in Madagascar wet tropical rainforests ⇑ Charline Henry a, , Jeanne-Françoise Raivoarisoa b, Angélo Razafimamonjy b, Heriniaina Ramanankierana c, Paul Andrianaivomahefa b, Marc-André Selosse d, Marc Ducousso e a AgroParisTech, Laboratoire des Symbioses Tropicales et Méditerranéennes, IRD/INRA/CIRAD/Montpellier SupAgro/Université Montpellier, TA10J, 34398 Montpellier Cedex 5, France b Ambatovy, Immeuble Tranofitaratra, 7ème étage, Rue Ravoninahitriniarivo, Ankorondrano, Antananarivo 101, Madagascar c Centre National de Recherches sur l’Environnement, Laboratoire de Microbiologie de l’environnement, Antananarivo, Madagascar d Institut de Systématique, Évolution, Biodiversité, ISYEB, UMR 7205, CNRS, MNHN, UPMC, EPHE, Muséum national d’Histoire naturelle, Sorbonne Universités, 57 rue Cuvier, CP50, 75005 Paris, France e CIRAD, Laboratoire des Symbioses Tropicales et Méditerranéennes, IRD/INRA/CIRAD/Montpellier SupAgro/Université Montpellier, TA10C, 34398 Montpellier Cedex 5, France article info abstract Article history: Ecological restoration in severely disturbed environments can fail because of lack of knowledge of the Received 21 April 2015 functioning of the original ecosystem. Nevertheless, facilitating establishment between plant species Received in revised form 10 September can help accelerate ecological succession, especially in stressful environments. Mycorrhizal symbiosis 2015 plays a key role in plant growth, particularly in harsh environments, and could also play a role in facilita- Accepted 11 September 2015 tion between plants, as mycorrhizal fungi can form a mycelial network that simultaneously interacts with the root systems of several plant species. In a high-elevation Malagasy tropical rainforest on acidic and iron-rich soil surrounding an active mining site, four genera of ectomycorrhizal plants are locally abun- Keywords: dant: Leptolaena, Sarcolaena, Uapaca and Asteropeia. A floristic survey showed that only Asteropeia seed- Ecological restoration Ectomycorrhizal community lings can grow on bare soil. Molecular analysis of ectomycorrhizal fungi ITS rDNA enabled us to Nurse plant describe ectomycorrhizal communities and their distribution among these four plant genera. Asteropeia Russulaceae, Boletales, Cortinariaceae and Thelephoraceae are abundant in these forests. There is exten- Madagascar sive sharing between ectomycorrhizal communities associated with Asteropeia mcphersonii and other ecto- mycorrhizal plants. There are also many mycorrhizal fungi species which are common to ectomycorrhizal communities of seedlings and adult trees. This abundance of generalist fungi allows us to envisage the use of A. mcphersonii in the ecological restoration of the mine site. Planting ectomycorrhizal fungi in the bare soil at the beginning of ecological restoration could allow them to grow, thereby establishing a source of inoculum to colonize other ectomycorrhizal plants and consequently facilitate their establishment. Ó 2015 Published by Elsevier B.V. 1. Introduction 1994; Callaway and Walker, 1997), suggests that interactions shift from mainly negative (i.e. competition) to mainly positive (i.e. Ecological restoration in environments disturbed by human facilitation) with increasing stress. This hypothesis has received activities, especially those where the substrate is bare and a suc- much observational support (e.g. Callaway et al., 2002) and may cession has to be restarted, is particularly challenging (Wong, apply in particular under conditions of extreme stress (He and 2003), and is often limited by insufficient knowledge of the pre- Bertness, 2014). disturbance ecosystem. In particular, the original community A particular form of facilitation which is useful in plant commu- may contain mechanisms that allow facilitation, i.e. the positive nity restoration is referred to as the ‘‘nurse effect” when an adult influence of one species on another that may be instrumental in plant (the nurse plant) promotes the establishment of seedlings restoration. Even though this assumption is under debate (e.g. (the target plants; Niering et al., 1963). It may be decisive for plant Bakker et al., 2013), stressful environments are likely to promote establishment in primary or secondary successions, especially in facilitation between plants. The so-called stress gradient hypothe- harsh environments (Walker and del Moral, 2003), and sometimes sis, which was proposed 20 years ago (Bertness and Callaway, involves microbial mediation (Duponnois et al., 2011). Mycorrhizal symbiosis, which concerns 80% of land plant species (van der ⇑ Corresponding author. Heijden et al., 2015; Wang and Qiu, 2006), is a mutualistic associ- E-mail address: [email protected] (C. Henry). ation between a fungus and the roots of a plant, which often http://dx.doi.org/10.1016/j.foreco.2015.09.017 0378-1127/Ó 2015 Published by Elsevier B.V. C. Henry et al. / Forest Ecology and Management 358 (2015) 202–211 203 depends on fungal colonization for its survival. This relationship is forest on sandy soil in southeast Madagascar; Tedersoo et al., crucial for both partners, since the plant supplies carbon to the soil 2011). Yet many mining projects require forest restoration on the fungus and, as a reward, receives nutrients and water from the fun- bare, hostile soils which remain after exploitation. Here we report gus through a symbiotic organ, the mycorrhiza (Smith and Read, a study conducted in the altitudinal tropical rain forests growing 2008). Mycorrhizal symbiosis plays a key role in plant nutrition on acidic and iron-rich soils at the foot of the Ambatovy mining and also in plant defence against soil biotic and abiotic aggression project, which will require restoration in the near future. In the (Selosse et al., 2004). For example, some ectomycorrhizal fungi mature forest, four species which are locally abundant as adults give the host plant resistance to heavy metals (Jourand et al., are ectomycorrhizal: Asteropeia mcphersonii (Asteropeiaceae; 2010), and, the absence of fungal partners in stressful environ- Ducousso et al., 2008), Leptolaena sp. and Sarcolaena sp. (Sarcolae- ments can thus seriously limit plant development (Cázares et al., naceae; Ducousso et al., 2004), and Uapaca densifolia (Phyllan- 2005; Feldhaar, 2011). taceae; Wang and Qiu, 2006). Seedlings of A. mcphersonii, One major reason why mycorrhizal symbiosis can help facilita- Leptolaena sp and U. densifolia are quite abundant, whereas tion is its network structure, by way of individual mycelia that col- Sarcolaena sp. seedlings are rare. We looked for species with a onize different plants, sometimes of different species (Selosse et al., potential nurse effect to help re-establish ectomycorrhizal tree 2006; Simard et al., 2012): one plant can thus provide fungal diversity by way of fungal partners. To locate an ideal nurse plant inoculum to another, in the form of already established and sup- to fulfil feature #1, a floristic survey was undertaken to identify ported mycelia. Such facilitation between plants where mycor- plants which spontaneously regenerate in the degraded environ- rhizas mediate a nurse effect has already been demonstrated in ment. Then, the ectomycorrhizal fungi spontaneously associated ectomycorrhizas (Horton et al., 1999; Richard et al., 2009), a kind with trees in different undisturbed sites were identified by molec- of mycorrhizal association common in trees and shrubs in most ular barcoding to check that the potential nurse species share fungi temperate and in some tropical regions (Smith and Read, 2008). with the seedlings (feature #2) and adults (feature #3a) of other This facilitation process implies that nurse and target plants are target species, or that the fungal communities in adults and seed- non-specific and share a large proportion of their ectomycorrhizal lings overlap (features #3b). We thus sought to determine if one of fungal partners. Indeed, this occurs in most cases (Smith and Read, the ectomycorrhizal trees combined all four features, which would 2008) and even host plants associating with a small number of facilitate the installation of other ectomycorrhizal genera in the ectomycorrhizal fungi do harbour generalist fungi, as exemplified framework of ecological restoration. by the genus Alnus (Bent et al., 2011; Bogar and Kennedy, 2013; Roy et al., 2013). Moreover, studies showing a preferential associ- 2. Materials and methods ation between certain fungi and certain plants (Ishida et al., 2007; Morris et al., 2008; Tedersoo et al., 2008, 2010) do not support 2.1. Study site strict specificity. Ectomycorrhizal fungal communities often dis- play fungal sharing between host species in temperate (e.g. Ambatovy mine extends over 1800 ha in Madagascar between Richard et al., 2005; Ryberg et al., 2009) and tropical environments latitudes 18°5201900S and 18°4904700S and between longitudes (Diédhiou et al., 2010; Smith et al., 2011, 2013). Still, the trend may 48°1902200E and 48°1700200E(Fig. 1), at an average altitude of vary among ecosystems, and in a wet Tasmanian sclerophyllous 1000 m above sea level. This is a mosaic of land locally disturbed forest, half the fungal species sampled more than once were only by human practice and primary forests in which 1759 plant species found on a single host species