Abstract

Orchid-fungus interaction networks often consist of many different fungi that interact with co-occurring orchids in complex ways, but so far it remains largely unclear which processes determine network structure and both ecological and evolutionary mechanisms have been invoked to explain network architecture. In this research, we tested the hypothesis that closely related orchids associate with similar mycorrhizal fungi and vice versa by investigating the architecture of the interaction network between orchid mycorrhizal fungi (OMF) and nine co-occurring epiphytic Dendrobium species. All species grew on the bark of a single tree species (Camelia sinensis) in a traditional tea garden in China, which allowed us to assess the role of evolutionary history in determining the assembly of orchid-fungus communities without the confounding effects of environmental variation. In total, 101 different fungal operational taxonomic units (OTUs) known to be mycorrhizal in orchids were found. Most of the identified mycorrhizal OTUs were members of the Serendipitaceae (80% of all identified mycorrhizal sequences). All orchid species associated with a large number of fungi (average number of links: 31.6 ± 3.8), and orchids from the same species tended to have significantly more similar fungal partners than orchids from different species. The network of interactions was significantly nested (NODF = 41.59, p < 0.01), but not significantly compartmentalized (M = 0.26, Mrandom = 0.27). Phylogenetic analyses showed that the interaction network was not significantly affected by the phylogenies of the orchids or the fungi. Overall, these results indicate that the studied orchid species associated with multiple fungi simultaneously, and that the network of associations was built on asymmetric and weak reciprocal dependences. Associating with multiple fungi may be a successful strategy of orchids to colonize vacant sites and to increase survival of established plants in epiphytic habitats.

Highlights

  • As one of the most species-rich flowering plant families, the Orchidaceae comprises more than 27,000 species that are widely distributed across the globe and occur in a broad range of habitats (Givnish et al, 2015; Weigelt et al, 2019)

  • The aim of this research was to answer the following questions: (1) Does mycorrhizal fungal community composition significantly differ between co-occurring Dendrobium species epiphytic to the same host plant species? (2) Is the Dendrobium–orchid mycorrhizal fungi (OMF) interaction network characterized by significant nestedness and/or modularity? (3) Can the structure of the observed orchid mycorrhizal network be explained by phylogenetic constraints?

  • These results differ from previous studies that have shown that the dominant fungal partners associating with Dendrobium species growing at other locations and habitats (e.g., Dendrobium crumenatum, Dendrobium speciosum, Dendrobium dicuphum, D. aphyllum, and D. cariniferum) were mainly members of the genus Tulasnella, while the fungi associating with Dendrobium nobile, Dendrobium sinense, and Dendrobium hancockii mainly belonged to Mycena and Epulorhiza

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Summary

Introduction

As one of the most species-rich flowering plant families, the Orchidaceae comprises more than 27,000 species that are widely distributed across the globe and occur in a broad range of habitats (Givnish et al, 2015; Weigelt et al, 2019). The presence of compatible orchid mycorrhizal fungi (OMF) has been regarded as one of the most important factors determining whether orchid plants can occur in a certain habitat or not and is a major factor driving the distribution and abundance of orchid populations (McCormick and Jacquemyn, 2014; McCormick et al, 2018). It has long been known that orchid species associate with different mycorrhizal fungi (Rasmussen, 1995). When multiple orchids co-occur at a given site, one orchid species may associate with more than one fungus at the same time, and these fungi may interact with other orchid species, so that multiple orchid species tap into a mycorrhizal network (Waterman et al, 2011; Jacquemyn et al, 2015a; Xing et al, 2019). Elucidating the structure of these interaction networks is important for understanding the co-evolutionary processes that shape orchid–fungus interactions

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