Waiting for fungi: the ectomycorrhizal invasion of lowland heathlands

Abstract

Summary1. In England, the loss of lowland heathland, a habitat of global conservation importance, is primarily due to the invasion of birch and pine. This encroachment has been researched in depth from a plant perspective but little is known about the role of mycorrhizal fungi. In lowland heathlands the resident dwarf shrubs form ericoid mycorrhizas whereas invading trees form ectomycorrhizas. Therefore, tree encroachment into heathlands can be regarded as the replacement of a resident mycorrhizal community by an invading one. 2. This study examined how fungi form mycorrhizas with Betula and Pinus in lowland heathlands. We addressed the question of whether there are mycorrhizal fungi that mediate invasion using a molecular ecology approach to compare the mycorrhizal inoculum potential of soil at three levels of invasion (uninvaded heathland, invaded heathland and woodland) and the fungi forming mycorrhizas on tree seedlings and trees across diverse sites. 3. We show that in lowland heathlands: (i) seedlings have severely limited access to ectomycorrhizal fungi relative to woodlands, (ii) there are few keystone spore-dispersed ectomycorrhizal fungi that can mediate tree invasion, (iii) tree seedlings can remain non-mycorrhizal for at least one year when no inoculum is present, even near saplings, and (iv) mycorrhizal seedlings achieve greater biomass than non-mycorrhizal seedlings. Within uninvaded heathland we detected only Rhizopogon luteolus, Suillus variegatus, S. bovinus (Pinus symbionts) and Laccaria proxima (primarily a Betula symbiont). 4. Synthesis. Overall, ectomycorrhizal inoculum in lowland heathlands is rare; most tree seedlings growing in heathland soil are not mycorrhizal due to limited spore dispersal, poorly developed spore banks and weak common mycorrhizal networks. These seedlings can persist awaiting mycorrhization to boost their growth.

Mycorrhizal co‐invasion and novel interactions depend on neighborhood context

“…Second, there is a survivorship bias in measuring ectomycorrhizas on established plants. That is, seedlings lacking mycorrhizal partners in the field would have a higher probability of mortality, filtering out seedlings lacking ectomycorrhizas (but see Collier and Bidartondo 2009). Third, there was a strong location bias in field sampling, such that only locations where Pseudotsuga had already established could be sampled.…”

“…Tree seedlings can survive for several years without ectomycorrhizal partners (Collier and Bidartondo 2009), but their growth is typically slowed or halted, which may reduce their competitive ability and consequently the speed of invasion. Nonetheless, where seedlings can survive, our results suggest that they accumulate fungal partners over time, increasing the probability that a mutualistic partner will arrive (Dickie et al 2002).…”

“…However, context may be important to invasion because neighboring ectomycorrhizal hosts can influence the ectomycorrhizal communities of seedlings, regardless of whether the neighboring host is of the same , Dickie and Reich 2005, Nara 2006 or of a different , Nara and Hogetsu 2004, Bogar and Kennedy 2013 species as the seedling. This neighborhood effect may be caused by an actively growing common mycorrhizal network (Fleming 1983, Newman 1988, Simard and Durall 2004 or by a soil spore bank (Ashkannejhad andHorton 2006, Collier andBidartondo 2009). Furthermore, plantations of introduced trees may be more likely to host native ectomycorrhizal fungi when native ectomycorrhizal hosts are nearby (Bahram et al 2013).…”

“…The greenhouse approach also differs from the field survey by focusing on ''early-stage'' fungi, capable of forming mycorrhizas on seedlings in the absence of active carbon subsidies from mature trees (Deacon et al 1983. Seedlings may be able to establish and persist for some time without ectomycorrhizas and may potentially accumulate symbionts over time (Dickie et al 2002, Collier andBidartondo 2009). The consequence of poor initial mycorrhization is widely reported to reduce nutrient uptake and plant growth, thus making seedlings less competitive against surrounding vegetation and more vulnerable to pathogens during the establishment phase (Marx 1972 …”

Ectomycorrhizal fungal spore bank recovery after a severe forest fire: some like it hot

“…Although tree seedlings are able to survive short periods without ectomycorrhizal (ECM) fungal associates (Collier and Bidartondo, 2009), pine regeneration is often limited by lack of ECM fungal inoculum (Nunez et al, 2009). Thus, the initial recovery of forests after these severe mega-fires likely depends in part on whether appropriate ECM fungal spores have survived and are available to serve as partners for regenerating forest trees.…”