Twenty years of research on fungal–plant interactions on Lyman Glacier forefront – lessons learned and questions yet unanswered
Highlights
► We present 20 years of community data collected at a receding glacier forefront. ► Plant establishment correlates with phylogenetic clustering of microbial communities. ► Decoupling plant and soil development is necessary to understand fungal communities. ► Controls of microbial community assembly require further study.
Introduction
Many alpine glaciers reached their glacial maximum during the Little Ice Age in the mid-19th century (Egli et al. 2001) and have been retreating over the past century and a half at increasing rates (Hodge et al., 1998, Dyurgerov and Meier, 2000, Pelto, 2006). Glacial retreat exposes a mineral substrate that is devoid of organic legacies and often deficient in mineral nitrogen (Matthews, 1992, Tscherko et al., 2003, Strauss et al., 2009), factors that globally limit ecosystem productivity (Vitousek et al. 1997). These nutrient limitations are often combined with extreme fluctuations of daily temperatures, limited barriers against wind damage, poor water retention and high irradiation, all of which may limit plant establishment and survival (Stocklin and Baumler, 1996, Jumpponen et al., 1999b, Lichter, 2000, Jones and del Moral, 2009). Additionally, glaciers and their forefronts most often occur at high latitudes and altitudes, characterized by short growing seasons and substantial winter snow cover. Together, these abiotic stressors make primary successional forefronts challenging environments to research, but they also provide unique opportunities to study the early assembly of communities (Cázares et al. 2005).
Many mechanisms controlling primary succession in plant communities have been recently clarified (Walker and del Moral, 2003, Pickett et al., 2009) and older theories reevaluated (Clements, 1916, Connell and Slatyer, 1977). Some of these insights have shifted views on community assembly processes in terrestrial ecosystems. For example, early successional community development seems not to depend on deterministic colonization by pioneering species but rather combines stochastic dispersal and establishment controls (Fastie, 1995, del Moral, 2009) that are later amended by deterministic processes such as biotic, competitive and facilitative controls (del Moral 2009).
Long-term studies in glacier forefronts are rare because of their remote locations and short accessible seasons, dictated by high altitudes and latitudes. Instead, glacier forefronts have often been subjected to a chronosequence approach (space-for-time substitution), in which distance from the glacier terminus is considered as a proxy for time since exposure (Pickett, 1989, Cázares et al., 2005, Walker et al., 2010). While suffering from potential correlations between position in the chronosequence and substrate chemistry, fluctuations in weather or climatic conditions, distance to propagule sources, or other environmental parameters (Fastie, 1995, Walker et al., 2010), the forefronts benefit from providing a single location wherein substrates of different ages can be observed in a relatively homogeneous environment (Matthews, 1992, Jumpponen et al., 1998, Cázares et al., 2005, Raffl et al., 2006).
In this contribution, we reflect on and synthesize more than 20 yr of research at a glacier forefront in Washington State’s North Cascades Mountains, which contain more than 700 glaciers (Post et al. 1971). Similarly to glaciers globally (Hodge et al., 1998, Dyurgerov and Meier, 2000), glaciers in the North Cascades have been receding in recent decades (Pelto, 2006, Pelto, 2011). To optimize our choice of a forefront environment, we explored several glaciers to find one that would best serve as the long-term study site. Our criteria included (1) reasonable accessibility, (2) a forefront with relatively little elevational change, (3) a subalpine habitat to allow establishment of ectomycorrhizal (EcM), ericoid mycorrhizal (ErM) and arbuscular mycorrhizal (AM) hosts and fungi as well as typically nonmycorrhizal plants, (4) a north-south orientation to minimize diurnal shade effects along the length of the forefront, and (5) accessibility for potential animal vectors of mycorrhizal spores. These criteria also served well for microbial and molecular studies. One forefront was almost ideal in all respects: the Lyman Glacier, in the Glacier Peak Wilderness Area, Wenatchee National Forest (Freeman 1941). The glacier and its recession have been photographed off and on since the late 19th Century (Freeman 1941) and later by periodic aerial photography by the U.S. Forest Service, including new colour aerial photographs taken specifically for our use. These resources allowed a reasonable description of the glacier’s recession and chronosequence (Jumpponen et al. 1998).
Many of our studies test hypotheses about the establishment and succession of communities. We have focused on the role of mycorrhizal fungi in primary plant succession and subsequent secondary succession. Early studies by Reeves et al. (1979) showed that in a desert ecosystem with a severely disturbed, secondary successional habitat, the early plant invaders were nonmycorrhizal species, whereas plants that dominated the adjacent nondisturbed system mostly formed associations with AM fungi. Reeves et al. (1979) also reviewed literature on primary succession of volcanic islands that showed early plant communities to be nonmycorrhizal. They hypothesized that the early nonmycorrhizal invaders were poor competitors and were therefore rapidly replaced when mycorrhizal hosts could establish after AM inoculum had entered the disturbed site. These AM hosts were argued to be better competitors and produced additional AM inoculum in the soil to enable other mycorrhizal plants to establish. Allen et al. (2005) reached similar conclusions on primary successional tephra resulting from the Mount St. Helens eruption. One of our early driving questions was whether or not a glacier forefront would exhibit similar primary and secondary successions.
While glacier systems differ in numerous characteristics and the conclusions may be context dependent, many general trends and patterns have proved consistent (Tscherko et al., 2003, Orwin et al., 2006). Here, we use our research on the Lyman Glacier forefront, which spans more than 20 yr, as a model. We first briefly review patterns of plant community establishment and trajectories, then compare plant and fungal communities. Finally, we identify critical areas that have received little attention and propose approaches to address them in fungal and/or microbial systems.
Section snippets
Community assembly and ecological filtering
As a general framework, we rely on assembly rules used in community ecology (Cole 1983; Hunt 1991). This community assembly model integrates traits and life histories and their contribution to organismal environmental tolerances (Jumpponen & Egerton-Warburton 2005). Factors determining successful establishment are considered as abiotic and biotic filters that select community components from local, regional and ecologically suited species pools (Weiher and Keddy, 1995, Weiher and Keddy, 2001,
Acknowledgements
The research at Lyman Glacier forefront has been supported by US National Science Foundation Grants DEB-9310006 (JMT), DEB-0344838 (AJ), DEB-0516456 (AJ) OPP-0221489 (AJ), National Science Foundation EPSCoR Grant 9874732 with matching support from the State of Kansas (AJ), Emil Aaltonen’s Foundation (AJ), and the US Forest Service Pacific Northwest Research Station. Shawn Brown is supported by the Department of Education GAANN program. We are grateful for the abiding logistical support of Ken
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