Woodland trees modulate soil resources and conserve fungal diversity in fragmented landscapes

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Abstract

Resource islands around woody plants are thought to define the structure and function of many semiarid and arid ecosystems, but their role in patterning of soil microbial communities remains largely unexamined in dry environments. This study examined soil resource distribution and associated fungal communities in two Allocasuarina luehmannii (buloke) remnants of semiarid north-western Victoria, Australia. These savannah-like woodlands are listed as endangered due to extensive clearing for agriculture. We used the DNA-based profiling technique T-RFLP and ordination-based statistical methods to compare fungal community compositions in surface soils from two remnants (located 1.6 km apart) and three sampling positions (beneath individual buloke canopies; grassy inter-canopy areas; and adjoining cleared paddocks). Resource island formation beneath buloke trees was clearly evident in soil physicochemical properties (e.g. threefold concentrations of total carbon and nitrogen in canopy versus non-canopy soils). This heterogeneity of resources was moderately correlated with soil fungal community compositions, which were distinct for each sampling position. We argue that fungal composition patterns reflected multiple roles of fungi in dryland ecosystems, namely: responses of saprotrophic fungi to tree organic matter inputs; specificity of ectomycorrhizal fungi to tree rooting zones; and fungal involvement in biological soil crusts that variably covered non-canopy soils. Our data did not indicate that buloke canopy areas were particular hotspots of soil fungal diversity, but that they increased landscape-level diversity by supporting a distinct suite of fungi. In addition, we provide evidence of phylogenetic differentiation of soil fungal communities between our two remnants, which adds to growing evidence of fungal genetic structure at localised scales. These findings highlight the importance of remnant trees in conserving both soil resources and microbial genetic diversity. In addition, evidence of differentiation of soil fungal phylogenetics between nearby but isolated remnants suggests that conserving soil fungal diversity requires conservation of host habitats over their entire (remaining) range, and indicates previously unseen consequences of tree loss from extensively cleared landscapes.

Introduction

Resource islands are a popular model for many semiarid and arid ecosystems (Ewing et al., 2007). These biogeochemical ‘hotspots' are often associated with woody vegetation in a herbaceous matrix, and are the result of plant nutrient accessions in throughfall, litter and roots, and of physical interception of wind- and water-borne material (Belnap et al., 2005, van der Valk and Warner, 2009). Relative to the herbaceous inter-patches, resource islands have an ameliorated microclimate and have greater stores of soil water and nutrients; in turn, these conditions favour plant growth and promote feedbacks between plant and soil (Ludwig et al., 2005). Indeed, it is thought that the nature and strength of these feedbacks ‘define the structure and function of arid ecosystems' (Belnap et al., 2005).

While patchiness of plants and soil resources in dry environments has been well documented, there has been little examination of the associated patterns in soil biota. A few studies have found that soil microorganisms ‘follow’ resources and are more abundant and more active in vegetated patches than inter-patches (Herman et al., 1995, Camargo-Ricalde and Dhillion, 2003, Ewing et al., 2007, Goberna et al., 2007). However, with the exception of some recent studies (e.g. Ewing et al., 2007, Orlando et al., 2007), the extent to which patch/inter-patch differences in microbial numbers also represent differences in microbial community composition remains largely unexamined in dry environments (Herman et al., 1995). This gap limits our knowledge of critical linkages between plants and soil biota, and of the likely environmental impacts of human-induced change, such as vegetation clearing, in semiarid and arid ecosystems (Wardle et al., 2004).

In addition to patch-scale factors, spatial patterning of soil microbial populations is influenced by population processes such as reproduction and dispersal (Ettema and Wardle, 2002). A long-held assumption has been that microbes have cosmopolitan distributions due to their large populations, short generation times, and capacity for long-distance dispersal (Green and Bohannan, 2006). However, recent studies based on molecular approaches provide strong evidence for spatial scaling of soil microbial diversity (Green and Bohannan, 2006, Zhou et al., 2008). For example, two studies measured medium-scale (i.e. <2 km) genetic structure in ectomycorrhizal fungi, which in both cases was related to limitations in spore dispersal (Peay et al., 2007, Carriconde et al., 2008). These findings support predictions that fungal populations will be particularly susceptible to broad-scale habitat loss due to less efficient dispersal and colonising abilities than bacteria (Hedlund et al., 2004), and lend support to the notion that conserving fungal genetic diversity requires conservation of host habitats over their entire geographic range (Gehring et al., 1998).

Recent studies have also indicated a dominant role for fungi in key processes within dryland soils. For example, Collins et al. (2008) presented evidence for fungal involvement in decomposition, nitrogen transformations, and nutrient translocation between plants and biological soil crusts in semiarid grasslands of New Mexico, USA. They argued that fungi assume particular functional importance in dryland soils because they can metabolize at higher temperatures and lower water potentials than bacteria (Collins et al., 2008). Molecular analyses of fungal communities in these grasslands indicated high functional diversity, with roots of a dominant grass colonised by at least 10 different orders, including endophytic, mycorrhizal, saprophytic, coprophilous, and plant pathogenic fungi (Porras-Alfaro et al., 2008). This high fungal diversity was largely attributed to ecosystem heterogeneity resulting from the above-described patchiness of plant and soil resources in dry environments.

We assessed soil fungal community composition in open-woodland remnants of semiarid north-western Victoria, Australia. These savannah-like systems are dominated by the evergreen tree ‘buloke’ (Allocasuarina luehmannii (R.T. Baker) L.A.S. Johnson), and are habitat for several endangered and threatened floral and faunal species. Nonetheless, they are subject to a serious ongoing threat from clearing for agriculture (Maron and Fitzsimons, 2007). We used the DNA-based fingerprinting technique Terminal Restriction Fragment Length Polymorphism (T-RFLP) for its benefits over other DNA-based techniques and its strength in comparative analyses (Thies, 2007). Multivariate ordination techniques were used to compare patterns in soil fungal community composition both within (canopy versus non-canopy) and between remnants, and to examine relationships with sample location and a range of soil properties. Our specific hypotheses were: (1) individual buloke trees would form resource islands within a broader herbaceous matrix; (2) buloke ‘islands' would support distinct soil fungal communities; and (3) soil fungal community composition would be distinguished on the basis of remnant location. More broadly, we aimed to describe the role of remnant trees in conserving soil fungal diversity and to highlight potentially unseen consequences of further tree loss in highly fragmented landscapes.

Section snippets

Study sites

Study sites were two remnant open-woodlands (Specht, 1981) located within a cropping and sheep station near Ninyeunook in north-western Victoria, south-eastern Australia (36°0′S, 143°24′E). The landform is flat to mildly undulating Quaternary alluvial plains of low elevation (<100 m above sea level). The soils have not been classified in detail but are broadly classified as red duplex soils or ‘Sodosols', with a strong texture contrast between the A horizon and sodic B horizon (Isbell, 2002).

Soil physicochemical properties

Canopy soils had significantly lower bulk density and significantly greater total C, total N, and available P than inter-canopy and disturbed soils of the same remnant (Table 1). In addition, canopy soils were moister and more acidic than inter-canopy but not disturbed soils (Table 1). Electrical conductivity (EC) was significantly greater in canopy than associated inter-canopy and disturbed soils of the south-east remnant, but was similar in canopy and disturbed soils of the north-west remnant

Buloke trees formed resource islands

We found clear evidence to support our first hypothesis that individual buloke trees form resource islands within a broader herbaceous matrix. Threefold concentrations of total C and total N in canopy versus inter-canopy soils (Table 1) are consistent with ratios in dryland woody systems both in Australia (Facelli and Brock, 2000, Tongway and Hindley, 2004), and elsewhere (Ewing et al., 2007, Goberna et al., 2007). The strength of the resource island effect reflected the high cover of canopy

Acknowledgements

This study was supported by The University of Melbourne and the North Central Catchment Management Authority (NCCMA) through a University of Melbourne Collaborative Research Grant. LTB and SK also acknowledge ongoing support from the Victorian Government Department of Sustainability and Environment. Special thanks to Geoff Park and Malory Weston (NCCMA) for support with study establishment, Gerd Bossinger for access to laboratory facilities, Trevor Meers for field assistance, and the Ninyeunook

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