Journal of Ecology 2011, 99, 764–776

doi: 10.1111/j.1365-2745.2011.01807.x

The roles of environmental filtering and colonization in the fine-scale spatial patterning of ground-layer plant communities in north temperate deciduous forests Julia I. Burton1*†, David J. Mladenoff1, Murray K. Clayton2,3 and Jodi A. Forrester1 1

Department of Forest and Wildlife Ecology, University of Wisconsin-Madison, 1630 Linden Dr., Madison, WI 53706, USA; 2Department of Plant Pathology, University of Wisconsin-Madison, 1630 Linden Dr., Madison, WI 53706, USA; and 3Department of Statistics, University of Wisconsin-Madison, 1210 W. Dayton St., Madison, WI 53706, USA

Summary 1. The majority of plant species in northern temperate deciduous forests are restricted to the ground layer, but the importance of colonization processes relative to environmental filtering in structuring spatial variation in ground-layer plant communities is poorly understood. 2. Using multivariate analyses, structural equation modelling and geostatistics, we examined interactions among ground-layer plant communities, the live overstorey and environmental gradients across a 70- to 90-year-old northern hardwood forest in Wisconsin (USA). We hypothesized that (i) fine-scale variation is related to environmental filtering rather than dispersal limitation and colonization processes; and (ii) exogenous ‘site’ filters exert more control than the composition and structure of the overstorey. 3. A transition from communities of spring ephemerals to communities of evergreen-dimorphic species is related to a hierarchy of controls driven by elevation, soil texture and associated effects on soil moisture, overstorey composition, and O-horizon and soil properties. An orthogonal axis distinguished among sparse communities associated with high levels of soil moisture early in the growing season and rich communities of early summer forbs associated with increasing O-horizon N:P and %Ca, and short-distance dispersal mechanisms. Indirect effects of tree species are significant, but cumulatively less important than exogenous site filters. 4. Synthesis. The spatial patterning of ground-layer plant communities is related to both environmental filtering and colonization. These patterns were related to species’ functional and dispersal characteristics, suggesting that processes structuring ground-layer plant communities are not merely neutral. Loose regulation of environmental and resource gradients resulting in a coarsegrained spatial patterning of plant communities observed in second-growth forests may therefore be related to a simplification in overstorey composition and the absence of heterogeneity accumulating through gap dynamics. Key-words: determinants of plant community diversity and structure, dispersal, environmental filtering, functional groups, herbaceous layer, soil resources, spatial patterning, structural equation modelling, understorey vegetation, Wisconsin

Introduction Understanding the relative importance of historical and environmental filters that drive variation in plant communities is a central goal for ecologists (Ricklefs 1987; Keddy 1992; Lam*Correspondence author. E-mail: [email protected] †Present address: 321 Richardson Hall, Oregon State University, Corvallis, OR 97331, USA.

bers, Chapin & Pons 1998; Harrison et al. 2006). Physiological filters can yield strong relationships between species distributions and environmental gradients, while biological filters (e.g. competition or predation), may constrain such distributions (McGill et al. 2006). In contrast, historical filters, such as disturbance or land-use history, can weaken relationships between species distributions and environmental gradients (Vellend et al. 2007) resulting in spatial patterns associated with colonization (Matlack 1994; Verheyen et al. 2003; Ozinga

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Forest ground-layer plant communities 765 et al. 2005; Damschen et al. 2008) and ecological drift associated with stochastic processes (Hubbell 2001; Gotelli & McGill 2006). Studies of fine-scale spatial variation in plant community structure can provide insights into how such processes interact across scales to influence vegetation locally (Leibold et al. 2004). Ground-layer plant communities of herb and shrub species comprise an important component of temperate deciduous forest ecosystems (Gilliam 2007), but are studied less frequently and intensively compared to tree species. Therefore, our knowledge of the physiology of individual species, and of species interactions and dynamics along environmental gradients, as well as our ability to predict the effects of changes in the structure of environmental gradients (i.e. due to disturbance and forest stand dynamics as well as climate change) is comparatively limited (Whigham 2004). Within temperate deciduous forests, ground-layer plant community structure has been associated with land-use history (Fraterrigo, Turner & Pearson 2006; Vellend et al. 2007), overstorey composition and structure (Beatty 1984; Scheller & Mladenoff 2002), disturbance (Moore & Vankat 1986; Roberts 2007), competition with tree seedlings and saplings (Miller, Mladenoff & Clayton 2002), interactions between earthworms and ungulate herbivory (Frelich et al. 2006) and soil properties (Rogers 1982; Beatty 1984; Reed et al. 1993), as well as colonization processes and seed dispersal mechanisms (Ehrle´n & Eriksson 2000; Miller, Mladenoff & Clayton 2002). However, a synthetic model of the myriad of direct and indirect interactions that structure ground-layer plant communities has yet to be tested. The relative importance of different environmental and dispersal filters for ground-layer plant community assembly may vary over space and time with land use and among forest stands in different stages of development. For instance, shortdistance dispersal can constrain the ability of many forest herb species to re-colonize recovering stands in earlier stages of development (Matlack 1994; Verheyen et al. 2003). However, endogenous biotic control over resource availability may increase over time (Odum 1969; Leuschner & Rode 1999) leading to linkages between the overstorey and understorey, and increasingly complex hierarchical interactions (Gilliam, Turrill & Adams 1995; Miller, Mladenoff & Clayton 2002; Gilliam 2007). Indeed, spatial patterns of understorey vegetation in primary and old-growth stands are more fine grained and patchy, with lower rates of species accumulation, relative to younger second-growth stands (Scheller & Mladenoff 2002; Burton et al. 2009). Within forests, fine-scale gradients of soil resources (e.g. moisture, N, P and Ca) and light are generated by multiple factors that interact across scales of space and time. Processes that affect moisture balance and the supply of soil nutrients are tied to exogenous site factors such as soil morphology and topography (Campbell & Norman 1998; Schaetzl & Anderson 2005). Layered upon physiographic factors are endogenous gradients related to the composition and structure of the overstorey, affecting both the radiation regime in the understorey (Canham et al. 1994) as well as the physical and chemical properties of soil at the scale of a single tree (c. 40 m2) to larger patches

(>1 ha). In particular, evidence suggests that tree species can exert control over nutrient cycling via litter inputs and uptake (Mladenoff 1987; Ferrari 1999; Lovett et al. 2004; Scharenbroch & Bockheim 2007; Weand et al. 2010). Furthermore, canopy gaps created by wind-throw and tree mortality can alter the local microclimate, resource levels and resource heterogeneity (Moore & Vankat 1986; Mladenoff 1987). The spatial and temporal distribution of such ‘micro-environmental gradients’ can influence patterns of competition among individuals, as well as population and community structure (Hutchings, John & Wijesinghe 2003; Neufeld & Young 2003). Thus, the fine-scale spatial patterning of forest ground-layer plant communities, simply in response to resource gradients, can be quite complex. Relationships between functional groupings of plant species and environmental gradients can provide evidence for environmental filtering, particularly when the traits suggest an advantage in the associated environment (McGill et al. 2006). Morphology tends to converge among forest herbs with similar leafing phenology suggesting that phenological guild reflects a key ecological strategy (Givnish 1987). For instance, spring ephemerals have relatively short leaf life span and higher rates of photosynthesis and respiration than early summer, late-summer and evergreen species and thus may require greater levels of resources to grow, survive and reproduce (Neufeld & Young 2003; Reich et al. 2003; Diaz et al. 2004). Additionally, many forest herb species have long pre-reproductive periods and short-distance dispersal mechanisms (Whigham 2004). The diversity of ecological strategies suggests the potential for niche differentiation along environmental gradients as well as dispersal limitation and ecological drift (Tilman 1990; Ehrle´n & Eriksson 2000; Gilbert & Lechowicz 2004; Ozinga et al. 2005; Gotelli & McGill 2006). Here we test the hypothesis that fine-scale variation in the composition of ground-layer plant communities is related to species functional groupings and environmental gradients rather than colonization and stochastic drift in a 70- to 90year-old second-growth northern hardwood forest. Specifically, we expected that the spatial distribution of plant communities within the forest is associated with the effects of interactions between exogenous site characteristics and the live overstorey on the distribution of environmental and resource gradients. We also test the hypothesis that exogenous site variables exert relatively greater control over community composition than do endogenous live overstorey structure variables. Therefore we (i) assess the relative importance of niche partitioning along environmental gradients vs. colonization; (ii) examine how exogenous site characteristics and the overstorey interact to affect the spatial patterning of plant communities in the forest understorey; and (iii) examine the relative importance of exogenous site characteristics vs. endogenous variation related to overstorey composition. We use a structural equation modelling (SEM) framework (e.g. Grace 2006) integrating sub-hypotheses suggested by theory as well as previous investigations (Grace et al. 2010). By examining networks of relationships among ground-layer plant communities,

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766 J. I. Burton et al. overstorey composition and structure and environmental variables, we quantify the relative importance of niche differentiation and colonization to better understand how the species pool is filtered by local processes in the forest understorey.

Materials and methods STUDY AREA

The study area is located within the Flambeau River State Forest on the loess plain of north-central Wisconsin, USA (Fig. 1). It is a rich, second-growth northern mesic forest (Curtis 1959) and the site of a long-term manipulative experiment that examines the effects of forest structure and deer exclusion on biodiversity and ecosystem function (e.g. Dyer et al. 2010; Stoffel et al. 2010). The field site consists of thirty-five 80 · 80 m (0.64 ha) permanent plots distributed across a 280-ha forest landscape. Each plot contains three circular subplots of 0.05, 0.14 and 0.23 ha. Forty-two permanent 4-m2 quadrats were established in each plot within the small (n = 10), medium (n = 16) and large (n = 16) subplots (Fig. 2). For this study, we focus on

pre-treatment data from a subsample of nine plots representative of the variation in overstorey composition and structure encountered at the site. We used a random subsample of 24 quadrats from each of the selected plots (n = 4, 7 and 13 from the small, medium and large subplots, respectively; n = 215; one plot with 23 quadrats). This subsample was selected for more intensive sampling of environmental variables because it was an economically and logistically feasible sample size. The overstorey includes one major age class of 70- to 90-year-old northern hardwoods dominated by sugar maple (Acer saccharum), basswood (Tilia americana) and white ash (Fraxinus americana), although scattered trees exceeding 100 years of age can be found (Table 1; all nomenclature follows the Flora of North America Editorial Committee 1993+). Soils are silt loams (Glossudalfs) of the Magnor, Ossmer and Freeon series overlaying dense till, all of which are subjected to seasonally perched (Magnor and Freeon) or high (Ossmer) water tables. The Ossmer series is relatively well drained compared to the Magnor and Freeon series, and distributed among lower elevations across the site, although the elevation gradient is subtle (c. 20 m of relief among the subplots in this analysis). To index variability in the local microclimate (e.g. attributable to soil series as well as local topography), subplot elevation, slope and aspect data were gathered from a digital elevation model (30 m resolution). January and July daily high temperatures (1980–1997) average )12 and 19 C, respectively (Daymet U.S. Data Center, http:// daymet.org), and the median length of the growing season is 105 frost-free days (base temperature = 0 C, 1971–2000, Midwest Regional Climate Center, http://mcc.sws.uiuc.edu).

FIELD DATA COLLECTION

Fig. 1. Location of study site in north-central Wisconsin. Inset shows location within the eastern USA.

Fig. 2. Plot detail with subplot and quadrat layout. Quadrats are distributed along cardinal axes within subplots. Quadrats are 2 · 2 metres (4 m2) and spatially integrate fine-scale measurements of forest structure, microclimate, plant communities and soil properties. Subplot sizes correspond to experimental gap treatments addressed in subsequent studies.

Ground-layer vegetation sampling was conducted in the spring (midApril – late-May) and midsummer (mid-June – late-July) in 2006 to account for all vascular plant species, which vary in leafing phenology. During each survey, the percentage cover of all vascular plant taxa 1–2.5%, >2.5– 5%, >5–15%, >15–25%, >25–50%, >50–75%, >75–95%, >95 to < 100%, and 100% (e.g. Gauch 1982). Classes included the range of values that is greater than the lower bound and equal to or less than the upper bound. Seasonal data sets were merged, retaining the largest cover classes when species were observed during multiple sampling periods. Cover classes were converted to mid-points for all analyses. In the midsummer survey, in addition to cover estimates, tree seedlings and saplings (