Clonal plants in disturbed mountain forests: Heterogeneity enhances ramet integration
Introduction
Clonal plants are extremely modular organisms that may effectively move through space foraging for resources, have the potential to share resources through an integrated system, can forestall the risks and costs of sexual reproduction, and are able to perpetuate locally well-adapted genotypes (Hutchings and Wijesinghe, 1997; Liu et al., 2016). These characteristics confer an advantage to clonal plants over nonclonal plants under heterogeneous resource conditions (Alpert, 1999; You et al., 2014). On the other hand, clonal plants are expected to allocate more resources to seeds when long-distance spreading is advantageous (Eriksson, 1997), under high probability of establishing seeds in newly formed gaps (Olejniczak, 2001) and under high local ramet density (Olejniczak, 2003). Spatial mosaic of microhabitats may impose limits to vegetative growth promoting seed production, but when ramet's growth increases as a concave function of resource level, the maintenence of integrated ramets should be favored (Caraco and Kelly, 1991). For these reasons, predicting the prevalence of vegetative reproduction in ecosystems of different disturbance regimes may not be straightforward, but how do we link this known advantage to disturbance regimes of ecosystems (Herben et al., 2018), especially when many of those regimes are changing and synergistic (Lucash et al., 2018)? Here we examine clonal plant response to disturbance focusing on the heterogeneity and species diversity created by the disturbance, potentially an underlying mechanism of clonal plant response, in an effort to improve our ability to manage public lands in the face of changing disturbance regimes in the Tatra Mountains (Western Carpathians), Slovakia and Poland.
Perhaps the best-studied characteristic of clonal plants is their physiological integration among ramets and its implications (Watson, 1986; Slade and Hutchings, 1987; Alpert and Stuefer, 1997; Schenk et al., 2008; Liu et al., 2016). Physiological integration and clonal growth allow for more plastic responses to, as well as specialization of, different modules to different conditions (Alpert and Stuefer, 1997) rendering advantages under high habitat heterogeneity, limited resources, and disturbance. Plastic module acclimation in non-clonal plants is also common but tends to be more subtle and much more difficult to study. Clonal plants that remain integrated have the capacity to both forage for resources and share those resources within a genet (Slade and Hutchings, 1987). Foraging occurs by increasing allocation to modules that acquire resources in high-resource areas; e.g., more ramets in open forest patches or more branching of rhizomes in nutrient-rich soils (Wijesinghe and Hutchings, 1997). Local resource surpluses are then shared across physiologically integrated modules. In this way, integrated clonal plants can place some ramets in high-stress environments that offer a particular resource, such as areas of high-light availability on beach sand (Alpert, 1999), where non-clonal plants would not be able to survive. Resource sharing is also ecologically relevant due to the economies of scale that are possible, such as developing an extensive root system benefiting multiple stems that individually could only support a much smaller root network. Such a system allows for ‘nursing’ of juvenile ramets (Araki and Kunii, 2008). Physiological integration also offers advantages when under attack from herbivores. Clonal plants appear to have greater compensation following herbivory as ramets share resources (Liu et al., 2007) and may employ early warning systems for induced defenses (Gomez et al., 2008), such as decreasing the palatability of younger ramets.
The interaction between clonal plants and disturbance has long been suggested. There are four responses or behaviors that only clonal plants are capable of, and all may help clonal plants respond to disturbance (Svensson et al., 2013). First, physiological integration may help when disturbance leads to increased heterogeneity of resources. Second, clonal plant’s ability to track resources (i.e., forage) allows them to take advantage of patchy suitable conditions. Third, short-range dispersal can lead to dominance and preeminence of quality patches. Fourth, assuming the clone can survive disturbance, its longevity results in persistence. Such traits confer advantages of clonal plants over nonclonal plants with disturbances like herbivory and with environments that are heterogeneous, but it is unclear if these traits help following other disturbances as clonal plants tend to be less dominant following disturbance (Klimeš et al., 1997). In an examination of plant traits related to disturbance regime in predominantly herbaceous flora, the traits of life span, clonal growth and resprouting showed a stronger relationship with the environment than leaf-height-seed traits (Herben et al., 2018).
Past research strongly suggests that clonal plants have advantages when local (within the scale of a genet) resources are heterogeneous, and that such advantage is lost when resources are homogeneous. The type of disturbance will ultimately determine local heterogeneity. While large-scale disturbance often lead to large-scale heterogeneity on the landscape (Kulakowski and Veblen, 2003), local areas may be homogenous. Part of this response stems from the general lack of dispersal ability of clonal plants that evolutionarily has given them more advantage in short-dispersal scenarios (Nakamaru et al., 2014) and local survival of disturbance rather than invasion subsequent to disturbance (Zobel and Antos, 2007).
Taken together, the type of disturbance and scale of disturbance will determine local heterogeneity, and thus potentially the response of clonal plants to disturbance. With climate change leading to changes in disturbance regimes, it is important to know relationships among plants and disturbance types for prediction and management (Kruhlov et al., 2018; Nolan et al., 2018). Knowing that clonal plants often make up more than 60% of vegetation communities (e.g., Klimešová and Doležal, 2011), understanding the dynamics of clonal plants is imperative.
We hypothesized that the dominance of clonal plants would be greatest in communities with the greatest structural (and thus resource) heterogeneity, and hypothesized that forest gap communities and disturbed sites left for natural regeneration would have the greatest heterogeneity. In addition, we examined the extent of clonal integration of forbs, grasses, and shrubs in canopy and large windthrow areas. We predicted that integration would be greatest for all growth forms in sites with the greatest local heterogeneity.
Section snippets
Sites and resource heterogeneity
Strong recent windstorms have occurred in the Tatra National Park in the Western Carpathians of Slovakia and Poland, Central Europe (Budzáková et al., 2013): 2004 and 2014. Both have impacted the Tatras ecosystem (Czortek et al., 2018; Potterf et al., 2019). Almost all portions of this blowdown were subsequently affected by spruce beetle outbreak or rarely burned as well. We examined these recent windthrows in two forms: those that were salvage logged and those not salvage logged; i.e., natural
Sites, temperature variability and resource heterogeneity
All plots showed temperature dynamics over the growing season. Windthrown plots that had been salvaged (DS) averaged the highest mean temperatures while natural forest plots (NF), natural gaps (NG) and windthrown plots naturally recovering (DR) averaged cooler temperatures (Fig. 2). Temperatures in canopy closed forest (NF) showed the most stable environment. Naturally-recovering windthrow plots (DR) were the most variable within any day in Poland – northern part of the Tatra Mountains (Fig. 1
Discussion
We examined clonal plant response to disturbance at both the community and population levels of recent large windthrows in the Tatra Mountains, Slovakia and Poland. We hypothesized that the dominance of clonal plants would be greatest in communities with the greatest structural (and thus resource) heterogeneity and temperature variation, and that clonal integration would be greatest for all growth forms in sites with the greatest local heterogeneity. First, heterogeneity did differ among
Author contribution
SBF, JS and PO contributed equally throughout the study, including initial concept, data collection and analysis, and manuscript preparation. ES and JN helped collect most of the data and provided initial analyses. MS and TB modeled the heterogeneity and temperature components of the study and helped revise the manuscript.
Acknowledgements
Authors would like to thank the University of Northern Colorado for funding the sabbatical of SBF and a portion of this research. Authors would also like to thank Slovak Academy of Science’s Institute of Botany(projects nr. VEGA 0119/19 and APVV 16-0431) and Polish Academy of Science’s Institute of Nature Conservationfor their collaboration and partial funding of this research. Andrzej Antoł helped in collecting data at Polish study plots.
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