Belowground plant functional ecology: Towards an integrated perspective

Abstract

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1. In recent years, belowground plant ecology has experienced a booming interest. This has resulted in major advances towards a greater understanding of belowground plant and ecosystem functioning focused on fine roots, mycorrhizal associations and nutrient acquisition.
2. Despite this, other important functions (e.g., on-spot persistence, space occupancy, resprouting after biomass removal) exerted by different belowground plant organs (e.g., roots, rhizomes, bulbs) remain largely unexplored.
3. Here, we propose a framework providing a comprehensive perspective on the entire set of belowground plant organs and functions. We suggest a compartment-based approach. We identify two major belowground compartments, that is, acquisitive and nonacquisitive, associated with biomass allocation into these functions. Also, we recommend the nonacquisitive compartment to be divided into structural (e.g., functional roles carried out by rhizomes, such as sharing of resources, space occupancy) and nonstructural (e.g., functional roles exerted by carbohydrates reserve affecting resprouting ability, protection against climate adversity) subcompartments. We discuss methodological challenges—and their possible solutions—posed by changes in biomass allocation across growth forms and ontogenetic stages, and in relation to biomass partitioning and turnover.
4. We urge the implementation of methods and approaches considering all the belowground plant compartments. This way, we would make sure that key, yet less-studied functions would be incorporated into the belowground plant ecology research agenda. The framework has potential to advance the understanding of belowground plant and ecosystem functioning by considering relations and trade-offs between different plant functions and organs. At last, we identify four major areas where using the proposed compartment-based approach would be particularly important, namely (a) biomass scaling, (b) clonality-resource acquisition relations, (c) linkages between resprouting and changing environmental conditions and (d) carbon sequestration.

A plain language summary is available for this article.

Foreign Language Abstract Funkční ekologie podzemních částí rostlinSummary in Czech

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V posledních letech zažívá ekologie podzemních částí rostlin velký zájem výzkumníků po celém světě. Tento zájem přispěl k lepšímu porozumění funkce podzemních částí rostlin, zejména jemných kořenů a mykorhizy, které hrají významnou roli při získávání vody a živin. Jiné důležité funkce rostlin, jako je přežívání na daném místě, obsazování prostoru, nebo schopnost regenerace po poškození těla, zprostředkované například zásobními kořeny a oddenky, však zůstávají opomíjeny. S cílem napravit tuto situaci, navrhujeme integrovaný přístup, který umožní komplexnější pohled na celou řadu podzemních rostlinných orgánů a jejich funkcí. Na příkladech z literatury ukazujeme, jak zaměření pouze na jemné kořeny může omezit naši schopnost poznat ekologii rostlin. Navrhujeme přístup založený na rozlišení základních funkčních specializací podzemních orgánů. Identifikujeme dva hlavní funkční podzemní kompartmenty, za prvé akviziční, tj. podílející se na získávání vody a živin, a za druhé neakviziční, tj. podílející se na propojování různých částí rostliny, na klonálním růstu a na regeneraci po narušení. Diskutujeme metodologické problémy spojené s implementací tohoto přístupu a o jejich možných řešeních. Přestavujeme rozdíly v investicích do těchto podzemních kompartmentů u různých růstových forem a během života rostliny, stejně tak problémy související se stanovením biomasy a jejím obratem. Závěrem vyzýváme výzkumníky, aby při studium ekologie aplikovali metody a přístupy, které berou v úvahu všechny podzemní orgány rostlin. Pouze tímto způsobem zajistíme, aby méně studované, avšak zcela klíčové funkce podzemních orgánů rostlin, byly začleněny do výzkumného plánu funkčních ekologů. Příkladem může být jejich využití pro lepší odhad sekvestrace uhlíku v podzemních orgánech rostlin, což je důležité pro tvorbu celosvětových geochemických modelů.

1 INTRODUCTION

Functional ecology is experiencing a booming interest focused on root traits and associated acquisitive function which were largely overlooked until recent years (Bardgett, Mommer, & De Vries, 2014; Weiher et al., 1999). In several key papers, new research lines and questions have been introduced, where conceptual and methodological problems have been discussed (Freschet & Roumet, 2017; McCormack et al., 2015, 2017). Novel frontiers in belowground research have been proposed by Laliberté (2017) who defined six areas in which plant ecologists should concentrate future efforts, namely redefining fine roots, integrating mycorrhizas, broadening the suite of root traits, upscaling belowground functional ecology from species to ecosystem level, quantifying root traits dimensionality and determining trait–environment linkages. These studies, along with other recent research focused on roots functionality (e.g., Iversen et al., 2017; McCormack, Adams, Smithwick, & Eissenstat, 2012; Valverde-Barrantes, Freschet, Roumet, & Blackwood, 2017; Weemstra et al., 2016), have been and remain useful in guiding and encouraging plant ecologists to considering belowground plant parts.

Despite the advances made in root ecology, our understanding of the functioning of belowground plant organs other than roots remains scarce. Belowground plant organs are not only those related to roots, but include leaf- and stem-derived organs, such as bulbs and rhizomes. These coarse organs may account for a large proportion of biomass allocated below the soil surface (e.g., Ringselle, Prieto-Ruiz, Andersson, Aronsson, & Bergkvist, 2017; Šťastná, Klimeš, & Klimešová, 2010) playing important functional roles. For example, rhizomes, tubers and bulbs provide herbs with the ability to grow clonally and regenerate (Klimeš, Klimešová, Hendriks, & van Groenendael, 1997), having potentially positive effects on plant survival. These organs also affect roots’ capacity to absorb water and nutrients because, for example, rhizomes may determine root spatial placement and longevity (Jónsdóttir & Watson, 1997). Rhizomes may also assist in translocating acquired resources among different clone parts rooting under different soil and microclimatic conditions (Stuefer, 1998). At last, even when ecologists would decide to focus only on roots, they cannot completely neglect the fact that roots may deploy other functions than the acquisitive one, such as storage of resources and buds, connection among ramets, and anchorage (Groff & Kaplan, 1988; Klimeš & Klimešová, 1999).

So far, the possibility to investigate the entire set of plant organs located belowground has been hindered by methodological problems. Aboveground, we can generally identify individuals, functional units, organs and traits. In contrast, recognition of organs belonging to one individual plant is not so straightforward belowground. In herbaceous species and communities, roots and rhizomes are intermingled with soil and with each other (intra- and interspecifically) and there is not a simple, direct method to separate them. Most commonly used practices to collect belowground organs are i) coring of soil samples and ii) observing fine roots growth in rhizotrons (Gregory, 2008; Hutchings & John, 2003). Tracking individual rhizomes and roots of particular species is indeed rare, and for herbaceous communities, it is virtually impossible (but see Pecháčková, During, Rydlová, & Herben, 1999). Nevertheless, thanks to recent progresses in molecular techniques, this problem has become increasingly solvable even for herbaceous communities (Herben et al., 2018; Hiiesalu et al., 2012; Mommer, Wagemaker, de Kroon, & Ouborg, 2008). A consequence of the coring procedure is the fragmentation of belowground organs so that information on their position (in relation to the original location of different organs belowground) is lost during the sampling process (Larreguy, Carrera, & Bertiller, 2011; Vaness, Wilson, & MacDougall, 2014). As soil-core sampling is an unavoidably destructive procedure, issues remain whether the research targets to obtain time-series data, such as biomass allocation over time. However, while limitations and challenges remain, in this work we provide possible solutions and suggestions on how to deal with these methodological problems.

Here, we aim at unifying the “fine-root-centred” point of view as recently presented by Laliberté (2017), Freschet and Roumet (2017) and McCormack et al. (2017) with our “all-belowground-organs” viewpoint. We envision a comprehensive approach designed for belowground plant ecology which considers different plant organs (e.g., roots, rhizomes, tubers, bulbs) and functions (e.g., resource absorption, space occupancy, storage) simultaneously. In this review, we provide first a synthetic overview of the array of different belowground plant functions exerted by different organs. Second, we define a compartment-based conceptual scheme, that is, associated with biomass allocation into different functions. Third, we describe the ecological relevance of considering plant biomass allocation into belowground structures and compartments, and the role of biomass turnover. At last, we identify future research directions where using the proposed compartment-based approach would be highly relevant.

2 BELOWGROUND PLANT FUNCTIONS: AN INTEGRATED OVERVIEW

Seeds buried in soils germinate towards two opposite poles: roots from one pole grow geotropically, while shoots from another pole grow heliotropically. Therefore, roots are normally located belowground and shoots aboveground—with exceptions, such as lianas, epiphytes or aquatic plants. A young root is unbranched and presents root hairs (or associations with mycorrhizas) absorbing resources in soil. As the root grows and starts branching, only its tips and youngest branches are able to acquire water and nutrients, whereas older root parts serve as supporting and conducting structures. In general, only the first three orders of root branches (i.e., the youngest ones) in trees, and fine roots in herbs are considered acquisitive—although this distinction is arbitrary (Freschet & Roumet, 2017; Weemstra et al., 2016). Old and thick roots often cease resource absorption but, at the same time, they exert other key functions, namely connecting belowground with aboveground plant organs, anchoring plants to the soil and stocking carbon (Kleyer & Mindén, 2015).

This basic functional scheme of shoots and roots is preserved in trees and annual plants (Figure 1a,b). However, for perennial herbs and shrubs, belowground is also the place where plants are safe from disturbances (e.g., fire, mowing, grazing; Dalgleish & Hartnett, 2009; Klimešová & Klimeš, 2007; Pausas, Lamont, Paula, Appezzato-da-Glória, & Fidelis, 2018) or climatic adversities (e.g., drought, frost; Raunkiaer, 1934; VanderWeide & Hartnett, 2015)—see Figure 1c,d. In this safe belowground space, plants can accumulate carbohydrates and reserve buds that could be then used for resprouting, that is, to restore the aboveground biomass following its removal (Clarke et al., 2013; Klimešová & Klimeš, 2007).

Figure 1

Schematic representation of biomass allocation and turnover across four growth forms of terrestrial plants. (a) tree, (b) annual herb, (c) perennial nonclonal herb, (d) perennial clonal herb. The four examples are based on authors’ observations and on Mokany et al. (2006). For simplicity, schemes b–d depict herbs in seasonal climates with aboveground parts persisting for 1 year, while aboveground organs in tropical herbs may last for longer (not showed). Similar growth forms to c and d may be exhibited by woody resprouters where aboveground parts persist for more years, but only belowground parts are able to survive severe damages (e.g., caused by fire) and are therefore longer lived than aboveground parts

To use and occupy the belowground space for stocking carbohydrates, plants may (a) exploit roots and/or (b) employ specialized stem-derived organs, for example, rhizomes (Klimešová & Klimeš, 2008). Such stems need adaptations to grow belowground especially during early stages of plant ontogeny, namely geotropic growth or contractile roots pulling stem-derived organs under the soil surface (Putz, 2002, 2006).

Similar to carbohydrates storage, buds can be stored belowground where they are protected against disturbances. Plants generally store and accumulate buds on stem-derived organs (Klimešová & Klimeš, 2007; Pausas et al., 2018), sometimes also on root-derived organs (Bartušková, Malíková, & Klimešová, 2017). Positioning of buds, therefore, does influence plant ability to cope with different disturbance severities (Bartušková & Klimešová, 2010; Malíková, Šmilauer, & Klimešová, 2010).

The ability to store buds and carbohydrates belowground can generate multistemmed growth forms, that is, perennial herbs, shrubs or trees (Figure 1c). Aboveground plant parts in these growth forms are younger than belowground parts that can persist for the whole plant life, ensuring the plant occupancy of a given spot (James, 1984; Midgley, 1996). Genet longevity in those plants is limited by longevity of the primary root (Klimešová, Nobis, & Herben, 2015). This limitation can be overcome when the belowground stems are able—in addition to the primary root—to produce other roots (i.e., adventitious) or if roots are able to produce shoots (Groff & Kaplan, 1988). The capacity to produce adventitious roots is connected with plant ability to progressively abandon old roots for new ones. This process has the potential to generate multiple rooting units (Aarssen, 2008), so giving rise to clonal multiplication and to lateral spreading (Figure 1d) which can have large ecological impacts. Clonal plants are indeed able to change position in a community by moving horizontally, placing new rooting units through clonal spacers— that is, rhizomes, stolons or roots with adventitious buds—far from maternal plants, potentially finding more benign microenvironments (Klimešová, Martínková, & Herben, 2018).

To sum up, belowground plant functions are numerous, that is, not only acquisition, involving different organs which can largely differ across ontogenetic stages and among growth forms (Figure 1). Detailed information about abundance of different growth forms across regions and biomes is scarce, limiting our understanding of how these understudied functions are common and relevant world-wide. We know the percentage of woody plants species is estimated to be 43%–48% globally (FitzJohn et al., 2014; Raunkiaer, 1934), and annuals are hypothesized to represent about 13% of the world flora (Raunkiaer, 1934). In addition, the estimated proportion of clonal plants at global scale is far from complete, and we can currently rely on information gained from regional floras only. For example, data for Central Europe show that 53% of species are clonal (Klimešová, Danihelka, Chrtek, de Bello, & Herben, 2017), in China approximately 40% (Ye et al., 2016), while in Australia only 9% of species are clonal (Zhang, Bonser, Chen, Hitchcock, & Moles, 2017). Furthermore, grassy biomes such as tropical savanna, temperate steppe or arctic tundra—which are most likely hosting an even higher proportion of clonal species compared to the above-mentioned examples—remain largely overlooked in terms of clonal data. Therefore, we recommend to expanding the knowledge about the less-known belowground plant functions and organs across different growth forms, ontogenetic stages and regions.

3 THE COMPARTMENT-BASED APPROACH

We suggest that the delimitation of functions associated with belowground organs can be done according to belowground compartments (Figure 2). We define two major belowground compartments in relation to biomass allocation. The first is the acquisitive compartment associated with the absorptive function (for an exhaustive description on this topic refer to Freschet & Roumet, 2017), whereas the second is the nonacquisitive compartment, informing on additional functions than absorption (Figure 2). The nonacquisitive compartment can be divided into i) structural and ii) nonstructural subcompartments. The former relates mainly to the functions of plant persistence and anchorage, resprouting ability, and, in clonal plants, of resource transport among different ramets and space occupancy (Figure 2). The latter refers predominantly to the amount and type of storage compounds plants can accumulate (e.g., several types of carbohydrates are found in different storage organs; Janeček, Lanta, Klimešová, & Doležal, 2011), allelopathy, plant–soil feedbacks, protection against drought, frost (Figure 2).

Figure 2

Illustration of the two major belowground plant compartments, acquisitive and nonacquisitive—further subdivided into structural and nonstructural—and associated belowground functions of plant economy, persistence and stress tolerance. Functions described by Freschet and Roumet (2017) are in light-grey boxes; dark-grey boxes indicate plant compartmentalization and associated functions as proposed in this manuscript. Trait nomenclature follows CLO-PLA (Freschet & Roumet, 2017; Klimešová et al., 2017; de Kroon & Visser, 2003). Italics in cells reports examples of traits considered useful to examine specific belowground plant compartments and functions (see also Ottaviani et al., 2017)

What becomes evident from visually inspecting Figure 2 is that if we limit belowground plant ecology research to the acquisitive organs, compartment and function, we will be telling the belowground plant ecology story partially. If other organs and nonacquisitive compartments are overlooked, we will miss the chance to improve the ecological understanding of different key functions, as well as their relations and trade-offs. This is particularly valid for the nonacquisitive functions—but indirectly also for acquisition (Figure 2). We provide two examples to further elucidate how these different functions and their compartments are interconnected and may affect each other.

With the first example, we show one of the existing, yet poorly understood relationships occurring between nutrient absorption and persistence in disturbed systems. There is broad evidence emphasizing the interplay between nutrient availability and plant resprouting ability (Bellingham & Sparrow, 2000; Clarke et al., 2013). Plants from nutrient-poor habitats tend to behave as resprouters more often than plants from nutrient-rich communities (Bellingham & Sparrow, 2000; Poorter et al., 2012). At the same time, plants experiencing nutrient scarcity recover and resprout (from belowground buds, using carbohydrates storage) less vigorously or less frequently after damage than plants found in nutrient-rich conditions (Clarke & Knox, 2009; Wise & Abrahamson, 2007). These findings call for further research aimed at disentangling the relationships and possible trade-offs between nutrient availability (using traits relevant to resource acquisition) and resprouting ability (using traits related to bud bank, resource storage).

The second example deals with clonal plants that employ structures enabling lateral spread and connection among ramets. These abilities promote plants to explore and share nutrients under resource limitation. There are three hypotheses addressing this task: (a) clonal plants may actively forage for nutrients in heterogeneous soils by placing ramets preferentially in nutrient-rich patches (He, Alpert, Yu, Zhang, & Dong, 2011; Xie, Song, Zhang, Pan, & Dong, 2014); (b) clonal plants can transport and relocate limiting resources from ramets growing in more benign (e.g., richer) patches to ramets found in more stressful (e.g., poorer) places through clonal spacers (Derner & Briske, 1998; Stuefer, 1998; Yu, Wang, He, Chu, & Dong, 2008); and (c) clonal plants harvest limiting soil resources over larger areas than nonclonal plants thanks to connections between their perennial rhizome and root systems (Jónsdóttir & Watson, 1997). In addition, clonal and nonclonal plants differ in their fine root architecture (Šmilauerová & Šmilauer, 2007) and growth plasticity (Weiser, Koubek, & Herben, 2016). Therefore, we can expect some relationships and trade-offs between the acquisitive function vs. growth and functioning of clonal network, and these aspects should be further examined.

4 BIOMASS ALLOCATION AND TURNOVER

4.1 Biomass allocation

A widely exploited estimate for plant investment into various functions is biomass partitioning, namely how much carbon plants allocate to aboveground vs. belowground compartments. Root: shoot ratio may serve as a good example of an “all-belowground-organs” viewpoint. The root: shoot ratio is generally considered a reliable measure of a plant investment into acquisition of belowground (e.g., H₂O and nutrients) vs. aboveground resources (e.g., light and CO₂; Bloom, Chapin, & Mooney, 1985; Poorter et al., 2012, 2015). However, in relation to the proposed compartment-based perspective, the root: shoot ratio appears to be a rough proxy, because it mixes different biomass compartments and functions (Mokany, Raison, & Prokushkin, 2006). For example, the core of trees’ belowground biomass consists of nonacquisitive thick roots (e.g., associated with carbohydrates storage function in fire-prone regions; James, 1984; Guerrero-Campo, Palacio, Perez-Rontome, & Monserrat-Martí, 2006). In herbs, the belowground biomass is partly formed by storage and bud-bearing stem-derived organs and partly by fine roots (Werger & Huber, 2006). Rather than weighing the belowground and aboveground biomass as per the root: shoot ratio, we suggest to considering the different belowground plant compartments separately, that is, biomass partitioning into acquisitive vs. nonacquisitive parts. This goal can be achieved by separating and weighing the individual organs related to different belowground compartments, such as fine roots (acquisitive compartment) and rhizomes, thick roots (nonacquisitive compartment). After analysing storage carbohydrates in coarse organs by standard methods (Janeček et al., 2011), nonstructural subcompartment could be also determined, that is, the proportion of biomass allocated into coarse organ(s) that is represented by storage compounds such as starch (Bartoš, Janeček, & Klimešová, 2011; Janeček et al., 2015).

Evaluating biomass partitioning into their respective belowground compartments for individual species has many unresolved challenges. Although the assessment can be relatively straightforward for trees and herbs growing individually (e.g., in pot experiments; Poorter et al., 2015), this could be problematic for communities such as meadows, steppes. In these herbaceous ecosystems, belowground organs of species composing these communities are intermingled (with each other and with soil), making the biomass quantification virtually impossible at species level (but see Pecháčková et al., 1999; Mommer et al., 2008; Herben et al., 2018). Pot experiments do not solve the problem as they are usually limited short-term studies, while the development of rhizomes and carbohydrates storage may require several years.

Another challenge is the completeness of the belowground biomass collected during sampling. For example, the recommended sampling depth for temperate grasslands is 30 cm (Mokany et al., 2006). This depth, while sufficient for sampling the entire rhizome biomass which is typically concentrated in the upper soil layers (Šťastná et al., 2010), is not enough for harvesting fine root data comprehensively (Jackson, Canadell, Mooney, Sala, & Schulze, 1996; Schenk & Jackson, 2002). This is observable from biomass data collected for fine roots and rhizomes of herbaceous communities in temperate Central Europe (Figure 3). From there, fine root biomass increases isometrically with aboveground biomass (slope of fine root vs. aboveground biomass ~1; Figure 3). On the contrary, rhizome biomass increases allometrically with aboveground biomass (slope of rhizome vs. aboveground biomass ~2; Figure 3). Since the entire biomass of rhizomes is generally collected by sampling at a depth of ~ 30 cm, we can assume that the observed allometric relation between rhizomes and aboveground biomass is realistic. However, the isometric relationship between fine root and aboveground biomass may be due to, or blurred by sampling limitations.

Figure 3

Relationship between fine roots and rhizomes biomass and aboveground biomass (model II linear regression). Data sourced from Czech temperate meadow communities (data from Fiala et al., 2012)

The least known compartment of belowground plant organs is the nonstructural subcompartment. Comparative analyses of carbohydrates allocated into belowground storage organs by modern methods are restricted to a handful of studies (e.g., Dvorský et al., 2015; Janeček et al., 2011; Palacio, Maestro, & Montserrat-Martí, 2007). From there, it emerges that herbs and shrubs have 10%–40% of carbohydrates biomass in belowground storage organs (Janeček et al., 2011). The amount of carbohydrates allocated into storage organs depends upon specific plant responses to disturbance (e.g., fire, grazing), climate seasonality, elevation (Clarke, Manea, & Leishman, 2016; Dvorský et al., 2015). Mechanisms behind these relations are still debated, since different ecological causes may generate the correlation between amount of storage and abiotic drivers (Martínez-Vilalta et al., 2016). One interpretation is that storage compounds serve either as carbon or as energy resource after plant damage or as osmotic protection against drought, frost hence operating as an effective strategy to cope with demanding environments (de Moraes, de Carvalho, Franco, Pollock, & Figueiredo-Ribeiro, 2016). Another, contrasting view sees the accumulation of photosynthates into belowground organs as a by-product, due to plants inability to use them for growing in response to nutrient shortage or cold stress (Chapin, Schulze, & Mooney, 1990; Kozlowski, 1992; Martínez-Vilalta et al., 2016). To disentangle the relative role of different environmental factor on resource storages, we would need novel experimental approaches controlling for various abiotic conditions.

Concluding, we recommend to (a) consider more refined indicators of plant biomass partitioning related to different belowground compartments, using, for example, fine root: rhizome ratio in conjunction with root: shoot ratio, (b) enlarge the belowground sampling effort, for example by sampling deeper to better account for fine root biomass, and (c) design suitable experiments aimed at unravelling the role of different ecological drivers in plant allocation into carbohydrates storage.

4.2 Biomass turnover

The estimation of belowground biomass belonging to different compartments without considering biomass turnover can lead towards ecological misinterpretation of results (for details, see McCormack et al., 2015). Indeed, biomass decay and turnover can mask plant allocation into distinct functions—for example, differences in carbon sequestration among different belowground compartments over time. In trees and annual herbs, longevity of coarse belowground organs is equal to that of aboveground parts (Figure 1). For perennial herbs growing in temperate climates, longevity of belowground parts exceeds that of aboveground biomass which is annual by definition (Figure 1). Estimating the age of coarse roots and rhizomes in herbs with secondary thickening is feasible by anatomically evaluating cross sections of annual growth rings (herbchronology; Poschlod & Schweingruber, 2005). In the case of regularly branched belowground stems, morphological marks on the surface of the rhizomes are assessed (e.g., Šťastná, Klimešová, & Doležal, 2012). Results obtained using these techniques reveal that rhizomes and coarse roots of herbs may persist from 1 year to several decades (Nobis & Schweingruber, 2013). Despite the recent advances made in herbchronology, there is still a vast number of plant species for which these methods cannot be used since no annual rings are distinguishable and/or no regular branching of rhizome is observable. Under these circumstances, we have approximate-only estimates based on plant demography and morphology, for example by using knowledge about speed of clonal spread per year, and clone size (Klimeš & Klimešová, 2005; de Witte & Stöcklin, 2010). These estimates show that the majority of herbs in temperate regions have their belowground bud-bearing organs (rhizomes, bulbs, tubers) persisting for several years and that species with optima at different positions along environmental gradients greatly vary in their persistence (Figure 4). Evaluation of biomass turnover in nonseasonal climates remains, however, an unresolved challenge because ring formation does not occur.

Figure 4

Persistence of rhizomes in relation to species optimum environment, that is, humidity (a), nutrients (b), light requirements (c) as inferred from Ellenberg values (1992). Data from Central Europe, based on more than 1,000 species. Persistence categories follow morphological classification as per CLO-PLA (Klimešová et al., 2017)

The fact that longevity of belowground organs varies considerably in herbs is well known to researchers studying clonal plants (Figure 5). Plants with long-lived rhizomes may have an ecological advantage when growing in stressful environments over plants having short-lived rhizomes, because older rhizomes can develop larger systems of belowground organs to harvest and share resources (Jónsdóttir & Watson, 1997; Klimeš, 2008; Klimeš et al., 1997).

Figure 5

Persistence categories of belowground organs in the clonal herbs Rumex thyrsiflorus (a), Cicerbita alpina (b) and Calamagrostis epigejos (c). The arrow indicates plant and organ age indexed according to a sliding colour gradient from dark to light representing, at its extremes, old and young belowground structures, respectively. Dotted lines denote soil surface. Persistence categories are based on morphological characteristics of species as per CLO-PLA (Klimešová et al., 2017)

Information on fine roots (and sampling consistency) is far greater and more refined for woody species than for herbaceous plant species and communities (Lauenroth & Gill, 2003; McCormack et al., 2012; Weemstra et al., 2016). Fine roots turnover in woody plants is generally lower than in herbs. Furthermore, among herbaceous species, low-latitude plants are characterized by faster turnover than those in high latitudes (Lauenroth & Gill, 2003). Also, data for fine roots turnover in herbaceous plants are usually gathered at community scale, because distinguishing fine roots turnover at species level is hard. Although recent successful attempts to accurately assess age of fine roots exist (e.g., Sun, Li, McCormack, Ma, & Guo, 2016), they are very laborious, time-consuming and therefore restricted to a small number of species. We propose that an upper limit to root longevity, yet not completely accurate and not always applicable, could be posed and quantified indirectly by dating the stem-derived parts from which roots are growing. Based on morphological observations from CLO-PLA database for Central European species (Figure 5), oldest parts of rhizomes very often have living roots (Klimešová & Klimeš, 2006). Roots on old rhizomes are still able to absorb water and nutrients (then transported and shared among ramets), hence are functionally active organs (d’Hertefeldt & Jónsdóttir, 1999). Notwithstanding, we argue that these old, yet functioning rhizomes are a good proxy for assessing the longevity and turnover of fine roots growing on them.

Issues occur also when assessing turnover of carbohydrates storage because such reserves have different turnover rate than the biomass of the organ in which they are stocked (Bartoš et al., 2011; Suzuki & Hutchings, 1997). Evidence from Central European temperate grasslands shows that biomass turnover rate of carbohydrates storage (formula from Lauenroth & Gill, 2003) may vary largely, that is, from 20% to 70% per year (based on data from Janeček et al., 2011). In addition, more detailed information about time oscillations of carbohydrates allocation in storage organs can be obtained by isotope labelling (e.g., Blessing, Werner, Siegwolf, & Buchmann, 2015; Nkurunziza & Streibig, 2011). Overall, the turnover rate and short-term carbohydrates’ dynamics occurring belowground reflect the aboveground plant growth and its changes caused by seasonality and disturbance (Bartoš et al., 2011; Werger & Huber, 2006). Gaining more detailed information on such eco-physiological relationships may assist in better understanding plant strategies related to carbohydrates storage.

At last, we suggest that assessing biomass allocation and turnover, while challenging, could be effectively scaled from community up to ecosystem level (McCormack et al., 2017) by implementing the proposed compartment-based approach. For example, studies on carbon sequestration generally neglect contribution of belowground biomass and consequently its role in ecosystem services is overlooked (e.g., Cornelissen, Song, Yu, & Dong, 2014). We therefore predict that studies considering belowground biomass allocation and turnover may emerge as an important research-line in ecosystem functioning and global change biology science.

5 FUTURE DIRECTIONS

The main target of this review was to provide an integrated perspective for the booming research-field of belowground plant ecology that, in our view, has not yet considered all the relevant belowground plant functions and organs. While for the acquisitive compartment (e.g., fine roots, mycorrhizal associations), comparable methodologies for collecting traits are becoming available (e.g., Freschet & Roumet, 2017; McCormack et al., 2017), this is not the case for the nonacquisitive belowground compartment (e.g., clonal and storage organs). Therefore, there is an urgent need for standardized procedures describing how to collect and assess traits related to nonacquisitive functions (Ottaviani, Martínková, Herben, Pausas, & Klimešová, 2017).

Summing up—in addition to the specific directions provided at the end of each paragraph—we identify four major research areas linking acquisitive and nonacquisitive belowground compartments that could be readily explored (with examples of research questions):

1. Biomass scaling: How are acquisitive vs. nonacquisitive belowground compartments related to aboveground plant biomass? How does this relationship change during ontogeny and in response to environmental forces?
2. Clonality vs. resource acquisition: Is there a trade-off between lateral spread and rooting depth? Does lateral spread interact with mycorrhizas and fine roots for resource-foraging? Is resource-sharing among ramets more relevant in heterogeneous soils than in homogeneous soils and in nutrient-poor environments than in nutrient-rich environments?
3. Resprouting vs. environmental conditions: Can we distinguish carbohydrates accumulated as a result of reduced growth from carbohydrates stored specifically for resprouting? How do plants respond to damage of belowground organs caused by herbivory, drought, or frost?
4. Carbon sequestration: How does longevity of belowground organs influence carbon cycling? Are plants able to reutilize storage carbohydrates from decaying belowground organs? If so, does the degree of carbohydrates reutilization depend on environmental conditions?

Addressing these key issues could largely broaden our understanding of belowground plant ecology and ecosystem functioning, particularly about relationships and trade-offs operating among different compartments, organs, traits and ultimately functions.

ACKNOWLEDGEMENTS

This research was supported by the Grant Agency of the Czech Republic (Centre of Excellence PLADIAS, 14-36079G and 16-19245S). We thank Tomáš Herben and James L. Tsakalos for providing insightful comments on previous versions of the manuscript and for improving the English language of the manuscript. We thank also anonymous referees and Journal editors for offering invaluable suggestions.

AUTHORS’ CONTRIBUTIONS

J.K. conceived the research idea and wrote the first draft of the manuscript. J.M. and G.O. assisted in developing and refining the research. All the co-authors significantly contributed to revisions.

DATA ACCESSIBILITY

This research used data available in CLO-PLA3 database and published in the manuscript by Fiala, Tůma, and Holub (2012).