Belowground plant functional ecology: Towards an

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Received: 14 February 2018 Accepted: 13 May 2018 DOI: 10.1111/1365-2435.13145

REVIEW

Belowground plant functional ecology: Towards an integrated perspective Jitka Klimešová1,2

| Jana Martínková1

1 Department of Functional Ecology, Institute of Botany, Czech Academy of Sciences, Třeboň, Czech Republic 2

Department of Botany, Faculty of Science, Charles University, Praha, Czech Republic Correspondence Gianluigi Ottaviani, Department of Functional Ecology, Institute of Botany, Czech Academy of Sciences, Dukelská 135, Třeboň, 37982, Czech Republic. Email: [email protected] Funding information Centre of Excellence PLADIAS, Grant/Award Number: 14-36079G and 16-19245S Handling Editor: Katie Field

| Gianluigi Ottaviani1

Abstract 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 lessstudied 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 tradeoffs 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. KEYWORDS

acquisitive and nonacquisitive compartments, belowground plant functions, biomass allocation and turnover, buds and carbohydrates storage, growth forms, ontogeny, rhizomes, roots

Functional Ecology. 2018;1–12.

wileyonlinelibrary.com/journal/fec © 2018 The Authors. Functional Ecology | 1 © 2018 British Ecological Society

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Functional Ecology 2

1 | I NTRO D U C TI O N

KLIMEŠOVÁ et al.

individual rhizomes and roots of particular species is indeed rare, and for herbaceous communities, it is virtually impossible (but

Functional ecology is experiencing a booming interest focused on

see Pecháčková, During, Rydlová, & Herben, 1999). Nevertheless,

root traits and associated acquisitive function which were largely

thanks to recent progresses in molecular techniques, this problem

overlooked until recent years (Bardgett, Mommer, & De Vries, 2014;

has become increasingly solvable even for herbaceous communities

Weiher et al., 1999). In several key papers, new research lines and

(Herben et al., 2018; Hiiesalu et al., 2012; Mommer, Wagemaker, de

questions have been introduced, where conceptual and method-

Kroon, & Ouborg, 2008). A consequence of the coring procedure

ological problems have been discussed (Freschet & Roumet, 2017;

is the fragmentation of belowground organs so that information on

McCormack et al., 2015, 2017). Novel frontiers in belowground

their position (in relation to the original location of different organs

research have been proposed by Laliberté (2017) who defined six

belowground) is lost during the sampling process (Larreguy, Carrera,

areas in which plant ecologists should concentrate future efforts,

& Bertiller, 2011; Vaness, Wilson, & MacDougall, 2014). As soil-core

namely redefining fine roots, integrating mycorrhizas, broadening

sampling is an unavoidably destructive procedure, issues remain

the suite of root traits, upscaling belowground functional ecology

whether the research targets to obtain time-series data, such as bio-

from species to ecosystem level, quantifying root traits dimension-

mass allocation over time. However, while limitations and challenges

ality and determining trait–environment linkages. These studies,

remain, in this work we provide possible solutions and suggestions

along with other recent research focused on roots functionality (e.g.,

on how to deal with these methodological problems.

Iversen et al., 2017; McCormack, Adams, Smithwick, & Eissenstat,

Here, we aim at unifying the “fine-root-centred” point of view as

2012; Valverde-Barrantes, Freschet, Roumet, & Blackwood, 2017;

recently presented by Laliberté (2017), Freschet and Roumet (2017)

Weemstra et al., 2016), have been and remain useful in guiding and

and McCormack et al. (2017) with our “all-belowground-organs”

encouraging plant ecologists to considering belowground plant

viewpoint. We envision a comprehensive approach designed for

parts.

belowground plant ecology which considers different plant organs

Despite the advances made in root ecology, our understanding

(e.g., roots, rhizomes, tubers, bulbs) and functions (e.g., resource ab-

of the functioning of belowground plant organs other than roots re-

sorption, space occupancy, storage) simultaneously. In this review,

mains scarce. Belowground plant organs are not only those related

we provide first a synthetic overview of the array of different be-

to roots, but include leaf- and stem-derived organs, such as bulbs

lowground plant functions exerted by different organs. Second, we

and rhizomes. These coarse organs may account for a large pro-

define a compartment-based conceptual scheme, that is, associated

portion of biomass allocated below the soil surface (e.g., Ringselle,

with biomass allocation into different functions. Third, we describe

Prieto-Ruiz, Andersson, Aronsson, & Bergkvist, 2017; Šťastná,

the ecological relevance of considering plant biomass allocation into

Klimeš, & Klimešová, 2010) playing important functional roles. For

belowground structures and compartments, and the role of bio-

example, rhizomes, tubers and bulbs provide herbs with the ability

mass turnover. At last, we identify future research directions where

to grow clonally and regenerate (Klimeš, Klimešová, Hendriks, & van

using the proposed compartment-based approach would be highly

Groenendael, 1997), having potentially positive effects on plant sur-

relevant.

vival. 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

2 | B E LOWG RO U N D PL A NT FU N C TI O N S : A N I NTEG R ATE D OV E RV I E W

clone parts rooting under different soil and microclimatic conditions (Stuefer, 1998). At last, even when ecologists would decide to focus

Seeds buried in soils germinate towards two opposite poles: roots

only on roots, they cannot completely neglect the fact that roots

from one pole grow geotropically, while shoots from another pole

may deploy other functions than the acquisitive one, such as storage

grow heliotropically. Therefore, roots are normally located below-

of resources and buds, connection among ramets, and anchorage

ground and shoots aboveground—with exceptions, such as lianas,

(Groff & Kaplan, 1988; Klimeš & Klimešová, 1999).

epiphytes or aquatic plants. A young root is unbranched and presents

So far, the possibility to investigate the entire set of plant organs

root hairs (or associations with mycorrhizas) absorbing resources in

located belowground has been hindered by methodological prob-

soil. As the root grows and starts branching, only its tips and young-

lems. Aboveground, we can generally identify individuals, functional

est branches are able to acquire water and nutrients, whereas older

units, organs and traits. In contrast, recognition of organs belong-

root parts serve as supporting and conducting structures. In general,

ing to one individual plant is not so straightforward belowground.

only the first three orders of root branches (i.e., the youngest ones)

In herbaceous species and communities, roots and rhizomes are

in trees, and fine roots in herbs are considered acquisitive—although

intermingled with soil and with each other (intra- and interspecif-

this distinction is arbitrary (Freschet & Roumet, 2017; Weemstra

ically) and there is not a simple, direct method to separate them.

et al., 2016). Old and thick roots often cease resource absorption

Most commonly used practices to collect belowground organs

but, at the same time, they exert other key functions, namely con-

are i) coring of soil samples and ii) observing fine roots growth in

necting belowground with aboveground plant organs, anchoring

rhizotrons (Gregory, 2008; Hutchings & John, 2003). Tracking

plants to the soil and stocking carbon (Kleyer & Mindén, 2015).

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KLIMEŠOVÁ et al.

F I G U R E 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 This basic functional scheme of shoots and roots is preserved in

To use and occupy the belowground space for stocking carbo-

trees and annual plants (Figure 1a,b). However, for perennial herbs

hydrates, plants may (a) exploit roots and/or (b) employ specialized

and shrubs, belowground is also the place where plants are safe

stem-derived organs, for example, rhizomes (Klimešová & Klimeš,

from disturbances (e.g., fire, mowing, grazing; Dalgleish & Hartnett,

2008). Such stems need adaptations to grow belowground especially

2009; Klimešová & Klimeš, 2007; Pausas, Lamont, Paula, Appezzato-

during early stages of plant ontogeny, namely geotropic growth or

da-Glória, & Fidelis, 2018) or climatic adversities (e.g., drought, frost;

contractile roots pulling stem-derived organs under the soil surface

Raunkiaer, 1934; VanderWeide & Hartnett, 2015)—see Figure 1c,d.

(Putz, 2002, 2006).

In this safe belowground space, plants can accumulate carbohy-

Similar to carbohydrates storage, buds can be stored below-

drates and reserve buds that could be then used for resprouting, that

ground where they are protected against disturbances. Plants gen-

is, to restore the aboveground biomass following its removal (Clarke

erally store and accumulate buds on stem-derived organs (Klimešová

et al., 2013; Klimešová & Klimeš, 2007).

& Klimeš, 2007; Pausas et al., 2018), sometimes also on root-derived

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organs (Bartušková, Malíková, & Klimešová, 2017). Positioning of

KLIMEŠOVÁ et al.

(Figure 2). We define two major belowground compartments in rela-

buds, therefore, does influence plant ability to cope with different

tion to biomass allocation. The first is the acquisitive compartment as-

disturbance severities (Bartušková & Klimešová, 2010; Malíková,

sociated with the absorptive function (for an exhaustive description on

Šmilauer, & Klimešová, 2010).

this topic refer to Freschet & Roumet, 2017), whereas the second is the

The ability to store buds and carbohydrates belowground can

nonacquisitive compartment, informing on additional functions than

generate multistemmed growth forms, that is, perennial herbs, shrubs

absorption (Figure 2). The nonacquisitive compartment can be divided

or trees (Figure 1c). Aboveground plant parts in these growth forms

into i) structural and ii) nonstructural subcompartments. The former

are younger than belowground parts that can persist for the whole

relates mainly to the functions of plant persistence and anchorage,

plant life, ensuring the plant occupancy of a given spot (James, 1984;

resprouting ability, and, in clonal plants, of resource transport among

Midgley, 1996). Genet longevity in those plants is limited by longevity

different ramets and space occupancy (Figure 2). The latter refers pre-

of the primary root (Klimešová, Nobis, & Herben, 2015). This limitation

dominantly to the amount and type of storage compounds plants can

can be overcome when the belowground stems are able—in addition to

accumulate (e.g., several types of carbohydrates are found in different

the primary root—to produce other roots (i.e., adventitious) or if roots

storage organs; Janeček, Lanta, Klimešová, & Doležal, 2011), allelopa-

are able to produce shoots (Groff & Kaplan, 1988). The capacity to pro-

thy, plant–soil feedbacks, protection against drought, frost (Figure 2).

duce adventitious roots is connected with plant ability to progressively

What becomes evident from visually inspecting Figure 2 is that if

abandon old roots for new ones. This process has the potential to gen-

we limit belowground plant ecology research to the acquisitive organs,

erate multiple rooting units (Aarssen, 2008), so giving rise to clonal

compartment and function, we will be telling the belowground plant

multiplication and to lateral spreading (Figure 1d) which can have large

ecology story partially. If other organs and nonacquisitive compart-

ecological impacts. Clonal plants are indeed able to change position in

ments are overlooked, we will miss the chance to improve the ecolog-

a community by moving horizontally, placing new rooting units through

ical understanding of different key functions, as well as their relations

clonal spacers— that is, rhizomes, stolons or roots with adventitious

and trade-offs. This is particularly valid for the nonacquisitive func-

buds—far from maternal plants, potentially finding more benign micro-

tions—but indirectly also for acquisition (Figure 2). We provide two

environments (Klimešová, Martínková, & Herben, 2018).

examples to further elucidate how these different functions and their

To sum up, belowground plant functions are numerous, that is,

compartments are interconnected and may affect each other.

not only acquisition, involving different organs which can largely

With the first example, we show one of the existing, yet poorly

differ across ontogenetic stages and among growth forms (Figure 1).

understood relationships occurring between nutrient absorption and

Detailed information about abundance of different growth forms

persistence in disturbed systems. There is broad evidence emphasiz-

across regions and biomes is scarce, limiting our understanding

ing the interplay between nutrient availability and plant resprouting

of how these understudied functions are common and relevant

ability (Bellingham & Sparrow, 2000; Clarke et al., 2013). Plants from

world-wide. We know the percentage of woody plants species is

nutrient-poor habitats tend to behave as resprouters more often than

estimated to be 43%–48% globally (FitzJohn et al., 2014; Raunkiaer,

plants from nutrient-rich communities (Bellingham & Sparrow, 2000;

1934), and annuals are hypothesized to represent about 13% of the

Poorter et al., 2012). At the same time, plants experiencing nutrient

world flora (Raunkiaer, 1934). In addition, the estimated propor-

scarcity recover and resprout (from belowground buds, using carbo-

tion of clonal plants at global scale is far from complete, and we

hydrates storage) less vigorously or less frequently after damage than

can currently rely on information gained from regional floras only.

plants found in nutrient-rich conditions (Clarke & Knox, 2009; Wise

For example, data for Central Europe show that 53% of species are

& Abrahamson, 2007). These findings call for further research aimed

clonal (Klimešová, Danihelka, Chrtek, de Bello, & Herben, 2017), in

at disentangling the relationships and possible trade-offs between

China approximately 40% (Ye et al., 2016), while in Australia only

nutrient availability (using traits relevant to resource acquisition) and

9% of species are clonal (Zhang, Bonser, Chen, Hitchcock, & Moles,

resprouting ability (using traits related to bud bank, resource storage).

2017). Furthermore, grassy biomes such as tropical savanna, tem-

The second example deals with clonal plants that employ struc-

perate steppe or arctic tundra—which are most likely hosting an

tures enabling lateral spread and connection among ramets. These

even higher proportion of clonal species compared to the above-

abilities promote plants to explore and share nutrients under resource

mentioned examples—remain largely overlooked in terms of clonal

limitation. There are three hypotheses addressing this task: (a) clonal

data. Therefore, we recommend to expanding the knowledge about

plants may actively forage for nutrients in heterogeneous soils by

the less-known belowground plant functions and organs across dif-

placing ramets preferentially in nutrient-rich patches (He, Alpert, Yu,

ferent growth forms, ontogenetic stages and regions.

Zhang, & Dong, 2011; Xie, Song, Zhang, Pan, & Dong, 2014); (b) clonal plants can transport and relocate limiting resources from ramets

3 | TH E CO M PA RTM E NT- B A S E D A PPROAC H

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

We suggest that the delimitation of functions associated with below-

plants thanks to connections between their perennial rhizome and

ground organs can be done according to belowground compartments

root systems (Jónsdóttir & Watson, 1997). In addition, clonal and

KLIMEŠOVÁ et al.

nonclonal plants differ in their fine root architecture (Šmilauerová

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allocate to aboveground vs. belowground compartments. Root:

& Šmilauer, 2007) and growth plasticity (Weiser, Koubek, & Herben,

shoot ratio may serve as a good example of an “all-belowground-

2016). Therefore, we can expect some relationships and trade-offs

organs” viewpoint. The root: shoot ratio is generally considered a

between the acquisitive function vs. growth and functioning of clonal

reliable measure of a plant investment into acquisition of below-

network, and these aspects should be further examined.

ground (e.g., H2O and nutrients) vs. aboveground resources (e.g., light and CO2; Bloom, Chapin, & Mooney, 1985; Poorter et al., 2012,

4 | B I O M A S S A LLO C ATI O N A N D T U R N OV E R 4.1 | Biomass allocation

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

A widely exploited estimate for plant investment into various func-

(e.g., associated with carbohydrates storage function in fire-prone

tions is biomass partitioning, namely how much carbon plants

regions; James, 1984; Guerrero-C ampo, Palacio, Perez-Rontome,

F I G U R E 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)

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KLIMEŠOVÁ et al.

& 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 eco-

F I G U R E 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)

systems, belowground organs of species composing these communities are intermingled (with each other and with soil), making the

et al., 2011). The amount of carbohydrates allocated into storage or-

biomass quantification virtually impossible at species level (but see

gans depends upon specific plant responses to disturbance (e.g., fire,

Pecháčková et al., 1999; Mommer et al., 2008; Herben et al., 2018).

grazing), climate seasonality, elevation (Clarke, Manea, & Leishman,

Pot experiments do not solve the problem as they are usually limited

2016; Dvorský et al., 2015). Mechanisms behind these relations are

short-term studies, while the development of rhizomes and carbohy-

still debated, since different ecological causes may generate the cor-

drates storage may require several years.

relation between amount of storage and abiotic drivers (Martínez-

Another challenge is the completeness of the belowground bio-

Vilalta et al., 2016). One interpretation is that storage compounds

mass collected during sampling. For example, the recommended sam-

serve either as carbon or as energy resource after plant damage or as

pling depth for temperate grasslands is 30 cm (Mokany et al., 2006).

osmotic protection against drought, frost hence operating as an ef-

This depth, while sufficient for sampling the entire rhizome biomass

fective strategy to cope with demanding environments (de Moraes,

which is typically concentrated in the upper soil layers (Šťastná et al.,

de Carvalho, Franco, Pollock, & Figueiredo-Ribeiro, 2016). Another,

2010), is not enough for harvesting fine root data comprehensively

contrasting view sees the accumulation of photosynthates into be-

(Jackson, Canadell, Mooney, Sala, & Schulze, 1996; Schenk & Jackson,

lowground organs as a by-product, due to plants inability to use them

2002). This is observable from biomass data collected for fine roots

for growing in response to nutrient shortage or cold stress (Chapin,

and rhizomes of herbaceous communities in temperate Central Europe

Schulze, & Mooney, 1990; Kozlowski, 1992; Martínez-Vilalta et al.,

(Figure 3). From there, fine root biomass increases isometrically with

2016). To disentangle the relative role of different environmental

aboveground biomass (slope of fine root vs. aboveground biomass ~1;

factor on resource storages, we would need novel experimental ap-

Figure 3). On the contrary, rhizome biomass increases allometrically

proaches controlling for various abiotic conditions.

with aboveground biomass (slope of rhizome vs. aboveground biomass

Concluding, we recommend to (a) consider more refined indica-

~2; Figure 3). Since the entire biomass of rhizomes is generally collected

tors of plant biomass partitioning related to different belowground

by sampling at a depth of ~ 30 cm, we can assume that the observed

compartments, using, for example, fine root: rhizome ratio in con-

allometric relation between rhizomes and aboveground biomass is re-

junction with root: shoot ratio, (b) enlarge the belowground sampling

alistic. However, the isometric relationship between fine root and abo-

effort, for example by sampling deeper to better account for fine

veground biomass may be due to, or blurred by sampling limitations.

root biomass, and (c) design suitable experiments aimed at unrav-

The least known compartment of belowground plant organs is the nonstructural subcompartment. Comparative analyses of car-

elling the role of different ecological drivers in plant allocation into carbohydrates storage.

bohydrates 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,

4.2 | Biomass turnover

2007). From there, it emerges that herbs and shrubs have 10%–40%

The estimation of belowground biomass belonging to different com-

of carbohydrates biomass in belowground storage organs (Janeček

partments without considering biomass turnover can lead towards

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KLIMEŠOVÁ et al.

ecological misinterpretation of results (for details, see McCormack

The fact that longevity of belowground organs varies consid-

et al., 2015). Indeed, biomass decay and turnover can mask plant al-

erably in herbs is well known to researchers studying clonal plants

location into distinct functions—for example, differences in carbon

(Figure 5). Plants with long-lived rhizomes may have an ecological

sequestration among different belowground compartments over

advantage when growing in stressful environments over plants hav-

time. In trees and annual herbs, longevity of coarse belowground

ing short-lived rhizomes, because older rhizomes can develop larger

organs is equal to that of aboveground parts (Figure 1). For peren-

systems of belowground organs to harvest and share resources

nial herbs growing in temperate climates, longevity of belowground

(Jónsdóttir & Watson, 1997; Klimeš, 2008; Klimeš et al., 1997).

parts exceeds that of aboveground biomass which is annual by defi-

Information on fine roots (and sampling consistency) is far

nition (Figure 1). Estimating the age of coarse roots and rhizomes in

greater and more refined for woody species than for herbaceous

herbs with secondary thickening is feasible by anatomically evaluat-

plant species and communities (Lauenroth & Gill, 2003; McCormack

ing cross sections of annual growth rings (herbchronology; Poschlod

et al., 2012; Weemstra et al., 2016). Fine roots turnover in woody

& Schweingruber, 2005). In the case of regularly branched below-

plants is generally lower than in herbs. Furthermore, among herba-

ground stems, morphological marks on the surface of the rhizomes

ceous species, low-latitude plants are characterized by faster turn-

are assessed (e.g., Šťastná, Klimešová, & Doležal, 2012). Results

over than those in high latitudes (Lauenroth & Gill, 2003). Also, data

obtained using these techniques reveal that rhizomes and coarse

for fine roots turnover in herbaceous plants are usually gathered

roots of herbs may persist from 1 year to several decades (Nobis &

at community scale, because distinguishing fine roots turnover at

Schweingruber, 2013). Despite the recent advances made in herb-

species level is hard. Although recent successful attempts to accu-

chronology, there is still a vast number of plant species for which

rately assess age of fine roots exist (e.g., Sun, Li, McCormack, Ma, &

these methods cannot be used since no annual rings are distinguish-

Guo, 2016), they are very laborious, time-consuming and therefore

able and/or no regular branching of rhizome is observable. Under

restricted to a small number of species. We propose that an upper

these circumstances, we have approximate-only estimates based

limit to root longevity, yet not completely accurate and not always

on plant demography and morphology, for example by using knowl-

applicable, could be posed and quantified indirectly by dating the

edge about speed of clonal spread per year, and clone size (Klimeš

stem-derived parts from which roots are growing. Based on morpho-

& Klimešová, 2005; de Witte & Stöcklin, 2010). These estimates

logical observations from CLO-PLA database for Central European

show that the majority of herbs in temperate regions have their

species (Figure 5), oldest parts of rhizomes very often have living

belowground bud-bearing organs (rhizomes, bulbs, tubers) persist-

roots (Klimešová & Klimeš, 2006). Roots on old rhizomes are still

ing for several years and that species with optima at different posi-

able to absorb water and nutrients (then transported and shared

tions along environmental gradients greatly vary in their persistence

among ramets), hence are functionally active organs (d’Hertefeldt

(Figure 4). Evaluation of biomass turnover in nonseasonal climates

& Jónsdóttir, 1999). Notwithstanding, we argue that these old, yet

remains, however, an unresolved challenge because ring formation

functioning rhizomes are a good proxy for assessing the longevity

does not occur.

and turnover of fine roots growing on them.

F I G U R E 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)

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KLIMEŠOVÁ et al.

F I G U R E 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) Issues occur also when assessing turnover of carbohydrates

predict that studies considering belowground biomass allocation

storage because such reserves have different turnover rate than the

and turnover may emerge as an important research-line in ecosys-

biomass of the organ in which they are stocked (Bartoš et al., 2011;

tem functioning and global change biology science.

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,

5 | FU T U R E D I R EC TI O N S

from 20% to 70% per year (based on data from Janeček et al., 2011). In addition, more detailed information about time oscillations of carbo-

The main target of this review was to provide an integrated perspec-

hydrates allocation in storage organs can be obtained by isotope label-

tive for the booming research-field of belowground plant ecology

ling (e.g., Blessing, Werner, Siegwolf, & Buchmann, 2015; Nkurunziza

that, in our view, has not yet considered all the relevant belowground

& Streibig, 2011). Overall, the turnover rate and short-term carbo-

plant functions and organs. While for the acquisitive compartment

hydrates’ dynamics occurring belowground reflect the aboveground

(e.g., fine roots, mycorrhizal associations), comparable methodologies

plant growth and its changes caused by seasonality and disturbance

for collecting traits are becoming available (e.g., Freschet & Roumet,

(Bartoš et al., 2011; Werger & Huber, 2006). Gaining more detailed

2017; McCormack et al., 2017), this is not the case for the nonac-

information on such eco-physiological relationships may assist in bet-

quisitive belowground compartment (e.g., clonal and storage organs).

ter understanding plant strategies related to carbohydrates storage.

Therefore, there is an urgent need for standardized procedures de-

At last, we suggest that assessing biomass allocation and turn-

scribing how to collect and assess traits related to nonacquisitive

over, while challenging, could be effectively scaled from community

functions (Ottaviani, Martínková, Herben, Pausas, & Klimešová,

up to ecosystem level (McCormack et al., 2017) by implementing

2017).

the proposed compartment-based approach. For example, studies

Summing up—in addition to the specific directions provided at

on carbon sequestration generally neglect contribution of below-

the end of each paragraph—we identify four major research areas

ground biomass and consequently its role in ecosystem services is

linking acquisitive and nonacquisitive belowground compartments

overlooked (e.g., Cornelissen, Song, Yu, & Dong, 2014). We therefore

that could be readily explored (with examples of research questions):

|


KLIMEŠOVÁ et al.

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.

AC K N OW L E D G E M E N T S 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.

AU T H O R S ’ C O N T R I B U T I O N S 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 ACC E S S I B I L I T Y This research used data available in CLO-PLA3 database and published in the manuscript by Fiala, Tůma, and Holub (2012).

ORCID Jitka Klimešová Jana Martínková Gianluigi Ottaviani

http://orcid.org/0000-0003-0123-3263 http://orcid.org/0000-0001-8158-0577 http://orcid.org/0000-0003-3027-4638

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S U P P O R T I N G I N FO R M AT I O N Additional supporting information may be found online in the Supporting Information section at the end of the article.

How to cite this article: Klimešová J, Martínková J, Ottaviani G. Belowground plant functional ecology: Towards an integrated perspective. Funct Ecol. 2018;00:1–12. https://doi. org/10.1111/1365-2435.13145