# Belowground persistence types relevant to severe disturbance

Jitka Klimešová, Daniel C Laughlin, Frances Siebert, Joana Bergmann, Shersingh Joseph Tumber-Dávila, Karl Andraczek, Aline B Bombo, Helge Bruelheide, Ying Fan, Grégoire T Freschet, et al.

► To cite this version:

Jitka Klimešová, Daniel C Laughlin, Frances Siebert, Joana Bergmann, Shersingh Joseph Tumber-Dávila, et al. Belowground persistence types relevant to severe disturbance. Trends in Plant Science, 2025, 30 (9), pp.992 - 1001. 10.1016/j.tplants.2025.06.010. hal-05240019

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Highlights

* Strategies of terrestrial plants to cope with disturbance can be classified based on the whole plant body, including belowground organs.

* On the basis of relative longevity of above- and belowground parts and the whole genet, we distinguish six plant functional types.

* The categories can be distinguished with a binary dichotomous key using existing information on woodiness, clonal growth capacity, and resprouting capacity.

* The new system will open new avenues of research in functional ecology, especially in disturbance-driven ecosystems.
1 Belowground persistence types relevant to severe
disturbance

3 Jitka Klimešová¹, Daniel C. Laughlin², Frances Siebert³, Joana Bergmann⁴, Shersingh Joseph

4 Tumber-Dávila⁵, Karl Andraczek⁶, Aline B. Bombo⁷, Helge Bruelheide⁸,⁶, Ying Fan⁹, Grégoire

5 T. Freschet¹⁰, Justus Hennecke¹¹, Cody Coyotee Howard¹², Saheed O. Jimoh², Liesje

6 Mommer¹³, Tsumbedzo Ramalevha¹⁴, Alexandra Weigelt¹⁵, Alessandra Fidelis¹⁶

7
8
9Department of Experimental and Functional Ecology, Institute of Botany Czech Academy of Sciences, Třeboň; Department of Botany, Faculty of Science, Charles University, Praha, Czech Republic; Orcid: 0000-0003-0123-3263

10
2Department of Botany, University of Wyoming, Laramie, WY 82071, USA

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3Unit for Environmental Sciences and Management, North-West University, South Africa

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⁴Leibniz Centre for Agricultural Landscape Research (ZALF), Müncheberg, Germany; Orcid: 0000-0002-2008-4198

13
⁵Department of Environmental Studies, Dartmouth College, Hanover, NH 03755, USA; Orcid: 0000-0001-7336-3943

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6German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Puschstr. 4, 04103 Leipzig; Systematic Botany
15
and Functional Biodiversity, Institute of Biology, Leipzig University, Leipzig, Germany; Leibniz Centre for Agricultural
16
Landscape Research (ZALF), Germany; Orcid: 0000-0002-2711-3326

17
⁷Lab of Vegetation Ecology, Instituto de Biociências, Universidade Estadual Paulista (UNESP), Rio Claro, Brazil; Orcid: 0000-0002-2292-4031

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⁸Institute of Biology/Geobotany and Botanical Garden, Martin Luther University Halle-Wittenberg, Am Kirchtor 1, 06108
20
Halle, Germany

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⁹Department of Earth and Planetary Sciences, Rutgers University, New Brunswick, NJ, USA; Orcid: 0000-0002-0024-7965

22
¹⁰Theoretical and Experimental Ecology Station, CNRS, Moulis, France; Orcid: 0000-0002-8830-3860

23
¹¹German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Puschstr. 4, 04103 Leipzig, and Systematic
24
Botany and Functional Biodiversity, Institute of Biology, Leipzig University, Leipzig, Germany

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¹²Department of Plant Biology, Ecology, and Evolution, Oklahoma State University, Stillwater, Oklahoma, USA; Orcid: 0000-0001-7662-9102

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¹³Forest Ecology and Forest Management Group, Wageningen University, The Netherlands; Orcid: 0000-0002-3775-0716

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¹⁴Unit for Environmental Sciences and Management, North West University, South Africa; Orcid: 0000-0002-9719-6243

29
¹⁵German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Puschstr. 4, 04103 Leipzig, and Systematic
30
Botany and Functional Biodiversity, Institute of Biology, Leipzig University, Leipzig, Germany

31
¹⁶Lab of Vegetation Ecology, Instituto de Biociências, Universidade Estadual Paulista (UNESP), Rio Claro, Brazil

32 Correspondence: [Jitka.Klimesova@ibot.cas.cz](mailto:Jitka.Klimesova@ibot.cas.cz) (Klimešová)

33

34 **Keywords**

35 clonality, lifespan, longevity, resprouting ability, seeder, woodiness

36

37 **Glossary**

38 **Avoidance** (in the context of severe disturbance): Plant strategy to survive a disturbance event by avoiding it in time (i.e., dormancy) or space (i.e., small stature)

40 **Bud bank**: Dormant meristems located on plant body parts hidden from disturbance, usually
41 belowground or aboveground but protected by bark

42 **Bud bearing organ**: Plant organs that house the bud banks and keep them alive for resprouting; these include aboveground stems protected by bark, belowground stems, rhizomes, tubers, and roots

45 **Bud protection**: Plant strategy to protect buds from damage, such as by growing thick bark
46 or by growing them belowground in soil

47 **Clonal growth organs**: Plant organs that enable lateral spread and multiplication (production of ramets), e.g. rhizomes
49 **Clonal plant**: Plants that reproduce vegetatively by producing offspring (ramets) through
50 vegetative growth and are genetically identical (forming a genet)

51 **Disturbance**: Events that damage plant parts (usually aboveground), such as fire and grazing.

52 We consider as 'severe' those disturbances events that remove all aboveground plant
53 biomass and often cause high mortality

54 **Genet**: A plant established from one zygote; it may be non-clonal plant or all physically
55 disconnected parts (rooting units) produced by clonal plant (and genetically identical)

56 **Herbaceous**: Plants that do not produce woody tissues aboveground and have no persistent
57 stems aboveground

58 **Plant economics spectrum**: A theoretical framework based on functional traits that
59 encompasses a gradient from fast-growing, short-lived species to slow-growing, long-lived
60 species

61 **Ramet**: A part of the genet that is capable of independent physical existence when
62 disconnected from the rest of a clone

63 **Resistance** (in the context of severe disturbance): Plant strategy for surviving disturbance
64 events by minimizing their impact, such as protecting plant tissues from damage, includes
65 adaptations like thick bark to resist fire or thorns to deter grazing

66 **Resprouter**: Plant species that survive severe disturbances (e.g., fire, grazing, flooding,
67 mowing) by resprouting from protected bud banks after partially or totally losing their
68 aboveground parts

69 **Seeder**: Population persistence relies on regeneration from seed banks

70 **Storage carbohydrates**: Carbohydrates accumulated in specialized (usually belowground)
71 storage organs, which may also bear bud banks

72 **Storage organs**: Plant (usually belowground) organs that store resources (mainly
73 carbohydrates) for resprouting after disturbance or dormancy, such as tubers or bulbs

74 **Tolerance** (in the context of severe disturbance): Plant strategy to survive a disturbance
75 event by losing aboveground parts and producing new ones by resprouting from storage and
76 bud-bearing organs usually located belowground

77 **Woody**: Plant that produces woody tissues, usually seen aboveground but also developed
78 belowground. The "wood" is not only formed by a secondary xylem produced by a vascular
79 cambium but also including lignified primary tissues (like in palms or bamboo)

80
81 Abstract

Despite recent advances in plant trait ecology, we identified a knowledge gap in understanding how plants strategize to cope with severe and recurrent disturbances. We propose a new classification system based on three hierarchical binary attributes: (i) woodiness, reflecting longevity of plant structures, (ii) clonality, indicating the ability to regenerate from both aboveground and belowground organs, and (iii) resprouting ability, referring to the ability to replace aboveground organs. This framework results in six Belowground Persistence Types (BPTs): 1—herbaceous seeder, 2—herbaceous non-clonal resprouter, 3—herbaceous clonal resprouter, 4—woody seeder, 5—woody non-clonal resprouter, and 6—woody clonal resprouter. This proposed classification system opens new avenues for research, especially concerning plant distributions in a world experiencing increasingly frequent and severe disturbance events.

93

94 Former disturbance-based life-form classifications

Recent advances in functional ecology have increased our understanding of plant adaptations to resource availability and their consequences for plant growth [1-5]. However, in addition to well-known trade-offs such as acquisition versus conservation of resources, plant form and function have also been shaped by major disturbances such as fire, grazing, flooding that destroy significant amounts of the plant's biomass. The functional traits for leaves and fine-roots, such as specific leaf area (SLA) and specific root length (SRL) that define the plant economic spectrum, do not capture how plants respond to severe disturbances [6], pinpointing a knowledge gap in our understanding of plant form and function.

Some of the functional traits that may help to understand plant strategies for persisting under different disturbance regimes, are already known (Table 1), but coherent usage across ecosystems and disturbance regimes is missing. For example, the size and depth of the bud bank are key traits relevant to disturbance [7,8] but the available studies using bud-bank traits are known from disturbance-prone tropical grasslands [9-11] and temperate grazed grasslands [12-14], but such trait information is missing in other ecosystems. Another example are storage carbohydrates, a necessary source of energy for resprouting after damage [15] which are scarcely studied in relation to disturbance; the majority of studies are focused on woody resprouters [16-19]. Similarly, we have rather limited data restricted to one particular disturbance type about the timing of life history events (e.g., flowering) or distribution of biomass and organs along the vertical axis of the plant, the traits that may help to reduce or avoid the most detrimental disturbance effects [20,21].

Knowing that severe disturbances are a strong agent of selection affecting the whole plant body (usually) from aboveground [22], while belowground organs serve for regeneration (but see [23]), we provide a coherent framework to integrate disturbance-related traits [8,24]. Although numerous plant life form classifications have been described over the past few centuries [25-27], only that of Raunkiaer [28] might be considered relevant to disturbance [29,30], even though the original motivation was to describe how plants survive adverse seasons (e.g., winter or dry season). Raunkiaer [28] categorized plants according to the
122 position of the highest bud on the plant from which seasonal regrowth occurs, representing a
123 spectrum ranging from tall, woody perennials which seasonally renew their biomass from
124 buds aboveground (phanerophytes) to smaller (often herbaceous) plants with renewal buds
125 closer to the soil surface or belowground (i.e., chamaephytes, hemicryptophytes, geophytes).
126 However, this classification is not suitable for grouping functional types in disturbance-prone
127 systems as it does not consider that the highest bud might not always be the most relevant
128 for regrowth after disturbance. Here, we propose the first life form classification system that
129 combines aboveground and belowground traits with a specific emphasis on the critical role of
130 belowground organs as adaptations to severe disturbance. For the purpose of this
131 classification, we consider adaptations to severe disturbances only since nearly all plants have
132 the ability to survive partial loss of aboveground biomass due to their modular structures [31].
133

134 A new classification system: Belowground Persistence Type (BPT)

135 We propose to classify terrestrial, vascular plants into six ordinal categories that
136 reflect the lifespan of the genet and adaptation to severe disturbance by investing into
137 belowground persistence. First, the system is based on the absolute lifespan of plant parts,
138 where herbaceous parts are relatively short-lived, and thus, cheaper to construct than
139 woody parts [32-34]. Second, the system integrates the relative lifespan of both
140 aboveground and belowground plant parts within the context of the lifespan of the genet, as
141 this reflects the ability of a plant to replace parts lost by disturbance. The simplest
142 developmental option for a plant is to grow and maintain above- and belowground parts
143 concurrently, and – excluding the short-lived fine-root, leaf, and flower parts – keep them
144 until the end of life and avoid losing them due to disturbance (i.e., the aboveground parts
145 are of the same age as belowground parts and the same age as the genet) [35]. However,
146 under conditions of severe recurrent aboveground disturbances (e.g., fire, grazing, mowing,
147 flooding), a plant may profit from a tolerance strategy by renewing lost parts. This happens
148 when plants adjust their body construction so that it positions resources and buds
149 belowground that otherwise would be located aboveground. The resulting belowground
150 organs enable plants to resprout after the loss of aboveground parts (i.e., belowground parts
151 are older than aboveground parts) [22,31]. Third, under conditions of severe aboveground
152 disturbance that also removes portions of the soil surface, both aboveground and
153 belowground parts may need to be replaced during the lifespan of the genet (i.e., both
154 belowground and aboveground parts are younger than the genet) [24; 35]. In these cases,
155 plants allocate proportionally even larger investments to belowground organs because the
156 plant must produce not only new aboveground parts but also new belowground parts (e.g.,
157 rhizomes and adventitious roots).

158 On the basis of the above-described absolute and relative age relationships, we can
159 distinguish the Belowground Persistence Types (BPTs) using the knowledge of three binary
160 attributes: woodiness, clonality, and resprouting ability (see Box 1 for detailed definitions of
161 each) by asking following questions:
162

(i) Is the plant woody or herbaceous? This is a first-level question because wood is more persistent and costly than herbaceous tissue, so woody plants usually invest more resources into the stem than herbaceous species. Woody plants, such as trees are, therefore, in general longer-lived than herbaceous plants do [32, 36].

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(ii) Is the plant clonal or non-clonal? This is the second-level question as plants produce independent rooting units over the course of their lives. Clonal plants, as a rule, lose the first shoot and root system growing from seed and produce new roots and shoots [37,38]. Above and belowground disturbances that involve damaging belowground biomass (e.g. ground fires, erosion, digging animals) may be detrimental to non-clonal plants that are dependent on their original main root system as they cannot replace it, while clonal plants may regenerate even after a disturbance affecting the soil profile and fragmenting the plant body [39,40].

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(iii) Does the plant have the ability to resprout? In other words, is the plant a seeder (not able to produce new aboveground parts after losing them by disturbance) or a resprouter (able to produce new aboveground parts after losing them by disturbance)? This is the third-level question as resprouting is possible due to bud-bearing organs [31,41], which are mainly located belowground. Seeders usually do not survive disturbances but instead regenerate from a seed bank [42-44]. Importantly, all clonal plants are capable of resprouting, but not all resprouters are clonal [45].

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The binary answers to these three tiered questions lead to six Belowground Persistence Types (BPTs): 1—herbaceous seeder (herbaceous seeders), 2—herbaceous non-clonal resprouter (herbaceous resprouters), 3—herbaceous clonal resprouter (clonal herbs), 4—woody seeder (woody seeders), 5—woody non-clonal resprouter (woody resprouters), and 6—woody clonal resprouter (clonal woody) (Box 1; Figure 1). This classification leads to a natural ordering of growth forms along a hypothesized ordinal gradient of genet lifespan where herbaceous seeders (type 1) are the shortest lived (often annuals) and clonal woody plants (type 6) are the longest living plants. Despite the preliminary evidence listed above, this idea needs further empirical testing, and we acknowledge that genet persistence can vary significantly along a broad gradient within and among the classes [46]. As measurements of plant (genet) age in clonal plants are methodologically challenging [47,48], further testing of the correlation strength between this ordinal classification and plant lifespan will be a future challenge.

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We argue that plants that are woody aboveground also have woody tissues belowground, while plants that are herbaceous aboveground may be non-woody or woody belowground [11]. An increasing knowledge about morphology and anatomy of belowground plant organs, would allow us to distinguish a separate category of plants that are herbaceous aboveground but woody belowground. The belowground woody organs, compared to herbaceous ones, indicate a longer organ lifespan that may be important for dealing with severe disturbance. An example of herbaceous plants that are woody belowground are 'belowground trees', such as *An dira humilis* (Fabaceae), in tropical grasslands (49). This

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strategy lengthens the persistence of their belowground organs compared to fleshy rhizomes [9, 50]. 202
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We note that the proposed classification is relevant to terrestrial vascular plants (i.e., 204 the vast majority of the global flora) with aboveground and belowground plant parts, but 205 excludes some epiphytes and aquatic plants that do not root in the soil. The classification is 206 expected to be relevant at the species level, but in some cases, populations of one species 207 may differ in their BPTs due to nutrient availability, soil type or disturbance history [e.g., 208 209 210

Disturbance regimes and how to describe them 211

To test whether Belowground Persistence Types (BPTs) reflect adaptations to 212 disturbance we need to know the characteristics of disturbance **that are important for** 213 **natural selection**. Disturbance regimes can be described in general terms as events with a 214 certain frequency (e.g., every 2 years), timing (e.g., the dry season), intensity/severity (e.g., 215 low-intensity fires with low temperatures and residence time) and extent (i.e., area 216 affected). However, at the community level, disturbance may be described by its effects on 217 the specific community, particularly the amount or type of biomass removed, area of bare 218 ground created, or number of species killed. Finally, for an individual plant or population, the 219 disturbance regime must be described as events that have a certain frequency and timing 220 regarding their plant individual or population characteristics (e.g., many times in the plant's 221 lifespan, at the time of flowering) as well as severity (e.g., from removing leaves or all 222 aboveground biomass, to impacting belowground tissues as well), and extent (i.e., how 223 224

Although severity, frequency and timing of disturbance measured on the 225 individual/population level might seem to be the most relevant to the question of species 226 adaptations, it has its limitations. Using individual-level definitions of disturbance regime, 227 species in one community may experience different severity of disturbance through, for 228 example, different phenology. Consequently, a BPT that is hypothetically well adapted to 229 severe disturbances are likely to be affected less by a disturbance than a non-adapted 230 species. Therefore, how the disturbance regime is defined depends on the scientific 231 question. When studying the performance of one species in the community (e.g., species 232 demography) it is useful to define disturbance regime in relation to the individual 233 /population but if we study community-level effects (e.g., biomass production, diversity, 234 species composition) we need to use a community-level definition of disturbance regime. 235 Finally, if we want to compare plant strategies (e.g., BPTs) concerning disturbance (e.g., 236 which strategies co-exist), it is necessary to define the disturbance regime as generally as 237 possible ("with respect to disturbance" in Table 2)—this is the approach we use in the 238 following examples. 239

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241 Application of Belowground Persistence Types
This BPT classification system can open new avenues of inquiry in functional ecology. While meant to be most informative to characterize plant strategies relevant in disturbance-prone environments, it also provides complementary information to other existing classification systems (e.g., Raunkiaer life forms [28]; vital attributes [42]; plant functional types [51]; resprouter-seeder scheme [53,54]) and more quantitative synthetic frameworks (e.g., Plant Economics Spectrum [1,4]; plant strategies under competition, stress, and disturbance [2]). We foresee the following applications:

(1) Ecologists can test whether these categories explain plant community composition and diversity patterns in relation to disturbance regimes (Box 2). To encourage progress, we have developed a set of testable hypotheses that predict the relative abundance of each BPT across a variety of disturbance regimes. For example, we predict fire-prone ecosystems with high fire frequency to have fewer herbaceous and woody seeders (Types 1 and 4), and more clonal herbs and clonal woody plants (Types 3 and 6) (for results from temperate flora see [39]). The ordinal classes also reflect an increasing ability to survive disturbance as an individual genet: herbaceous and woody seeders (Types 1 and 4) are at the opposite ends of the gradient of disturbance return time (duration between two consecutive disturbances) due to differences in ontogenetic timing. For example, the woody seeders (Type 4) need decades, while annual plants (Type 1) need only one growing season to complete their life cycle. The resprouters are typical for the middle of the gradient, where disturbance events are not too frequent to prohibit the accumulation of resources in belowground organs (Types 2 and 5). Clonal plants can be found in places with more frequent and severe disturbance than non-clonal resprouters but, due to variability of traits in their belowground organs (e.g., morphological origin, longevity), they inhabit a larger range of the disturbance gradient (Box 2) (for temperate flora see [39]).

(2) The BPT categories may also be useful for understanding resource storage, as resprouting is only possible when the bud bank is accompanied by storage carbohydrates [11]. It is our opinion that the capability to store resources has been overlooked in plant economics theory and is probably independent of carbon acquisition itself [55]. Bud-bearing organs of stem and root origin may directly participate in storage (e.g., rhizomes, lignotubers), or storage could occur in specialized tissues or structures attached to them (e.g., storage leaves in bulbs or root tubers attached to rhizomes). We predict that herbaceous resprouters (Type 2) and woody resprouters (Type 5) store the most resources belowground. Clonal herbaceous plants (Type 3) and clonal woody plants (Type 6) will have intermediate storage capability. Lastly, woody seeders (Type 4) and herbaceous seeders (Type 1) will store the least amount of resources belowground (woody seeders predominantly store resources aboveground).

(3) We expect that the different BPTs impose morphological constraints on other traits, including the plant economics traits of leaves and fine roots. It holds true especially for woody versus herbaceous plants and for resprouters versus seeders [56]. Clonal and non-clonal herbaceous plants may not differ in the most often measured leaf and root acquisitive traits (e.g. specific root length, root diameter, root tissue density, root and leaf nitrogen, specific leaf area, leaf dry matter content; for temperate plants see [56]). Rooting depth and/or root
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lignin content are affected by plant clonality and woodiness [57]. Hence, investing in
belowground storage organs may result in investing less into other functions, for example,
seed production, competitive ability, and overall space occupancy [58].

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(4) Conducting plant trait analyses separately on different BPTs will enable ecologists to test whether plant traits are modified according to the organization of the whole plant body, as proposed earlier by McIntyre et al. [30], where the authors used Raunkiaer life forms. However, since McIntyre et al. [30], we have gained greater knowledge about plant traits, such as bud bank traits that may be useful in understanding trait coordination among and within BPTs. The connection between traits of the plant economics spectrum (e.g., leaf nitrogen concentration, specific leaf area), traits relevant to disturbance (e.g., bud bank size and protection), and our proposed BPTs may deepen our knowledge about environmental factors shaping plant strategies beyond stress, especially resource scarcity, which is the most often studied environmental challenge.

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(5) Similarly to Raunkiaer's life forms, BPTs might help explain changes in plant functional variation occurring along environmental gradients. We can expect that the evolution of different BPTs has been influenced by the seasonality of climate and temperature gradients from the Equator to the Poles [59-61]. Importantly, along this gradient, not only is the temperature changing but also disturbance regimes (e.g., fire frequency). The effects of temperature on plant functional traits are not well understood [62], yet temperature affects many biological processes, such as the formation of wood (or more generally lignification, [63]). Integrating seasonality and broad temperature gradients with BPT is crucial for understanding plant responses to damage from disturbance, especially in relation to climate change and changes in temperature seasonality.

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(6) Testing the relationship between BPTs and plant adaptation to severe disturbance regimes will help us conceptualize not only differences in their distribution but also their coexistence. The coexistence might be enabled because the disturbance regime is never uniform in time and/or space, and, moreover, it might affect plant species in one community differently according to their BPT. For example, herbaceous seeders (Type 1) likely occur most frequently in regions with low fire frequency, whereas plants with the ability to resprout (Types 2–3 and 5–6) may co-occur in varied abundances in regions with moderate to high fire frequency depending on precipitation patterns, and their interactions and timing with fire seasons. Reasoning in terms of BPTs brings about a necessity to thoroughly describe disturbance regimes, including disturbance severity, timing, frequency, and extent [22] (see also preceding section and Table 2).

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The hypothesized relationships described above, while not exhaustive, highlight how
this new classification can improve our understanding of plant ecology by better representing
the global range of plant life forms based on both above- and belowground characteristics.

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321
322 **Concluding remarks**

323 The six Belowground Persistence Types (BPTs) introduced here provide a more holistic
324 perspective on functional ecology. Specifically, we argue that this classification, based on
325 woodiness, resprouting ability and clonality can improve our ability to summarize the above
326 and belowground traits that provide adaptations to disturbance regimes and thus drive plant
327 distribution.

328 This ordinal, simple classification scheme can be easily adopted by experts in plant
329 ecology, but also by non-experts alike, enabling its application across a large diversity of
330 species across the globe. This will promote understanding of variation of plant distribution in
331 different ecosystems, including ones that experience severe and frequent disturbances. In this
332 classification, belowground plant organs play a key role, and should therefore be more
333 thoroughly studied.

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336

337 Acknowledgements

338 This paper is a joint effort of the working group sUnderfoot kindly supported by sDiv, the
339 German Synthesis Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig,
340 funded by the German Research Foundation (FZT 118, 202548816). We are indebted to Alena
341 Bartušková for preparing the figures; JK was supported by Praemium Academiae awarded by
342 Academy of Sciences of the Czech Republic. AF was supported by Fundação de Amparo à
343 Pesquisa do Estado de São Paulo (FAPESP 2023/16620-0), and Conselho Nacional
344 Desenvolvimento Científico e Tecnológico (CNPq 312689/2021-7).

345

346 References

347 1. Wright, I.J. et al. (2004) The worldwide leaf economics spectrum. Nature 428, 821–827

348 2. Grime, J.P. (2006) *Plant strategies, vegetation processes, and ecosystem properties*. John
349 Wiley & Sons

350 3. Bergmann, J. et al. (2020) The fungal collaboration gradient dominates the root economics
space in plants. Sci. Adv. 6, eaba3756

352 4. Weigelt, A. et al. (2021) An integrated framework of plant form and function: the
353 belowground perspective. New Phytol. 232, 42–59

354 5. Carmona, C.P. et al. (2021) Fine-root traits in the global spectrum of plant form and
function. Nature 597, 683–687

356 6. Weiher, E. et al. (1999) Challenging Theophrastus: A common core list of plant traits for
357 functional ecology. J. Veg. Sci. 10, 609–620

358 7. Klimešová, J. and Klimeš, L. (2007) Bud banks and their role in vegetative regeneration—a
359 literature review and proposal for simple classification and assessment. Perspect. Pl.
360 Ecol. Evol. Syst. 8, 115–129

361 8. Ott, J.P. et al. (2019) The ecology and significance of below-ground bud banks in plants.
362 Ann. Bot. 123, 1099–1118

363 9. Bombo, A.B. et al. (2022) Fire exclusion changes belowground bud bank and bud-bearing
364 organ composition jeopardizing open savanna resilience. Oecologia 199, 153–164
365 10. Bombo, A.B. et al. (2022) Fire and herbivory shape belowground bud banks in a semi-arid African savanna. Afr. J. Range For. Sci. 39, 16–26

367 11. Bombo, A.B. et al. (2024) Belowground organs and bud bank: Insights on morphoanatomical functional traits related to fire. Folia Geobot. 58, 259–273

369 12. Russell, M.L. et al. (2015) Season of fire manipulates bud bank dynamics in northern mixed-grass prairie. Plant Ecol. 216, 835–846

371 13. Qian, J. et al. (2021) Belowground bud bank and its relationship with aboveground vegetation under watering and nitrogen addition in temperate semiarid steppe. Ecol. Indic. 125, 107520

374 14. Ott, J.P. and Hartnett. D.C. (2015) Bud-bank and tiller dynamics of co-occurring C₃ caespitose grasses in mixed-grass prairie. Am. J. Bot. 102, 1462–1471

376 15. Pausas, J.G. and Keeley, J.E. (2014) Evolutionary ecology of resprouting and seeding in fire-prone ecosystems. New Phytol. 204, 55–65

378 16. Olano, J.M. et al. 2006. Carbohydrate storage in five resprouting Florida scrub plants across a fire chronosequence. New Phytol. 170, 99–106

380 17. Reed, C.C. and Hood S.M. (2024) Nonstructural carbohydrates explain post-fire tree mortality and recovery patterns. Tree Physiology 44, tpad155

382 18. Janeček, Š. et al. (2015) Effects of disturbance regime on carbohydrate reserves in meadow plants. AoB Plants 7, plv123

384 19. Janeček, Š. and Klimešová, J. (2014) Carbohydrate storage in meadow plants and its depletion after disturbance: do roots and stem-derived organs differ in their roles? Oecologia 175, 51–61

387 20. Klimešová, J. et al. (2008) Plant functional traits in studies of vegetation changes in response to grazing and mowing: towards a use of more specific traits. Preslia 80, 245–253

390 21. Bartušková, A. et al. (2015) Changes in biomass allocation in species rich meadow after abandonment: Ecological strategy or allometry? Persp. Pl. Ecol. Evol. Syst. 17, 379–387

393 22. Bellingham, P.J. and Sparrow, A.D. (2000) Resprouting as a life history strategy in woody plant communities. Oikos 89, 409–416

395 23. Andersen, D.C., 1987. Below-Ground Herbivory in Natural Communities: A Review Emphasizing Fossorial Animals. Q. Rev. Biol. 62, 261–286

397 24. Klimešová, J. and Klimeš, L. (2003) Resprouting of herbs in disturbed habitats: is it adequately described by Bellingham-Sparrow's model? Oikos 103, 225–229

399 25. Cain, S.A. (1950) Life-Forms and Phytoclimate. Bot. Rev. 16, 1–32

400 26. Barkman, J.J. (1988) New system of plant growth forms and phenological plant types. In Plant form and vegetation structure (Werger, M.J.A. et al., eds), pp 9–44, SPB Academic Publishing bv

403 27. Duckworth, J.C. et al. (2000) Plant functional types: an alternative to taxonomic plant community description in biogeography? Prog. Phys. Geogr. 24, 515–542

405 28. Raunkiaer, C. (1934) *The Life Forms of Plants and Statistical Plant Geography being the collected papers of C. Raunkiær* (Egerton, F.N., ed), Oxford University Press, Ayer Co Pub.

408 29. Lavorel, S. et al. (1997) Plant functional classifications: from general groups to specific groups based on response to disturbance. Trends Ecol. Evol. 12, 474–478

410 30. McIntyre, S. et al. et al. (1999) Disturbance response in vegetation – towards a global perspective on functional traits. J. Veg. Sci. 10, 621–630.
412 31. Vesk, P.A. and Westoby, M. (2004) Sprouting ability across diverse disturbances and vegetation types worldwide. J. Ecol. 92, 310–320

414 32. Givnish, T.J. (1995) Roles of stem architecture in plant performance. In *Plant stems: Physiology and functional morphology* (Gartner, B.L., ed), pp. 3–49, Academic Press

416 33. Hallé, F. et al. (1978) *Tropical Trees and Forests. An Architectural Analysis*. Springer

417 34. Jeník, J. (1994) Clonal growth in woody plants: A review. Folia Geobot. Phytotax. 29, 291–306

419 35. Klimešová, J. et al. (2018) Belowground plant functional ecology: towards an integrated perspective. Fun. Ecol. 32, 2115–2126

421 36. Baudisch, A. et al. (2013) The pace and shape of senescence in angiosperms. J. Ecol. 101, 596–606

423 37. Groff, P.A. and Kaplan, D.R. (1988) The relation of root systems to shoot systems in vascular plants. Bot. Rev. 54, 387–422

425 38. Aarssen, L.W. (2008) Death without sex—the ‘problem of the small’ and selection for reproductive economy in flowering plants. Evol. Ecol. 22, 279–298

427 39. Herben, T et al. (2018) Effects of disturbance frequency and severity on plant traits: An assessment across a temperate flora. Fun. Ecol. 32, 799–808

429 40. Klimešová, J. and Herben, T. (2024) Belowground morphology as a clue for plant response to disturbance and productivity in a temperate flora. New Phytol. 242, 61–76

432 41. Pausas, J.G. (2016) Towards understanding resprouting at the global scale. New Phytol. 209, 945–954

434 42. Noble, I.R. and Slatyer, R.O. (1980) The use of vital attributes to predict successional changes in plant communities subject to recurrent disturbances. Vegetatio 43, 5–21

436 43. Bond, W.J. and Midgley, J.J. (2003) The Evolutionary Ecology of Sprouting in Woody Plants. Int. J. Plant Sci. 164, S103–S114

438 44. Klimešová, J. and Martínková, J. (2022) Clonal growth, resprouting, and vegetative propagation of weeds. In *Persistence strategies of Weeds* (Upadhyaya, M.K. et al., eds.), pp. 200–218, Wiley Blackwell

441 45. Martínková, J. et al. (2020) Response of clonal versus non-clonal herbs to disturbance: Different strategies revealed. Persp. Plant Ecol. Evol. Syst. 44, 125529

443 46. Thomas, H. (2013) Senescence, ageing and death of the whole plant. New Phytol. 197, 696–711

445 47. Schweingruber, F.H. and Poschlod, P. (2005) Growth rings in herbs and shrubs: life span, age determination and stem anatomy. For. Snow Landsc. Res. 79, 195–415.

447 48. de Witte, L.C. and Stöcklin, J. 2010. Longevity of clonal plants: why it matters and how to measure it. Ann. Bot. 106, 859–870

449 49. Simon, M.F. and Pennington, T. (2012) Evidence for Adaptation to Fire Regimes in the Tropical Savannas of the Brazilian Cerrado. Int. J. Plant Sci. 173, 711–723

451 50. Pausas, J.G. et al. (2018) Unearthing belowground bud banks in fire-prone ecosystems. New Phytol. 217, 1435–1448

453 51. Tsakalos, J.L. et al. (2019) Trait-based formal definition of plant functional types and functional communities in the multispecies and multi-traits context. Ecol. Complex. 40, 100787

456 52. Sosnová, M. et al. (2014) To resprout or not to resprout? Modeling population dynamics of a root-sprouting monocarpic plant under various disturbance regimes. Plant Ecol. 215, 1245–1254
459 53. Keeley, J.E. & Zedler, P.H. (1978) Reproduction of Chaparral Shrubs After Fire: A Comparison of Sprouting and Seeding Strategies. Am. Midl. Nat. 99, 142–161
460
461 54. Bond, W.J. and van Wilgen, B.W. (1996) Surviving fires — vegetative and reproductive responses. In *Fire and Plants*. Springer.
462
463 55. Lubbe, F.C. et al. (2021) Carbohydrate storage in herbs: the forgotten functional dimension of the plant economic spectrum. Ann. Bot. 127, 813–825
464
465 56. Chelli, S. et al. (2024) Unravelling the clonal trait space: Beyond above-ground and fine-root traits. J. Ecol. 121, 730–740
466
467 57. Klimešová, J. and Herben, T. (2023) The hidden half of the fine root differentiation in herbs: nonacquisitive belowground organs determine fine-root traits. Oikos 2023, e08794
468
469
470 58. Midgley, J.J. (1996) Why the World's Vegetation Is Not Totally Dominated by Resprouting Plants; Because Resprouters Are Shorter than Reseeders. Ecography 19, 92–95
471
472 59. Lamont, B.B. et al. (2017) African geochemical evolution in response to fire; frost came later. Evol. Ecol. 31, 603–617
473
474 60. Zizka, A. et al. (2022) The evolution of insular woodiness. PNAS 119, e2208629119
475
476 61. Klimeš, A. et al. (2022) The ecological drivers of growth form evolution in flowering plants. J. Ecol. 110, 1525–1536
477 62. Laughlin, D.C. (2023) *Plant strategies: the demographic consequences of functional traits in changing environments*. Oxford University Press
478
479 63. Crivellaro, A. et al. (2022) Biogeographic implication of temperature-induced plant cell wall lignification. Comm. Biol. 5, 767
480
481 64. Herben, T. and Klimešová, J. (2020) Evolution of clonal growth forms in angiosperms. New Phytol. 225, 999–1010
482
483 65. Fidelis, A. and Zirondi, H.L. (2021) And after fire, the Cerrado flowers: A review of post-fire flowering in a tropical savanna. Flora 280, 151849
484
485 66. Clarke, P.J. et al. (2013) Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire. New Phytol. 197, 19–35
486
487 67. Keeley, J.E. et al. (2011) Fire as an evolutionary pressure shaping plant traits. TiPS 16, 406–411
488
489 68. Klimeš, L. and Klimešová, J. (2002) The effects of mowing and fertilization on carbohydrate reserves and regrowth of grasses: do they promote plant coexistence in species-rich meadows? Evol. Ecol. 15, 363–382
490
491
492 69. Díaz, S. et al. (2006) Plant trait responses to grazing – a global synthesis. Glob. Change Biol. 13, 313–341
493
494 70. Bartušková, A. et al. (2021) Comparative analysis of root sprouting and its vigour in temperate herbs: anatomical correlates and environmental predictors. Ann. Bot. 127, 931–941
495
496
497 71. Chiminazzo, M.A. et al. (2023) To protect or to hide: Why not both? An investigation of fire-related strategies in Cerrado woody species. Flora 306, 152350
498
499 72. Charles-Dominique, T. et al. (2016) Spiny plants, mammal browsers, and the origin of African savannas. PNAS E5572–E5579
500
501 73. Mezzomo, P. et al. (2024) Variation in induced responses in volatile and non-volatile metabolites among six willow species: Do willow species share responses to herbivory? Phytochemistry 114222
502
503
504 74. Charles-Dominique, T. et al. (2019) The architectural design of trees protects them against large herbivores. Fun. Ecol. 31, 1710–1717
505
506 75. Sosnová, M. et al. (2014) To resprout or not to resprout? Modeling population dynamics

507 of a root-sprouting monocarpic plant under various disturbance regimes. Plant Ecol.

508 215, 1245–1254

509 76. Jonášová, M. and Prach, K. (2008) The influence of bark beetles outbreak vs. salvage

510 logging on ground layer vegetation in Central European mountain spruce forests.

511 Biol. Conserv. 141, 1525–1535

512

513

514

515

516
517 Box 1. The classification system of Belowground Persistence Types

518 The classification system of **Belowground Persistence Types** integrates below and aboveground plant organs to
describe multiple adaptations to disturbance regimes based on three hierarchical, binary attributes: woodiness,
519 clonality, and resprouting ability. Below are the decision-making steps shown in the dichotomous key (Figure 1).
520
521

522 Woody vs. herbaceous
523 We understand woodiness to be plant tissue that is lignified due to pronounced lateral cambia activity, producing
524 new conducting (wood) and cork (protecting) tissues. We also include those species that thicken abnormally (for
525 example those using multiple concentric cambia) or lack secondary thickening but are lignified and persistent for
526 more than one season (palms, bamboo). Plants that are woody aboveground are also woody belowground.
527 However, plants that are herbaceous aboveground may be woody or non-woody belowground [11]. The
528 belowground woodiness for herbs is not properly known and requires additional study. The woody tissue is more
529 costly concerning carbon investment than herbaceous tissue and usually also more resistant to disturbance.
530
531 Clonal vs. non-clonal
532 A clonal plant is capable of splitting during its lifespan into at least two genetically identical but physically
533 independent individuals (ramets). This is possible due to producing either adventitious roots on stems or
534 adventitious shoots on roots, or both [37], and it enables the existence of multiple rooting units. Clonal growth
535 organs (organs that enable clonal growth and that bear buds for seasonal renewal and regeneration after
damage) are either of shoot or root origin. Clonal growth organs of shoot origin are for example rhizomes, stem
536 tubers, or stolons, while clonal growth organs of root origin are horizontal roots with adventitious buds. The
537 original rooting unit (main axis) established from a seed disintegrates over the plant lifespan and the connection
538 among ramets (made by stolon, root, or rhizome) decomposes; therefore, the genet persists far longer than any
539 single above- or belowground organ in clonal plants.
540
541

542 Resprouter vs. seeder
543 Resprouting herbs and woody plants can replace lost aboveground parts after damage. The resprouting is
544 enabled by a bud bank and by storage of carbohydrates belowground, in organs like lignotubers or xylopodia
545 [50], where they are protected from the majority of disturbance types. Seeders do not invest excessively into
546 belowground storage and bud-bearing organs and when their aboveground parts are damaged, plant individuals
547 die, and the population regenerates from the seed bank. Seeders rely on the persistence of the population and
548 not on that of the individual.
549

550 Figure 1. The dichotomous key for determination of Belowground Persistence Types is based on three hierarchical
551 questions: Is the plant woody? Is the plant clonal? Is the plant a resprouter?
552
553 Box 2. Distribution of the Belowground Persistence Types along a gradient of disturbance
554 return time (under recurrent severe disturbance).
555
556 Due to their modular construction, nearly all plants are able to resprout after mild damage
557 removing only part of their aboveground biomass, while severe disturbance may kill plants
558 that are not adapted [31]. Although we anticipate a relatively narrow disturbance niche for
559 resprouters and seeders, we expect that clonal plants (Figure 1 types 3 and 6) will be more
560 abundant along a gradient of disturbance frequency owing to their growth flexibility. Clonality
561 is provided by morphologically different organs, which also exhibit different and variable
562 traits. These organs display significant diversity concerning their positioning (either at the soil
563 surface or deeper), the size of the bud bank, content of carbohydrates (ranging from
564 substantial storage organs to small storage units), and their lateral extent within the soil [64].
565 This diversity can lead to slightly different functions, costs, and preferences for different
566 environments and disturbance regimes. Non-clonal resprouters (types 2 and 5) have shallower
567 and smaller bud banks than most clonal plants and cannot regenerate after fragmenting plant
bodies. Seeders (types 1 and 4) have a distinct strategy concerning disturbance frequency.

552
553
Box 2. Distribution of the Belowground Persistence Types along a gradient of disturbance
554
return time (under recurrent severe disturbance).
555
Due to their modular construction, nearly all plants are able to resprout after mild damage
556
removing only part of their aboveground biomass, while severe disturbance may kill plants
557
that are not adapted [31]. Although we anticipate a relatively narrow disturbance niche for
558
resprouters and seeders, we expect that clonal plants (Figure 1 types 3 and 6) will be more
559
abundant along a gradient of disturbance frequency owing to their growth flexibility. Clonality
560
is provided by morphologically different organs, which also exhibit different and variable
561
traits. These organs display significant diversity concerning their positioning (either at the soil
562
surface or deeper), the size of the bud bank, content of carbohydrates (ranging from
563
substantial storage organs to small storage units), and their lateral extent within the soil [64].
564
This diversity can lead to slightly different functions, costs, and preferences for different
565
environments and disturbance regimes. Non-clonal resprouters (types 2 and 5) have shallower
566
and smaller bud banks than most clonal plants and cannot regenerate after fragmenting plant
567
bodies. Seeders (types 1 and 4) have a distinct strategy concerning disturbance frequency.
568 This strategy in its extreme concerns annual herbs which must time their life cycle between
569 two severe disturbance events within a single growing season [40].

570
571 Figure I.- Hypothesized distribution of the **Belowground Persistence Types** along a gradient of
572 disturbance return time with hump shaped (first increasing and then decreasing) investment
573 into resprouting (highlighted by intensity of shading). The disturbance return time ranges from
574 less than a year to many decades.

575
576
577
<table><caption>Table 1. Examples of plant functional traits relevant to disturbance and their functions</caption><thead><tr><th>Strategy</th><th>Trait</th><th>Function</th><th>Refs.</th></tr></thead><tbody><tr><td rowspan="4">Avoidance</td><td>Phenology of flowering</td><td>Plants separate vegetative growth from flowering to reduce the probability that flowering and fruiting organs are grazed or burned.</td><td>[20, 65]</td></tr><tr><td>Phenology of dormancy</td><td>Plants survive the disturbance in dormant stage as seeds in the seed bank or as dormant belowground organs (bulbs and tubers).</td><td>[66, 67]</td></tr><tr><td>Plant height</td><td>Small and prostrate plants lose a relatively lower amount of biomass than erect and tall plants in grasslands due to mowing.</td><td>[68]</td></tr><tr><td>Shoot architecture</td><td>Plants with basal rosette lose smaller amounts of biomass than plants with leafy shoots in grasslands due to mowing or grazing.</td><td>[68,69]</td></tr><tr><td rowspan="4">Tolerance</td><td>Bud bank size</td><td>For resprouting after disturbance, dormant buds located on specialized organs out of reach of disturbance, usually in soil, are necessary.</td><td>[8]</td></tr><tr><td>Bud bank depth and protection</td><td>The deeper the bud bank is located in the soil the better it is protected from disturbance. Especially when dealing with soil disturbance, plants need deep bud banks. Bud banks may also be located close to the soil surface or may be on aboveground part of the stem and protected by bark, wood or leaves.</td><td>[70,71]</td></tr><tr><td>Carbohydrate storage</td><td>For resprouting after disturbance, storage of carbohydrates located in specialized organs out of reach of disturbance is necessary.</td><td>[45]</td></tr><tr><td>Bud bearing organ type</td><td>Belowground storage and bud-bearing organs (e.g. rhizomes, bulbs, tubers) vastly differ in their location in the soil profile, amount of storage carbohydrates and buds, and therefore, respond differently to different types of disturbance.</td><td>[40,50]</td></tr><tr><td rowspan="4">Resistance</td><td>Spinescence</td><td>Protects plants from grazing.</td><td>[72]</td></tr><tr><td>Bark thickness</td><td>Protection of buds, conduits and meristems from fire.</td><td>[66]</td></tr><tr><td>Secondary compound composition</td><td>Secondary metabolites either serve as constitutive defense or are induced by herbivore attacks, and then, may have either direct effects on herbivores (non-volatile) or indirect effects (volatile) through attracting predators and parasites.</td><td>[73]</td></tr><tr><td>Cage-like architecture</td><td>Branching pattern limiting the accessibility of leaf biomass to herbivores.</td><td>[74]</td></tr></tbody></table>
<table><thead><tr><th>Disturbance regime descriptors</th><th>Frequency /timing</th><th>Severity/ intensity</th><th>Extent</th><th>Example 1 – Ploughed arable land [75]</th><th>Example 2 – fire prone tropical grassland [49]</th><th>Example 3 – Logged boreal forest [76]</th></tr></thead><tbody><tr><td>With respect to disturbance</td><td>How often per year / timing in a season</td><td>Force (e.g., temperature of fire, speed of wind)</td><td>Area affected</td><td>Ploughing yearly at the end of growing season</td><td>Low intensity fire (500 °C) with short residence time (minutes) every 1–3 years at the end of the dry season</td><td>Logging of tree layer once per 100 years</td></tr><tr><td>At level of plant community</td><td>Timing in relation to accumulated biomass, or to seasonal changes in palatability</td><td>Removed biomass, creating bare soil patches, killing dominant species?</td><td>Percentage of a community affected</td><td>Aboveground biomass destroyed, plants uprooted, fragmented and buried in soil</td><td>Fuel (dry aboveground biomass of herbs) removed; burning, unprotected green plant parts</td><td>Trees old enough for logging cut at the base and understory subjected to mechanical damage by machinery</td></tr><tr><td>At level of the plant individual/ population</td><td>Timing in relation to plant life cycle (vulnerable stages of ontogeny or seasonal development, e.g., flowering)</td><td>Quantity and quality of removed biomass (removed organs)</td><td>Number of plants in population affected</td><td>Annual herb Rorippa palustris killed by uprooting after setting seeds</td><td>Removal of aboveground dry biomass of perennial non-clonal resprouter Andira humilis</td><td>All mature trees of Picea abies killed while saplings survived</td></tr></tbody></table>
**Outstanding questions**

(1) Do individual disturbance regimes select for different BPTs?

(2) In which disturbance regime can several BPTs coexist?

(3) Which bud bank traits (size, vertical distribution), clonal traits (lateral spread, type of clonal growth organ), architectural traits (distribution of leaves along shoot in herbs) or phenological traits (onset of flowering length of flowering) improve predictive power of BPTs and shall be used together with them?

(4) Do BPTs covary with other plant ecological strategies (e.g. the plant economics spectrum)?

(5) How might climate change and shifts in disturbance regimes affect the distribution and abundance of the six BPTs, and how can this classification system help predict these changes?
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Disturbance return time