# Trade-offs between extreme-temperature tolerance, avoidance and facilitation in tropical alpine plants

Carlos Martorell, Fabien Anthelme, Hugo Tovar, Flor Vega-Ramos

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Carlos Martorell, Fabien Anthelme, Hugo Tovar, Flor Vega-Ramos. Trade-offs between extreme-temperature tolerance, avoidance and facilitation in tropical alpine plants. Alpine Botany, In press, 10.1007/s00035-025-00345-z. http://dx.doi.org/10.1007/s00035-025-00345-z

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# Trade-offs between extreme-temperature tolerance, avoidance and facilitation in tropical alpine plants

Carlos Martorell<fnref n="1" />,<fnref n="2" /> · Fabien Anthelme<fnref n="2" /> · Hugo Tovar<fnref n="3" /> · Flor Vega-Ramos<fnref n="4" />

Received: 26 June 2025 / Accepted: 27 October 2025

© The Author(s) 2025

## Abstract

Alpine plants resist extremely high and low temperatures by either tolerance or avoidance, which depend mostly on physiology or growth forms, respectively. Facilitation by neighboring species that buffer extreme temperatures can also be envisaged as avoidance. We tested whether avoidance capacity differs among growth forms; whether there is an avoidance-tolerance trade-off both across species and growth-forms; and if species with low avoidance or tolerance depend most on facilitation. In 35 tropical-alpine species with five growth forms, we measured avoidance as the capacity to buffer high- and low-air temperatures (i.e., as differences between plant and air temperature), and cold tolerance as the temperature that damages half of the leaf surface. We used spatial associations between species as a proxy for facilitation. Thermal-avoidance capacity differed among growth forms. Rather than avoiding high temperatures, leaves warmed above air temperature during the day perhaps enhancing photosynthesis. However, such warming was associated to increased chances of nighttime freezing. The avoidance-tolerance trade-off was confirmed. As expected, the least tolerant species were more associated to nurse plants. However, this was also the case of the best avoiders, which should resist on their own. By linking facilitation with insights from the avoidance-tolerance framework, we found that trade-offs drive alpine-plant strategies to form a continuum between two extremes: Mats warm-up and cool-down rapidly, perhaps increasing photosynthesis but investing more on cold-tolerance mechanisms. At the other extreme, shrubs avoid extreme temperatures but they might not reach optimal photosynthetic temperatures and depend on facilitation during establishment when they are still morphologically immature.

**Keywords** Thermal decoupling · Growth forms · LT₅₀ · Stress amelioration · Stress resistance

## Introduction

Alpine plants from different latitudes experience extreme high and low temperatures over the year or even over the course of a single day: temperatures may fall well below freezing at night and soil surface may reach up to 80 °C during the day (Luteyn et al. 1999; Körner 2003). To thrive under such stressful temperatures, organisms must display stress resistance, i.e., the capacity to endure extreme temperatures while remaining relatively undamaged. Stress resistance arises from stress avoidance and/or tolerance (Levitt 1972). Avoidance occurs when organisms do not experience the stressor. Low temperatures may be avoided by animals that spend the night in underground burrows or by plants that retain heat at night through thermal insulation (Ramsay 2001; Körner 2003; Sklenář et al. 2016). In contrast, tolerant species reach thermal equilibrium with their environment and remain undamaged. Tolerance to cold

<footnote>Carlos Martorell
martorell@ciencias.unam.mx</footnote>

<footnote n="1">¹ Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Mexico City, Mexico</footnote>

<footnote n="2">² AMAP, Univ. Montpellier, IRD, CIRAD, CNRS, INRAE, Montpellier, France</footnote>

<footnote n="3">³ Computational Genomics Division, Instituto Nacional de Medicina Genómica, Mexico City, Mexico</footnote>

<footnote n="4">⁴ Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico</footnote>
conditions may arise through supercooling if the cytoplasm remains fluid below 0 °C, or by mechanisms that prevent cell damage by ice formation (Squeo et al. 1991; Sklenář et al. 2010; Rada et al. 2019).

Extreme-temperature avoidance depends heavily on the growth form of plants. Alpine-plant growth forms experience different degrees of decoupling, measured as the difference between plant and environmental—typically air-temperature. Positive decoupling values indicate that the plant is warmer than the air, and negative ones, that the plant is colder (Ramsay 2001; Körner 2003; Sklenář et al. 2016). For instance, tussock grasses have marcescent leaves that provide thermal insulation, and thus display a positive decoupling at night (Ramsay 2001; Sklenář et al. 2016). Similarly, the compact form and large amounts of water stored in bulky cushion plants delay temperature change at day and night, as shown by significant decoupling (Taschler and Neuner 2004; Anthelme et al. 2014; Sklenář et al. 2016). Plant height is also important for extreme-temperature avoidance. Because the most extreme air and soil temperatures occur near the soil surface (Squeo et al. 1991; Sklenář et al. 2010, 2016; Wundram et al. 2010), the buds of many tussocks and acaulescent rosettes occur several centimeters underground, and taller plants remain cooler than short ones during the hottest hours of the day and warmer during the night, although the opposite pattern may also occur (Sklenář et al. 2016; Blonder et al. 2020). Plant growth forms drive the avoidance of cold air temperatures through positive decoupling (Hedberg and Hedberg 1979; Ramsay 2001; Sklenář et al. 2016). In contrast, overheating avoidance at noon via negative decoupling from air has been rarely reported. Instead, alpine plants are usually warmer than air during the day, probably to avoid suboptimally-low temperatures for photosynthesis, even at the risk of high-temperature damage (Körner 2003; Sklenář et al. 2010, 2016). Optimal leaf temperature for photosynthesis in extratropical alpine plants seems to be about 20 °C (Körner and Diemer 1987; Körner 2003; Löffler and Pape 2020), although near the equator such values may be between 10 and 20 °C (Schulze et al. 1985; Fetene et al. 1997; Cabrera et al. 1998; Rada et al. 2008; Cruz Aguilar 2022; Sanchez et al. 2025).

Although tolerance to extreme temperatures depends largely on physiological mechanisms rather than on the morphological traits that drive avoidance, differences in tolerance between growth forms have also been widely documented (Squeo et al. 1991; Rada et al. 2019). Both types of resistance are costly: for instance, marcescent leaves that insulate tussocks reduce photosynthetic radiation assimilation (Monteiro et al. 2011), or huge amounts of anti-freeze molecules that need to be produced nightly have a strong energetical cost (Rada et al. 1985). Because of such costs,

plants may only invest in tolerance if avoidance is weak or vice versa. Sparse data suggest that the plants that experience lower minimum temperatures tend to be more tolerant to cold (e.g., Körner 2003; Larcher et al. 2010), although there are clear exceptions (Sklenář et al. 2010). Similar patterns are seemingly observed for high-temperature tolerance, which is greater for growth-forms that reach higher temperatures during the day (Buchner and Neuner 2003). However, current evidence on the avoidance and tolerance of alpine plants and their trade-offs remains sparse and anecdotic, and has not been analyzed formally.

Stress avoidance in alpine plants can also be driven at the interspecific level through plant-plant interactions. Facilitation is a widespread phenomenon in alpine environments, via the positive effects of nurse plants on beneficiary species (Callaway et al. 2002; Anthelme and Dangles 2012). It is frequently the result of plants attenuating environmental constraints in their neighborhood, allowing other species to thrive (Brooker and Callaghan 1998; Callaway et al. 2002). Stress resistance plays an important role in this interaction, with species that are more sensitive to stress being facilitated more frequently or strongly than their resistant counterparts (Liancourt et al. 2005; Michalet et al. 2006; Maestre et al. 2009). While facilitation in alpine environments frequently results from enhancing water and nutrient availability (Anthelme et al. 2012; Ale et al. 2018), many reports link it to extreme-temperatures buffering (Callaway et al. 2002; Cavieres et al. 2007; Anthelme et al. 2014; Pugnaire et al. 2015; Malatesta et al. 2016; Pedraza et al. 2020). However, little is known about the types of resistance in the context of facilitation.

Thus, the interplay of extreme-temperature tolerance and avoidance either through plant morphology, physiology or facilitation is likely to be an important driver of the organization and dynamics of alpine communities, especially under a warmer climate. Moreover, understanding it may prove relevant in the current context of rapid climate change. It remains, nevertheless, mostly unexplored. The same can be said about facilitation as an alternative to extreme-temperature resistance, despite being acknowledged as one of the areas that require further attention to improve our understanding of alpine life (Rada et al. 2019). Moreover, the distinction between tolerance and avoidance has been absent from the discussion of facilitation despite the fact that the relative importance of both strategies changes with stress intensity (e.g., Rada et al. 2019) or among taxonomic groups (e.g., Lancaster and Humphreys 2020), and thus may have important implications for the stress-gradient hypothesis or in determining community composition.

In this contribution, we explore the relationships between thermal avoidance, tolerance and plant-plant interactions (via extreme temperature attenuation) as drivers of alpine
plant strategies in the face of extreme temperatures. To do
so, we used field and laboratory data from a tropical alpine
ecosystem in Mexico. We tested the following hypotheses:
(1) Because heat exchange and the immediate environment
that plants experience depend mostly on morphological
attributes, we expect thermal avoidance capacity of plants to
differ among growth forms. (2) Avoidance and tolerance are
complementary and costly, leading to trade-offs: plants that
invest more on one form of resistance devote less resources
to the other. Thus, we expect a negative correlation between
the capacities to avoid and to tolerate low temperatures
both across species and growth-forms. (3) If facilitation is
driven by the buffering of thermal stress, we expect that the
most resistant species—either because they avoid or tolerate
extreme temperatures—are less frequently associated with
benefactor plants than the least resistant ones.

**Methods**

**Study site and species**

Fieldwork was conducted in the Iztaccíhuatl volcano (19° 11' N, 98° 39' W) in Southern Mexico. This tropical-alpine ecosystem occurs between 3900 and 4600 m a.s.l. We selected it because tropical alpine regions gather a large number of alpine-plant growth forms (Hedberg and Hedberg 1979). Rainfall in Iztaccíhuatl occurs between May and October, totaling 1150 mm annually. Snow falls occasionally between December and March and lasts a few days, exposing plants to extreme temperatures. As in most tropical-alpine systems (Luteyn et al. 1999; Körner 2003), annual changes in mean temperature are small (just 2 °C) but daily oscillations are large (32 °C; Tovar-Romero 2010). Such rapid fluctuations potentially allow for strong decoupling from air temperatures even if heat exchange is slowed down even briefly.

We studied 35 plant species (Appendix S1), i.e., those
that were sufficiently abundant for us to find enough

isolated, adult individuals in a small area such as to moni-
tor them closely. Species were classified into five growth
forms (Fig. 1) following Halloy (1990): (1) Mats (i.e.,
plaques; n=4 species) are compact plants with several short
branches and tiny leaves forming a flat plaque. The dis-
tance between apical meristems is shorter than leaf length.
(2) Tussocks (n=6) have numerous apices tightly packed
against each other slightly below ground level, with slender
(> 50 times longer than wide) and relatively vertical leaves.
Dead leaves often remain on the plant, acting as a thermal
insulator. (3) Rosettes (n=13) have very short internodes
and comparatively long leaves growing radially from a
well-defined, short stem. When they branch, the number of
apices is small and their separation is typically larger than
the leaf length. (4) Forbs (n=7) are erect or prostrate herbs
with developed branches and apices distant from each other.
(5) Shrubs (n=5) have evidently lignified stems. To include
at least four species in each growth form we worked at two
sites: Altzomoni (3957 m a.s.l.) and Cruz de Rosas (4569 m
a.s.l.). Both sites faced due west and had moderate slope (21
and 15° respectively), with tussocks being dominant at the
low-elevation site, but a mixture of tussock and mat patches
at Cruz de Rosas.

**Hypothesis 1: Growth forms and temperature avoidance**

For five days at each site in September 2008, we measured
in situ temperatures of one individual of each species every
hour for 15 h, starting 1 h before dawn. Every day a new
healthy, adult individual of each species was studied, so we
had five individuals per species. All days and nights were
clear. Because temperatures and resistance mechanisms
may depend on distance to soil surface (Sklenář et al. 2010,
2016; Wundram et al. 2010; Rada et al. 2019), we measured
thermal conditions near the plant’s apex. We recorded (1)
the surface temperature of a fully developed leaf (or dense
set of leaves when these were too small to measure individ-
ually, as in tussocks and mats) with an infrared thermometer

<figure><img src="image_2.png" /><figcaption>**Fig. 1** Examples of growth forms. **A** Tussock (*Festuca tolucensis*). **B** Rosette (*Draba nivicola*). **C** Shrub (*Lupinus elegans*). **D** Forb (*Stachys eriantha*). **E** mat (*Arenaria bryoides*)

Photos: Diego García Meza (A, C, D, E), Fabien Anthelme (B)</figcaption></figure>
and (2) the temperature of a bud with a thermocouple. Both measurements relate to important processes for the plant: photosynthesis and growth, as the buds contain the meristems. In mats, it we could not insert thermocouples in the tiny buds (<0.5 mm). However, they are so tightly packed among leaves having the same size and exposure to the air that temperature differences between both were likely negligible (Nobel 1999) and thus assumed that the bud and leaf temperatures were the same. Air temperature was measured hourly 30 cm above ground near the center of the area where the plants were measured (Details in appendix S1).

Our measure of avoidance, i.e., the ability of plants to decouple from the environmental temperature, was the difference between the plant and air temperatures 1 h before sunrise and at 13:00 h solar time. These times correspond to the daily temperature minima and maxima, respectively, making them critical for assessing decoupling. This was done for each individual plant, altogether with its minimum and maximum temperatures, and the variance of the daily temperatures. To test whether these variables differ between growth forms, we used phylogenetic generalized linear mixed-effects models (PGLMM, details in appendix S1) setting species and day as crossed random factors using the package phyr (Ives et al. 2020) for R (R Core Team 2024). All the models were compared using the Akaike Information Criterion (AIC), considering that models with ΔAIC>2 had relatively little support. As a coarse indicator of whether temperatures are tuned to the optimum for photosynthesis, we calculated the duration of the period when leaves had temperatures within 5 °C of two putative optima: 15 and 20 °C. These two values were chosen because they are typical of plants from nearly-equatorial and extratropical mountains, and Iztaccíhuatl lies at an intermediate latitude between both.

<table><caption>**Table 1** ΔAIC (Akaike information Criterion) values for models of leaf and bud temperature</caption><thead><tr><td>Response variable</td><td>Leaves</td><td>Buds</td></tr></thead><tbody><tr><td>Decoupling, dawn</td><td>34.9</td><td>22.7</td></tr><tr><td>Decoupling, 13:00</td><td>33.4</td><td>34.9</td></tr><tr><td>Daily variation</td><td>63.7</td><td>61.1</td></tr><tr><td>Minimum</td><td>37.4</td><td>30.0</td></tr><tr><td>Maximum</td><td>86.0</td><td>33.8</td></tr></tbody></table>

The models that included growth form as explanatory variables were always the best, having a ΔAIC=0. This table shows the ΔAIC values of the null models, which were large and thus could be rejected with great confidence. Thermal decoupling values were calculated with respect to air at 30 cm. Daily variation is the standard deviation of hourly temperatures. Minimum and maximum are the respective daily temperatures

## Hypothesis 2: Avoidance-tolerance trade-off

To characterize tolerance, we experimentally determined the temperature at which half of the leaf tissue was damaged by subfreezing temperatures, or $LT_{50}$ (Nobel 1999). From the lower-elevation species used in the previous experiment, we selected those that occurred near roads to allow for rapid transportation. In winter 2010, we collected 20 complete, isolated individuals per species, and kept them for 10 d under a 12/12 h light/dark cycle at 15/5 °C. We kept the 13 species that endured transplantation well (appendix S1) for further analysis (Table 1). We marked three fully developed, undamaged leaves on each plant using ink. For each species, three individuals were exposed to each of five low-temperature treatments (–15, –20, –25, –30, and –35 °C). To do so, plants were transferred to an ultrafreezer at room temperature, which was then turned on and let to cool down until it reached the target temperature. Plants were then kept in the dark at that temperature for 1 h. An additional five individuals per species remained in the growth chamber as controls. One week later, the damaged fraction of the selected leaves was measured. The average damage across the three leaves was calculated. To isolate the effect of the low-temperature treatments, we subtracted the mean damage observed in the control plants from the treatment values (Details in appendix S1).

To test for the avoidance-tolerance trade-off at the species level, we compared thermal decoupling of the leaf at dawn in the field and $LT_{50}$ values through phylogenetic generalized least squares (PGLS) regression using package lme4 (Pinheiro and Bates 2000). To check if the pattern holds for growth forms, we first conducted PGLS ANOVA to assess whether $LT_{50}$ differed among growth forms, and then calculated the correlation between the mean $LT_{50}$ of each growth form and its mean leaf-decoupling at dawn.

## Hypothesis 1: Plant-plant interactions and thermal resistance

Plant-plant interactions were inferred from spatial associations. Because species interactions could change with thermal stress (Callaway et al. 2002), we studied eight sites distributed between 3957 and 4579 m a.s.l. (appendix S1). Based on the literature (Reid et al. 2010; Catorci et al. 2011; Liczner and Lortie 2014; Malatesta et al. 2016; Pedraza et al. 2020) and on field observations, we expected mats and tussocks to be the best facilitators at Iztaccíhuatl. As in other alpine areas (Alados et al. 2007), vegetation forms tight patches surrounded by bare soil. A patch could contain a single plant or several species within well-defined boundaries. At each site, we delimited an area containing between 100 and 200 patches, and recorded the species composition
of all patches. The number of times that two species co-
occur in the patches of a site in the absence of interactions
should follow a hypergeometric distribution (Wright and
Biehl 1982), with which we calculated the probability *q* of
the observed number of co-occurrences. The association
index *A* was defined as the *q*th-quantile from a *z* distribution,
resulting in a symmetric distribution centered around zero.
Positive values indicate species aggregation, while negative
values suggest avoidance. *A*-values were calculated sepa-
rately for all species in association with either tussock or
mat species (Details and biological rationale in appendix
S1).

To assess the relationship between associations and
resistance to extreme temperatures, we conducted PGLMM
regressions. We modeled association index *A* as a function
of leaf and bud decoupling measured at dawn and at 13:00 h, as well as LT<sub>50</sub> values. Species and site were included as
crossed random factors.

Results

Growth forms and temperature avoidance

As expected from hypothesis 1, thermal decoupling from
air, maximum and minimum temperatures and variance
differed among growth forms, with the null models receiv-
ing little support (Table 1). Temperatures were similar for
leaves and buds (Fig. 2). In general, plants that experienced
the highest temperature maxima also experienced the low-
est minima, showing great temperature variations (Fig.
2A). Mats experienced the strongest fluctuations, reaching
on average maxima of 30 °C (and up to 52 °C) and min-
ima below –6 °C. Daily fluctuations diminished for forbs,
rosettes and tussocks, in that order, and were the smallest for
shrubs, whose mean maxima was 22 °C and minima 3 °C
(Fig. 2A). Tussock- and shrub-leaves often remained above
freezing temperatures at dawn, whereas this never occurred
in mats and very rarely in forbs (Fig. 2A). Similar trends
were observed for the thermal decoupling between air, buds
and leaves. Mats were the most decoupled, reaching about
10 °C above air temperature at 13:00 h and some 8 °C below
air temperature at dawn. In contrast, shrubs remained near
the temperature of the air throughout the day (Table 1; Fig.
2B).

Contrary to what would be expected if decoupling buff-
ered extreme temperatures, plants were usually colder than
air at dawn and warmer near noon. Instead, positive decou-
pling allowed leaves to approach 20 °C, the likely optimal
temperature for photosynthesis in extratropical mountains,
for up to 32% more time than would be expected if leaves
where in thermal equilibrium with their environment (Table

2). In contrast, if a photosynthetic optimum near 15 °C is assumed, daytime decoupling would shorten the period when near optimal leaf temperature occurs by up to 41%. In both scenarios, decoupling resulted in potentially detrimental high leaf temperatures, especially in mats (Table 2).

Avoidance-tolerance trade-off

Our expectation that LT₅₀ differed among growth forms was strongly supported by the data (the null model, in which growth forms had no effect, had ΔAIC=25.0 and can be discarded). Mats had the lowest LT₅₀, with half of its photosynthetic surface undamaged down to -48.9 °C. Shrubs and rosettes, on the other hand, suffered similar damage at -29.7 °C and -31.4 °C, respectively. Tussocks and forbs showed intermediate values (Fig. 2C). Note that in some species the estimated LT₅₀ values were below -35 °C and thus were obtained by extrapolation (See appendix for details).

As expected from the trade-off hypothesis (hypothesis 2),
species that experienced colder nighttime temperatures suf-
fered less damage by lower temperatures (Fig. 3; the null
model’s ΔAIC=2.55). The same trend was observed con-
sidering growth forms instead of individual species: LT₅₀
values and leaf decoupling at dawn averaged over growth
forms were correlated (r=0.72; the model where r=0 had
a ΔAIC=2.33).

Plant-plant interactions and thermal resistance

A total of 94.2% of the sampled species were positively associated with tussocks whereas 85.5% were associated positively with mats. In line with hypothesis 3 that the least resistant species require more facilitation, associations with tussocks and mats became more positive as tolerance to low temperatures, measured as LT<sub>50</sub>, diminished (Fig. 4), but the evidence was not conclusive (null models had less support but could not be discarded; AIC<2, Table 3). Contrary to our expectations, the species with the best capacity to avoid heat by themselves, i.e., those with the least positive bud thermal decoupling at noon, were the most positively associated with tussocks and mats (Fig. 5C, H; Table 3; the trend for tussocks seemed to depend strongly on a single species, but removing it did not change the result). The same pattern held for leaf thermal decoupling and association with tussocks (Fig. 5C). Also contrary to what was expected, evidence suggests that species that kept their leaves warm at night were the most positively associated with mats (Fig. 5E; Table 3). In all analyses that considered thermal decoupling, the null model could be safely discarded (Table 3).
<figure><img src="image_3.png" /><figcaption>**Fig. 2** Temperature, thermal decoupling from air and LT<sub>50</sub> values per growth form. **A** Maximum and minimum leaf and bud daily temperatures. **B** Leaf and bud decoupling relative to air temperature at 30 cm above ground at dawn and at 13:00 h solar time. **C** Temperature at which half of the leaf surface (LT<sub>50</sub>) is damaged. Horizontal black line=median. Box=interquartile range</figcaption></figure>

<figure><img src="image_4.png" /></figure>
<table><caption>**Table 2** Potential effects of daytime thermal decoupling on photosynthesis assuming that optima are near 20 °C (left columns) or 15 °C (right columns)</caption><thead><tr><th rowspan="2"></th><th colspan="2">Optimum: 20 ± 5 °C</th><th colspan="2">Optimum: 15 ± 5 °C</th></tr><tr><th>Change</th><th>Excess</th><th>Change</th><th>Excess</th></tr></thead><tbody><tr><td>Forb</td><td>26.4 ± 18.1</td><td>3.6 ± 1.4</td><td>-21.8 ± 4.4</td><td>16.9 ± 2.7</td></tr><tr><td>Mat</td><td>10.3 ± 34.6</td><td>25.0 ± 10.2</td><td>-41.5 ± 11.8</td><td>34.2 ± 6.4</td></tr><tr><td>Rosette</td><td>32.2 ± 9.1</td><td>13.5 ± 3.2</td><td>-25.0 ± 4.4</td><td>26.0 ± 3.7</td></tr><tr><td>Shrub</td><td>5.5 ± 10.6</td><td>5.0 ± 2.5</td><td>-15.1 ± 2.1</td><td>13.7 ± 4.1</td></tr><tr><td>Tussock</td><td>19.2 ± 14.4</td><td>6.7 ± 2.9</td><td>-16.5 ± 6.9</td><td>17.5 ± 54</td></tr></tbody></table>

Change: percent change (mean ± SE, %) in the duration of the period when leaves are near the optimum due to decoupling. Excess: fraction of the daytime hours (mean ± SE, %) that leaf temperatures exceed the putative optimum by >5 °C

<figure><img src="image_5.png" /><figcaption>**Fig. 3** Relationship between leaf thermal decoupling from air at dawn and the temperature at which half of the photosynthetic tissue dies (LT₅₀)</figcaption></figure>

<table><caption>**Table 3** ΔAIC (Akaike information Criterion) for models of associations with tussocks or Mats depending on avoidance (decoupling) and tolerance (LT₅₀)</caption><thead><tr><th></th><th>Variable</th><th>Tussocks</th><th>Mats</th></tr></thead><tbody><tr><td rowspan="5">Avoidance</td><td>Bud, 13:00 h</td><td><strong>0.00</strong></td><td><strong>0.00</strong></td></tr><tr><td>Leaf, 13:00 h</td><td>1.10</td><td>4.23</td></tr><tr><td>Bud, dawn</td><td>2.83</td><td>4.70</td></tr><tr><td>Leaf, dawn</td><td>3.39</td><td>0.59</td></tr><tr><td>Null</td><td>4.68</td><td>6.30</td></tr><tr><td rowspan="2">Tolerance</td><td>LT<sub>50</sub></td><td><strong>0.00</strong></td><td><strong>0.00</strong></td></tr><tr><td>Null</td><td>1.21</td><td>1.69</td></tr></tbody></table>

Both sets of models are based on different numbers of observations and thus cannot be compared. Bold letters highlight the best model. Models with similar support to the best one (ΔAIC<2) are in italics

# Discussion

## Avoidance of extreme temperatures across growth forms

Avoidance of harmful cold temperatures during the night and of photosynthetically suboptimal cool temperatures by

<figure><img src="image_6.png" /></figure>

<figure><img src="image_7.png" /><figcaption>**Fig. 4** Spatial associations (mean ± se) with tussocks and mats as function of low-temperature tolerance. Zero indicates no association</figcaption></figure>

day has driven the discussion on the evolution of alpine growth forms (Hedberg and Hedberg 1979; Luteyn et al. 1999; Ramsay 2001; Körner 2003; Sklenář et al. 2016). Our results concur with the widespread occurrence of positive leaf decoupling, i.e., leaf temperature being above that of air, during the day in high-elevation systems (Luteyn et al. 1999; Körner 2003; Sklenář et al. 2016). Without the additional warmth provided by thermal decoupling, our plants would not have even approached 20 °C, the temperature that seems to maximize photosynthetic rates in some tropical and extratropical alpine plants (Table 2; Körner and Diemer 1987; Cabrera et al. 1998; Körner 2003; Rada et al. 2008; Löffler and Pape 2020; Cruz Aguilar 2022). Such positive effect of warming would be consistent with the monotonic increases in photosynthetic rates over natural (e.g., Rada et al. 1992; Cabrera et al. 1998; Sanchez et al. 2025) or experimental (Solarte et al. 2022) temperature gradients observed in tropical alpine plants. Nevertheless, a photosynthetic optimum near or below 15 °C, such as that reported for other species (e.g., Hedberg and Hedberg 1979; Schulze et al. 1985; Fetene et al. 1997), would rule out such
<figure><img src="image_8.png" /><figcaption>**Fig. 5** Associations (mean ± se) with tussocks and mats as functions of leaf and bud decoupling (°C) at dawn and at 13:00 h. Trend lines are shown for models with the best AIC support. Zero indicates no association</figcaption></figure>

interpretation of positive daytime decoupling as a low-temperature avoidance mechanism (Table 2). We must bear in mind, however, that tropical alpine plants have a remarkable capacity to adjust their photosynthetic optima to profit from warmer temperatures (Rada et al. 1992, 2008, 2019), making the latter scenario less likely.

In contrast with some previous work (e.g., Hedberg and Hedberg 1979; Ramsay 2001; Sklenář et al. 2016), we found almost no evidence for higher leaf or bud temperatures than air at dawn except for shrubs and a few tussocks. However, we must bear in mind that decoupling was measured with respect to air at 30 cm above the soil, and that environmental temperatures near the soil surface could be lower (Squeo et al. 1991; Sklenář et al. 2010, 2016; Wundram et al. 2010). Thus, small plants may be warmer than their immediate environment, in line with the positive decoupling expected if it is a mechanism of resistance to extreme cold.

There is general agreement in the literature as to which growth forms tend to warm up the most during the day. Cushion plants and mats are excellent heat traps, reaching up to 25 °C above air temperature (Körner 2003; Kleier and Rundel 2009). In order of decreasing positive decoupling, cushions and mats are followed by rosettes, low-stature forbs or shrubs, tussocks, erect forbs, shrubs and trees (Ramsay 2001; Körner 2003). Our results match this overall arrangement. This sequence was mirrored at dawn, reflecting negative decoupling: growth forms that warmed during the day tended to cool more at night.

These results could highlight a dilemma for plants if there is an evolutionary pressure to maximize photosynthesis, because warming up during the day comes at the cost of rapid cooling and potential frost injury at night. The trend of some growth forms to experience the most

extreme temperatures both at noon and dawn, while others remain stable, may be quite general for a few reasons: (1) The extreme temperatures observed in growth forms that develop close to the soil surface (e.g., mats and rosettes) probably reflects corresponding cold and heat extremes in their immediate environment. Air-temperature fluctuations become moderate with distance to the soil surface, as do those of tall plants as shrubs (Squeo et al. 1991; Sklenář et al. 2010, 2016; Wundram et al. 2010). (2) Mats, cushions and many rosettes have predominantly horizontal outlines, increasing their exposure to the midday sun and to radiative heat loss at night (Nobel 1999; Körner 2003). (3) Thermal insulation or water accumulation retard temperature increase- and decrease-rates equally (Nobel 1999), so they would result in more stable temperatures throughout the day-night cycle in comparison with species that lack such attributes.

## A trade-off between tolerance and avoidance in alpine plants

The temperatures that we recorded fall well within the tolerance ranges reported for most alpine plant species, yet may still be challenging. High-elevation plants usually have LT₅₀ values between -15 and -10 °C (Körner 2003; Taschler and Neuner 2004; Larcher et al. 2010; Rada et al. 2019), and even -70 °C for exposed cushion plants in winter (Larcher et al. 2010). The respective high-temperature tolerance values (HT₅₀) range between 35 and 55 °C (Larcher and Wagner 1976; Körner 2003; Larcher et al. 2010; Leon-Garcia and Lasso 2019; Sklenář et al. 2023). While most of our plant's temperatures were within these low and high-temperature tolerance values, we must bear in mind that these
correspond to very serious injury, and less-extreme tem-
perature may already be detrimental. Initial photosystem
damage may occur at 30 °C in some alpine plants (Neuner
and Buchner 2012), a temperature that several of our plants
reached. The leaf minimum and maximum temperatures
that we observed in *Mexerion sarmentosum* (−1.3 ± 2.1 and
32.4 ± 2.57 °C, mean ± sd) suffice to reduce life expectancy
to nearly a half of that observed in the thermally-buffered
vicinity of tussocks (Pedraza et al. 2020). The case of
mats is worth considering. They could reach up to 52 °C,
approaching the HT₅₀ values mentioned above, and remain
long periods above the optimal photosynthetic tempera-
tures of alpine plants (Table 2; Körner and Diemer 1987;
Cabrera et al. 1998; Körner 2003; Löffler and Pape 2020).
Even assuming higher optima near 25 °C, models show that
the temperatures experienced by mats can severely reduce
carbon uptake of alpine species (Wentz et al. 2019). Addi-
tionally, mats faced very sharp temperature changes, even
increasing up to 35 °C in just 1 h after sunrise. This puts a
heavy evaporative demand on the leaves while the under-
ground water is frozen and thus inaccessible (Rada et al.
2019). This may explain why mats and cushion plants are
among the most heat-tolerant alpine species (Larcher and
Wagner 1976; Larcher et al. 2010).

Both avoidance and tolerance are costly (Rada et al. 1985;
Luteyn et al. 1999; Taschler and Neuner 2004; Monteiro et al.
2011). Thus, for a species that is sufficiently resistant to local
temperatures through high avoidance, investing in tolerance
would report no further benefits but represent a cost instead,
and vice-versa. Neither is it adaptive to lack any form of
resistance. Accordingly, we found no species in the top left
(high avoidance and tolerance) or bottom right (low resis-
tance) corners of Fig. 3, which figured a trade-off between
avoidance and tolerance. The same trade-off was observed
when considering growth forms. Because, as already dis-
cussed, growth forms are expected to drive avoidance but
not tolerance, the differences in tolerance observed between
growth forms are probably an indirect consequence of the
avoidance-tolerance trade-off. The exception to the general
trend (Fig. 2C) were tussocks, which should be somewhere
between rosettes and shrubs based on their decoupling, but
were more tolerant than expected. This result aligns with
previous findings showing that tussocks are among the most
tolerant to low temperatures in other alpine areas (Körner
2003; Taschler and Neuner 2004; Sumner and Venn 2022).

Our results suggest a fairly general range of plant strat-
egies used by plants to deal with thermally-challenging
alpine environments. In many alpine systems, including
ours, the growth forms that are most tolerant to low temper-
ature, cushion plants and mats, are followed by small forbs
and rosettes, tussocks, and shrubs (Squeo et al. 1991; Tas-
chler and Neuner 2004; Rada et al. 2019). This ordering is

consistent with patterns of daytime avoidance (decoupling)
observed by us and other authors. It likely reflects a wide-
spread consequence of the physical correlation between day
and night temperatures, shaped by the avoidance-tolerance
trade-off. Thus, mats appear to be maximizing their temper-
ature during the day, perhaps to enhance photosynthesis, at
the expense of heavy investments in cold tolerance, as their
temperatures drop significantly at night. Their rapid heat-
ing may activate photosynthesis early in the morning, but
likely requires heat tolerance at noon. Shrubs, in the other
extreme of the strategy gradient, seem to rely on avoid-
ance of extreme temperatures and require no investments in
physiological tolerance, but may be limited by slow photo-
synthesis due to their low daytime temperatures.

Facilitation: an avoidance mechanism at interspecific
level?

Facilitation in alpine environments is a widespread phenom-
enon at all latitudes (Callaway et al. 2002; Anthelme and
Dangles 2012). It results, in part, from benefactor species
buffering extreme temperatures experienced by other plants
in their vicinity (Callaway et al. 2002; Cavieres et al. 2007;
Anthelme et al. 2014; Pugnaire et al. 2015; Malatesta et al.
2016; Pedraza et al. 2020). Probably because of this, asso-
ciations in our sampling were more frequent and positive
with tussocks, which strongly buffer temperature extremes
in their vicinity (Catorci et al. 2011; Malatesta et al. 2016;
Pedraza et al. 2020), than with thermally-unstable mats.

High-temperature buffering has been found to be the
main driver of facilitation in some mountains (Cavieres et al.
1998; Onipchenko et al. 2009). We lack HT₅₀ data, but, as it
happens at dawn, decoupling at noon and tolerance to heat-
ing are probably correlated, as suggested by published data
(Buchner and Neuner 2003; Sklenář et al. 2023). Alpine-
plant meristems are particularly intolerant to extreme tem-
peratures (Larcher and Bauer 1981; Larcher et al. 2010; but
see von Büren and Hiltbrunner 2022). If the (in)tolerance of
the meristem to overheating is the most important driver of
facilitation, it would explain why bud decoupling at noon
was the best predictor of association strength. However,
decoupling (and probably tolerance) at dawn and at 13:00 h
were strongly correlated, so it is impossible to untangle the
effects of high and low temperature on facilitation strength.

Species that cannot resist extreme temperatures should
be more reliant on facilitators than temperature-resistant
species (Liancourt et al. 2005; Michalet et al. 2006; Maestre
et al. 2009). In line with this idea, cold-tolerant species were
less strongly associated with tussocks or mats than spe-
cies with more positive LT₅₀ values. But, contrary to what
could be expected, species that were able to buffer thermal
extremes by themselves were more strongly associated with
tussocks or mats than species with low avoidance. Given the negative correlation between tolerance and avoidance, it is not surprising that their effects on association strength were opposite, but the question arises about why lack of tolerance rather than avoidance should drive facilitation. Spatial associations are likely the result of greater survival rates, especially those of seedlings, near facilitators (Dahle et al. 2024). Tolerance seems to remain constant over the life cycle of alpine plants (Taschler and Neuner 2004; Rada et al. 2019). In contrast, seedlings may be unable to avoid thermal stress because they are yet to develop the morphological traits that allow them to buffer temperatures, such as thick barks, tall stems, or large amounts of insulating marcescent leaves (Luteyn et al. 1999; Körner 2003). Facilitation, by keeping plants warm at dawn or cool at noon, has the same effect as decoupling. Thus, during early growth, facilitation may be substituting for the capacity of plants to regulate their own temperature, especially in those species that are good avoiders as adults. As plants develop, facilitative decoupling can be replaced by the capacity to decouple autonomously.

## Concluding remarks

Low- and high-temperature avoidance, tolerance, and species interactions were all correlated, leading to diverse trade-offs. Enhanced photosynthesis through daytime warming in some species may come at the cost of nighttime exposure to subfreezing temperatures, likely requiring large investments in cold tolerance. Such costs might only be sustainable if daytime warming does improve photosynthesis. Mats exemplified this strategy. At the other extreme of the trade-off gradient, shrubs avoided extreme temperatures and thus investments in tolerance, but at the cost of typically suboptimal temperatures for photosynthesis. Due to the probable inability of seedlings from avoider species to thermally decouple on their own, tolerance may be essential for establishing in the absence of benefactors. Notably, the two growth forms most tolerant to low temperatures, mats and tussocks, are probably the most important benefactors in this community. This suggests that tolerant species may act as pioneers, establishing on bare soil, and later facilitating colonization by avoider species, which depend on the more stable thermal conditions provided by their benefactors.

Our data and interpretations enable us to build a bridge between two conceptual frameworks applied to arctic-alpine environments and which explain much of the vegetation composition in these systems: plant resistance to environmental stress through avoidance and tolerance, and positive interspecific interactions. We suggest that facilitation can be viewed as a form of avoidance operating at the interspecific level, whereas traditional avoidance acts at the

individual level. These two forms of avoidance appear to be interchangeable throughout the plant life cycle: seedlings relying on benefactors until they develop the necessary morphological traits necessary for autonomous thermal avoidance.

**Supplementary Information** The online version contains supplementary material available at https://doi.org/10.1007/s00035-025-00345-z.

**Acknowledgements** Andrea Campuzano conducted the low-temperature tolerance experiments, and Parque Nacional Izta-Popo-Zoquiapan provided logistic support.

**Author contributions** CM conceived the general research, analyzed the data and lead writing. FA contributed to design the general structure of the paper, provided key conceptual insights, and was very involved in writing. HT and FVR conducted most of the fieldwork and provided feedback on the manuscript.

**Funding** Dirección General Asuntos del Personal Académico-Universidad Nacional Autónoma de México provided funding through grant PAPIIT-IN217607 and through a Programa de Apoyos para la Superación del Personal Académico 6-months sabbatical fellowship to CM.

Data availability Data and code are publicly available in Figshare: https://doi.org/10.6084/m9.figshare.29120249.

## Declarations

**Conflict of interest** The authors declare no competing interests.

**Open Access** This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

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