The mountainous region of the Andes is a center of biodiversity and endemism (Myers et al., 2000). In particular, the high Andean forests and páramos contain a high number of plant species in a small area, displaying unique adaptations to extreme environmental conditions (Valencia et al., 2020; Caballero-Villalobos et al., 2021). However, the plants inhabiting these ecosystems are highly threatened by changes in hydrological cycles, temperature increases, and habitat loss, due to anthropogenic activities such as land use change and expansive agriculture (Espitia Villarraga, 2018; Caballero-Villalobos et al., 2021). These activities have also been magnified worldwide by the effects of climate change (Toivonen et al., 2011; Montalvo et al., 2018; Chacón-Moreno et al., 2021; Singh et al., 2021).

Polylepis quadrijuga Bitter is a native tree of the Eastern Cordillera of Colombia and is cataloged as critically endangered (Boza Espinoza, 2023). These plants grow above the treeline (ca. 3,200–3,600 m.a.s.l), below or interspersed with the páramo ecosystem, and despite their limited geographical distribution, they form monodominant but highly diverse forests. It has been documented that these forests contain a variety of endemic and endangered avifauna, such as Diglossa gloriosissima or the yellow-eared parrot (Leptosittaca branickii) (Peña and Rangel, 2007). The trunks of Polylepis harbor numerous species of bryophytes (mosses) and lichens (Pulido Herrera, 2016). Additionally, species of Polylepis provide ecosystem services, acting as carbon sinks, protecting water sources through runoff regulation, reducing soil erosion, and aiding in the retention of nutrients and sediments (Peña and Rangel, 2007; Cuyckens and Renison, 2018; Montalvo et al., 2018; Boza Espinoza and Kessler, 2022).

Despite their importance, Polylepis forests have been exploited for centuries for dendroenergetic purposes (Cuyckens and Renison, 2018; Boza Espinoza and Kessler, 2022). Additionally, the ongoing expansion of agricultural and livestock frontiers has led to the fragmentation and isolation of species such as P. quadrijuga (Ramos et al., 2013; Caballero-Villalobos et al., 2021). These relicts or man-made patches (Toivonen et al., 2011; Rangel and Arellano Peña, 2010) are highly susceptible to climate change due to the stressful conditions caused by high altitudes, low temperatures, and high humidity (Macek et al., 2009; Kessler et al., 2014; Caballero-Villalobos et al., 2021). One approach to understand and identify how different populations of P. quadrijuga respond to the current climatic conditions and anthropogenic disturbance is through the study of functional traits (Violle et al., 2007; Garnier et al., 2015).

Functional traits are morphological, physiological or phenological characteristics that are inherited and that influence fitness (Garnier et al., 2015). Therefore, functional traits help us understand how populations respond to the biotic and abiotic factors of a specific habitat. For instance, it has been found that altitudinal gradients (Rozman et al., 2013; Pandey et al., 2018), fragmentation (Ramos et al., 2013), mining, agricultural and livestock activities (Ding et al., 2012; Soteras et al., 2016; Ji et al., 2022), and the composition and interactions of soil microbiological communities can alter the functional diversity (Soteras et al., 2016; Gazol et al., 2017) and increase the intraspecific variability of species (Aubin et al., 2016; Gazol et al., 2022). Additionally, anthropogenic disturbances, such as land use changes and fragmentation, significantly impact abiotic conditions such as soil nutrients and moisture, temperature, and light levels (Vitousek et al., 1997). These disturbances can favor species or individuals with specific functional traits and reduce trait diversity in a population or community, which can in turn, affect ecosystem functioning and increase competitive exclusion (e.g., Flynn et al., 2011; Laliberté and Tylianakis, 2012; Mouillot et al., 2013).

Previous studies on functional traits in Polylepis species, such as P. tarapacana (distributed in Peru, Chile, Bolivia, and Argentina), which has a near threatened conservation status (Boza Espinoza, 2023), have found a complex interplay between water stress, elevation (Hertel and Wesche, 2008; Macek et al., 2009; Toivonen et al., 2018), nutrient availability (Toivonen et al., 2014) and seasonality (Kessler et al., 2014). These factors have a greater effect on trees than anthropogenic disturbance (e.g., fire, fragmentation and/or agricultural practices; Soteras et al., 2015; Soteras et al., 2016). Polylepis tarapacana is distributed in countries with stronger temperature seasonality and in drier conditions, therefore, we expect a different functional response compared to P. quadrijuga. Additionally, the severe fragmentation experienced by P. quadrijuga populations, will likely cause a different functional response, compared to P. tarapacana. Plants exposed to higher abiotic stress in response to low temperatures and high solar radiation, rather than recent anthropogenic disturbance (Ramos et al., 2013; Weemstra et al., 2016) will show conservative trait values. This would be reflected in higher specific leaf area (SLA) (Weemstra et al., 2016), wood density (WD) (Garnier and Navas, 2012; Reich, 2014), leaf thickness (LT) (Macek et al., 2009) and leaf dry matter content (LDMC) (Garnier and Navas, 2012), and lower values of leaf area (LA) (Ramos et al., 2013; Macek et al., 2009) and branching frequency (BF) (Semchenko et al., 2018). Conversely, plants associated with anthropogenic disturbance will tend to have acquisitive functional trait values, such as high values of specific root length (SRL) (Wright et al., 2004; Weemstra et al., 2016; Bergmann et al., 2020), root tip abundance (RTA) (Hertel and Wesche, 2008), root branching index (RBI) (Pierick et al., 2021) and low values of root diameter (ARD) (Ma et al., 2018; Bergmann et al., 2020) and root tissue density (RTD) (Bergmann et al., 2020) (Supplementary Table S1).

There are also substantial knowledge gaps regarding the belowground symbiosis in the genus Polylepis, such as the association with mycorrhizae, which has only been assessed in P. australis (Menoyo et al., 2007; Menoyo et al., 2009; Soteras et al., 2013; Soteras et al., 2014; Soteras et al., 2015; Soteras et al., 2016). Colonization by symbionts, such as N-fixing bacteria and mycorrhizae are key to enhance the nutrient uptake capacity of plants and is considered as a belowground functional trait (Pérez-Harguindeguy et al., 2013). In P. australis, the arbuscular mycorrhizal fungi (AMF) communities are present under various types of disturbances, such as grazing or fire, and no significant differences in colonization have been found between these disturbances. However, other studies in tropical mountains have shown that anthropogenic disturbance, such as intensive land use (Barnola and Montilla, 1997) and fertilization (Jefwa et al., 2012), significantly reduces fungal communities and colonization (Ji et al., 2022). This could decrease, in turn, the nutrient uptake by plants and affect their growth and survival (e.g., Begum et al., 2019).

Regardless of whether populations experience human disturbance, we expect individuals of P. quadrijuga to exhibit a coordinated functional response (e.g., Messier et al., 2017; Carvalho et al., 2020). This expectation is supported by the fact that traits are interlinked in a plant’s growth, survival and reproduction, and these share similar environmental pressures. Therefore, both sets of traits should respond in unison (Violle et al., 2007; Reich, 2014; Messier et al., 2017). Previous studies at the local scale (Hu et al., 2019) have shown a coordination between leaf and root traits, aligning with the “do it yourself” strategy (Bergmann et al., 2020). These traits have proven to be reliable indicators of plant metabolic activity in response to environmental factors such as temperature in temperate regions (Ding et al., 2024) and the degree of succession (Hu et al., 2019). Generally, traits tend to be more conservative in colder climates and later successional stages.

In this study, we aim to evaluate the intraspecific functional trait variability between different populations of Polylepis quadrijuga (Rosaceae) with two levels of disturbance (measured as the proximity to anthropogenic activity and fragmentation) and conservation in high-Andean forests of the Colombian eastern mountain range. We expect to find (1) a functional conservation strategy for populations with high abiotic stress and low anthropogenic disturbance, and an acquisitive strategy for high anthropogenic disturbance sites. (2) We also hypothesize that AMF colonization will be impacted by anthropogenic disturbance, similar to what has been shown in species from tropical mountains. (3) We anticipate a functional coordination between above- (leaves and stems) and belowground traits (roots) of P. quadrijuga. This knowledge is critical in the establishment of conservation strategies for an endangered species such as P. quadrijuga, taking into account the anthropogenic pressures experienced by different populations.

Our analyses show that Polylepis quadrijuga responds to different environmental changes caused by anthropogenic disturbance. According to our first hypothesis, we expected that individuals under high disturbance (road fragmentation, near crops and livestock) would have trait values reflecting an acquisitive strategy. Based on our results, populations exposed to a high disturbance level mainly differed in aboveground functional traits and had higher values of leaf area (LA) and specific leaf area (SLA), and lower values of leaf dry matter content (LDMC) and wood density (WD), compared to populations with a low disturbance level. These traits are characteristic of an acquisitive functional strategy (Wright et al., 2004; Reich, 2014), which is in line with our hypothesis. In the second hypothesis, we expected less AMF colonization in highly disturbed sites in response to land use change, which our results corroborated (Figure 4). For the last hypothesis, we had proposed that there would be coordination between above- and belowground traits. We found that these traits are not coordinated, and root traits are more similar between disturbance levels (Figure 3).

Climate was similar for páramo sites that were located nearby (Supplementary Figure S1). Therefore, locations such as SFF-La Rusia (East) and Sumapaz-Guerrero only differed in their levels of disturbance (low and high, respectively), yet displayed varying responses in both above- and belowground functional traits. This response aligns with findings from previous studies in Polylepis (Toivonen et al., 2014), indicating that functional traits not only respond to shifts in climate but also to the specific requirements of each species (Martínez-Vilalta et al., 2010). In this case, to stress conditions that may be caused by anthropogenic activities. Likewise, increased disturbance levels in tropical mountain ecosystems (e.g., shifting cultivation and logging) intensify the impact of abiotic filters, leading to the emergence of species with traits tailored to such disturbances (Ding et al., 2012; Feng et al., 2014; Singh et al., 2021). In this regard, P. quadrijuga populations exhibit a functional response to the anthropogenic alterations they have undergone in recent decades, including deforestation (Caballero-Villalobos et al., 2021) and fragmentation for agricultural purposes (Ramos et al., 2013; Boza Espinoza and Kessler, 2022). As a result of these anthropogenic activities, most Polylepis forests are currently restricted to areas that are difficult to access (Kessler et al., 2014; Toivonen et al., 2018).

On the one hand, individuals in sites with high disturbance levels may exhibit significantly different functional traits, potentially facilitating rapid growth and reproduction (an acquisitive strategy). This could be attributed to intense trait filtering, which enables them to mitigate the diverse environmental changes induced by the disturbance (Schellenberger Costa et al., 2017). High trait values of LA, SLA and LT had been reported in fragmented populations of P. quadrijuga as a strategy for light harvesting (Velez et al., 1998; Ramos et al., 2013). Individuals exposed to the edge also changed their leaf composition by increasing the lignin content in the parenchyma, antioxidant and flavonoids substance to reduce photo-oxidation damage (Velez et al., 1998; Ramos et al., 2013). Nevertheless, the trend of increasing leaf size with leaf thickness represents a unique functional pattern observed in P. quadrijuga. In other Polylepis species, an increase in leaf size is typically accompanied by a decrease in leaf thickness (Macek et al., 2009; Toivonen et al., 2014).

On the other hand, sites with low disturbance have conservative functional traits: plants invest more carbon in leaf and stem tissues, so their growth is slow as a response to the abiotic filters of their environment (Reich, 2014; Firn et al., 2019). Populations of P. quadrijuga in these sites also tend to have thinner leaves (Figure 4: LA). Interestingly, this pattern contrasts with previous findings where low SLA and high LDMC were associated with low water and nutrient availability in P. rugulosa, P. tarapacana and P. tomentella (Macek et al., 2009). However, recent studies have shown that SLA is not a good indicator of the nutrient amount in the soil because it also changes with light intensity (Hodgson et al., 2011; Singh and Negi, 2018; Firn et al., 2019). The observed high LDMC values in this study may represent a response to environmental conditions that could potentially cause damage, such as wind, sun, or hail (Pérez-Harguindeguy et al., 2013). Structural responses to environmental harshness such as low temperatures, rather than by anthropogenic disturbance, have also been observed in P. subsericans (Toivonen et al., 2018), P. racemosa, P. pauta, P. sericea, P. pepei (Kessler et al., 2014), P. tomentella, P. rugulosa and P. tarapacana (Macek et al., 2009).

The lack of coordination between the leaf economic spectrum (LES) and root economic spectrum (RES) observed in our study could be attributed to root traits responding multidimensionally to biotic and abiotic factors (Weemstra et al., 2016). Interestingly, sites with low disturbance levels have more compact soils (high apparent density) and display roots with lower root diameter (ARD) and higher branching frequency (BF) values (Ma et al., 2018; Semchenko et al., 2018). Such traits are typically suited for soils that are easy to explore, which is not ideal for compact soils (Weemstra et al., 2016; Bergmann et al., 2020). Consequently, the roots of these populations may rely on the colonization of arbuscular mycorrhizae (AMF) to acquire the necessary nutrients (Barnola and Montilla, 1997). Therefore, root responses may not align as clearly with the LES gradient. Additionally, of the seven belowground functional traits evaluated, only three showed significant differences between high and low disturbance sites. This finding is consistent with other studies on Polylepis, which have noted that belowground traits do not tend to vary as much as the aboveground and do not clearly align with a RES strategy (Hertel and Wesche, 2008; Toivonen et al., 2014; Valverde-Barrantes, et al., 2016).

Previous findings have shown that AMF colonization does not necessarily correlate with an increase in ARD (Maherali, 2014) and, in more acidic soils, AMF plays an important role in nitrogen (N) uptake (Camenzind et al., 2016). Although, in our study there was no evidence of differences in soil N content between sites, there is a greater limitation of N at higher elevations in tropical mountains (Soethe et al., 2008; Fisher et al., 2013). Additionally, we found a lower percentage of AMF colonization in sites with a high level of disturbance. It is possible that the colonization of AMF in P. quadrijuga is less resilient to anthropogenic disturbance compared to P. australis (Soteras et al., 2015; Soteras et al., 2016). One possible reason for this difference could be the specific environmental conditions of tropical mountains where P. quadrijuga is found. Previous studies have shown that AMF colonization in tropical mountains subjected to agrochemicals, tillage, or human management significantly decreases their colonization rate (Barnola and Montilla, 1997; Jefwa et al., 2012).

This is the first study (we know of) exploring the intraspecific functional trait variability of P. quadrijuga under different disturbance levels. Our findings underscore the sensitivity of this species to anthropogenic disturbance, but also its resilience. Polylepis quadrijuga exhibits high plasticity in its aboveground functional traits, enabling it to adjust its ecological performance in response to both abiotic and anthropogenic disturbances, such as land use change and fragmentation. This plasticity may be crucial for resisting stress and invasive species (Ferrero et al., 2022; Kaushik et al., 2022). We recommend conducting more detailed studies on the effects of anthropogenic activities such as cattle ranching, fire, or mining on the functional traits and interactions between foliar and root traits of each Polylepis species. In addition, it is important to study the AMF associated with P. quadrijuga and to evaluate how the identity of the fungi changes with disturbance. This information could be key in restoration efforts of P. quadrijuga’s monodominant forests. Further research is also needed to enhance our understanding of the microclimate in these populations. Studies on P. quadrijuga have used platforms like WorldClim (Fajardo-Gutiérrez et al., 2018; Caballero-Villalobos et al., 2021; Bedoya-Canas et al., 2024), which may not yield precise results for an accurate climatic characterization of these populations. Therefore, it is important to use on-site climatic sensors to understand the microclimatic conditions of these populations. As observed in this and other studies in Polylepis (e.g., Hertel and Wesche, 2008; Macek et al., 2009; Toivonen et al., 2011; Toivonen et al., 2014; Ramos et al., 2013), the functional traits of P. quadrijuga adjust to various biotic and abiotic conditions. It is crucial to determine and implement conservation and restoration strategies for these forests, which provide numerous ecosystem services. Conservation efforts for P. quadrijuga should prioritize fragmented populations or those facing stressful conditions such as livestock grazing or agricultural activities. These strategies should aim to create microhabitats that promote the establishment of this endangered species.