Received: 18 February 2020 | Revised: 26 October 2020 | Accepted: 22 December 2020 DOI: 10.1002/ece3.7182 ORIGINAL RESEARCH Seeing the wood despite the trees: Exploring human disturbance impact on plant diversity, community structure, and standing biomass in fragmented high Andean forests Mariasole Calbi1,2 | Francisco Fajardo-Gutiérrez3 | Juan Manuel Posada4 | Robert Lücking1 | Grischa Brokamp1 | Thomas Borsch1,2 1Botanischer Garten und Botanisches Museum Berlin, Freie Universität Berlin, Abstract Berlin, Germany High Andean forests harbor a remarkably high biodiversity and play a key role in 2 Institut für Biologie – Systematische providing vital ecosystem services for neighboring cities and settlements. However, Botanik und Pflanzengeographie, Freie Universität Berlin, Berlin, Germany they are among the most fragmented and threatened ecosystems in the neotropics. 3Jardín Botánico de Bogotá José Celestino To preserve their unique biodiversity, a deeper understanding of the effects of an- Mutis, Bogotá, Colombia thropogenic perturbations on them is urgently needed. Here, we characterized the 4Biology Department, Faculty of Natural Sciences, Universidad del Rosario, Bogotá, plant communities of high Andean forest remnants in the hinterland of Bogotá in 32 Colombia 0.04 ha plots. We assessed the woody vegetation and sampled the understory and Correspondence epiphytic cover. We gathered data on compositional and structural parameters and Mariasole Calbi, Freie Universität Berlin, compiled a broad array of variables related to anthropogenic disturbance, ranging Königin-Luise-Straße 6-8, 14195 Berlin, Germany. from local to landscape-wide metrics. We also assessed phylogenetic diversity and Email: [email protected] functional diversity. We employed nonmetric multidimensional scaling (NMDS) to se- Funding information lect meaningful variables in a first step of the analysis. Then, we performed partial re- This research was funded by the Federal dundancy analysis (pRDA) and generalized linear models (GLMs) in order to test how Ministry of Education and Research of Germany (BMBF, ColBioDiv—01DN17006). selected environmental and anthropogenic variables are affecting the composition, We also acknowledge support by the diversity, and aboveground biomass of these forests. Identified woody vegetation Frauenförderung and the Open Access Publication Fund of the Freie Universität and understory layer communities were characterized by differences in elevation, Berlin. temperature, and relative humidity, but were also related to different levels of human influence. We found that the increase of human-related disturbance resulted in less phylogenetic diversity and in the phylogenetic clustering of the woody vegetation and in lower aboveground biomass (AGB) values. As to the understory, disturbance was associated with a higher diversity, jointly with a higher phylogenetic dispersion. The most relevant disturbance predictors identified here were as follows: edge ef- fect, proximity of cattle, minimum fragment age, and median patch size. Interestingly, AGB was efficiently predicted by the proportion of late successional species. We therefore recommend the use of AGB and abundance of late successional species as indicators of human disturbance on high Andean forests. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2021 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 2110 | www.ecolevol.org Ecology and Evolution. 2021;11:2110–2172. CALBI ET al. | 2111 KEYWORDS aboveground biomass, biodiversity, bosque altoandino, Colombia, cryptic forest degradation, understory 1 | INTRODUCTION Bogotá, the capital of Colombia, which is situated at approximately 2,600 m altitude. With a population of around 9 million inhabitants, High Andean tropical montane forests (herein bosques altoandinos) Bogotá is by far the largest city in the Andean high montane forest can be found between ca. 2,700 and 3,300 m in the Northern Andes, belt, putting tremendous pressure on the surrounding ecosystems. extending from Venezuela to Ecuador, with considerable levels of Remnants of high Andean forests near Bogotá are mostly affected by species diversity and endemism (Gentry & Ortiz, 1993; Girardin rural activities, which include logging, fires, and agriculture, typically et al., 2014; Killeen et al., 2007; Still et al., 1999; Young, 1992). resulting in soil compaction, low fertility, and/or erosion (Armenteras These forests provide vital ecosystem services to the neighbor- et al., 2003; Linares & Ríos, 2004; Posada & Norden, unpublished re- ing cities and settlements, such as the regulation of water fluxes sults). Bosques altoandinos in the surroundings of Bogotá have mostly (Armenteras et al., 2003; Chaves & Arango, 1998; Linares & been studied using phytosociological analysis of plot inventory data Ríos, 2004; Rangel, 2000) or carbon capture and storage (Brown & (Avella et al., 2014; Cantillo Higuera & Gracia, 2013; Cleef, 1981; Kappelle, 2001; Torres et al., 2012). Cortés, 2008; Sturm & Rangel, 1985; Van der Hammen, 2008). Bosques altoandinos have been subjected to extensive anthropo- Beyond such floristically oriented approaches, few studies have genic transformation across their natural range. In Colombia, large addressed the effects of disturbance on these forest ecosystems. portions of the forest cover were cleared during the past four centu- Some preliminary research works on forest succession and regen- ries and turned into agricultural or residential areas, in order to satisfy eration were carried out as thesis works (Acuña, 2013; Restrepo the growing demand for resources of an increasing human popula- Abadia, 2016). In a recent study, Rodríguez-Alarcón et al. (2018) tion (Brown & Kappelle, 2001; Cavelier et al., 2001; Etter et al., 2008; found a negative effect of forest fragmentation on functional diver- Heath & Binswanger, 1996; Sánchez-Cuervo et al., 2012; Wassenaar sity and aboveground biomass, a first indication that more complex et al., 2007). Such a reduction of forest cover can not only lead to parameters such as functional diversity are indeed related to ecosys- loss of biodiversity but also to a lower structural integrity and resil- tem services such as carbon storage. However, studies that simulta- ience of the remaining fragments (Mori et al., 2013). Changes in spe- neously consider multiple disturbance predictors and different plant cies composition also go along with shifts in functional diversity and communities response variables were so far lacking. biological interactions (Bovendorp et al., 2019; Diaz & Cabido, 2001; According to the available literature, the most relevant distur- Flynn et al., 2011; Petchey & Gaston, 2002, 2007; Poos et al., 2009; bance factors, which variation proved to be significantly related to Swenson, 2014). Eventually, this affects ecosystem services (González differences in forest species composition or diversity metrics, are et al., 2011; Menon et al., 2007; Rangel, 2000; Torres et al., 2012). as follows: age of forest fragment (Köster et al., 2009; Laurance In the recent past, forest cover has increasingly been monitored using et al., 2006), proximity to houses or roads and people and livestock remote sensing techniques. For the Colombian high Andean forests, this density (Ribeiro et al., 2015, 2016), edge effect, and proximity to has shown modest signs of recovery in some areas (Calbi et al., 2020; pastures (Parra Sánchez et al., 2016; Werner & Gradstein, 2009), as Etter, 2002; Rubiano et al., 2017; Sánchez-Cuervo et al., 2012; but see well as forest cover fragmentation metrics (Fahrig, 2003; Hertzog Anselm et al., 2018). However, remote sensing cannot detect cryptic et al., 2019; Laurance et al., 2006). Nonetheless, it has not yet been forms of forest degradation, such as selective logging or understory tested whether these factors would be still relevant when a larger grazing. Even plot-based surveys focusing on trees may not reveal such number of variables are considered simultaneously. For this reason, alterations. Yet, cryptic forest degradation has significant impact on soil we conducted a comprehensive integrated assessment of the po- erosion, successional dynamics, and regeneration, since understory and tential effects of multiple environmental and disturbance variables epiphytic plants are major drivers of ecosystem functioning (Nilsson on the taxonomic, phylogenetic, and functional diversity of the two & Wardle, 2005). Understanding the effects of anthropogenic distur- main forest layers (tree layer and understory) and on epiphytes cover. bance on all major forest components, that is, tree, shrub, understory, We therefore hypothesized that anthropogenic disturbance as a and epiphyte layers, is therefore essential to elaborate and implement whole, understood as a composite variable sensu Paine et al. (1998), effective strategies for the sustainable management of these forest affects the composition, and aboveground biomass of bosques al- ecosystems (Battles et al., 2001; Fahey & Puettmann, 2007; Halpern toandinos, with impacts on community diversity metrics, that is, & Spies, 1995; Roberts & Gilliam, 1995). In addition, multiple predictor taxonomic, phylogenetic, and functional diversity. We also hypoth- and response variables should be analyzed simultaneously to properly esized that our comprehensive analysis would identify significant