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Biodiversity and Conservation

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Open Access 22-10-2024 | Original Research

Prioritization of important plant areas for conservation of frailejones (Espeletiinae, Asteraceae) in the Northern Andes

Authors: Clara Morales-Rozo, Ian S. Acuña-Rodríguez, Juan C. Benavides, Víctor J. Rincón-Parra, Mauricio Diazgranados

Published in: Biodiversity and Conservation | Issue 14/2024

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Abstract

The tropical Andes region harbors areas that are highly significant for biodiversity at both global and local scales. However, despite the severe conservation threats that this region has to confront, conservation initiatives are limited, by funding and because of the need for more information to decide which areas are priorities for conservation. Identifying Important Plant Areas (IPAs) offers a valuable methodology for establishing conservation priorities, a particularly complex task in a mega-biodiverse region such as the northern Andean tropics. Due to its iconic recognition and conservation value, this study focused on the Espeletiinae subtribe (Asteraceae) as a model group; hence, the distribution data for 138 species was compiled from 5560 georeferenced records. Using the IPA methodology, we divided the study area, this is, the distribution area of the subtribe in the Andean tropics, into 220 Units of Analysis (UA) represented by 10 × 10 km plots. Refined species’ distribution areas, incorporating richness, threatened species, and ecosystem-based richness distributions, were analyzed using newly generated maps to evaluate the conservation value of each UA. Our analysis identified 176 UAs with some level of relevance using sub-criterion cA1 (with 59 species) and 51 UAs using sub-criterion cB (with 76 species). Integrating both criteria, we classified 11 UAs as high-priority, 62 as medium-priority, and 147 as low-priority, highlighting the IPAs that require focused conservation efforts. Two identified high-priority IPAs are located in Venezuela and nine in Colombia, predominantly associated with the Eastern Cordillera. These areas concentrate between 7 and 12 species. They are mainly linked to the páramo complexes of Colombia and the Sierra Nevada in Venezuela, primarily within Cool Temperate Moist Grassland ecosystems on mountains. Our results provide a spatial planning procedure and analytical tool for decision-makers to guide conservation management and actions across northern Andes.

Supplementary Material 1. Location of all High-priority Important Plant Areas of frailejones (Espeletiinae, Asteraceae) in the Northern Andes Supplementary file1 (DOCX 4831 KB)

Communicated by Daniel Sanchez Mata.

Supplementary Information

The online version contains supplementary material available at https://doi.org/10.1007/s10531-024-02939-1.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Introduction

Biodiversity is declining at an accelerated rate in the current century. About 25% of the animal and plant species assessed worldwide are under some risk of extinction, suggesting that nearly one million species face possible disappearance (Antonelli et al. 2020; Nic Lughadha et al. 2020). The primary threat to plant diversity, particularly in the tropics, is habitat loss and fragmentation (Steege et al. 2015). This is exacerbated by converting tropical forests into pastures and commercial monocultures, which has replaced small-scale farming, encouraging forest loss and diminished ecosystem services (Dirzo et al. 2014; Ferrer-Paris et al. 2019; Kleemann et al. 2022). Conservation efforts for plant diversity are often hindered by a lack of current, accessible information, which complicates the prioritization of conservation actions (Darbyshire et al. 2017; Neo et al. 2021; Paton et al. 2020). Moreover, fewer plant-based conservation initiatives receive substantially less support than those focusing on animals (Margulies et al. 2019). Therefore, there is an urgent need to identify plant conservation priorities, with this information made readily available to policymakers at all levels to enhance conservation decision-making.

Conservation efforts often prioritize areas with the most diversity in response to the biodiversity crisis. However, these efforts are often hampered by a lack of information, limited access to up-to-date information, or outdated information that prevents prioritizing conservation actions (Darbyshire et al. 2017; Neo et al. 2021; Paton et al. 2020). The impact of outdated or inaccessible data on plant diversity is significant, further complicating the process and severely limiting the ability to make informed decisions. By contrast, due to its more familiar recognition (compared with plants), or to its more iconic effect, animal wildlife groups are most used to determine conservation areas (e.g., specific points of residence) and their management priorities (e.g., initiatives such as the Important Bird Areas (IBAs) and Key Biodiversity Areas (KBAs) (BirdLife 2014; Smith et al. 2018). Nevertheless, despite the essential ecological role of plants as primary producers, they are often under-represented in conservation research (Di Marco et al. 2017) and are frequently absent in global or national conservation planning schemes (Corlett 2016). In this regard, the identification of Important Plant Areas (IPAs) (Darbyshire et al. 2017; Plantlife 2018) may contribute to fulfill pivotal gaps of information that are crucial for conservation of functional ecosystems, such as the biodiversity distribution of the primary producers of the targeted habitats. This appears to be especially relevant in biodiverse regions such as the tropics, in which where a wide variety of plant communities coexist at local scales, underpinning ecosystems ecology structurally, with exceptional concentrations of endemic species, as well as being a key source and sink of Neotropical plant diversity (Myers et al. 2000; Pérez-Escobar et al. 2022).

In brief, the IPAs methodology considers species richness and geographical extent, prioritizing both, the threatened plants and their habitats, by identifying critical sites in which conservation efforts should be focused (Plantlife 2018). The methodology is based on three criteria: threatened species (A), botanical richness (B), and threatened habitats (C). Each criterion is assessed systematically across the area of interest under different metrics, and IPAs are selected as those zones in which adequate conditions of each criterion converge (Plantlife 2018). IPAs have been implemented in many countries in the last two decades, showing their value by providing information to practitioners and policymakers involved in conservation at national and regional levels. In Europe, this approach has been implemented in places such as Ireland (Walsh et al. 2019), Italy (Blasi et al. 2011a, b; Marignani and Blasi 2012), Spain (Sánchez de Dios et al. 2017), and the United Kingdom, in which candidate sites for IPAs were identified based on the knowledge of both the vascular flora and fungal diversity (Clubbe et al. 2020). Outside Europe there are some examples in Malaysia (Hamidah et al. 2020) and Saudi Arabia (Al-Abbasi et al. 2010), from which several lists of threatened and endemic plant species have been produced (Couch et al. 2019a, 2019b; Darbyshire et al. 2019). In the Americas, the IPAs methodology has been mainly implemented in low-lands tropical ecosystems (i.e., rainforest, cloud forests, and montane habitats) through the Tropical Important Plant Areas (TIPAs) program (Anderson et al. 2016), this, due to their characteristic as biodiversity hotspots (Myers et al. 2000). In addition, a methodology for IPA identification in Colombia has been proposed based on the global IPA criteria, adjusting for the country’s rich diversity and the lack of reliable species distribution data to promote plant information in biodiversity conservation planning (Diazgranados and Castellanos 2018). This methodology has been recently applied to evaluate useful plants from Colombia (Kor et al. 2022; Kor and Diazgranados 2023). However, this approach has not been implemented in other areas or with other species groups.

The northern tropical Andes is one of the planet’s most significant biodiversity hotspots (Myers et al. 2000). Covering approximately 158 million hectares (Agudelo-Hz and Armenteras 2017), this region hosts about 6.7% of the world’s endemic plant species (Myers et al. 2000) and 55% of South America’s flora (Jørgensen et al. 2012), with an endemism rate of 60% (Buytaert et al. 2011). This region extends from 11°N n the northernmost tip of South America to 23°S in northern Argentina, and is characterized by varied mosaics shaped by the spatial and environmental heterogeneity promoted by its stunning topography (Herzog et al. 2012; Tovar et al. 2022). The ecosystems that it harbors provide essential services such as soil protection, carbon storage, and water supply for millions of people (Buytaert et al. 2011; Diazgranados et al. 2021; Peters et al. 2019; Rowland et al. 2019), supporting the livelihoods of over 50 million individuals (Cincotta et al. 2000). However, despite their significance, the region’s mountain ecosystems still need to be studied. Recent research has advanced our understanding (e.g., Berrio-Giraldo et al. 2021; Cuesta et al. 2020; Feeley et al. 2011; Gámez et al. 2020; Kolář et al. 2016; Mavárez et al. 2019), but there remains a dearth of large-scale studies assessing biodiversity trends, the role of threatened species, and overall species richness and ecosystem richness. Addressing these gaps is an essential research priority for this decade (Christmann et al. 2023; Gleeson et al. 2016).

As a good example of the biotic response to the environmental variability of the Andean tropics, the Espeletiinae subtribe (Asteraceae) stands out as one of the most diverse and specialized plant groups in the region, showing remarkable taxonomic, morphological, and ecological variation among tropical high-elevation species (Diazgranados 2012a, b, c; Diazgranados and Barber 2017; Mavárez 2019; Pouchon et al. 2021). This subtribe exemplifies some of the fastest adaptive radiation on the planet (Madriñán et al. 2013; Pouchon et al. 2018) suggesting great versatility to cope with different environments. Species of Espeletiinae range from the lower limits of montane cloud forests (~ 1300 m) to the edges of tropical glaciers (~ 4600 m) (Diazgranados 2012a, b, c). They display growth forms, from trees to giant and dwarf rosettes and decumbent forms (Monasterio and Sarmiento 1991; Rada et al. 2019). The Rosettes have evolved independently in several mountainous regions worldwide, including East Africa, Hawaii, and the Tropical Andes (Hedberg and Hedberg 1979; Monasterio and Sarmiento 1991; Rada 2016).

In the Andean tropics, this subtribe is widely distributed and abundant across the high Andean forest and páramos of Colombia and Venezuela, with a more limited presence in Ecuador, where only one species is found in the northern and the Sierra de Llanganates (Diazgranados 2012a; Pouchon et al. 2018). Within its distribution, the Espeletiinae species serve as biodiversity surrogates. First, they act as ecosystem engineers by increasing local organic matter and nutrient content, reducing daily soil temperature fluctuations and freezing events, and enhancing nearby vascular plant diversity and cover (Mora et al. 2019). Second, their standing dead biomass, including decaying leaves, supports diverse insect and decomposer communities (Ancona et al. 2005; Sturm 1990). Third, their rhizosphere hosts a variety of microbiota, including mycorrhizae and phosphorus solubilizers (Cepeda et al. 2005; Garcés et al. 2005). Furthermore, Espeletiinae species play a crucial role in pollination networks within high-altitude tropical ecosystems (Berry and Calvo 1994b, a; Pelayo et al. 2019, 2021). In addition, this group of plants has been extensively studied, so there is sufficient information on the threat categories based on the IUCN Red List of Threatened Species (IUCN 2022a) and accessible geographical data on their geographic distribution (Instituto de Investigación de Recursos Biológicos Alexander von Humboldt 2016) to enable the implementation of the IPA methodology.

Building on the previous work on identifying IPAs in tropical countries (Diazgranados and Castellanos 2018), we aimed to apply the IPA methodology in a highly biodiverse region, specifically in the northern tropical Andes. One of the challenges in prioritizing areas for biodiversity conservation in tropical regions and developing countries is more abundant and reliable data. To address this, we gathered high-quality georeferenced data for all the Espeletiinae species across their entire distribution range, covering Ecuador, Colombia, and Venezuela. We identified potential IPAs for these plants and discussed the methods, criteria, and challenges in managing occurrence data and associated metadata. This study represents the first regional-level application of the IPA concept in the northern Andes. It provides a practical example of a systematic conservation approach to Espeletiinae, whose species are cataloged as flag, umbrella, and key species, which makes them a practical example of biodiversity surrogates, contributing to maintaining ecosystems, their ecosystem services and the associations with more than 125 animal species (Diazgranados 2012a, b, c; García et al. 2005).

Materials and methods

Study area

Our study aimed to prioritize conservation areas for all species within the Espeletiinae subtribe. We used the entire reported distribution range of the subtribe across Ecuador, Colombia, and Venezuela, where nearly 80% of the species occur between − 70.5° and − 73°W longitude and 5.5° and 9°N latitude (Diazgranados 2012a). The elevation range of Espeletiinae spans from approximately 1300 m to over 4000 m. However, we set the minimum elevation used since the limit was 1000 m as the lower cut level to establish our area. Consequently, the study area was delimited by geographic coordinates 66°W to 81°W and 6°S to 12°N, encompassing a total area of 320,502.79 km² (Fig. 1).

We created a mask to include the land above 1000 m of elevation by utilizing the contour tool from ArcMap v10.5 (ESRI 2011). This polygon was based on the 90-m resolution DEM from the Shuttle Radar Topographic Mission (SRTM) (Jarvis et al. 2008) and the plant record coordinates. Subsequently, we rasterized the study area polygon into 10 × 10 km cells, which acted as the units of analysis (UA) for the entire study area (Fig. 2 numeral 2). Following the concept of representativeness of Systematic Conservation Planning (Margules and Sarkar 2007), the chosen size of UAs effectively captures the geographical heterogeneity of the study area. Combining this with a scoring procedure (classification system) allows for assigning a value to each UA based on its importance in biodiversity (Walsh 2016). This evaluation is based on one or more criteria, such as species richness, rarity, and habitat (Hamidah et al. 2020). The R package “raster” (Hijmans 2017) was used to create the rasterized polygon. We assigned a unique identification number to each UA, to assess the IPA criteria, resulting in the identification of a total of 4101 UAs.

Quality assessment of data and georeferencing

We used georeferenced occurrence data of the subtribe Espeletiinae (hereafter: the “records”) available from the Global Biodiversity Information Facility (GBIF 2022) and the Instituto de Investigación de Recursos Biológicos Alexander von Humboldt (Castellanos and Diazgranados 2016). We based our taxonomic classification system on Diazgranados and Barber (2017) and Cuatrecasas (Cuatrecasas 1976a, b), which is still broadly used by many herbaria. This classification includes 8 genera: Carramboa Cuatrec., Coespeletia Cuatrec., Espeletia Mutis ex Humb. & Bonpl., Espeletiopsis Cuatrec., Libanothamnus Ernst, Ruilopezia Cuatrec. Tamania Cuatrec. (Cuatrecasas 1976a, b) and Paramiflos Cuatrec. (Cuatrecasas 1995). A recent classification (Mavárez 2021) proposes only one genus (Espeletia). Being aware there are ongoing efforts by various labs to redefine the classification of the group, we decided to maintain Cuatrecasas’ system. Full species names including authors can be found in the supplementary information (Fig. 2 numeral 1, Online Resource TS1).

The compiled information was checked for quality and precision following a set of standardized criteria: (i) duplicate coordinates were removed; (ii) records whose coordinates only had one or no decimal positions or with a precision lower than 10 km were revised in Google Earth Pro (v. 7.3.6.9345), validating the reported data only if the record occurred in the geographic areas reported for the subtribe (Diazgranados 2012b, 2012a; Mavárez et al. 2019; Mavárez 2021); (iii) records found within anthropic Corine land cover types (Tsendbazar et al. 2020), such as Cultivated (n = 161, 3%) or Urban / built up (n = 26, 0.5%), as well as those on permanent water bodies (n = 9, 0.2%) or Snow and Ice lancovers (n = 6, 0.1%), were filtered out; (iv) species names were reconciled using the taxonomic backbone of Plants of the World Online (POWO 2023; http://www.plantsoftheworldonline.org), which was also used as a reference for the genera classification; and v) species were considered threatened according to the classification on the IUCN Red List (IUCN 2022a) including: critically endangered (CR), vulnerable (VU), or endangered (EN). As a result of the quality-check process, we consolidated the most up-to-date species data for the Espeletiinae subtribe, with updated calculations based on threat and richness criteria.

IPAs criteria

Our work builds upon a previous proposal to implement IPAs (Diazgranados and Castellanos 2018). This proposal draws on the global IPA criteria (Darbyshire et al. 2017; Plantlife 2018), with some adjustments to account for the region’s rich diversity and the challenges of accessing sufficient reliable species distribution data. The methodology addresses the following steps that are involved in the process of IPA prioritization: (i) Identification using existing data and specified criteria; (ii) Confirmation through field surveys; (iii) Delineation of geographical boundaries; and (iv) Validation and Publication. We focus on the first, based on the available records.

We applied thresholds defined in the methodology under criteria A and B only (see below), as our focus is on the Espeletiinae subtribe as biodiversity surrogates (Table 1). The exact sub-criteria applied were chosen based on the data availability. We did not evaluate the third criterion (C) that indicates “The area constitutes an extraordinary case of habitat, vegetation type or ecosystem in a national, regional or global context”, considering that this research focused on a botanical group and not on an area or habitat. The methods applied for the different criteria and sub-criteria are described below. All processes were automated in the R language and statistical environment v.4.3.1 (R Core Team 2023), using the packages: rgdal (Bivand et al. 2017), raster (Hijmans 2017), sp (Bivand et al. 2013), ggplot2 (Wickham 2016) and vegan (Oksanen et al. 2014).

Table 1

Evaluated criteria and applied methodology

IPA higher level and sub-criteria	Thresholds (Diazgranados and Castellanos 2018)	Global thresholds (Darbyshire et al. 2017)
(cA) Threatened species
cA1: Globally threatened species	Sites supporting ≥ 1% of the population are registered	Sites are known, thought, or inferred to contain ≥ 1% of the global population AND/OR ≥ 5% “best sites” for that species nationally, whichever is most appropriate
cA3: Nationally threatened species (criterion A3 was taken as inclusive of A2)	Sites supporting ≥ 10% of the national population
cA4: Highly restricted range endemic (HRR) species	Site supporting ≥ 10% of the population with a range of highly restricted endemic (HRR) species (EOO ≤ 100 km²)
cA5: Range-restricted endemic (RRE) species	Site supporting ≥ 10% of the population with a range-restricted endemic (RRE) species (EOO > 100 km² y ≤ 5000 km²)	Not included
(cB) Botanical richness
cB1: Highest estimated richness of the ecosystem type	Sites that contain the highest estimated species richness by type of ecosystem	For each habitat or vegetation type: up to 10% of the national resource can be selected within the whole national IPA network OR the 5 “best sites” nationally
cB2: Areas that together support 10% of an ecosystem’s diversity	Sites with estimated plant richness complementary to B1 so that together they add 10% of the total ecosystem diversity	Not included

List of criteria applied in this evaluation for the development of the conservation proposal of Espeletiinae based on the Important Plant Areas (IPAs) methodology. The assessment thresholds applied (Diazgranados and Castellanos 2018) are listed compared to those proposed globally (Darbyshire et al. 2017)

We applied criterion A (cA), which entails that “The site supports significant, viable or potentially viable populations of one or more globally, regionally or nationally threatened species” has six sub-criteria (or indicators), where the cA1, cA2, and cA3 based on the extinction risks of the different species, the cA4, and cA5 on endemism’s and the cA6 on species of particular interests (axiophytes) (Table 1). Based on the consolidated dataset, we focus on cA1, cA3 (assuming it includes cA2), cA4, and cA5. For criteria cA1 and cA3, we used global threat IUCN classifications, and those with a national classification were considered (Diazgranados and Castellanos-Castro 2021; IUCN 2022a). For criterion cA1, we selected the species under the prioritized threat categories, considering the count of their occurrences within UA. We calculated the occurrence for each species in a UA over the total possible number of species in a UA. Based on this value, we evaluated those UAs that contained at least 1% of the threatened species. We followed the same procedure to evaluate cA3, selecting the UAs that contained at least 10% of the species (Fig. 2 numeral 3).

We used the highly restricted range (HRR) for criterion cA4, whose area of occurrence was ≤ 100 km². Criterion cA5 considered the restricted range (RRE) whose extension area of occurrence was > 100 km² but ≤ 5.000 km², following the concepts of Diazgranados and Castellanos (2018) and IUCN (2022b) (Table 1; Fig. 2 numeral 3). To obtain sub-criteria cA4 and cA5, we calculated the extent of occurrence (EOO) for each species by determining its minimum convex polygon for each species with function “ConBatch” available in the R-package rCAT (Joppa et al. 2016; Moat 2020). We counted species within each UA considering the previously mentioned areas (HRR and RRE) and calculated each UA’s occurrence percentage over the total, prioritizing those UAs that contained at least 10% of the total estimated species richness of each ecosystem (Fig. 2 numeral 3).

For criterion B (cB) (Table 1), we identified the UA with the highest species richness within each ecosystem type (B1). We calculated the Chao1 index using the “Specpool” function from the R-package vegan, which estimates species richness based on Espeletiinae records within each UA and ecosystem type. We then selected the UA with the highest estimated richness according to the Chao1 index for criterion B1 (Chao and Jost 2012). To calculate criterion B2, we used UAs prioritized in criterion cB1 that contained complementary species. We aggregated these UAs with different species until we reached at least 10% of the total complementary richness per ecosystem (Fig. 2 numeral 3). We used the World Terrestrial Ecosystems data layer (Sayre 2022), with a spatial resolution of 250 m, to delimit the ecosystems for this analysis in each UA. This map integrates global climate and terrain settings with vegetation and land cover types, identifying 431 distinct ecosystems worldwide (Sayre 2022; Sayre et al. 2020).

Mapping IPAs

We followed a systematic procedure to prioritize Important Plant Areas (IPAs) in the northern Andes. We assessed all UAs that met the thresholds outlined in Table 1 for each subcriterion and applied a scoring scale based on two factors: (i) conservation concern and (ii) species richness. For criterion A, we classify the conservation concern UAs with a score from 1 (lowest value) to 4 (highest value). We assign the highest value to highly restricted range endemism (HRR) species, assuming that the extent of the area of occurrence is more crucial than the threat. For species richness, we used Jenks Natural Breaks to categorize UAs from lowest to highest, where the lowest value indicates the lowest species richness and the highest value indicates the highest species richness for each UA. Each resulting UA was superimposed on the terrestrial ecosystem map for criterion B to identify the matching ecosystems and applied the same scoring approach.

We combine the scoring results of each criterion from the sum of these scores to obtain a new overall score (Fig. 2 numeral 4). This approach aligns with similar methodologies used in previous studies (Blasi et al. 2011a, b; Walsh et al. 2019). Based on their scores, UAs were classified as high, medium, or low priority. For the spatial representation of the IPAs, we utilized ArcMap’s “Calculate Field” tool to organize and display the classifications according to their priority levels (high, medium, and lower).

Results

Criteria evaluation and IPAs-identification

We identified 138 species belonging to eight genera within the subtribe Espeletiinae: Coespeletia, Espeletia, Espeletiopsis, Libanothamnus, Paramiflos, Ruilopezia, and Tamania. These taxa were derived from a comprehensive analysis of 5560 records across 220 UA (Online Resource TS1). Initially, we had 7129 records, but after applying filtering criteria, we narrowed the database down to 5560 records (78% of the original), most due to geographical issues, such as low-precision coordinates, or plant records outside the designated study area (26% of the original). By implementing quality control measures for georeferencing and data assessment, we compiled a robust database that provides valuable insights into the distribution patterns, richness, conservation status, and extent of occurrence of the species composing the Espeletiinae subtribe. The top five species with the largest number of records in the database were: E grandiflora (569 records, 10%), E. schultzii (338, 6%), E. corymbosa (299; 5%), and E. hartwegiana (277; 5%). Most records corresponded to species within the genus Espeletia (3428 records, 62%), followed by Espeletiopsis (908; 16%), Ruilopezia (394; 7%), Coespeletia (332; 6%), Libanothamnus (269; 5%), Carramboa (112; 2%), Paramiflos (79; 1%) and Tamania (38; 1%).

For cA1 (UAs with proportion of globally threatened species above 1%), we identified 176 UAs (4.3%, of the study area). The 176 selected UAs contained 59 species (39% of the subtribe) represented by 343 records (6% of the study area, Table 2). The main species under a globally threatened were: Paramiflos glandulosus–VU (20 UAs), Espeletia conglomerata–VU (18 UAs), E. brassicoidea–VU (17 UAs), E. tunjana–EN (15 UAs), Tamania chardonii–EN (13 UAs) and Espeletiopsis jimenez-quesadae–VU (12 UAs) (Fig. 2, Online Resource TS2).

Table 2

Results of the analysis for each evaluated criterion

Criteria		Country
Criteria		Colombia	Venezuela	Ecuador
cA1	Species of globally threatened species	54 (92%)	14 (24%)	0
	UAs area under cA1 (6 UAs in common)	154	28	0
cA3	Species threatened at the national level	51 (100%)	7 (14%)	0
cA3	UAs area under cA3 (4 UAs in common)	77	7	0
cA4	Species in EOO species equal to or less than 100 km²	26 (53%)	24 (49%)	0
cA4	UAs area under cA4 (2 UAs in common)	26	32	0
cA5	Species in EOO greater than 100 km² but less than or equal to 5000 km²	26 (53%)	24 (49%)	0
cA5	UAs area under cA5 (1 UAs in common)	26	32	0
cB2	Species richness	46 (66%)	24 (34%)	2 (3%)
cB2	UAs area under cB2	41	6	4
IPAs combining criteria	cA (UAs). UA shared: 8	155	37	0
	cA richness (UAs). UA shared: 8	155	37	0
	cB richness by ecosystems (UAs)	41	6	3
	Total IPAs (UAs)	168	41	3
	Total IPAs (UAs)	220

Information is displayed on the number of species and spatial coverage (areas in km²) where assessments occurred by each evaluated criterion in each country. The area corresponds to the sum of UAs that had results. The percentage corresponds to the total number of species found for each criterion

Complementarily, for criterion cA3 (UAs with nationally threatened species above 10%), we found that 51 species (33% of the subtribe) with 141 records (3%) appeared as threatened, and they were present in 80 UAs (2% of total records, Online Resource TS3). The species present in the highest number of UAs were Libanothamnus divisoriensis–EN (6 UAs), E. annemariana–EN, Espeletiopsis purpurascens–EN and E. brassicoidea–VU (5 UAs). For cA4 (UAs with species area of occurrence ≤ 100 km²), we found 75 records (1%) in 57 UAs (1%) (Table 2), encompassing 49 species (32%). The species with the highest number of UAs in cA4 were Ruilopezia cardonae and R. emmanuelis (4 UAs), E. discoidea, E. tenorae and R. ruizii (3 UAs) (Online Resource TS4). Similarly, for criterion cA5 (UAs with species area of occurrence > 100 km² but ≤ 5000 km²), we identified 75 records (1%) in 57 UAs (1%), corresponding to 49 species (32%). The species with the highest number of UAs were R. cardonae, R. emmanuelis (4 UA), E. discoidea, E. tenorae and R. ruizii (3 UAs) (Fig. 2, Table 2, Online Resource TS5).

We found that the eastern cordillera in Colombia and Venezuela had the highest scores for each cA sub-criterion based on their results and reclassification using a continuous scale. The criteria that exhibited the highest values for thresholds of IPAs were cA1 (globally threatened species) and cA3 (nationally threatened species). In contrast, a lower number of UAs were observed to meet the thresholds to accomplish the criteria cA4 (HRR species) and cA5 (RRE species) (Fig. 2). In terms of species richness for cA, low values (1–3) and medium values (4–5) are concentrated in the eastern Colombian mountain range, extending into Venezuela, with few areas in the same mountain range with high values (> 6). Dispersed areas of high values are also evident in the Colombian Massif, Eastern Cordillera, and Serranía del Perijá (Fig. 3). Table 2 shows the number of species and spatial coverage (in km²), where assessments were conducted for each evaluated criterion in each country.

Overlaying all UAs with the ecosystem layer for criterion B revealed a total area of 3920.47 km² across 15 ecosystem types (Fig. 4, Table 3, Online Resource TS6). Colombia had the highest number of identified UAs (207), spanning 12 ecosystems. These UAs were predominantly located in high-altitude ecosystems, particularly within the central and eastern mountain ranges. In Venezuela, 34 UAs were associated with four ecosystem types, while Ecuador had a unique ecosystem type, with only one UA coinciding with it. The ecosystems identified in all three countries correspond to medium to high elevations, typical habitats for the subtribe. The top five ecosystems with the highest estimated species richness, according to the Chao1 index, were Warm Temperate Dry Cropland on Plains (3 species, Chao1 = 0.75), Warm Temperate Dry Cropland on Plains (3 spp., Chao1 = 0.44), Polar Moist Forest on Mountains (5 spp., Chao1 = 0.43), Cool Temperate Moist Forest on Mountains (9 spp., Chao1 = 0.36) and Cool Temperate Moist Shrubland on Mountains (11 species, Chao1 = 0.47).

Table 3

Evaluation of cB, richness and ecosystems

Type of ecosystem	Number of species	Chao1 Index	Representativeness (%)	Colombia	Venezuela	Ecuador
				Total UAs: 207 (76%)	Total UAs: 34 (15%)	Total UAs: 4 (2%)
				Total richness
Cool Temperate Moist Cropland on Mountains	10	27	0.22	2745	0	0
Cool Temperate Moist Forest on Mountains	9	14	0.36	3871	0	0
Cool Temperate Moist Grassland on Mountains	8	47	0.17	0	449	0
Cool Temperate Moist Shrubland on Mountains	11	19	0.47	1094	0	0
Polar Moist Forest on Mountains	5	7	0.43	2274	0	301
Polar Moist Grassland on Mountains	26	93	0.13	546	1253	0
Polar Moist Shrubland on Mountains	18	53	0.15	2601	0	0
Warm Temperate Dry Cropland on Mountains	13	28	0.32	1702	0	0
Warm Temperate Dry Cropland on Plains	3	4	0.75	1208	0	0
Warm Temperate Dry Forest on Mountains	5	15	0.33	0	553	0
Warm Temperate Moist Cropland on Mountains	25	57	0.26	7935	0	0
Warm Temperate Moist Grassland on Mountains	11	50	0.22	1704	0	0
Warm Temperate Moist Settlement on Mountains	3	9	0.44	1081	0	0
Warm Temperate Moist Shrubland on Mountains	5	23	0.22	440	0	0
Sub-Tropical Dry Forest on Mountains	2	3	0.33	0	119	0

Presents the estimated richness by ecosystem, assessed using the Chao1 index, for the Espeletiinae subtribe. The table displays the ecosystems with the highest estimated richness based on the World Terrestrial Ecosystems data layer (Sayre 2022). It includes the number of species occurring in each ecosystem, the Chao1 index calculation, and the representativeness, corresponding to the proportion of species richness estimates based on Chao1. The table also shows the richness corresponding to each country’s total records within UAs by type of ecosystem

Espeletiinae IPAs distribution in the tropical Andes

Based on the obtained results from each criterion, we identified high-priority IPAs throughout the eastern cordillera of Colombia and Venezuela (11 UAs) (Fig. 5, Supplementary Material, Online Resource TS7). IPAs of medium (62 UAs) and low priority (147 UAs) are distributed in the central mountains of Colombia and Venezuela, with some UAs in the eastern mountains of Colombia and northern Ecuador (Fig. 5). Colombia had the highest number of records (3620; 65%) and reported species (94). Venezuela was the second country with the highest diversity of Espeletiinae, with fewer records (1753; 31.5%) and species (71). Ecuador had the lowest number of records (187 records; 3.4%) with only species (Espeletia pycnophylla). The highest priority IPAs are likely associated with “paramo” ecosystems (sensu: Van der Hammen and Cleef 1986) in the eastern cordillera of Colombia towards Venezuela, such as the Sumapaz, Cruz Verde, Pisba, Rechíniga, Cocuy, and Almorzadero páramos, which coincide with five different ecosystem types (Online Resource TS8). Medium-priority IPAs followed a similar pattern to the high-priority ones, with two additional areas located in the Central Cordillera, specifically in the Colombian Massif, Nevado del Tolima, and Serranía del Perijá in Colombia, associated with nine different ecosystem types (Online Resource TS8). Low-priority IPAs were dispersed along the páramo complexes of the Central Cordillera, the Sierra Nevada de Santa Marta, and in the northern region of Ecuador, linked to ten different ecosystem types (Online Resource TS8).

Discussion

Aiming to provide actualized tools that facilitate the development of public and private conservation initiatives in the tropical Andes, we implemented the IPA methodology with a multi-criteria perspective, focusing on the current distribution of an iconic taxa for this region such as the Espeletiinae subtribe. We were able to identify 220 units of analysis (i.e., 10 × 10 km grid cells) that fulfill the requirements for an IPA designation, representing 5.4% of the 4101 UAs established within the subtribe’s distribution range. However, since these IPAs differ in their criteria estimation, they were not equally relevant in terms of the methodological assessment. After prioritizing the selected IPAs based on their observed criteria values, we defined three levels of priority among the 220 selected IPAs: high-priority (11 IPAs, 5%), medium-priority (58 IPAs, 26%), and low-priority (143 IPAs, 65%); suggesting that most of the subtribe diversity is highly clustered in specific areas of the tropical Andes region.

One important aspect of this methodology is its multicriteria approach, which incorporate not only aspects of the richness and diversity of the referred taxa, but also information regarding the spatial distribution of their associated ecosystems and the threaten level of both species and environments (Florentín et al. 2022; Hamidah et al. 2022; Maxwell et al. 2018; Özden et al. 2016). Consequently, our assessment of the IPA criteria was based on the concept of “important populations of global, regional, or national conservation concern” (Diazgranados and Castellanos 2018), which explicitly include the assessment of the extinction risk among the analyzed species, and their related ecosystems, at different special scales (i.e., global, regional, or national). In this regard, through the analysis of criteria cA1 and cA3, we found, for example, that 44% of species (68 spp.) for cA1 and 38% (58 spp.) for cA3 had some risk of extinction according to the IUCN (2022b) and Diazgranados and Castellanos-Castro (2021). These findings highlight that the Espeletiinae subtribe exhibits high extinction threat assessments when compared to the estimates reported in the IUCN, where only 15% of plant diversity has been evaluated on the Red List, and approximately 40% of vascular plant species have some category of extinction threat at a global scale in Southern America, Northern America, and tropical Asia (Nic Lughadha et al. 2020). Consequently, the identified IPAs will contribute to protecting and managing sites of importance for the subtribe by focusing the attention of potential decision makers on the most threatened species within the analyzed group (Anderson 2002; Darbyshire et al. 2017).

Nevertheless, besides the aforementioned compilation of secondary information describing the conservation status of the subtribe species, the application of criteria cA4 and cA5 of the IPA methodology also generates an empirical estimation of how conserved the Espeletiinae species in the region are. In this sense, through the calculation of the extent of occurrence (EOO) for each species, we were able to establish for all taxa if they were a Highly Restricted Range Endemic (HRR) species (cA4) or a Range-Restricted Endemic (RRE) species (cA5). In this way, while the EOO was reported in the IUCN for 88 species of the subtribe (Diazgranados and Castellanos-Castro 2021; IUCN 2022a; Mavárez 2019), we recalculate it for all species on our list, providing an actualization of this estimations for those species that were already evaluated, and new preliminary conservation assessments for other 65 species (Darbyshire et al. 2017). Interestingly, the results were similar between criteria (34% (58 spp.) for cA4 and 37% (57 spp.) for cA5), suggesting that besides RRE species have a relatively wider distribution compared to HRR species, likely facing similar conservation challenges due to their limited range.

Consequently, despite HRR species are theoretically more sensitive to threats associated with habitat degradation and land-use changes (Pérez-Escobar et al. 2018) as well as climate change (Mavárez 2019; Valencia et al. 2020), their similar proportion suggests that the observed pattern could be influenced by the geography of the Andes and climatic fluctuations, which have played a role in the diversification and concentration of the subtribe within its distribution range (Cuatrecasas 2013). According to Pouchon et al. (2021), the distribution of the subtribe is associated with various ecological niches that align with typical environmental gradients found in the páramos. Phylogenetic relationships between species traits shape these niches, encompassing factors such as climate and habitat. As a result, adaptation syndromes have emerged for both vegetative and reproductive traits. One such adaptation syndrome could attribute to the ecotone between closed vegetation (such as forests and subpáramo) and open vegetation (referred to as true páramo), where distinct lineages have repeatedly differentiated based on specific vegetative traits associated with tree and rosette morphotypes (Monasterio and Sarmiento 1991). Additionally, the transitions between herbaceous/rosette and woody growth forms, which are characteristic of open and closed habitats among Andean taxa, contribute to the overall pattern of adaptation (Dušková et al. 2017; Kolář et al. 2016). Another adaptation syndrome is linked to reproductive traits, particularly the emergence of a morphological development syndrome in the larger capitula, corollas, and achenes in specific lineages occurring at higher elevations or super-páramo habitats, suggesting a limitation in long-distance pollination and seed dispersal (Berry and Calvo 1994b, a; Diazgranados and Barber 2017), which may be the underlying cause of these results.

The implementation of criteria that involve extinction risk assessments in the IPAs methodology allows the spatialization of the conservation status for a complex group of species, in our case the Espeletiinae subtribe. Indeed, the evaluation of the extinction risk has been suggested as a tool to supports and inform the planning and prioritization of important conservation areas where plant diversity is actually threatened (Clubbe et al. 2020; Darbyshire et al. 2017; Nic Lughadha et al. 2020). For instance, in Europe, this approach has been applied to managing and conserving fungi (Dahlberg et al. 2010). Red List assessments, including National Red Lists, have been used to identify areas of significance for fungi in the United Kingdom (Genney et al. 2009) and the United States (Molina et al. 2006). Similarly, Couch et al. (2019a, b) described how extinction risk assessments have facilitated conservation funds for populations classified as Endangered or Critically Endangered in Senguelen (Guinea), leading to modifications in construction plans and supporting the financing of seed storage programs and the development of propagation protocols. This became of high relevance for the tropical Andes since it represents a complex territory in which the development of human communities has had a profound impact on local ecosystems resulting in a rapid and ongoing land use and cover transformation driven by current development models (Guarderas et al. 2022). Moreover, despite previous assessments of the IPA methodology in tropical regions (Bolivia, British Virgin Islands, Cameroon, Ethiopia, Guinea-Conakry, Indonesia New Guinea, Mozambique, and Uganda) (Darbyshire et al. 2017), this study is the first to conduct such effort in the Tropical Andes region, using the entire distribution range of an iconic plant group.

While the results obtained by the implementation of the IPA methodology are useful for prioritizing in situ conservation measures, it is necessary to delve into the potential management of these areas (Diazgranados and Barber 2017). For instance, it is crucial to evaluate the role of the protected area system in addressing climate change, human activities, and their impact on plant distribution (Valencia et al. 2020). IPAs can support existing legally protected areas, such as Protected Areas and Protection Forests under Permanent Reserve Forests, in the same way as Key Biodiversity Areas, Important Bird Areas, and High Conservation Value Forests (Brancalion et al. 2019; Chazdon et al. 2009; Donald et al. 2019; KBA Secretariat 2022; Plumptre et al. 2019). The designation of these multiple-use areas should be considered complementary and mutually supportive as they provide necessary site-based protection for biotic assemblages and the ecosystem (Blasi et al. 2011a, b; Hamidah et al. 2020; Marignani and Blasi 2012). Site-based protection also conserves ecosystem services. In the case of Espeletiinae, many of these services are derived, including soil protection, erosion control, water regulation, and the provision of construction materials, medicinal compounds, and cultural use, among others (Diazgranados and Castellanos-Castro 2021). Therefore, from a conservation perspective, protecting a botanical group also helps sustain the ecosystems they are found in, and it is crucial in formulating and implementing management plans for the assessed areas, promoting shared responsibility between decision-makers and users of ecosystem services. This underscores the importance of long-term commitments to manage, conserve, and implement areas and species while providing legal protection (Hamidah et al. 2020, 2022). It is important to note that even if a species occurs within the boundaries of a protected area, there is no guarantee of its effective management due to resource (Clubbe et al. 2020; Corlett 2016; Nic Lughadha et al. 2020).

Implementing the IPA methodology typically involves using grid cells, though there has yet to be a consensus on selecting an optimal cell size. The choice of cell size often depends on factors such as the taxonomic group under study, available data, and the size of the study area. In our study, we selected a cell size encompassing the entire distribution range of the subtribe and allowing the methodology to be applied across a large and diverse area. This cell size enabled clear visualization of the results and aligns with other studies that have used similar approaches (Blasi et al. 2011a, b; Hamidah et al. 2020), even in smaller areas (Marignani and Blasi 2012; Sánchez de Dios et al. 2017; Walsh et al. 2019). The identified IPAs align intuitively with the biogeographical distribution of the subtribe, reinforcing the validity of our approach. However, exploring different cell sizes, combinations, and additional algorithms is a necessary next step to refine our results further and ensure effective in situ conservation.

Prospects and directions for the future implementation of IPAs

Our species list of the Espeletiinae subtribe represents the most up-to-date compilation available. However, during our analysis, we discovered that some species’ presence records date back to 1800, underscoring the crucial need to validate record information and verify the existence of these species under current in situ conditions. Consequently, our findings may overlook valuable information regarding the identification of IPAs. Similar remarks have been documented in other studies focused on conservation planning, including those specifically addressing IPAs (Blasi et al. 2011a, b; Hamidah et al. 2020). Confirming species distribution within the current ecological and ecosystem context is essential, particularly for outdated occurrence records (Cuesta et al. 2017). Various approaches can be employed to mitigate data limitations, such as using alternative data sources like surrogate taxa (Beier et al. 2015) or employing environmental predictor variables to develop species distribution models (SDMs) (Guisan and Thuiller 2005; Zurell et al. 2020). On the other hand, obtaining biological information is the initial phase of a multifaceted process of identifying conservation areas, which should encompass social, political, and economic factors (Darbyshire et al. 2017; Kress et al. 1998), which could be an important future focus for IPA identification.

Additionally, incorporating the habitat-based Criterion C from the IPA methodology, although not applied in this study, could enhance future research by providing a broader perspective on species distribution. This approach, combined with future analyses that integrate existing data on threatened ecosystems (Etter et al. 2017) and species.

Kor et al. (2022), would refine the prioritization of sites and offer greater detail for conservation decisions. Currently, only Colombia has robust and detailed information for ecosystems and species, while Venezuela and Ecuador are encouraged to strengthen their data to enable more comprehensive comparisons and analyses.

We want to emphasize that our data only represents the total number of species recorded in a particular area and do not assess the species’ current state. Some researchers have suggested that absolute numbers are not the best indicator of diversity; thus, other criteria such as phylogenetic uniqueness and position (Erwin 1991), phylogenetic distance (Sánchez de Dios et al. 2017), Environmental DNA (eDNA) sampling (Thomsen and Willerslev 2015) the concentration of endangered taxa, or richness of indicator taxa (Darbyshire et al. 2017; Yahi et al. 2012), may be a better measure for conservation purposes. Additionally, when identifying regions with high diversity, it is necessary to consider additional biological information about the species that can be provided by taxonomists, field biologists, decision-makers, and local naturalists (Anderson et al. 2016; Hamidah et al. 2022; Sanchez et al. 2021). Although we used the distribution range of an entire botanical group, these results can be comparable with other plant taxa, enhancing the power of site-based prioritization when compared within the area evaluated in this study.

Considering that we only used occurrence records, it is crucial to include additional aspects for a more comprehensive prioritization of IPAs. For example, some species of Espeletiinae have been documented in secondary succession sites, acting as colonizers in areas disturbed by agriculture or grazing (Sarmiento et al. 2003). In some areas, these species can also be colonizers in the paramization processes of high Andean forests (Llambí 2015). Therefore, considering criterion C could thus provide more robust information about the species’ status concerning habitat type, vegetation, and ecosystem. Furthermore, incorporating other criteria, such as species with broad distribution, abundant populations, or emblematic status—characteristics seen in many Espeletiinae species—can further support systematic conservation planning for selecting and prioritizing key sites. Additionally, including other information that allows detailed comparisons with data from permanent monitoring sites (e.g., GLORIA-Andes) (Gámez et al. 2020; Llambí and Cuesta 2014) on species distribution changes over time, which show more complex response patterns than mere species loss or migration to different altitudinal ranges, is necessary to enhance the methodology’s applicability.

Conclusions

This research presents a prioritization framework for conserving Espeletiinae (Asteraceae) in key plant areas across its range. It exemplifies applying a systematic conservation approach and represents the first implementation of the Important Plant Area (IPA) methodology at a regional level. Analyzing records addressing information gaps is essential to validate data under in situ conditions and reduce uncertainty and biases, resulting in more precise identification of high, medium, and low-priority areas. It is worth noting that Espeletiinae is found in a region known for its exceptional ecosystem diversity and botanical richness, and it also experiences significant human impact. Therefore, it is essential to consider additional information, such as analysis of cover types and human footprint, which may not be fully available in the evaluated area. This is especially relevant given reports of some species within the subtribe acting as colonizers in high Andean forest paramization processes and areas disturbed by agriculture or grazing.

We have identified 11 high-priority Important Plant Areas (IPAs) primarily located in Colombia, associated with the páramo complexes of Colombia and the Sierra Nevada in Venezuela. These areas are mainly situated within Cool, Temperate, Moist Grassland ecosystems in mountainous regions. We found that medium and low-priority IPAs exhibit a similar distribution pattern. Our identification process considered species’ distribution areas, the presence of threatened species, and ecosystem-based richness distributions. Our findings offer a spatial planning procedure and analytical tool for decision-makers to guide conservation management and actions across the study area. However, the scope of these findings largely depends on the availability and quality of biodiversity information. Therefore, these efforts must be supported by updated information accessible through consultation platforms, such as public data repositories. Our results can be compared across multiple botanical groups and support a broader application of area-based conservation approaches.

Acknowledgements

We are grateful to all the collaborators and contributors of the Global Biological Information Facility (GBIF) for making their data available. This study would not have been possible without the support of the Vicerrectoría Académica of the Pontificia Universidad Javeriana through the teaching and research assistance program framework. We thank Alejandra Narvaez-Vallejo and Fabio Ávila for their helpful comments on an earlier version of the manuscript.

Declarations

Competing interest

The authors declare no competing interests.

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Supplementary Information

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Title: Prioritization of important plant areas for conservation of frailejones (Espeletiinae, Asteraceae) in the Northern Andes
Authors: Clara Morales-Rozo
Ian S. Acuña-Rodríguez
Juan C. Benavides
Víctor J. Rincón-Parra
Mauricio Diazgranados
Publication date: 22-10-2024
Publisher: Springer Netherlands
Published in: Biodiversity and Conservation / Issue 14/2024
Print ISSN: 0960-3115
Electronic ISSN: 1572-9710
DOI: https://doi.org/10.1007/s10531-024-02939-1

Snow leopard phylogeography and population structure supports two global populations with single refugial origin

Open Access
Original Research

Conserved lands unable to maintain butterfly communities in a biodiversity hotspot

Original Research

Bryophytes in managed lowland forests of Slovakia (Central Europe): looking into species diversity across different forest types

Open Access
Original Research

Effects of an amazonian dam on taxonomic, functional and phylogenetic diversity of non-volant small mammals

Original Research

Eutrophication is better indicated by functional traits than taxonomic composition of macroinvertebrate assemblages in floodplain lakes

Original Research

Anthropogenic impacts drive habitat suitability in South Asian bats

Open Access
Original Research

Springer Professional

Prioritization of important plant areas for conservation of frailejones (Espeletiinae, Asteraceae) in the Northern Andes

Abstract

Supplementary Information

Publisher's Note

Introduction

Materials and methods

Study area

Quality assessment of data and georeferencing

IPAs criteria

Mapping IPAs

Results

Criteria evaluation and IPAs-identification

Espeletiinae IPAs distribution in the tropical Andes

Discussion

Prospects and directions for the future implementation of IPAs

Conclusions

Acknowledgements

Declarations

Competing interest

Publisher's Note

Supplementary Information

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Conserved lands unable to maintain butterfly communities in a biodiversity hotspot

Bryophytes in managed lowland forests of Slovakia (Central Europe): looking into species diversity across different forest types

Effects of an amazonian dam on taxonomic, functional and phylogenetic diversity of non-volant small mammals

Eutrophication is better indicated by functional traits than taxonomic composition of macroinvertebrate assemblages in floodplain lakes

Anthropogenic impacts drive habitat suitability in South Asian bats