Endemic Species of Butterflies: Importance of Protected Areas in Tropical Montane Endemism Conservation

Abstract

Protected areas play a key role in containing and protecting most of the endemic biodiversity of megadiverse places, underscoring their importance as custodians of biological richness. Colombia, one of the most species-rich countries, also has one of the highest rates of deforestation globally. The Colombian National Natural Parks (NNPs) system is one of the mechanisms for protecting natural landscape ecosystems and biota. Based on the role of butterflies as bioindicators in biodiversity mapping, we compiled records of endemic butterfly species from entomological collections and the literature to assess the importance of protected areas in endemic species conservation. The NNPs harbor records of 127 endemic species, representing 65% of the 196 endemic butterfly species recorded in Colombia. Most of these endemic species, 93 species, have been recorded in only one NNP, here defined as “unique” species. These species are mainly distributed along the Andes Cordillera. Among all the NNPs, Sierra Nevada de Santa Marta holds the highest number of both total and unique endemic species. Extrapolating this pattern to the broader Andean Biota supports the idea that protected areas play a key role in containing and protecting much of Northern South American endemic biodiversity, underscoring their importance as custodians of biological richness.

1. Introduction

Tropical mountain systems host highly diverse regions with small-range species in unique mixtures of rapid speciation, high extinction rates, and some species persisting over time [1]. The tropical Andes is the region with the highest plant diversity [2] and global richness in both early-diverged and recently evolved species of vertebrates, serving as a living museum of global biodiversity [1]. Unfortunately, these species and places face threats from human activities [3] and global climate change [4]. Colombia, due to its topography and geographical position as a bridge between the biotas of Central and South America, is recognized as one of the most biodiverse countries in the world. Its territory includes areas from two of the biodiversity Hotspots described by Myers et al. [2]: Chocó/Darién/Western Ecuador and the tropical Andes. It is also listed among the world’s megadiverse countries by Mittermier et al. [5]. This diversity is supported by records showing high numbers of species across various taxonomic groups of plants and animals [6,7]. At the same time, Colombia faces high rates of deforestation and transformation of natural cover, with the Amazonian foothills currently experiencing the greatest loss of natural forest cover [8,9]. This trend is also advancing in other significant regions of the country [9]. This combination of exceptional biological richness and accelerated landscape transformation poses a constant threat to biodiversity, a problem extended to the Tropical Andes. However, the National Natural Parks (NNPs) system—one of Colombia’s long-standing state policies regarding environmental conservation—has played an important role in mitigating this loss. Despite challenges, it has proven effective in preventing greater transformation in the natural areas it protects [10,11].

The NNPs comprise 61 protected areas covering nearly 23 million hectares, corresponding to approximately 21% of Colombia’s marine and terrestrial surface [12]. These protected areas serve various conservation objectives and are designated accordingly as National Natural Park (NNP), Flora and Fauna Sanctuary (FFS), Flora Sanctuary (FS), Fauna Sanctuary (FaS), National Natural Reserve (NNRs), Via Park (VP), or Unique Natural Area (UNA). However, regardless of designation, they all share a common role: as legally protected, they have been less affected by the expansion of the anthropic transformation. For this study, all seven categories offer a similar level of protection and will be collectively referred to as National Natural Parks (NNPs). Based on their geographical location, Colombia’s Special Administrative Unit of National Natural Parks has grouped them into six regions: Amazon, Western Andes, North Eastern Andes, Caribbean, Orinoquia, and Pacific [12]. Given that several NNPs still lack comprehensive or detailed inventories of their biological diversity [13], this study aims to identify records of Colombian endemic butterfly species collected within these protected areas, to assess the importance of NNPs as a refuge for these unique species.

We selected butterflies due to their well-established utility as bioindicators or focal species, capable of reflecting ecological patterns that can be extrapolated to the broader biota of a given region [14,15,16]. Butterflies are insects of the order Lepidoptera, currently classified within the superfamily Papilionoidea, which includes more than 18,000 species documented worldwide [17]. As larvae, butterflies are mainly specific to their host plants, and even at a local scale, they exhibit stratification along gradients of light, wind, humidity, temperature, and altitude [15,16,18,19]. Additionally, they represent one of the most diverse groups of diurnal insects [16,17]. In tropical regions, butterfly species richness is especially high at local level, which allows for detailed biodiversity comparisons and mapping analyses [20,21]. In Colombia, 3877 butterfly species have been recently recorded [22], making it the most butterfly-rich country in the world. This exceptional richness is further emphasized by the fact that Colombian species represent nearly 54% of the 7171 species recorded in South America, and 47% of the 8174 species found across the Neotropics [23]. A significant proportion of these species are endemic to Colombia. While an initial estimate by Garwood et al. [24] identified 289 endemic species, a more recent update by Huertas et al. [25] revised this number to 192. These numbers reflect Colombia’s extraordinary biological diversity.

Butterflies are a taxonomic group composed primarily of environmental specialist species, with a smaller proportion of generalist species [21]. Along tropical altitudinal gradients, they tend to be distributed in distinct belts, with some species adapted to warmer lowland conditions and others to cooler high-elevation environments [19,26,27,28,29]. Although endemism occurs throughout the altitudinal range, mountainous areas tend to harbor a greater number of species. Most endemic butterfly species in Colombia have been recorded in the Andean region and the Sierra Nevada de Santa Marta [25]. Currently, almost every mountain range in Colombia, above 3000 m in elevation, has endemic species of butterflies [25,26], likely as a result of climatic cycles over the past 15 million years [30], which affected the entire biota. The altitudinal stratification of butterflies was likely shaped by the successive migrations of vegetation belts across mountains [26,30]. These plant migrations were driven by global cycles of cooling and warming during the Neogene, which intensified during the Pleistocene, thereby also forcing the migration of associated fauna species [31,32]. During such climatic cycles, speciation processes are intensified in mountain ranges, as topography influences gene flow by either limiting or facilitating connectivity between populations [33,34]. These evolutionary events, combined with complex topography, broad altitudinal gradients, and high rainfall, have likely contributed to Colombia’s extraordinary biological diversity, clearly reflected in its highly diverse butterfly fauna. Today, the Andes is the home of the highest rate of altitudinal specialist butterfly species in the tropics [27,28], although much of this biodiversity remains unexplored.

Consequently, by leveraging the ability of butterflies to serve as bioindicator species and reveal broader biotic distribution patterns, this study examined the distribution of the endemic butterfly species recorded within Colombia’s NNPs. Butterflies were used as a focal group to assess the importance of these protected areas in conserving the country’s endemic biota and, by extension, the Tropical Andes, the richest region on Earth.

2. Materials and Methods

We compiled information on the geographic distribution of endemic Colombian butterflies collected within the protected areas of the NNPs. To do this, we verified the lists of endemic species proposed by Garwood et al. [22] and Huertas et al. [25], and reviewed specimen records from the following entomological collections: University of Antioquia-Medellin Entomology Collection (official acronym: UAEC), Institute of Natural Sciences-Collection of Zoology National University of Colombia-Bogota (INC-NHM), Francisco Luis Gallego Entomological Museum, National University of Colombia-Medellín (FLGEM), National Taxonomic Collection of Insects-Tibaitatá (NTCI), National University-Bogotá Agronomy Entomological Museum (NUBA), and the Entomological Collection of the Alexander von Humboldt Institute (AvHI). These data were obtained from taxonomic reviews conducted before 2010 (see Supplementary Materials Annex S1 for details). This information was supplemented with updated data from the collections of the Natural History Museum Pontifical Javeriana University-Bogotá (MPJU), the La Salle University Museum (LSM), and the personal collection of Jean Francoise Le Crom (CJFL).

The specimen records from collections were complemented with a review of holotype photographs and other specimens available on the Butterflies of America website [35]. Locality data were recorded only when sufficiently reliable or detailed, and when they provided enough information to associate the specimen with a protected area within the NNP system. In addition, we reviewed 175 bibliographic references, including original species descriptions, local inventories, taxonomic revisions, and undergraduate, master’s, and doctoral theses that contained records of Colombian endemic species (see Supplementary Materials Annex S2). Due to various taxonomic updates and new records identified during the process, the taxonomic and distributional status of several species was reassessed to ensure that those previously considered endemic [22,24,25] are indeed restricted to Colombia and can be confidently classified as Colombian endemism.

The data obtained were used to associate records of specimens collected within any of the 55 continental NNPs registered at the time of this study. The presence of at least one individual of an endemic species, either deposited in entomological collections or documented in the literature (with associated voucher specimens), was considered positive evidence of that species’ occurrence in the respective National Natural Park (NNP). It is worth noting that several species considered endemic by Garwood et al. (2021) [24] were later found to have records in other countries, or their taxonomic status or rank was changed. As a result, the number of endemic species listed by Garwood et al. [24] was reduced, and our revised list aligns more closely with those proposed by Huertas et al. [25]. The maps were constructed using Historical US Geological Survey (USGS) Topographic Maps available using ArcGIS 11 and edited for legends.

3. Results

Records from entomological collections, online databases, and literature reviews indicate that 127 endemic butterfly species endemic to Colombia have been recorded in 24 of the 55 continental NNPs (

Table 1. Number of butterfly endemic species recorded in the park areas of the Colombian National Natural Park System.

Region	National Natural Park Name	Endemic Species Recorded	* Unique Endemic Species Recorded
Caribbean	Sierra Nevada de Santa Marta	28	27
North Eastern Andes	Iguaque	18	12
North Eastern Andes	Chingaza	17	6
Western Andes	Puracé	14	6
Western Andes	Tatamá	12	8
Pacific	Farallones de Cali	11	6
Western Andes	Los Nevados	10	5
North Eastern Andes	Sumapáz	10	1
Pacific	Munchique	9	5
North Eastern Andes	El Cocuy	8	4
Western Andes	Las Orquídeas	3	3
North Eastern Andes	Serranía de los Yariguíes	6	3
North Eastern Andes	Guanenta Alto Rio Fonce	4	1
Western Andes	Otún Quimbaya	3	2
Western Andes	Nevado del Huila	3	2
Amazon	Serranía de Chiribiquete	2	2
Western Andes	Selva de Florencia	2	1
North Eastern Andes	Pisba	2	1
North Eastern Andes	Tamá	2	0
North Eastern Andes	Serranía de la Macarena	1	0
Amazon	Serranía de los Churumbelos—Auka Wasi	1	0
North Eastern Andes	Los Estoraques	1	0
Western Andes	Galeras	1	1
Amazon	Alto Fragua—Indi Wasi	1	0
Amazon	Plantas Medicinales Orito Ingi Ande	1	0

* Butterfly species recorded in only one National Natural Park area.

, Supplementary Material [SM], Annex S2). In contrast, no endemic species were recorded in 31 NNPs, despite several of these parks having had butterfly sampling events. These 127 species represent 65% of the 196 butterfly endemic species recorded for the country in this study and in literature [22,25]. An additional five endemic species were collected in páramo ecosystems located less than 20 km from Las Hermosas and Las Orquídeas NNPs (Table 1, SM Annex S2).

Of the 127 endemic species, 125 species were recorded in NNPs located in mountainous areas above 1000 m above sea level (m.a.s.l.), primarily associated with Andean Forest, high Andean Forest, and páramo ecosystems. Only two endemic species—Euptychia efraini Ríos-Málaver, 2019 and Cartea chiribiquetensis Salazar & Constantino, 2007—both not included in the list by Huertas et al. [25], were recorded in lowland NNPs with altitudes below 500 m.a.s.l., specifically in Chiribiquete NNP (Supplementary Material Annex S2).

The NNP with the highest number of endemic species recorded was Sierra Nevada de Santa Marta (SNSM), with 28 species, followed by Iguaque (18 species) and Chingaza (17 species). Other parks such as Purace, Tatamá, Farallones, Los Nevados, and Sumapaz had between 10 and 15 endemic species (Figure 1, Table 1). Eight additional NNPs reported between three and nine endemic species, while another ten NNPs had records of at least one endemic species (Figure 1, Table 1).

When analyzing the number of endemic species recorded in only one NNP, hereafter defined as “unique” endemics, Sierra Nevada de Santa Marta (SNSM) again stands out, with 27 unique endemic species, the highest among all parks (Figure 2, Table 1). In contrast, many NNPs located along the Eastern Cordillera share several endemic species; therefore, they individually report fewer unique species. Within this region, Iguaque (12 unique endemic species), Tatamá (8), Chingaza (6), Puracé (6), and Farallones (6) are the parks with the highest numbers of unique endemics in the Colombian Andean zone.

Notably, 14 NNPs harbor between one and five unique endemic species recorded. Overall, 93 of the 139 endemic butterfly species found within the NNP system (67% of the total) have been recorded in only one park (Figure 2, SM Annex S2).

The distribution range of most endemic species appears to be restricted to a single NNP, as evidenced by the low numbers of endemics recorded in more than one park (SM Annex S2). Only twenty-six species have records in two NNPs; five species in three NNPs, and just two—Lymanopoda mirabilis Staudinger, 1897 and Pedaliodes cocytia (C & R Felder, 1867)—in four NNPs. The only species recorded in five parks was Pedaliodes nebris (Thieme, 1905), although all five parks—El Cocuy, Gunentá, Iguaque, Chingaza and Sumapaz—are located along the Eastern Cordillera (SM Annex S2).

When we compare these distribution results (127 endemic butterfly species recorded in NNPs, of which 93 are unique) with the Colombian list of threatened butterfly species, only 8 of the listed species (

Table 2. Number of butterfly species recorded in protected areas of the Colombian National Natural Parks System that are included in the official national lists of threatened species. EN: Endangered. VU: Vulnerable. NT: Near Threatened.

National Natural Park Name	Red Data Book of Terrestrial Arthropods of Colombia [36]				Colombian Minambiente Resolution 1912 of 2017 [37]
	Categories				Categories
	EN	VU	NT	Total	EN	VU	NT	Total
Santa Marta	* 1	* 2	0	* 3	* 2	* 1	0	* 3
Chingaza	* 1	0	0	* 1	* 1	0	0	* 1
Farallones	1	1	0	2	2	1	0	3
Tatamá	0	1	0	1	0	1	0	1

* Asterisk indicates Colombian endemic species.

) are found in NNPs—and just 4 of them are endemic to Colombia. These findings highlight the need for more comprehensive research to ensure a greater representation of Colombian endemic butterflies in the official lists of threatened species.

As a complement to the previous analyses, it is possible to identify priority areas for further exploration of endemic butterfly species within the NNP system, based on the distribution records compiled in this study (Figure 3). Although butterfly specimens have been collected in several parks, sampling efforts need to be increased in NNPs such as Paramillo, Picachos, Catatumbo, Tatamá, Las Hermosas, Nevado del Huila, Doña Juana Cascabel, Tamá, Cocuy, and Las Orquídeas (Figure 3).

In some cases, endemic species have been described in the vicinity of NNPs but have not yet been recorded within the park boundaries, likely due to limited sampling. Examples include Pedaliodes philinae Pyrcz & Prieto, 2013, and Pedaliodes adrianae Pyrcz & Prieto, 2013, described near Páramo de Frontino (department of Antioquia), which is only 10 km from Las Orquídeas NNP, and Penaincisalia celosia Prieto, 2016, and Lymanopoda flammigera Pyrcz, Prieto & Boyer, 2018, described near Páramo de las Domínguez (department of Valle del Cauca), located less than 20 km from Las Hermosas NNP—parks where these species have not yet been recorded.

A second level of priority includes NNPs with more complete historical inventories but little recent sampling, particularly in their high-altitude areas. These include Sierra Nevada de Santa Marta (SNSM), Yariguíes, Nevado del Huila, Puracé, and Yaigojé-Apaporis, as well as Tinigua and La Macarena (Figure 3).

Lowland parks were not prioritized in this study as endemic butterfly species occurring below 2000 m.a.s.l. tend to have better inventory coverage—especially in the eastern Amazon region and the Pacific coast—and broader distribution ranges that include neighboring countries (Figure 3).

4. Discussion

According to our results, a significant portion of Colombia’s National Natural Parks (NNPs) lack adequate butterfly inventories (Figure 3), despite butterflies being one of the insect groups with the greatest number of records and local studies [21], and Colombia, currently, is one of the countries with recent compilations of species list in South America [22,23,24,25]. This suggests that the situation may be similar, or even worse, for other insect groups and broader components of the Tropical Andean biota.

These findings are consistent with analyses of species records from NNPs deposited in the Biodiversity Information System for the Colombian biota (SiB Colombia) and GBIF [38], which also highlight the need for more comprehensive sampling across many protected and unprotected areas. This limitation stems from the fact that current inventories in Colombian NNPs and the Tropical Andes are not the result of systematic data collection, but rather reflect the concentration of sampling efforts in a few specific parks, often those near urban centers or with easier access [13].

Despite these limitations, the protected areas currently hold records for 65% of the 196 endemic butterfly species recognized for Colombia by Huertas et al. [22] and confirmed in this study (including 2 additional species; see SM Annex S2). Of these, approximately 70% have been recorded in only 1 of the 55 continental NNPs—mainly those located in the Andean region and the isolated mountain system of the SNSM.

Given the bioindicator role of butterflies [14,15,16,18], these patterns may reflect broader trends in the distribution of Andean endemic biota. These endemic species would be restricted to only one of these protected areas and their surroundings. This confirms the uniqueness and importance of the Andean montane biota and demonstrates the key role of protected areas as custodians of this biological richness, as well as the need to intensify biological inventories in most protected areas.

The sampling effort carried out in Colombia’s National Natural Parks (NNPs) appears to be independent of the number of endemic butterfly species recorded. Of the nine NNPs that account for more than 70% of the 1.1 million biological records uploaded to SiB Colombia [13]—most of which correspond to plants, birds, and mammals, rather than butterflies—the top parks are, in order, Farallones, Tayrona, Otún-Quimbaya, Flamencos, Tatamá, Rosario, Yariguies, Gorgona, and Salamanca.

However, none of these parks appear among the four NNPs with the highest number of endemic butterfly species identified in this study—SNSM, Iguaque, Chingaza, and Purace—and only two (Farallones and Tatamá) are among those with the highest number of unique endemic species (Table 1). This suggests that the number of endemic butterfly species recorded in a given park is not directly related to the overall sampling effort conducted there. Instead, this pattern may be associated with the presence of isolated mountainous areas above 2000 m.a.s.l., which coincides with Fjeldså & Lovett [33] and Laurance et al. [34], who identified topography as a major driver of biological richness in tropical regions.

Another highly relevant aspect is that most of the Colombian endemic species recorded in this study are restricted to small, isolated areas of páramo and adjacent high Andean Forests. These ecosystems often cover less than 500 km² (50,000 ha), and only rarely exceed 5000 km² (500,000 ha) [39]. These area thresholds align with those used by the International Union for Conservation of Nature (IUCN) [40] under criterion B to assess whether a species should be categorized “Endangered” (EN), based on its geographic range—measured as either extent of occurrence (B1) and/or area of occupancy (B2).

The application of this criterion depends on the available data. For B1, the total area is calculated as the extent of the polygon defined by the outermost known occurrence records. For B2, it refers to the sum of the discrete areas where the species is known to occur [40].

Under these IUCN criteria, many of the unique endemic species recorded in isolated páramos within NNPs such as Yariguíes, Farallones, Paramillo, and Tatamá—each with paramo areas of less than 10,000 ha (Alexander von Humboldt Biological Resources Research Institute, IAvH [39])—could potentially qualify as Critically Endangered (CR), having a known distribution area of under 100 km². According to the IAvH, Colombia has 36 defined paramo areas, none of which exceed 500,000 ha per park [39]. This supports the recommendation to classify at least all paramo-endemic species as Endangered, given that their known extent of occurrence is under 5000 km². This condition can be extended to most endemic butterfly species of this ecosystem in the Northern Tropical Andes.

Furthermore, any endemic species specialized in páramo or high Andean Forest and restricted to the Northern Andes and a single branch of Colombia’s three Andean mountain ranges (Western, Central, or Eastern Cordillera), the Venezuelan Andes (the Serranía del Perijá and the Cordillera de Mérida) or some of the Guyana Tepuis would qualify, at minimum, as Vulnerable (VU). This is because the extent of these vegetation types in each range usually does not exceed two million hectares [39].

A critical case is that of the Sierra Nevada de Santa Marta (SNSM), the park with the highest number of endemic and unique butterfly species recorded, and a total páramo area of 1510 km² (151,021 ha, IavH [39]). In this case, all 27 endemic species recorded would, at minimum, qualify as Endangered (EN) based on their restricted geographic distribution. Similar events can occur in mountain systems as the Serranía del Perijá or the Cordillera de Mérida. However, this information should be complemented with studies evaluating whether these species, especially the unique ones, also meet additional IUCN criteria for inclusion in its threatened species categories [40].

These criteria include the following: severe fragmentation of populations or habitats; presence in fewer than five known localities; or evidence of declines or extreme fluctuations in extent of occurrence, area of occupancy, number of localities, or subpopulations [40]. Some of these aspects are currently under evaluation by the authors of this study.

Furthermore, as paramo and high Andean Forest specialists, these high-altitude species [Annex S2] are particularly vulnerable to the effects of global warming [41,42,43,44], adding to the pressures from direct human-driven habitat transformation and degradation [3,45].

As previously mentioned, only eight butterfly species are currently in Colombia’s official or published threatened species lists [36,37], of which only four, currently, are endemic: Arhuaco ica Adams & Bernard, 1977, Heliconius heurippa Hewitson, 1854, Lymanopoda caeruleata Godman & Salvin, 1880, and Morpho rhodopteron Godman & Salvin, 1880. We expect this list to increase as more detailed studies on the distribution and population size of the Northern Andes endemic butterfly species are completed—a pattern that may also apply to other groups within the Colombian biota.

Colombia’s National Natural Parks (NNPs) host more than half of the country’s endemic butterfly species, most of which are restricted to isolated and sparsely populated mountainous regions, particularly páramo and high Andean Forest ecosystems in the Andean region and the SNSM. Given the well-established role of butterflies as bioindicators organisms, this pattern can likely be extrapolated to other taxonomic groups, supporting the hypothesis that NNPs play a critical role in safeguarding Colombia’s endemic biodiversity, especially its most unique elements. This can be extended to other protected areas of the tropical Andes.

Due to the restricted geographic ranges of these species, many Colombian endemic butterflies would likely qualify for threatened categories under IUCN criteria. Species limited to small, isolated páramos should be considered Critically Endangered (CR); those confined to a single branch of the Andes or to the SNSM may qualify as Endangered (EN); and most endemics could at least meet the criteria for Vulnerable (VU) status. Further research is needed to confirm these assessments, including additional distribution records, locality data, and analyses of population trends and spatial fluctuations for each species.