Habitat fragmentation threatens the survival of populations and species in two main ways. Firstly, smaller, isolated populations in habitats with high fragmentation are more vulnerable to stochastic events (Fischer and Lindenmayer, 2007). These may be the result of environmental catastrophes, particularly in the context of increasingly extreme climatic events, random genetic processes, with the loss of evolutionary potential through genetic drift (Lienert, 2004; Honnay and Jacquemyn, 2007) or demographic processes, with year-to-year variability in reproductive success (Tomimatsu and Ohara, 2010; Jacquemyn et al., 2012). Secondly, with the reduction in area of natural habitat, the abiotic conditions of the surrounding landscape change, with consequent negative impact on plant reproduction (Aguilar et al., 2006; Aguilar et al., 2019) and biotic interactions (Brosi, 2009; Briggs et al., 2013).

The impact of habitat transformation (Ritchie and Roser, 2013; Winkler et al., 2021) on ecological characteristics of species has been well-studied from diverse perspectives, such as life histories characteristics (Kolb and Diekmann, 2005; Bruna et al., 2009), extinction probabilities (Fréville et al., 2007), plant animal interactions (Benítez-Malvido and Arroyo-Rodríguez, 2008; Benitez-Malvido et al., 2016) and reproductive success (Brudvig et al., 2015; Vellend et al., 2017).

Following the theory of island biogeography, fragments of native habitat can be considered as islands within a “sea” of transformed terrain. In a mosaic of patches of different land use, the dominant, usually non-native background in a transformed landscape is known as the matrix (Fischer and Lindenmayer, 2007). Spatial matrix types, such as cattle pasture, different agricultural systems, or urbanization, have differential impacts on the connectivity between native habitat fragments, altering resource availability, as well as the activity of pollinators, seed dispersers, and herbivores (Jules and Shahani, 2003; Debinski, 2006).

For example, fragmentation and loss of habitat quality affect pollinator communities, including the so-called “orchid bees” (Apidae: Euglossini), impacting home ranges (Brosi, 2009) and reproductive success (Newman et al., 2013). Small, isolated plant populations are expected to have lower reproductive success when dependent on non-resident pollinators (Murren, 2002).

The tropical Andes represent a hotspot of biodiversity (Myers et al., 2000; Liang et al., 2022) and endemism (Gentry, 1982; Olson and Dinerstein, 1998) and at the same time is one of the geographical areas with the highest rate of anthropogenic habitat transformation (Etter and van Wyngaarden, 2000; Etter et al., 2006). These anthropogenic changes can influence demographic dynamics (Rodríguez-Echeverry and Leiton, 2021), survivorship or persistence of populations (Philpott et al., 2008). Nonetheless, our understanding of the impact of habitat transformation in this biodiverse region is limited (Hoang and Kanemoto, 2021; Winkler et al., 2021). In the neotropics, the influence of modified landscape mosaics on the diversity of birds, bats (Harvey and González Villalobos, 2007), insects (Vandermeer et al., 2019), and trees (Philpott et al., 2008) have been documented, however there are only a few studies focused on epiphytes (Richards et al., 2020), including epiphytic orchids (García-González and Riverón-Giró, 2013; Raventós et al., 2018), with only one study in the Andes (Parra Sánchez et al., 2016).

Epiphytic plants grow on the trunk, branches, twigs, and even the leaves (Alvarenga and Pôrto, 2007) of a plant host, the phorophyte, enabling growth in higher light conditions. Vascular epiphytes are one of the most dominant guilds of species in the tropics and are potentially highly impacted and endangered by habitat transformation (Hernández-Pérez and Solano, 2015; Osie et al., 2022). The distribution and survival of epiphytes is influenced by the landscape structure, phorophyte diversity, the age of the forest and tree size (Hietz, 1999).

The main plant families with epiphytic species are Bromeliaceae and Orchidaceae (Zotz, 2013). Some epiphytic species can also be rupiculous, growing on rock substrate, while others may also be terrestrial. Those species that are exclusively epiphytic are often limited to a particular ecological niche in a restricted zone of the architecture of the tree (Catling et al., 1986; Medeiros, 2010). The so-called twig epiphytes use as their substrate the smallest branch size, most often located in the outer fringe of the tree canopy (Ventre-Lespiaucq et al., 2017). Obligate twig epiphytes often are characterized by their accelerated life cycle, psigmoid or terete leaves, and thickened seed testa (Chase, 1987; Zotz, 2007).

Orchids specialized as twig epiphytes, while numerous, are phylogenetically restricted to Oncidiinae and Vandeae clade (Chase, 1987; Gravendeel et al., 2004). A limited amount of information of the life history of these species is available [Tolumnia variegata (Sw.) Braem, Calvo and Horvitz, 1990; Ackerman et al., 1996; Erycina crista-galli (Rchb.f.) N.H.Williams and M.W.Chase, Mondragón et al., 2007; Ionopsis utricularioides (Sw.) Lindl., García-González and Riverón-Giró, 2013] and most of the supposed advantages of being a twig epiphyte are circumstantial. It is commonly assumed that the advantage in being in the outer rim of the canopy twig epiphytes is the higher availability of light. However, this advantage may have tradeoffs (Ventre-Lespiaucq et al., 2017) including a greater risk of dehydration (Chase, 1987). A study in T. variegata found that plants located on twigs at the canopy edge had a reproductive disadvantage compared with those located within the tree canopy (Tremblay et al., 2010). Increased light availability may result in higher reproductive potential (flower production) but could also result in lower survival of the smaller individuals (for example because of desiccation), resulting in an overall decrease in the long-term persistence of the population.

Twig epiphytic orchids are often transitory pioneer species and frequently colonize phorophytes in transformed habitats. Given the tolerance of twig epiphytes to higher light intensities (Ventre-Lespiaucq et al., 2017), such populations on trees in transformed, open environment may be perceived to be as healthy as those in undisturbed forest habitat. However, this perspective may be misleading as the number of individuals may be temporary.

Our study aims to evaluate the impact of habitat transformation on the twig epiphytic species, Rodriguezia granadensis (Lindl) Rchb.f. This orchid is commonly distributed across Andean premontane and montane forests. Although endemic to Colombia, its natural tendency to colonize isolated phorophytes in open pastures is a major contributing factor to its classification of least concern (LC) in national red-list evaluations (Calderón-Sáenz, 2007; López-Gallego and Morales, 2021).

We used an approach which includes the complete life history of the species, following individuals in a mark-recapture approach and population projection matrices (PPM), comparing the demographic structure and dynamics in native forest fragments and on isolated phorophytes in pastures across two contrasting landscapes. We aim to understand the potential different demographic responses in each landscape and land use, thereby drawing inferences on the dynamics of orchid twig epiphyte populations in varying anthropogenically modified environments. We hope our findings may inform landscape management practices to promote orchid conservation in this biodiverse region.

As a null model, we would expect no differences in population dynamics between the two landscapes, a matrix dominated by either coffee crop or sugar cane and cattle grassland, nor between native forest and pastureland cover populations. If the main driver for the niche occupancy of twig epiphytes in the outer tree canopy is to maximize exposure to light, it could be expected that populations on isolated trees in an open environment such as pastures would present more favorable demographic parameters, with a higher population growth rate and stability. Specifically, we aim to determine whether population dynamics of twig epiphytes are similar in native forest and pastures in the two regions across 2 years of survey considering the following parameters (1) deterministic population growth rate, (2) transient dynamics and (3) non-linear elasticity (transfer function) of the different life stages, (4) reproductive potential (fruit set), and (5) recruitment.

We surveyed a total of 4,650 plants, in 12 sub-sites of both native forest and pasture land cover sub-sites in three sites each in two regions with differing landscape composition: shade-coffee dominated, and pasture-dominated (Supplementary Table 1). A total of 1,636 individuals died across the survey period (Supplementary Table 2).

This is the first study to compare the demographic patterns of a twig epiphytic orchid between populations in native and transformed habitat matrices in the tropical Andes. Our findings of less favorable population dynamics for R. granadensis in transformed compared with forest land covers, and between two contrasting landscape structures has important implications for the evaluation of the conservation status of this species and will inform landscape management practices to promote conservation of other similar twig epiphytic orchids in this biodiverse region.

Previous studies of tropical epiphytic communities have shown that species diversity and abundance decrease over gradients of increasing human impact (Larrea and Werner, 2010; Hylander and Nemomissa, 2017). However, in the present study, the populations of R. granadensis colonizing isolated fruit or shade trees within a transformed pasture matrix had a higher density of plants per phorophyte compared with the forest sub-sites (Supplement Table 1). This may be partly explained as isolated trees in open pastures tend to grow larger and wider crowns (Elias et al., 2021).

In Andean human-transformed landscape, Köster et al. (2011) found that tree traits explain 60% of the epiphytic community composition in an Ecuadorian cloud forest, where the isolated trees act as steppingstones that permit some persistence of epiphytes outside of the forest in a changing landscape mosaic (Köster et al., 2009; Elias et al., 2021). In these circumstances some species become denser and more abundant outside of the forest, possibly as a response to scarce available of phorophytes (Larrea and Werner, 2010), as well as changing abiotic conditions.

Nonetheless, studies in other epiphytic species have shown that in transformed habitat, population density initially increases quickly, only to later decrease, often leading to extinction, depending on time and distance to the forest source of seeds (Pellegrino et al., 2015; Hylander and Nemomissa, 2017). Thus, the high-density populations of R. granadensis in open pasture found in this study may be of a transient nature. Continued population monitoring over a longer period is needed to gauge this temporal effect.

The abundance of reproductive adults and fruit set was greater in the forest environment (Supplementary Table 3). Native forests likely comprise a more suitable ecological niche and adequate pollinator community compared to isolated trees within a pasture matrix. With increasing isolation of phorophytes from the native forests, a reduction in the number of Euglossine pollinators visiting these isolated patches has been observed (Briggs et al., 2013).

Our study reveals that the demographic health of orchid twig epiphytes is negatively influenced in transformed environments; hence, in both landscape structures, the forest sub-sites showed higher asymptotic population growth rate with greater resilience (inertia, reactivity) and a lower short-term population decline. Population growth simulation across multiple time periods suggests that the forest populations are less likely to go extinct as compared to pasture sub-sites. The likelihood of extinction of forest sites within a 20-year period is 20% (lambda mean 1.021), while pasture sites have a 45% (lambda mean 0.938) probability of extinction (Figure 2; Supplementary Table 5). According to Criterion C for the IUCN Red List evaluations, a species may be categorized as vulnerable with less than 1,000 mature individuals in each subpopulation and/or a probability of extinction of 10% in 10 years. While it is likely that R. granadensis has more than a total of 10,000 individuals across its range (the central aspect of criterion C), our findings indicate that the likelihood of subpopulation extinction is high even in the forest environment.

Only a small number of multi-period censuses of orchid population dynamics have been undertaken in the tropics, and these have similarly found a negative impact on orchid populations in landscapes with anthropogenic activity. In a study of three epiphytic species growing on coffee trees, Oncidium poikilostalix (Kraenzl.) M.W.Chase and N.H.Williams, Lepanthes acuminata Schltr. and Telipogon helleri (L.O.Williams) N.H.Williams and Dressler in Chiapas México, lambda was greater in populations in unmanaged coffee plantations compared with managed plantations (García-González et al., 2017; Raventós et al., 2018). In the terrestrial tropical invasive species, Oeceoclades maculata (Lindl.) Lindl. a higher population growth rate was noted within a Mexican forest than in a managed coffee plantation (Riverón-Giró et al., 2019). While in Phaius flavus (Blume) Lindl. in southeast China, Li et al. (2022) found that populations tended to decrease, and this change was attributed to the low germination rate in the wild and the loss of adult individuals caused by anthropogenic disturbances. In this current study, individual plants tended to remain in the same stage from one census to the next (Supplementary Table 2). Such stasis as the predominant life history process has also been registered in other neotropical epiphytic orchids (Tremblay and Hutchings, 2002; Crain et al., 2019). In general, in iteroparous forest plants with long lifespans, multi-year reproductive adult stages, and generation overlap, populations often consist of a preponderance of adults of varying sizes that remain in the same stage and contribute to population recruitment through the reproductive (Fe) stage (Silvertown et al., 1996). In contrast, iteroparous plants in open habitat plants typically exhibit populations with predominantly growth (G) and reproductive (Fe) transitions (Silvertown et al., 1993; Franco and Silvertown, 2004). Our data show that R. granadensis populations in an open habitat retain the forest strategy, with persistence of adults, lower generational turnover, fewer seedlings and juveniles that survive to adulthood, slower growth rates, all leading to declining populations.

Population convergence time to a stable state distribution was lower for forest sites than in pastures, which suggest that forest habitat may be beneficial for population stability and promoting higher population resiliency (Supplementary Table 5). Furthermore, values for inertia and reactivity, amplification and attenuation had wider intervals for forest populations, and so greater resilience in the face of changing environmental circumstances, including habitat transformations or climate change. Rapid fluctuations in the population size through time (Figure 4) could be advantageous if a population can increase rapidly after a size reduction due to stochastic phenomena. However, it may also suggest vulnerability if the fluctuation results in a rapid decrease in population size, as noted in Lepanthes caritensis Tremblay and Ackerman, Dendrophylax lindenii (Lindl.) Benth. ex Rolfe, Broughtonia cubensis Cogn (Raventós et al., 2015,b; Tremblay et al., 2015; Crain et al., 2019).

Most of the transient dynamics simulations for R. granadensis reflect the tendency for rapid reduction and high probability of extinction in about five to 10 years. Although some subsites showed population growth (Cl, Pi, H, Y forest and Pi, H pastures), the remaining subsites were near “equilibrium” without increased tendency to growth for more than 10 years. Even though populations are near equilibrium this does not necessarily guarantee that these populations will persist. A number of studies have shown that even when population sizes fluctuate, they are vulnerable to extinction when stochastic events are common (Raventós et al., 2015b; Crain et al., 2019). Twig epiphytes may be highly vulnerable to stochastic events, as loss of small branches as a consequence of the architectural growth of trees and competition with surrounding trees may result in reduced niche availability for these obligate small branch epiphytes.

Inherent fluctuations of epiphytic and twig epiphytic habit represent important constrictions for population growth, structure and distribution of R. granadensis. Transient dynamics are highly influenced by the initial vector and therefore linked to explosion or extinction and stochastic phenomena (García-González et al., 2017; Raventós et al., 2018). The pattern and intensity of fluctuation in population size may be exacerbated by natural phenomena. For example, in Central American and Caribbean orchid populations, the growth rate and high intensity fluctuations are mediated by stochastic disturbance due to large storms or hurricanes (Crain et al., 2019; Ortiz-Rodríguez et al., 2020; Raventós et al., 2021).

Perturbation analysis allows us to identify the effects of probable changes in each transition on the growth rate (Stott et al., 2011). In R. granadensis the stasis stages may be the most elastic as small changes the parameters could result in large, non-linear changes in population growth rates, most often showing a pattern close to a narrow inverted “U.”

Our analyses show that R. granadensis populations have lower survival probability when colonizing phorophytes dispersed in a pasture matrix as compared to forest sites. The diminished persistence of this orchid in a modified landscape can likely be considered an extinction debt. Colonization of isolated trees may prevent extinction in the short term, but the persistence of these sites may depend on the dynamics of the sink-source and the distance from a more suitable forest fragment (Pellegrino et al., 2015; Hylander and Nemomissa, 2017). While orchid populations within the forest and pasture landscape may function as a sink-source dynamic, the importance of the source vs. sink processes are presently little understood. Apposite questions include: how important is this process for the persistence of pasture populations, and is the direction of the seed source always from forest to pastures sites? Moreover, stochastic processes linked with the natural population dynamics of the species are drivers of epiphyte presence and persistence, and subsequently their interaction in land transformation and habitat fragmentation need to be considered (Armbrecht, 2003; Rivera-Pedroza et al., 2019; Zewdie et al., 2022).

The endemic twig epiphyte, R. granadensis, is present in anthropogenically-transformed land covers, but analysis of asymptotic and transitory dynamics indicates that these populations have lower viability than those in native forest fragments. Populations on isolated trees have lower generational turnover, fewer seedlings and juveniles that survive to adulthood, slower growth rates, and, in general, declining populations. Our data suggests that the demographic dynamics of epiphytic orchids are of a fluctuating nature, which makes them more vulnerable to disturbances and stochastic events. Since R. granadensis is a species categorized as of least concern (LC) according to IUCN Red List criteria, a more hopeful pattern in its population dynamics was expected, especially since it is found more or less frequently in disturbed landscapes. This contradiction in the health of a species when comparing observed long-term population growth rates and IUCN criteria may in part be that IUCN criteria used are those which do not explicitly include the ecology and long-term dynamics of the species but a snapshot of the population based on multiple assumptions which may not be predictors of the future health for some species.

The original contributions presented in this study are included in this article/Supplementary material, further inquiries can be directed to the corresponding author.

NO-C collected the data and ran the analysis. All authors contributed equally on writing and approved the submitted version.