1 Introduction
Habitat loss and fragmentation are two of the biggest threats to the survival of non-human primates (Crooks et al., 2017). High forest dependence makes primates vulnerable to deforestation and habitat fragmentation, and these threats increasingly force them to inhabit isolated small forest patches that are surrounded by anthropogenic activities. Consequently, populations have declined dramatically, with non-human primates being one of the most vulnerable groups threatened with extinction (Arroyo-Rodríguez and Dias, 2010; Estrada et al., 2017). Although the effects and modalities of these impacts differ for different species, habitat fragmentation poses a significant threat to their survival (Dirzo et al., 2014; Fahrig, 2003). Habitat fragmentation leads to reduced available habitats (Marsh, 2003), increased marginal effects (Laurance et al., 2002), the disruption of gene flow (Ricardo et al., 2021), lack of resources (Arroyo-Rodriguez et al., 2007), disease transmission (Gabriel et al., 2018), and changes in sensitivity to climate change and human disturbance (Onderdonk & Chapman, 2000). In addition, habitat fragmentation even affects the behavior of primates by altering their activity time allocation, roaming distance, and foraging (Campera et al., 2014; Chaves & César Bica-Marques, 2013; Chaves et al., 2012; Irwin, 2008).
Foraging activity is one of the most important behavioral activities for animals to complete (Rayner et al., 2010). Non-human primates mostly inhabit forest habitats, and, thus, they have developed characteristics that are suitable for forest survival, such as highly flexible eating habits and seasonal use of food and resources (Estrada & Coates-Estrada, 1996). However, several of these characteristics may influence their ability to live in fragmented forests (Onderdonk & Chapman, 2000). For example, spatiotemporal variations in the availability of food resources may limit the proliferation of certain specialized fruit primates (Estrada & Coates-Estrada, 1996; Irwin, 2008). Additionally, when the size of the fragments decreases, the forest plant diversity decreases and the vegetation structure degrades (Arroyo Rodríguez et al., 2007), which may lead to a decrease in the food supply of the species that inhabit the fragments (Zanette et al., 2000; Fahrig, 2003). Therefore, habitat fragmentation may affect the foraging ecology of species by affecting the habitat quality, such as the presence, abundance, or phenology of food plant resources. The longer habitat fragmentation persists, the greater the differences in the flora composition, vegetation structure, and plant phenological cycles between the forest patches (Arroyo-Rodriguez & Mandujano, 2006; Hill & Curran, 2003). For example, the abundance of large trees varies between forest fragments (Arroyo-Rodriguez & Mandujano, 2006; Arroyo-Rodriguez et al., 2007; Chapman et al., 2007; Dunn et al., 2009; Onderdonk & Chapman, 2000).
However, species do not always passively face changes in habitat and often respond through ecological, behavioral, and genetic adaptations that consist of appropriate adjustments to their survival patterns (Begon et al., 1996). Different species often adopt different foraging and dietary strategies to cope with forest fragmentation and seasonal changes in food distribution and availability. For example, some primates become more flexible in their diet, and some specialized foragers show flexibility in responding to temporal changes in food availability and habitat disturbances (Fahrig, 2003; Hou et al., 2018; Kifle & Bekele, 2021). Furthermore, Johns (1991) found that there were clear differences in the feeding time, food composition, feeding routes, and group patterns between the species in fragmented and non-fragmented habitats. In addition, the diets of some species differ between intact forests and forest fragments, suggesting that primates exhibit some foraging flexibility (Chaves et al., 2012; Chaves & César Bica-Marques, 2013). This flexible response of primates may include increasing or decreasing dietary diversity, where they consume locally abundant tree species and exotic and secondary successive species, such as vines or climbing plants, or increase their leaf consumption (de Luna et al., 2017; Dias et al., 2014; Irwin, 2008; Onderdonk & Chapman, 2000).
François’ langur (Trachypithecus francois (de Pousargues, 1898)) is one of the most threatened non-human primates in the world and is listed as endangered by the International Union for Conservation of Nature (IUCN 2022). Currently, François’ langurs are only distributed in a small area of the karst mountain forests from Vietnam to China, and their distribution is separated by roads, farmlands, and towns into more than 40 independent subpopulations, with a total population of less than 2000 individuals (Zhou et al., 2018). In China, the wild population size of this langur is 1589–1718 individuals (Yi et al., 2023). In recent years, habitat fragmentation has had a dramatic impact on the François’ langur’s population size and behavioral response (Li et al., 2007; Li et al., 2009; Huang et al., 2008). Although habitat fragmentation has had an overall negative impact on the survival of François’ langur, studies of their relatives (Trachypithecus leucocephalus Tan, 1957) have shown that they can adapt to habitat fragmentation through shifts in their activity patterns and dietary choices (Huang et al., 2005; Zhou & Huang, 2021). Given the many differences between the species, rapid habitat changes, and increased human activity, it is critical to improve our understanding of how François’ langur has adapted to this fragmented habitat. As previous studies have not focused on some of the highly representative geographical populations, we attempted to explore this aspect.
To better understand the feeding ecology and adaptation to extremely fragmented environments in François’ langurs, the diet composition of wild François’ langurs was investigated over 10 months in Encheng National Nature Reserve (ECNNR), which includes an extremely fragmented habitat in Southwest Guangxi, China. Firstly, the diets and their seasonal changes were determined. Secondly, the relationship between food composition and food availability was analyzed, and the feeding strategy of the François’ langurs was determined. Finally, the flexibility of the foraging strategy of the langurs was examined. The hypotheses are as follows:
1) Fragments are often characterized by reduced food availability for primates due to changes in forest structure, including the reduction in the number of large trees and increases in the abundance of pioneer species, exotic species, and lianas (Zhu et al., 2004). We hypothesized that François’ langurs eat fewer food species and more lianas in extremely fragmented habitats due to lower food diversity.
2) Primates prefer fruits and young leaves and are affected by seasonal fluctuations in food resources (Tsuji et al., 2013). Thus, we hypothesized that during the dry season, François’ langurs consume fewer young leaves and more alternative type foods, e.g., insects, mature leaves, and flowers, and that the consumption of fruits and young leaves increases with their availability.
3) When preferred foods are scarce, primates usually consume fallback foods (Marshall & Wrangham, 2007). Primates in tropical monsoon forests rely mainly on mature leaves and seeds as fallback foods (Zhang et al., 2017, 2021). Therefore, we predict that the consumption of fallback foods, especially mature leaves, is inversely proportional to the availability of their preferred foods.