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.